Sleep Disruption Worsens Seizures: Neuroinflammation as a Potential Mechanistic Link
Abstract
:1. Introduction
2. Sleep Disturbances in Epilepsy
2.1. Insomnia
2.2. Obstructive Sleep Apnea in Epilepsy
2.3. Excessive Daytime Sleepiness in Epilepsy
Effects of Anti-Epileptic Drugs on Excessive Daytime Sleepiness
2.4. Animal Studies
3. Circadian Rhythms in Epilepsy
4. Sleep Disruption and Neuroinflammation
4.1. Sleep Deprivation-Induced Neuroinflammation
4.2. Hypoxia Induced Neuroinflammation in Obstructive Sleep Apnea
5. Targeting Neuroinflammation in Epilepsy
5.1. Danger Signals and Pro-Inflammatory Cytokines
5.2. COX-2/Prostaglandin E2 Signaling Pathway
5.3. Glia
5.4. BBB Leakage
5.5. miRNAs
6. Evidence for Sleep Deprivation-Induced Neuroinflammation in Epileptic Rodents
7. Management of Sleep Disruption in Epilepsy
7.1. Surgery
7.2. Ketogenic Diet
7.3. Positive Airway Pressure
7.4. Melatonin
7.5. Chronotherapies
7.6. Cognitive Behavioral Therapy
7.7. Pharmacological Therapies
8. Conclusions and Future Directions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Hirshkowitz, M.; Whiton, K.; Albert, S.M.; Alessi, C.; Bruni, O.; DonCarlos, L.; Hazen, N.; Herman, J.; Adams Hillard, P.J.; Katz, E.S.; et al. National Sleep Foundation’s updated sleep duration recommendations: Final report. Sleep Health 2015, 1, 233–243. [Google Scholar] [CrossRef]
- Hertenstein, E.; Gabryelska, A.; Spiegelhalder, K.; Nissen, C.; Johann, A.F.; Umarova, R.; Riemann, D.; Baglioni, C.; Feige, B. Reference Data for Polysomnography-Measured and Subjective Sleep in Healthy Adults. J. Clin. Sleep Med. 2018, 14, 523–532. [Google Scholar] [CrossRef]
- World Health Organization. Available online: https://www.who.int/news-room/fact-sheets/detail/epilepsy (accessed on 20 October 2021).
- Devinsky, O.; Hesdorffer, D.C.; Thurman, D.J.; Lhatoo, S.; Richerson, G. Sudden unexpected death in epilepsy: Epidemiology, mechanisms, and prevention. Lancet Neurol. 2016, 15, 1075–1088. [Google Scholar] [CrossRef]
- Lamberts, R.J.; Thijs, R.D.; Laffan, A.; Langan, Y.; Sander, J.W. Sudden unexpected death in epilepsy: People with nocturnal seizures may be at highest risk. Epilepsia 2012, 53, 253–257. [Google Scholar] [CrossRef]
- Nobili, L.; de Weerd, A.; Rubboli, G.; Beniczky, S.; Derry, C.; Eriksson, S.; Halasz, P.; Hogl, B.; Santamaria, J.; Khatami, R.; et al. Standard procedures for the diagnostic pathway of sleep-related epilepsies and comorbid sleep disorders: An EAN, ESRS and ILAE-Europe consensus review. Eur. J. Neurol. 2021, 28, 15–32. [Google Scholar] [CrossRef] [PubMed]
- Espinosa-Garcia, C.; Zeleke, H.; Rojas, A. Impact of Stress on Epilepsy: Focus on Neuroinflammation-A Mini Review. Int. J. Mol. Sci. 2021, 22, 4061. [Google Scholar] [CrossRef]
- Kim, E.J.; Dimsdale, J.E. The effect of psychosocial stress on sleep: A review of polysomnographic evidence. Behav. Sleep Med. 2007, 5, 256–278. [Google Scholar] [CrossRef] [Green Version]
- Riemann, D.; Spiegelhalder, K.; Feige, B.; Voderholzer, U.; Berger, M.; Perlis, M.; Nissen, C. The hyperarousal model of insomnia: A review of the concept and its evidence. Sleep Med. Rev. 2010, 14, 19–31. [Google Scholar] [CrossRef] [PubMed]
- Pavlova, M. Circadian Rhythm Sleep-Wake Disorders. Continuum 2017, 23, 1051–1063. [Google Scholar] [CrossRef]
- Pavlova, M.K.; Ng, M.; Allen, R.M.; Boly, M.; Kothare, S.; Zaveri, H.; Zee, P.C.; Adler, G.; Buchanan, G.F.; Quigg, M.S. Proceedings of the Sleep and Epilepsy Workgroup: Section 2 Comorbidities: Sleep Related Comorbidities of Epilepsy. Epilepsy Curr. 2021, 21, 210–214. [Google Scholar] [CrossRef] [PubMed]
- Joels, M. Stress, the hippocampus, and epilepsy. Epilepsia 2009, 50, 586–597. [Google Scholar] [CrossRef] [PubMed]
- Im, H.J.; Park, S.H.; Baek, S.H.; Chu, M.K.; Yang, K.I.; Kim, W.J.; Yun, C.H. Associations of impaired sleep quality, insomnia, and sleepiness with epilepsy: A questionnaire-based case-control study. Epilepsy Behav. 2016, 57, 55–59. [Google Scholar] [CrossRef]
- Pineda, E.; Shin, D.; Sankar, R.; Mazarati, A.M. Comorbidity between epilepsy and depression: Experimental evidence for the involvement of serotonergic, glucocorticoid, and neuroinflammatory mechanisms. Epilepsia 2010, 51 (Suppl. S3), 110–114. [Google Scholar] [CrossRef] [PubMed]
- Bazil, C.W. Epilepsy and sleep disturbance. Epilepsy Behav. 2003, 4 (Suppl. S2), 39–45. [Google Scholar] [CrossRef] [PubMed]
- Malow, B.A.; Bowes, R.J.; Lin, X. Predictors of sleepiness in epilepsy patients. Sleep 1997, 20, 1105–1110. [Google Scholar] [CrossRef] [Green Version]
- Staniszewska, A.; Maka, A.; Religioni, U.; Olejniczak, D. Sleep disturbances among patients with epilepsy. Neuropsychiatr. Dis. Treat. 2017, 13, 1797–1803. [Google Scholar] [CrossRef] [Green Version]
- Khachatryan, S.G.; Ghahramanyan, L.; Tavadyan, Z.; Yeghiazaryan, N.; Attarian, H.P. Sleep-related movement disorders in a population of patients with epilepsy: Prevalence and impact of restless legs syndrome and sleep bruxism. J. Clin. Sleep Med. 2020, 16, 409–414. [Google Scholar] [CrossRef]
- Quigg, M.; Bazil, C.W.; Boly, M.; St Louis, E.K.; Liu, J.; Ptacek, L.; Maganti, R.; Kalume, F.; Gluckman, B.J.; Pathmanathan, J.; et al. Proceedings of the Sleep and Epilepsy Workshop: Section 1 Decreasing Seizures-Improving Sleep and Seizures, Themes for Future Research. Epilepsy Curr. 2021, 21, 204–209. [Google Scholar] [CrossRef]
- Cohen, H.B.; Dement, W.C. Sleep: Suppression of rapid eye movement phase in the cat after electroconvulsive shock. Science 1966, 154, 396–398. [Google Scholar] [CrossRef]
- Raol, Y.H.; Meti, B.L. Sleep-wakefulness alterations in amygdala-kindled rats. Epilepsia 1998, 39, 1133–1137. [Google Scholar] [CrossRef] [Green Version]
- Rondouin, G.; Baldy-Moulinier, M.; Passouant, P. The influence of hippocampal kindling on sleep organization in cats. Effects of alpha-methylparatyrosine. Brain Res. 1980, 181, 413–424. [Google Scholar] [CrossRef]
- Tanaka, T.; Naquet, R. Kindling effect and sleep organization in cats. Electroencephalogr. Clin. Neurophysiol. 1975, 39, 449–454. [Google Scholar] [CrossRef]
- Krushinskii, L.V. Genetic studies in the experimental pathophysiology of higher nervous activity. Byull.Mosk. Obshch. Isp. Prir. Otdel Biol. 1959, 64, 105–117. [Google Scholar]
- Oganesyan, G.A.; Vataev, S.I. Effect of generalized seizures on the structure of the sleep-waking cycle and the EEG in rats with an inherited predisposition to audiogenic convulsions. Neurosci. Behav. Physiol. 1997, 27, 578–584. [Google Scholar] [CrossRef]
- Drinkenburg, W.H.; Coenen, A.M.; Vossen, J.M.; van Luijtelaar, E.L. Sleep deprivation and spike-wave discharges in epileptic rats. Sleep 1995, 18, 252–256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foldvary-Schaefer, N.; Grigg-Damberger, M. Sleep and epilepsy: What we know, don’t know, and need to know. J. Clin. Neurophysiol. 2006, 23, 4–20. [Google Scholar] [CrossRef]
- Badawy, R.A.; Curatolo, J.M.; Newton, M.; Berkovic, S.F.; Macdonell, R.A. Sleep deprivation increases cortical excitability in epilepsy: Syndrome-specific effects. Neurology 2006, 67, 1018–1022. [Google Scholar] [CrossRef]
- Fountain, N.B.; Kim, J.S.; Lee, S.I. Sleep deprivation activates epileptiform discharges independent of the activating effects of sleep. J. Clin. Neurophysiol. 1998, 15, 69–75. [Google Scholar] [CrossRef]
- Malow, B.A.; Passaro, E.; Milling, C.; Minecan, D.N.; Levy, K. Sleep deprivation does not affect seizure frequency during inpatient video-EEG monitoring. Neurology 2002, 59, 1371–1374. [Google Scholar] [CrossRef]
- Morin, C.M.; Benca, R.M. Insomnia nature, diagnosis, and treatment. Handb. Clin. Neurol. 2011, 99, 723–746. [Google Scholar] [CrossRef]
- Morin, C.M.; LeBlanc, M.; Daley, M.; Gregoire, J.P.; Mérette, C. Epidemiology of insomnia: Prevalence, self-help treatments, consultations, and determinants of help-seeking behaviors. Sleep Med. 2006, 7, 123–130. [Google Scholar] [CrossRef] [PubMed]
- Olfson, M.; Wall, M.; Liu, S.M.; Morin, C.M.; Blanco, C. Insomnia and Impaired Quality of Life in the United States. J. Clin. Psychiatry 2018, 79. [Google Scholar] [CrossRef]
- Khatami, R.; Zutter, D.; Siegel, A.; Mathis, J.; Donati, F.; Bassetti, C.L. Sleep-wake habits and disorders in a series of 100 adult epilepsy patients–a prospective study. Seizure 2006, 15, 299–306. [Google Scholar] [CrossRef] [Green Version]
- Piperidou, C.; Karlovasitou, A.; Triantafyllou, N.; Terzoudi, A.; Constantinidis, T.; Vadikolias, K.; Heliopoulos, I.; Vassilopoulos, D.; Balogiannis, S. Influence of sleep disturbance on quality of life of patients with epilepsy. Seizure 2008, 17, 588–594. [Google Scholar] [CrossRef] [Green Version]
- Vendrame, M.; Yang, B.; Jackson, S.; Auerbach, S.H. Insomnia and epilepsy: A questionnaire-based study. J. Clin. Sleep Med. 2013, 9, 141–146. [Google Scholar] [CrossRef] [Green Version]
- Moser, D.; Pablik, E.; Aull-Watschinger, S.; Pataraia, E.; Wober, C.; Seidel, S. Depressive symptoms predict the quality of sleep in patients with partial epilepsy--A combined retrospective and prospective study. Epilepsy Behav. 2015, 47, 104–110. [Google Scholar] [CrossRef]
- Quigg, M.; Gharai, S.; Ruland, J.; Schroeder, C.; Hodges, M.; Ingersoll, K.S.; Thorndike, F.P.; Yan, G.; Ritterband, L.M. Insomnia in epilepsy is associated with continuing seizures and worse quality of life. Epilepsy Res. 2016, 122, 91–96. [Google Scholar] [CrossRef] [PubMed]
- Planas-Ballve, A.; Grau-Lopez, L.; Jimenez, M.; Ciurans, J.; Fumanal, A.; Becerra, J.L. Insomnia and poor sleep quality are associated with poor seizure control in patients with epilepsy. Neurologia 2020, S0213-4853(19)30139-2. [Google Scholar] [CrossRef] [PubMed]
- Yang, K.I.; Grigg-Damberger, M.; Andrews, N.; O’Rourke, C.; Bena, J.; Foldvary-Schaefer, N. Severity of self-reported insomnia in adults with epilepsy is related to comorbid medical disorders and depressive symptoms. Epilepsy Behav. 2016, 60, 27–32. [Google Scholar] [CrossRef] [Green Version]
- Frucht, M.M.; Quigg, M.; Schwaner, C.; Fountain, N.B. Distribution of seizure precipitants among epilepsy syndromes. Epilepsia 2000, 41, 1534–1539. [Google Scholar] [CrossRef] [PubMed]
- Nollet, M.; Wisden, W.; Franks, N.P. Sleep deprivation and stress: A reciprocal relationship. Interface Focus 2020, 10, 20190092. [Google Scholar] [CrossRef]
- Vgontzas, A.N.; Bixler, E.O.; Lin, H.M.; Prolo, P.; Mastorakos, G.; Vela-Bueno, A.; Kales, A.; Chrousos, G.P. Chronic insomnia is associated with nyctohemeral activation of the hypothalamic-pituitary-adrenal axis: Clinical implications. J. Clin. Endocrinol. Metab. 2001, 86, 3787–3794. [Google Scholar] [CrossRef]
- Rodenbeck, A.; Huether, G.; Ruther, E.; Hajak, G. Interactions between evening and nocturnal cortisol secretion and sleep parameters in patients with severe chronic primary insomnia. Neurosci Lett 2002, 324, 159–163. [Google Scholar] [CrossRef]
- Varkevisser, M.; Van Dongen, H.P.; Kerkhof, G.A. Physiologic indexes in chronic insomnia during a constant routine: Evidence for general hyperarousal? Sleep 2005, 28, 1588–1596. [Google Scholar] [PubMed] [Green Version]
- Manni, R.; Politini, L.; Ratti, M.T.; Marchioni, E.; Sartori, I.; Galimberti, C.A.; Tartara, A. Sleep hygiene in adult epilepsy patients: A questionnaire-based survey. Acta Neurol. Scand. 2000, 101, 301–304. [Google Scholar] [CrossRef]
- Park, J.G.; Ramar, K.; Olson, E.J. Updates on definition, consequences, and management of obstructive sleep apnea. Mayo Clin. Proc. 2011, 86, 549–554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chopra, S.; Rathore, A.; Younas, H.; Pham, L.V.; Gu, C.; Beselman, A.; Kim, I.Y.; Wolfe, R.R.; Perin, J.; Polotsky, V.Y.; et al. Obstructive Sleep Apnea Dynamically Increases Nocturnal Plasma Free Fatty Acids, Glucose, and Cortisol During Sleep. J. Clin. Endocrinol. Metab. 2017, 102, 3172–3181. [Google Scholar] [CrossRef]
- DeMartino, T.; Ghoul, R.E.; Wang, L.; Bena, J.; Hazen, S.L.; Tracy, R.; Patel, S.R.; Auckley, D.; Mehra, R. Oxidative Stress and Inflammation Differentially Elevated in Objective Versus Habitual Subjective Reduced Sleep Duration in Obstructive Sleep Apnea. Sleep 2016, 39, 1361–1369. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giorelli, A.S.; Passos, P.; Carnaval, T.; Gomes Mda, M. Excessive daytime sleepiness and epilepsy: A systematic review. Epilepsy Res. Treat 2013, 2013, 629469. [Google Scholar] [CrossRef]
- Devinsky, O.; Ehrenberg, B.; Barthlen, G.M.; Abramson, H.S.; Luciano, D. Epilepsy and sleep apnea syndrome. Neurology 1994, 44, 2060–2064. [Google Scholar] [CrossRef]
- Vaughn, B.V.; D’Cruz, O.F.; Beach, R.; Messenheimer, J.A. Improvement of epileptic seizure control with treatment of obstructive sleep apnoea. Seizure 1996, 5, 73–78. [Google Scholar] [CrossRef] [Green Version]
- Malow, B.A.; Levy, K.; Maturen, K.; Bowes, R. Obstructive sleep apnea is common in medically refractory epilepsy patients. Neurology 2000, 55, 1002–1007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foldvary-Schaefer, N.; Andrews, N.D.; Pornsriniyom, D.; Moul, D.E.; Sun, Z.; Bena, J. Sleep apnea and epilepsy: Who’s at risk? Epilepsy Behav. 2012, 25, 363–367. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manni, R.; Terzaghi, M.; Arbasino, C.; Sartori, I.; Galimberti, C.A.; Tartara, A. Obstructive sleep apnea in a clinical series of adult epilepsy patients: Frequency and features of the comorbidity. Epilepsia 2003, 44, 836–840. [Google Scholar] [CrossRef] [Green Version]
- Lin, Z.; Si, Q.; Xiaoyi, Z. Obstructive sleep apnoea in patients with epilepsy: A meta-analysis. Sleep Breath 2017, 21, 263–270. [Google Scholar] [CrossRef] [PubMed]
- Jain, S.V.; Simakajornboon, S.; Shapiro, S.M.; Morton, L.D.; Leszczyszyn, D.J.; Simakajornboon, N. Obstructive sleep apnea in children with epilepsy: Prospective pilot trial. Acta Neurol. Scand. 2012, 125, e3–e6. [Google Scholar] [CrossRef]
- Zanzmera, P.; Shukla, G.; Gupta, A.; Singh, H.; Goyal, V.; Srivastava, A.; Behari, M. Markedly disturbed sleep in medically refractory compared to controlled epilepsy—A clinical and polysomnography study. Seizure 2012, 21, 487–490. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jaseja, H.; Goyal, M.; Mishra, P. Drug-Resistant Epilepsy and Obstructive Sleep Apnea: Exploring a Link Between the Two. World Neurosurg. 2021, 146, 210–214. [Google Scholar] [CrossRef]
- Kumar, J.; Solaiman, A.; Mahakkanukrauh, P.; Mohamed, R.; Das, S. Sleep Related Epilepsy and Pharmacotherapy: An Insight. Front. Pharmacol. 2018, 9, 1088. [Google Scholar] [CrossRef]
- International Classification of Sleep Disorders, 3rd ed.; Darien, I.L. (Ed.) American Academy of Sleep Medici: Dallas, TX, USA, 2014. [Google Scholar]
- Manni, R.; Politini, L.; Sartori, I.; Ratti, M.T.; Galimberti, C.A.; Tartara, A. Daytime sleepiness in epilepsy patients: Evaluation by means of the Epworth sleepiness scale. J. Neurol. 2000, 247, 716–717. [Google Scholar] [CrossRef]
- de Weerd, A.; de Haas, S.; Otte, A.; Trenite, D.K.; van Erp, G.; Cohen, A.; de Kam, M.; van Gerven, J. Subjective sleep disturbance in patients with partial epilepsy: A questionnaire-based study on prevalence and impact on quality of life. Epilepsia 2004, 45, 1397–1404. [Google Scholar] [CrossRef]
- Chen, N.C.; Tsai, M.H.; Chang, C.C.; Lu, C.H.; Chang, W.N.; Lai, S.L.; Tseng, Y.L.; Chuang, Y.C. Sleep quality and daytime sleepiness in patients with epilepsy. Acta Neurol. Taiwan 2011, 20, 249–256. [Google Scholar] [PubMed]
- Krishnan, P.; Sinha, S.; Taly, A.B.; Ramachandraiah, C.T.; Rao, S.; Satishchandra, P. Sleep disturbances in juvenile myoclonic epilepsy: A sleep questionnaire-based study. Epilepsy Behav. 2012, 23, 305–309. [Google Scholar] [CrossRef]
- Vignatelli, L.; Bisulli, F.; Naldi, I.; Ferioli, S.; Pittau, F.; Provini, F.; Plazzi, G.; Vetrugno, R.; Montagna, P.; Tinuper, P. Excessive daytime sleepiness and subjective sleep quality in patients with nocturnal frontal lobe epilepsy: A case-control study. Epilepsia 2006, 47 (Suppl. S5), 73–77. [Google Scholar] [CrossRef]
- Gammino, M.; Zummo, L.; Bue, A.L.; Urso, L.; Terruso, V.; Marrone, O.; Fierro, B.; Daniele, O. Excessive Daytime Sleepiness and Sleep Disorders in a Population of Patients with Epilepsy: A Case-Control Study. J. Epilepsy Res. 2016, 6, 79–86. [Google Scholar] [CrossRef] [Green Version]
- Johns, M.W. A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep 1991, 14, 540–545. [Google Scholar] [CrossRef] [Green Version]
- de Almeida, C.A.; Lins, O.G.; Lins, S.G.; Laurentino, S.; Valenca, M.M. Sleep disorders in temporal lobe epilepsy. Arq. Neuropsiquiatr. 2003, 61, 979–987. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khachatryan, S.G.; Attarian, H.P. Excessive daytime sleepiness could be multifactorial in adults with epilepsy. J. Clin. Sleep Med. 2020, 16, 1395–1396. [Google Scholar] [CrossRef] [PubMed]
- Chihorek, A.M.; Abou-Khalil, B.; Malow, B.A. Obstructive sleep apnea is associated with seizure occurrence in older adults with epilepsy. Neurology 2007, 69, 1823–1827. [Google Scholar] [CrossRef]
- Garbarino, S. Excessive daytime sleepiness in obstructive sleep apnea: Implications for driving licenses. Sleep Breath 2020, 24, 37–47. [Google Scholar] [CrossRef]
- Placidi, F.; Marciani, M.G.; Diomedi, M.; Scalise, A.; Pauri, F.; Giacomini, P.; Gigli, G.L. Effects of lamotrigine on nocturnal sleep, daytime somnolence and cognitive functions in focal epilepsy. Acta Neurol. Scand. 2000, 102, 81–86. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.Y.; Tang, X.D.; Huang, L.L.; Zhong, Z.Q.; Lei, F.; Zhou, D. The acute effects of levetiracetam on nocturnal sleep and daytime sleepiness in patients with partial epilepsy. J. Clin. Neurosci. 2012, 19, 956–960. [Google Scholar] [CrossRef] [PubMed]
- Klobucnikova, K.; Kollar, B.; Martiniskova, Z. Daytime sleepiness and changes of sleep architecture in patients with epilepsy. Neuroendocrinol. Lett. 2009, 30, 599–603. [Google Scholar] [PubMed]
- Giorelli, A.S.; Neves, G.S.; Venturi, M.; Pontes, I.M.; Valois, A.; Gomes Mda, M. Excessive daytime sleepiness in patients with epilepsy: A subjective evaluation. Epilepsy Behav. 2011, 21, 449–452. [Google Scholar] [CrossRef]
- Bonanni, E.; Galli, R.; Maestri, M.; Pizzanelli, C.; Fabbrini, M.; Manca, M.L.; Iudice, A.; Murri, L. Daytime sleepiness in epilepsy patients receiving topiramate monotherapy. Epilepsia 2004, 45, 333–337. [Google Scholar] [CrossRef]
- Romigi, A.; Izzi, F.; Marciani, M.G.; Torelli, F.; Zannino, S.; Pisani, L.R.; Uasone, E.; Corte, F.; Placidi, F. Pregabalin as add-on therapy induces REM sleep enhancement in partial epilepsy: A polysomnographic study. Eur. J. Neurol. 2009, 16, 70–75. [Google Scholar] [CrossRef]
- de Haas, S.; Otte, A.; de Weerd, A.; van Erp, G.; Cohen, A.; van Gerven, J. Exploratory polysomnographic evaluation of pregabalin on sleep disturbance in patients with epilepsy. J. Clin. Sleep Med. 2007, 3, 473–478. [Google Scholar] [CrossRef] [Green Version]
- Suchecki, D.; Tiba, P.A.; Tufik, S. Paradoxical sleep deprivation facilitates subsequent corticosterone response to a mild stressor in rats. Neurosci. Lett. 2002, 320, 45–48. [Google Scholar] [CrossRef]
- Brianza-Padilla, M.; Sanchez-Munoz, F.; Vazquez-Palacios, G.; Huang, F.; Almanza-Perez, J.C.; Bojalil, R.; Bonilla-Jaime, H. Cytokine and microRNA levels during different periods of paradoxical sleep deprivation and sleep recovery in rats. PeerJ 2018, 6, e5567. [Google Scholar] [CrossRef] [Green Version]
- Wadhwa, M.; Kumari, P.; Chauhan, G.; Roy, K.; Alam, S.; Kishore, K.; Ray, K.; Panjwani, U. Sleep deprivation induces spatial memory impairment by altered hippocampus neuroinflammatory responses and glial cells activation in rats. J. Neuroimmunol. 2017, 312, 38–48. [Google Scholar] [CrossRef]
- McEwen, B.S. Sleep deprivation as a neurobiologic and physiologic stressor: Allostasis and allostatic load. Metabolism 2006, 55, S20–S23. [Google Scholar] [CrossRef] [PubMed]
- Yehuda, S.; Sredni, B.; Carasso, R.L.; Kenigsbuch-Sredni, D. REM sleep deprivation in rats results in inflammation and interleukin-17 elevation. J. Interferon Cytokine Res. 2009, 29, 393–398. [Google Scholar] [CrossRef]
- Irwin, M.R.; Wang, M.; Campomayor, C.O.; Collado-Hidalgo, A.; Cole, S. Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch. Intern. Med. 2006, 166, 1756–1762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bellesi, M.; de Vivo, L.; Chini, M.; Gilli, F.; Tononi, G.; Cirelli, C. Sleep Loss Promotes Astrocytic Phagocytosis and Microglial Activation in Mouse Cerebral Cortex. J. Neurosci. 2017, 37, 5263–5273. [Google Scholar] [CrossRef]
- Guan, Z.; Peng, X.; Fang, J. Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Res. 2004, 1018, 38–47. [Google Scholar] [CrossRef]
- Zielinski, M.R.; Kim, Y.; Karpova, S.A.; McCarley, R.W.; Strecker, R.E.; Gerashchenko, D. Chronic sleep restriction elevates brain interleukin-1 beta and tumor necrosis factor-alpha and attenuates brain-derived neurotrophic factor expression. Neurosci. Lett. 2014, 580, 27–31. [Google Scholar] [CrossRef] [Green Version]
- Manchanda, S.; Singh, H.; Kaur, T.; Kaur, G. Low-grade neuroinflammation due to chronic sleep deprivation results in anxiety and learning and memory impairments. Mol. Cell Biochem. 2018, 449, 63–72. [Google Scholar] [CrossRef]
- Hsu, J.C.; Lee, Y.S.; Chang, C.N.; Chuang, H.L.; Ling, E.A.; Lan, C.T. Sleep deprivation inhibits expression of NADPH-d and NOS while activating microglia and astroglia in the rat hippocampus. Cells Tissues Organs 2003, 173, 242–254. [Google Scholar] [CrossRef] [PubMed]
- Opp, M.R.; Krueger, J.M. Interleukin-1 is involved in responses to sleep deprivation in the rabbit. Brain Res. 1994, 639, 57–65. [Google Scholar] [CrossRef]
- Hall, S.; Deurveilher, S.; Robertson, G.S.; Semba, K. Homeostatic state of microglia in a rat model of chronic sleep restriction. Sleep 2020, 43. [Google Scholar] [CrossRef]
- Sasaki, Y.; Ohsawa, K.; Kanazawa, H.; Kohsaka, S.; Imai, Y. Iba1 is an actin-cross-linking protein in macrophages/microglia. Biochem. Biophys. Res. Commun. 2001, 286, 292–297. [Google Scholar] [CrossRef]
- Ito, D.; Tanaka, K.; Suzuki, S.; Dembo, T.; Fukuuchi, Y. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 2001, 32, 1208–1215. [Google Scholar] [CrossRef] [Green Version]
- Orihuela, R.; McPherson, C.A.; Harry, G.J. Microglial M1/M2 polarization and metabolic states. Br. J. Pharmacol. 2016, 173, 649–665. [Google Scholar] [CrossRef]
- Guo, Y.; Hong, W.; Wang, X.; Zhang, P.; Korner, H.; Tu, J.; Wei, W. MicroRNAs in Microglia: How do MicroRNAs Affect Activation, Inflammation, Polarization of Microglia and Mediate the Interaction Between Microglia and Glioma? Front. Mol. Neurosci. 2019, 12, 125. [Google Scholar] [CrossRef]
- Davis, C.J.; Clinton, J.M.; Krueger, J.M. MicroRNA 138, let-7b, and 125a inhibitors differentially alter sleep and EEG delta-wave activity in rats. J. Appl. Physiol. 2012, 113, 1756–1762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Balusu, S.; Van Wonterghem, E.; De Rycke, R.; Raemdonck, K.; Stremersch, S.; Gevaert, K.; Brkic, M.; Demeestere, D.; Vanhooren, V.; Hendrix, A.; et al. Identification of a novel mechanism of blood-brain communication during peripheral inflammation via choroid plexus-derived extracellular vesicles. EMBO Mol. Med. 2016, 8, 1162–1183. [Google Scholar] [CrossRef] [PubMed]
- Chung, W.S.; Clarke, L.E.; Wang, G.X.; Stafford, B.K.; Sher, A.; Chakraborty, C.; Joung, J.; Foo, L.C.; Thompson, A.; Chen, C.; et al. Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 2013, 504, 394–400. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Davis, C.H.; Kim, K.Y.; Bushong, E.A.; Mills, E.A.; Boassa, D.; Shih, T.; Kinebuchi, M.; Phan, S.; Zhou, Y.; Bihlmeyer, N.A.; et al. Transcellular degradation of axonal mitochondria. Proc. Natl. Acad. Sci. USA 2014, 111, 9633–9638. [Google Scholar] [CrossRef] [Green Version]
- Chung, W.S.; Allen, N.J.; Eroglu, C. Astrocytes Control Synapse Formation, Function, and Elimination. Cold Spring Harb. Perspect. Biol. 2015, 7, a020370. [Google Scholar] [CrossRef] [Green Version]
- Bellesi, M.; de Vivo, L.; Tononi, G.; Cirelli, C. Effects of sleep and wake on astrocytes: Clues from molecular and ultrastructural studies. BMC Biol. 2015, 13, 66. [Google Scholar] [CrossRef] [Green Version]
- Cirelli, C.; Faraguna, U.; Tononi, G. Changes in brain gene expression after long-term sleep deprivation. J. Neurochem. 2006, 98, 1632–1645. [Google Scholar] [CrossRef]
- Collop, N.A.; Salas, R.E.; Delayo, M.; Gamaldo, C. Normal sleep and circadian processes. Crit. Care Clin. 2008, 24, 449–460. [Google Scholar] [CrossRef] [PubMed]
- Morris, C.J.; Purvis, T.E.; Hu, K.; Scheer, F.A. Circadian misalignment increases cardiovascular disease risk factors in humans. Proc. Natl. Acad. Sci. USA 2016, 113, E1402–E1411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Amihaesei, I.C.; Mungiu, O.C. Main neuroendocrine features and therapy in primary sleep troubles. Rev. Med. Chir. Soc. Med. Nat. Iasi 2012, 116, 862–866. [Google Scholar] [PubMed]
- Bernard, C. Circadian/multidien Molecular Oscillations and Rhythmicity of Epilepsy (MORE). Epilepsia 2021, 62 (Suppl. S1), S49–S68. [Google Scholar] [CrossRef]
- Cano-Lopez, I.; Gonzalez-Bono, E. Cortisol levels and seizures in adults with epilepsy: A systematic review. Neurosci. Biobehav. Rev. 2019, 103, 216–229. [Google Scholar] [CrossRef]
- Khan, S.; Nobili, L.; Khatami, R.; Loddenkemper, T.; Cajochen, C.; Dijk, D.J.; Eriksson, S.H. Circadian rhythm and epilepsy. Lancet Neurol. 2018, 17, 1098–1108. [Google Scholar] [CrossRef]
- Gerstner, J.R.; Smith, G.G.; Lenz, O.; Perron, I.J.; Buono, R.J.; Ferraro, T.N. BMAL1 controls the diurnal rhythm and set point for electrical seizure threshold in mice. Front. Syst. Neurosci. 2014, 8, 121. [Google Scholar] [CrossRef] [Green Version]
- Li, P.; Fu, X.; Smith, N.A.; Ziobro, J.; Curiel, J.; Tenga, M.J.; Martin, B.; Freedman, S.; Cea-Del Rio, C.A.; Oboti, L.; et al. Loss of CLOCK Results in Dysfunction of Brain Circuits Underlying Focal Epilepsy. Neuron 2017, 96, 387–401. [Google Scholar] [CrossRef] [Green Version]
- McClelland, S.; Brennan, G.P.; Dube, C.; Rajpara, S.; Iyer, S.; Richichi, C.; Bernard, C.; Baram, T.Z. The transcription factor NRSF contributes to epileptogenesis by selective repression of a subset of target genes. Elife 2014, 3, e01267. [Google Scholar] [CrossRef]
- Terrone, G.; Frigerio, F.; Balosso, S.; Ravizza, T.; Vezzani, A. Inflammation and reactive oxygen species in status epilepticus: Biomarkers and implications for therapy. Epilepsy Behav. 2019, 101, 106275. [Google Scholar] [CrossRef]
- Wang, G.; Zhu, Z.; Xu, D.; Sun, L. Advances in Understanding CREB Signaling-Mediated Regulation of the Pathogenesis and Progression of Epilepsy. Clin. Neurol. Neurosurg. 2020, 196, 106018. [Google Scholar] [CrossRef] [PubMed]
- Hodges, S.L.; Lugo, J.N. Therapeutic role of targeting mTOR signaling and neuroinflammation in epilepsy. Epilepsy Res. 2020, 161, 106282. [Google Scholar] [CrossRef]
- Matsumoto, H.; Ajmonemarsan, C. Cellular Mechanisms in Experimental Epileptic Seizures. Science 1964, 144, 193–194. [Google Scholar] [CrossRef]
- Van Dongen, H.P.; Maislin, G.; Mullington, J.M.; Dinges, D.F. The cumulative cost of additional wakefulness: Dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep 2003, 26, 117–126. [Google Scholar] [CrossRef] [PubMed]
- Redwine, L.; Dang, J.; Irwin, M. Cellular adhesion molecule expression, nocturnal sleep, and partial night sleep deprivation. Brain Behav. Immun. 2004, 18, 333–340. [Google Scholar] [CrossRef] [PubMed]
- Born, J.; Lange, T.; Hansen, K.; Molle, M.; Fehm, H.L. Effects of sleep and circadian rhythm on human circulating immune cells. J. Immunol. 1997, 158, 4454–4464. [Google Scholar]
- Redwine, L.; Hauger, R.L.; Gillin, J.C.; Irwin, M. Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in humans. J. Clin. Endocrinol. Metab. 2000, 85, 3597–3603. [Google Scholar] [CrossRef]
- Vgontzas, A.N.; Papanicolaou, D.A.; Bixler, E.O.; Kales, A.; Tyson, K.; Chrousos, G.P. Elevation of plasma cytokines in disorders of excessive daytime sleepiness: Role of sleep disturbance and obesity. J. Clin. Endocrinol. Metab. 1997, 82, 1313–1316. [Google Scholar] [CrossRef] [PubMed]
- Mills, P.J.; von Känel, R.; Norman, D.; Natarajan, L.; Ziegler, M.G.; Dimsdale, J.E. Inflammation and sleep in healthy individuals. Sleep 2007, 30, 729–735. [Google Scholar] [CrossRef] [Green Version]
- Quigg, M. Circadian rhythms: Interactions with seizures and epilepsy. Epilepsy Res. 2000, 42, 43–55. [Google Scholar] [CrossRef]
- Janz, D. The grand mal epilepsies and the sleeping-waking cycle. Epilepsia 1962, 3, 69–109. [Google Scholar] [CrossRef]
- van Campen, J.S.; Valentijn, F.A.; Jansen, F.E.; Joëls, M.; Braun, K.P. Seizure occurrence and the circadian rhythm of cortisol: A systematic review. Epilepsy Behav. 2015, 47, 132–137. [Google Scholar] [CrossRef]
- Ramgopal, S.; Thome-Souza, S.; Loddenkemper, T. Chronopharmacology of anti-convulsive therapy. Curr. Neurol. Neurosci. Rep. 2013, 13, 339. [Google Scholar] [CrossRef] [Green Version]
- Zarowski, M.; Loddenkemper, T.; Vendrame, M.; Alexopoulos, A.V.; Wyllie, E.; Kothare, S.V. Circadian distribution and sleep/wake patterns of generalized seizures in children. Epilepsia 2011, 52, 1076–1083. [Google Scholar] [CrossRef]
- Gurkas, E.; Serdaroglu, A.; Hirfanoglu, T.; Kartal, A.; Yılmaz, U.; Bilir, E. Sleep-wake distribution and circadian patterns of epileptic seizures in children. Eur. J. Paediatr. Neurol. 2016, 20, 549–554. [Google Scholar] [CrossRef] [PubMed]
- Karafin, M.; St Louis, E.K.; Zimmerman, M.B.; Sparks, J.D.; Granner, M.A. Bimodal ultradian seizure periodicity in human mesial temporal lobe epilepsy. Seizure 2010, 19, 347–351. [Google Scholar] [CrossRef] [Green Version]
- Durazzo, T.S.; Spencer, S.S.; Duckrow, R.B.; Novotny, E.J.; Spencer, D.D.; Zaveri, H.P. Temporal distributions of seizure occurrence from various epileptogenic regions. Neurology 2008, 70, 1265–1271. [Google Scholar] [CrossRef] [PubMed]
- Pavlova, M.K.; Lee, J.W.; Yilmaz, F.; Dworetzky, B.A. Diurnal pattern of seizures outside the hospital: Is there a time of circadian vulnerability? Neurology 2012, 78, 1488–1492. [Google Scholar] [CrossRef] [PubMed]
- Guilhoto, L.M.; Loddenkemper, T.; Vendrame, M.; Bergin, A.; Bourgeois, B.F.; Kothare, S.V. Higher evening antiepileptic drug dose for nocturnal and early-morning seizures. Epilepsy Behav. 2011, 20, 334–337. [Google Scholar] [CrossRef]
- Gowers, W.R. Epilepsy and Other Chronic Convulsive Disease; William Wood & Company:: London, UK, 1885; Volume 1. [Google Scholar]
- Minecan, D.; Natarajan, A.; Marzec, M.; Malow, B. Relationship of epileptic seizures to sleep stage and sleep depth. Sleep 2002, 25, 899–904. [Google Scholar] [CrossRef] [Green Version]
- Roulet Perez, E.; Davidoff, V.; Despland, P.A.; Deonna, T. Mental and behavioural deterioration of children with epilepsy and CSWS: Acquired epileptic frontal syndrome. Dev. Med. Child. Neurol. 1993, 35, 661–674. [Google Scholar] [CrossRef] [PubMed]
- Galanopoulou, A.S.; Bojko, A.; Lado, F.; Moshé, S.L. The spectrum of neuropsychiatric abnormalities associated with electrical status epilepticus in sleep. Brain Dev. 2000, 22, 279–295. [Google Scholar] [CrossRef]
- Carreño, M.; Fernández, S. Sleep-Related Epilepsy. Curr. Treat Options Neurol. 2016, 18, 23. [Google Scholar] [CrossRef] [PubMed]
- Janz, D. Epilepsy with grand mal on awakening and sleep-waking cycle. Clin. Neurophysiol. 2000, 111 (Suppl. S2), S103–S110. [Google Scholar] [CrossRef]
- Billiard, M.; Besset, A.; Passouant, P. The place of sleep disorder centers in the evaluation and treatment of chronic insomniacs. Int. J. Neurol. 1981, 15, 56–61. [Google Scholar]
- Rodriguez, I.; Niedermeyer, E. The aphasia-epilepsy syndrome in children: Electroencephalographic aspects. Clin. Electroencephalogr. 1982, 13, 23–35. [Google Scholar] [CrossRef]
- Halassa, M.M.; Florian, C.; Fellin, T.; Munoz, J.R.; Lee, S.Y.; Abel, T.; Haydon, P.G.; Frank, M.G. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 2009, 61, 213–219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nadjar, A.; Blutstein, T.; Aubert, A.; Laye, S.; Haydon, P.G. Astrocyte-derived adenosine modulates increased sleep pressure during inflammatory response. Glia 2013, 61, 724–731. [Google Scholar] [CrossRef] [PubMed]
- Krueger, J.M.; Nguyen, J.T.; Dykstra-Aiello, C.J.; Taishi, P. Local sleep. Sleep Med. Rev. 2019, 43, 14–21. [Google Scholar] [CrossRef]
- Garofalo, S.; Picard, K.; Limatola, C.; Nadjar, A.; Pascual, O.; Tremblay, M.E. Role of Glia in the Regulation of Sleep in Health and Disease. Compr. Physiol. 2020, 10, 687–712. [Google Scholar] [CrossRef] [PubMed]
- Deurveilher, S.; Golovin, T.; Hall, S.; Semba, K. Microglia dynamics in sleep/wake states and in response to sleep loss. Neurochem. Int. 2021, 143, 104944. [Google Scholar] [CrossRef] [PubMed]
- Ingiosi, A.M.; Opp, M.R.; Krueger, J.M. Sleep and immune function: Glial contributions and consequences of aging. Curr. Opin. Neurobiol. 2013, 23, 806–811. [Google Scholar] [CrossRef] [Green Version]
- Besedovsky, L.; Lange, T.; Haack, M. The Sleep-Immune Crosstalk in Health and Disease. Physiol. Rev. 2019, 99, 1325–1380. [Google Scholar] [CrossRef] [Green Version]
- Krueger, J.M.; Majde, J.A.; Rector, D.M. Cytokines in immune function and sleep regulation. Handb. Clin. Neurol. 2011, 98, 229–240. [Google Scholar] [CrossRef] [Green Version]
- Breder, C.D.; Dinarello, C.A.; Saper, C.B. Interleukin-1 immunoreactive innervation of the human hypothalamus. Science 1988, 240, 321–324. [Google Scholar] [CrossRef]
- Breder, C.D.; Tsujimoto, M.; Terano, Y.; Scott, D.W.; Saper, C.B. Distribution and characterization of tumor necrosis factor-alpha-like immunoreactivity in the murine central nervous system. J. Comp. Neurol. 1993, 337, 543–567. [Google Scholar] [CrossRef]
- Krueger, J.M.; Walter, J.; Dinarello, C.A.; Wolff, S.M.; Chedid, L. Sleep-promoting effects of endogenous pyrogen (interleukin-1). Am. J. Physiol. 1984, 246, R994–R999. [Google Scholar] [CrossRef] [Green Version]
- Shoham, S.; Davenne, D.; Cady, A.B.; Dinarello, C.A.; Krueger, J.M. Recombinant tumor necrosis factor and interleukin 1 enhance slow-wave sleep. Am. J. Physiol. 1987, 253, R142–R149. [Google Scholar] [CrossRef] [PubMed]
- Imeri, L.; Bianchi, S.; Opp, M.R. Inhibition of caspase-1 in rat brain reduces spontaneous nonrapid eye movement sleep and nonrapid eye movement sleep enhancement induced by lipopolysaccharide. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291, R197–R204. [Google Scholar] [CrossRef] [Green Version]
- Kushikata, T.; Fang, J.; Krueger, J.M. Interleukin-10 inhibits spontaneous sleep in rabbits. J. Interferon Cytokine Res. 1999, 19, 1025–1030. [Google Scholar] [CrossRef] [PubMed]
- Sawada, M.; Suzumura, A.; Hosoya, H.; Marunouchi, T.; Nagatsu, T. Interleukin-10 inhibits both production of cytokines and expression of cytokine receptors in microglia. J. Neurochem. 1999, 72, 1466–1471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bluthe, R.M.; Kelley, K.W.; Dantzer, R. Effects of insulin-like growth factor-I on cytokine-induced sickness behavior in mice. Brain Behav. Immun. 2006, 20, 57–63. [Google Scholar] [CrossRef] [Green Version]
- Tay, T.L.; Savage, J.C.; Hui, C.W.; Bisht, K.; Tremblay, M.E. Microglia across the lifespan: From origin to function in brain development, plasticity and cognition. J. Physiol. 2017, 595, 1929–1945. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolf, S.A.; Boddeke, H.W.; Kettenmann, H. Microglia in Physiology and Disease. Annu. Rev. Physiol. 2017, 79, 619–643. [Google Scholar] [CrossRef] [PubMed]
- He, J.; Hsuchou, H.; He, Y.; Kastin, A.J.; Wang, Y.; Pan, W. Sleep restriction impairs blood-brain barrier function. J. Neurosci. 2014, 34, 14697–14706. [Google Scholar] [CrossRef] [Green Version]
- Xanthos, D.N.; Sandkuhler, J. Neurogenic neuroinflammation: Inflammatory CNS reactions in response to neuronal activity. Nat. Rev. Neurosci. 2014, 15, 43–53. [Google Scholar] [CrossRef]
- Mullington, J.M.; Simpson, N.S.; Meier-Ewert, H.K.; Haack, M. Sleep loss and inflammation. Best Pract. Res. Clin. Endocrinol. Metab. 2010, 24, 775–784. [Google Scholar] [CrossRef] [Green Version]
- Hurtado-Alvarado, G.; Pavon, L.; Castillo-Garcia, S.A.; Hernandez, M.E.; Dominguez-Salazar, E.; Velazquez-Moctezuma, J.; Gomez-Gonzalez, B. Sleep loss as a factor to induce cellular and molecular inflammatory variations. Clin. Dev. Immunol. 2013, 2013, 801341. [Google Scholar] [CrossRef]
- Hurtado-Alvarado, G.; Dominguez-Salazar, E.; Pavon, L.; Velazquez-Moctezuma, J.; Gomez-Gonzalez, B. Blood-Brain Barrier Disruption Induced by Chronic Sleep Loss: Low-Grade Inflammation May Be the Link. J. Immunol. Res. 2016, 2016, 4576012. [Google Scholar] [CrossRef] [Green Version]
- Armulik, A.; Genove, G.; Mae, M.; Nisancioglu, M.H.; Wallgard, E.; Niaudet, C.; He, L.; Norlin, J.; Lindblom, P.; Strittmatter, K.; et al. Pericytes regulate the blood-brain barrier. Nature 2010, 468, 557–561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Medina-Flores, F.; Hurtado-Alvarado, G.; Contis-Montes de Oca, A.; Lopez-Cervantes, S.P.; Konigsberg, M.; Deli, M.A.; Gomez-Gonzalez, B. Sleep loss disrupts pericyte-brain endothelial cell interactions impairing blood-brain barrier function. Brain Behav. Immun. 2020, 89, 118–132. [Google Scholar] [CrossRef]
- Ye, S.M.; Johnson, R.W. An age-related decline in interleukin-10 may contribute to the increased expression of interleukin-6 in brain of aged mice. Neuroimmunomodulation 2001, 9, 183–192. [Google Scholar] [CrossRef]
- Vishwas, D.K.; Mukherjee, A.; Haldar, C.; Dash, D.; Nayak, M.K. Improvement of oxidative stress and immunity by melatonin: An age dependent study in golden hamster. Exp. Gerontol. 2013, 48, 168–182. [Google Scholar] [CrossRef] [PubMed]
- Everson, C.A.; Toth, L.A. Systemic bacterial invasion induced by sleep deprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 278, R905–R916. [Google Scholar] [CrossRef] [PubMed]
- Aho, V.; Ollila, H.M.; Rantanen, V.; Kronholm, E.; Surakka, I.; van Leeuwen, W.M.; Lehto, M.; Matikainen, S.; Ripatti, S.; Harma, M.; et al. Partial sleep restriction activates immune response-related gene expression pathways: Experimental and epidemiological studies in humans. PLoS ONE 2013, 8, e77184. [Google Scholar] [CrossRef]
- Okun, M.L.; Giese, S.; Lin, L.; Einen, M.; Mignot, E.; Coussons-Read, M.E. Exploring the cytokine and endocrine involvement in narcolepsy. Brain Behav. Immun. 2004, 18, 326–332. [Google Scholar] [CrossRef]
- Tanaka, S.; Honda, M.; Toyoda, H.; Kodama, T. Increased plasma IL-6, IL-8, TNF-alpha, and G-CSF in Japanese narcolepsy. Hum. Immunol. 2014, 75, 940–944. [Google Scholar] [CrossRef]
- Mignot, E.; Tafti, M.; Dement, W.C.; Grumet, F.C. Narcolepsy and immunity. Adv. Neuroimmunol. 1995, 5, 23–37. [Google Scholar] [CrossRef]
- Partinen, M.; Kornum, B.R.; Plazzi, G.; Jennum, P.; Julkunen, I.; Vaarala, O. Narcolepsy as an autoimmune disease: The role of H1N1 infection and vaccination. Lancet Neurol. 2014, 13, 600–613. [Google Scholar] [CrossRef]
- Gerashchenko, D.; Shiromani, P.J. Different neuronal phenotypes in the lateral hypothalamus and their role in sleep and wakefulness. Mol. Neurobiol. 2004, 29, 41–59. [Google Scholar] [CrossRef]
- Zee, P.C.; Turek, F.W. Sleep and health: Everywhere and in both directions. Arch. Intern. Med. 2006, 166, 1686–1688. [Google Scholar] [CrossRef] [PubMed]
- Almeida, C.M.; Malheiro, A. Sleep, immunity and shift workers: A review. Sleep Sci 2016, 9, 164–168. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakano, Y.; Miura, T.; Hara, I.; Aono, H.; Miyano, N.; Miyajima, K.; Tabuchi, T.; Kosaka, H. The effect of shift work on cellular immune function. J. Hum. Ergol. 1982, 11, 131–137. [Google Scholar]
- Mohren, D.C.; Jansen, N.W.; Kant, I.J.; Galama, J.; van den Brandt, P.A.; Swaen, G.M. Prevalence of common infections among employees in different work schedules. J. Occup. Environ. Med. 2002, 44, 1003–1011. [Google Scholar] [CrossRef] [Green Version]
- Nagai, M.; Morikawa, Y.; Kitaoka, K.; Nakamura, K.; Sakurai, M.; Nishijo, M.; Hamazaki, Y.; Maruzeni, S.; Nakagawa, H. Effects of fatigue on immune function in nurses performing shift work. J. Occup. Health. 2011, 53, 312–319. [Google Scholar] [CrossRef]
- van Mark, A.; Weiler, S.W.; Schroder, M.; Otto, A.; Jauch-Chara, K.; Groneberg, D.A.; Spallek, M.; Kessel, R.; Kalsdorf, B. The impact of shift work induced chronic circadian disruption on IL-6 and TNF-alpha immune responses. J. Occup. Med. Toxicol. 2010, 5, 18. [Google Scholar] [CrossRef] [Green Version]
- Copertaro, A.; Bracci, M.; Gesuita, R.; Carle, F.; Amati, M.; Baldassari, M.; Mocchegiani, E.; Santarelli, L. Influence of shift-work on selected immune variables in nurses. Ind. Health 2011, 49, 597–604. [Google Scholar] [CrossRef] [Green Version]
- Dinges, D.F.; Douglas, S.D.; Zaugg, L.; Campbell, D.E.; McMann, J.M.; Whitehouse, W.G.; Orne, E.C.; Kapoor, S.C.; Icaza, E.; Orne, M.T. Leukocytosis and natural killer cell function parallel neurobehavioral fatigue induced by 64 hours of sleep deprivation. J. Clin. Investig. 1994, 93, 1930–1939. [Google Scholar] [CrossRef]
- Dinges, D.F.; Douglas, S.D.; Hamarman, S.; Zaugg, L.; Kapoor, S. Sleep deprivation and human immune function. Adv. Neuroimmunol. 1995, 5, 97–110. [Google Scholar] [CrossRef]
- Wilder-Smith, A.; Mustafa, F.B.; Earnest, A.; Gen, L.; Macary, P.A. Impact of partial sleep deprivation on immune markers. Sleep Med. 2013, 14, 1031–1034. [Google Scholar] [CrossRef]
- Irwin, M.; Mascovich, A.; Gillin, J.C.; Willoughby, R.; Pike, J.; Smith, T.L. Partial sleep deprivation reduces natural killer cell activity in humans. Psychosom. Med. 1994, 56, 493–498. [Google Scholar] [CrossRef] [PubMed]
- Axelsson, J.; Rehman, J.U.; Akerstedt, T.; Ekman, R.; Miller, G.E.; Hoglund, C.O.; Lekander, M. Effects of sustained sleep restriction on mitogen-stimulated cytokines, chemokines and T helper 1/ T helper 2 balance in humans. PLoS ONE 2013, 8, e82291. [Google Scholar] [CrossRef]
- Irwin, M.; McClintick, J.; Costlow, C.; Fortner, M.; White, J.; Gillin, J.C. Partial night sleep deprivation reduces natural killer and cellular immune responses in humans. FASEB J. 1996, 10, 643–653. [Google Scholar] [CrossRef] [PubMed]
- Fondell, E.; Axelsson, J.; Franck, K.; Ploner, A.; Lekander, M.; Balter, K.; Gaines, H. Short natural sleep is associated with higher T cell and lower NK cell activities. Brain Behav. Immun. 2011, 25, 1367–1375. [Google Scholar] [CrossRef]
- Biron, C.A. Initial and innate responses to viral infections--pattern setting in immunity or disease. Curr. Opin. Microbiol. 1999, 2, 374–381. [Google Scholar] [CrossRef]
- Biron, C.A.; Nguyen, K.B.; Pien, G.C.; Cousens, L.P.; Salazar-Mather, T.P. Natural killer cells in antiviral defense: Function and regulation by innate cytokines. Annu. Rev. Immunol. 1999, 17, 189–220. [Google Scholar] [CrossRef] [PubMed]
- Imai, K.; Matsuyama, S.; Miyake, S.; Suga, K.; Nakachi, K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: An 11-year follow-up study of a general population. Lancet 2000, 356, 1795–1799. [Google Scholar] [CrossRef]
- Irwin, M.R.; Olmstead, R.; Carroll, J.E. Sleep Disturbance, Sleep Duration, and Inflammation: A Systematic Review and Meta-Analysis of Cohort Studies and Experimental Sleep Deprivation. Biol. Psychiatry 2016, 80, 40–52. [Google Scholar] [CrossRef] [Green Version]
- Irwin, M.R.; Opp, M.R. Sleep Health: Reciprocal Regulation of Sleep and Innate Immunity. Neuropsychopharmacology 2017, 42, 129–155. [Google Scholar] [CrossRef] [Green Version]
- Irwin, M.R.; Witarama, T.; Caudill, M.; Olmstead, R.; Breen, E.C. Sleep loss activates cellular inflammation and signal transducer and activator of transcription (STAT) family proteins in humans. Brain Behav. Immun. 2015, 47, 86–92. [Google Scholar] [CrossRef] [Green Version]
- Irwin, M.R.; Wang, M.; Ribeiro, D.; Cho, H.J.; Olmstead, R.; Breen, E.C.; Martinez-Maza, O.; Cole, S. Sleep loss activates cellular inflammatory signaling. Biol. Psychiatry 2008, 64, 538–540. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maiti, P.; Singh, S.B.; Sharma, A.K.; Muthuraju, S.; Banerjee, P.K.; Ilavazhagan, G. Hypobaric hypoxia induces oxidative stress in rat brain. Neurochem. Int. 2006, 49, 709–716. [Google Scholar] [CrossRef]
- Sha, S.; Tan, J.; Miao, Y.; Zhang, Q. The Role of Autophagy in Hypoxia-Induced Neuroinflammation. DNA Cell Biol. 2021, 40, 733–739. [Google Scholar] [CrossRef] [PubMed]
- Li, R.C.; Row, B.W.; Gozal, E.; Kheirandish, L.; Fan, Q.; Brittian, K.R.; Guo, S.Z.; Sachleben, L.R., Jr.; Gozal, D. Cyclooxygenase 2 and intermittent hypoxia-induced spatial deficits in the rat. Am. J. Respir. Crit. Care Med. 2003, 168, 469–475. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhan, G.; Serrano, F.; Fenik, P.; Hsu, R.; Kong, L.; Pratico, D.; Klann, E.; Veasey, S.C. NADPH oxidase mediates hypersomnolence and brain oxidative injury in a murine model of sleep apnea. Am. J. Respir. Crit. Care Med. 2005, 172, 921–929. [Google Scholar] [CrossRef] [Green Version]
- Aviles-Reyes, R.X.; Angelo, M.F.; Villarreal, A.; Rios, H.; Lazarowski, A.; Ramos, A.J. Intermittent hypoxia during sleep induces reactive gliosis and limited neuronal death in rats: Implications for sleep apnea. J. Neurochem. 2010, 112, 854–869. [Google Scholar] [CrossRef]
- Sapin, E.; Peyron, C.; Roche, F.; Gay, N.; Carcenac, C.; Savasta, M.; Levy, P.; Dematteis, M. Chronic Intermittent Hypoxia Induces Chronic Low-Grade Neuroinflammation in the Dorsal Hippocampus of Mice. Sleep 2015, 38, 1537–1546. [Google Scholar] [CrossRef]
- Nzou, G.; Wicks, R.T.; VanOstrand, N.R.; Mekky, G.A.; Seale, S.A.; El-Taibany, A.; Wicks, E.E.; Nechtman, C.M.; Marrotte, E.J.; Makani, V.S.; et al. Author Correction: Multicellular 3D Neurovascular Unit Model for Assessing Hypoxia and Neuroinflammation Induced Blood-Brain Barrier Dysfunction. Sci. Rep. 2020, 10, 20384. [Google Scholar] [CrossRef]
- Banks, W.A. Anorectic effects of circulating cytokines: Role of the vascular blood-brain barrier. Nutrition 2001, 17, 434–437. [Google Scholar] [CrossRef]
- Xiong, X.Y.; Liu, L.; Yang, Q.W. Functions and mechanisms of microglia/macrophages in neuroinflammation and neurogenesis after stroke. Prog. Neurobiol. 2016, 142, 23–44. [Google Scholar] [CrossRef] [PubMed]
- Kenneth, N.S.; Rocha, S. Regulation of gene expression by hypoxia. Biochem. J. 2008, 414, 19–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, D.Y.; Liou, H.C.; Tang, C.H.; Fu, W.M. Hypoxia-induced iNOS expression in microglia is regulated by the PI3-kinase/Akt/mTOR signaling pathway and activation of hypoxia inducible factor-1alpha. Biochem. Pharmacol. 2006, 72, 992–1000. [Google Scholar] [CrossRef]
- Cummins, E.P.; Berra, E.; Comerford, K.M.; Ginouves, A.; Fitzgerald, K.T.; Seeballuck, F.; Godson, C.; Nielsen, J.E.; Moynagh, P.; Pouyssegur, J.; et al. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc. Natl. Acad. Sci. USA 2006, 103, 18154–18159. [Google Scholar] [CrossRef] [Green Version]
- Shin, D.H.; Li, S.H.; Yang, S.W.; Lee, B.L.; Lee, M.K.; Park, J.W. Inhibitor of nuclear factor-kappaB alpha derepresses hypoxia-inducible factor-1 during moderate hypoxia by sequestering factor inhibiting hypoxia-inducible factor from hypoxia-inducible factor 1alpha. FEBS J. 2009, 276, 3470–3480. [Google Scholar] [CrossRef]
- van Uden, P.; Kenneth, N.S.; Webster, R.; Muller, H.A.; Mudie, S.; Rocha, S. Evolutionary conserved regulation of HIF-1beta by NF-kappaB. PLoS Genet. 2011, 7, e1001285. [Google Scholar] [CrossRef] [Green Version]
- Butturini, E.; Boriero, D.; Carcereri de Prati, A.; Mariotto, S. STAT1 drives M1 microglia activation and neuroinflammation under hypoxia. Arch. Biochem. Biophys. 2019, 669, 22–30. [Google Scholar] [CrossRef]
- Chen, S.; Ye, J.; Chen, X.; Shi, J.; Wu, W.; Lin, W.; Lin, W.; Li, Y.; Fu, H.; Li, S. Valproic acid attenuates traumatic spinal cord injury-induced inflammation via STAT1 and NF-kappaB pathway dependent of HDAC3. J. Neuroinflammation 2018, 15, 150. [Google Scholar] [CrossRef]
- He, Y.; Hara, H.; Nunez, G. Mechanism and Regulation of NLRP3 Inflammasome Activation. Trends Biochem. Sci. 2016, 41, 1012–1021. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Voet, S.; Srinivasan, S.; Lamkanfi, M.; van Loo, G. Inflammasomes in neuroinflammatory and neurodegenerative diseases. EMBO Mol. Med. 2019, 11. [Google Scholar] [CrossRef] [PubMed]
- Mao, Z.; Liu, C.; Ji, S.; Yang, Q.; Ye, H.; Han, H.; Xue, Z. The NLRP3 Inflammasome is Involved in the Pathogenesis of Parkinson′s Disease in Rats. Neurochem. Res. 2017, 42, 1104–1115. [Google Scholar] [CrossRef]
- Wu, X.; Gong, L.; Xie, L.; Gu, W.; Wang, X.; Liu, Z.; Li, S. NLRP3 Deficiency Protects Against Intermittent Hypoxia-Induced Neuroinflammation and Mitochondrial ROS by Promoting the PINK1-Parkin Pathway of Mitophagy in a Murine Model of Sleep Apnea. Front. Immunol. 2021, 12, 628168. [Google Scholar] [CrossRef]
- Vezzani, A.; Granata, T. Brain inflammation in epilepsy: Experimental and clinical evidence. Epilepsia 2005, 46, 1724–1743. [Google Scholar] [CrossRef] [PubMed]
- Vezzani, A.; Dingledine, R.; Rossetti, A.O. Immunity and inflammation in status epilepticus and its sequelae: Possibilities for therapeutic application. Expert. Rev. Neurother. 2015, 15, 1081–1092. [Google Scholar] [CrossRef] [Green Version]
- Vezzani, A.; Balosso, S.; Ravizza, T. Neuroinflammatory pathways as treatment targets and biomarkers in epilepsy. Nat. Rev. Neurol. 2019, 15, 459–472. [Google Scholar] [CrossRef] [PubMed]
- Vezzani, A.; French, J.; Bartfai, T.; Baram, T.Z. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2011, 7, 31–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marchi, N.; Granata, T.; Janigro, D. Inflammatory pathways of seizure disorders. Trends Neurosci. 2014, 37, 55–65. [Google Scholar] [CrossRef] [Green Version]
- Rana, A.; Musto, A.E. The role of inflammation in the development of epilepsy. J. Neuroinflammation 2018, 15, 144. [Google Scholar] [CrossRef]
- Levesque, M.; Biagini, G.; de Curtis, M.; Gnatkovsky, V.; Pitsch, J.; Wang, S.; Avoli, M. The pilocarpine model of mesial temporal lobe epilepsy: Over one decade later, with more rodent species and new investigative approaches. Neurosci. Biobehav. Rev. 2021, 130, 274–291. [Google Scholar] [CrossRef]
- Dey, A.; Kang, X.; Qiu, J.; Du, Y.; Jiang, J. Anti-Inflammatory Small Molecules To Treat Seizures and Epilepsy: From Bench to Bedside. Trends Pharmacol. Sci. 2016, 37, 463–484. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.; Wang, D.; Guo, D. Interictal cytokine levels were correlated to seizure severity of epileptic patients: A retrospective study on 1218 epileptic patients. J. Transl. Med. 2015, 13, 378. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alvim, M.K.M.; Morita-Sherman, M.E.; Yasuda, C.L.; Rocha, N.P.; Vieira, E.L.; Pimentel-Silva, L.R.; Henrique Nogueira, M.; Barbosa, R.; Watanabe, N.; Coan, A.C.; et al. Inflammatory and neurotrophic factor plasma levels are related to epilepsy independently of etiology. Epilepsia 2021, 62, 2385–2394. [Google Scholar] [CrossRef] [PubMed]
- Zhong, R.; Chen, Q.; Li, M.; Zhang, X.; Lin, W. Elevated Blood C-Reactive Protein Levels in Patients With Epilepsy: A Systematic Review and Meta-Analysis. Front. Neurol. 2019, 10, 974. [Google Scholar] [CrossRef]
- Holtman, L.; van Vliet, E.A.; Aronica, E.; Wouters, D.; Wadman, W.J.; Gorter, J.A. Blood plasma inflammation markers during epileptogenesis in post-status epilepticus rat model for temporal lobe epilepsy. Epilepsia 2013, 54, 589–595. [Google Scholar] [CrossRef]
- Gouveia, T.L.; Vieira de Sousa, P.V.; de Almeida, S.S.; Nejm, M.B.; Vieira de Brito, J.M.; Cysneiros, R.M.; de Brito, M.V.; Salu, B.R.; Oliva, M.L.; Scorza, F.A.; et al. High serum levels of proinflammatory markers during epileptogenesis. Can omega-3 fatty acid administration reduce this process? Epilepsy Behav. 2015, 51, 300–305. [Google Scholar] [CrossRef] [Green Version]
- Riazi, K.; Galic, M.A.; Kuzmiski, J.B.; Ho, W.; Sharkey, K.A.; Pittman, Q.J. Microglial activation and TNFalpha production mediate altered CNS excitability following peripheral inflammation. Proc. Natl. Acad. Sci. USA 2008, 105, 17151–17156. [Google Scholar] [CrossRef] [Green Version]
- De Caro, C.; Leo, A.; Nesci, V.; Ghelardini, C.; di Cesare Mannelli, L.; Striano, P.; Avagliano, C.; Calignano, A.; Mainardi, P.; Constanti, A.; et al. Intestinal inflammation increases convulsant activity and reduces antiepileptic drug efficacy in a mouse model of epilepsy. Sci. Rep. 2019, 9, 13983. [Google Scholar] [CrossRef] [Green Version]
- Ho, Y.H.; Lin, Y.T.; Wu, C.W.; Chao, Y.M.; Chang, A.Y.; Chan, J.Y. Peripheral inflammation increases seizure susceptibility via the induction of neuroinflammation and oxidative stress in the hippocampus. J. Biomed. Sci. 2015, 22, 46. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, J.; Min, H.J.; Shin, J.S. Increased levels of HMGB1 and pro-inflammatory cytokines in children with febrile seizures. J. Neuroinflammation 2011, 8, 135. [Google Scholar] [CrossRef] [Green Version]
- Shi, Y.; Zhang, L.; Teng, J.; Miao, W. HMGB1 mediates microglia activation via the TLR4/NF-kappaB pathway in coriaria lactone induced epilepsy. Mol. Med. Rep. 2018, 17, 5125–5131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kan, M.; Song, L.; Zhang, X.; Zhang, J.; Fang, P. Circulating high mobility group box-1 and toll-like receptor 4 expressions increase the risk and severity of epilepsy. Braz. J. Med. Biol. Res. 2019, 52, e7374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, N.; Liu, H.; Ma, B.; Zhao, T.; Chen, Y.; Yang, Y.; Zhao, P.; Han, X. CSF high-mobility group box 1 is associated with drug-resistance and symptomatic etiology in adult patients with epilepsy. Epilepsy Res. 2021, 177, 106767. [Google Scholar] [CrossRef] [PubMed]
- Walker, L.E.; Frigerio, F.; Ravizza, T.; Ricci, E.; Tse, K.; Jenkins, R.E.; Sills, G.J.; Jorgensen, A.; Porcu, L.; Thippeswamy, T.; et al. Molecular isoforms of high-mobility group box 1 are mechanistic biomarkers for epilepsy. J. Clin. Investig. 2017, 127, 2118–2132. [Google Scholar] [CrossRef] [Green Version]
- Fu, L.; Liu, K.; Wake, H.; Teshigawara, K.; Yoshino, T.; Takahashi, H.; Mori, S.; Nishibori, M. Therapeutic effects of anti-HMGB1 monoclonal antibody on pilocarpine-induced status epilepticus in mice. Sci. Rep. 2017, 7, 1179. [Google Scholar] [CrossRef] [Green Version]
- Li, G.; Bauer, S.; Nowak, M.; Norwood, B.; Tackenberg, B.; Rosenow, F.; Knake, S.; Oertel, W.H.; Hamer, H.M. Cytokines and epilepsy. Seizure 2011, 20, 249–256. [Google Scholar] [CrossRef] [Green Version]
- Vezzani, A.; Baram, T.Z. New roles for interleukin-1 Beta in the mechanisms of epilepsy. Epilepsy Curr. 2007, 7, 45–50. [Google Scholar] [CrossRef] [Green Version]
- Iori, V.; Frigerio, F.; Vezzani, A. Modulation of neuronal excitability by immune mediators in epilepsy. Curr. Opin. Pharmacol. 2016, 26, 118–123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dai, S.; Zheng, Y.; Wang, T.; Chen, Z. HMGB1, neuronal excitability and epilepsy. Acta Epileptol. 2021, 3, 13. [Google Scholar] [CrossRef]
- Leal, B.; Chaves, J.; Carvalho, C.; Rangel, R.; Santos, A.; Bettencourt, A.; Lopes, J.; Ramalheira, J.; Silva, B.M.; da Silva, A.M.; et al. Brain expression of inflammatory mediators in Mesial Temporal Lobe Epilepsy patients. J. Neuroimmunol. 2017, 313, 82–88. [Google Scholar] [CrossRef]
- Jiang, J.; Yang, M.S.; Quan, Y.; Gueorguieva, P.; Ganesh, T.; Dingledine, R. Therapeutic window for cyclooxygenase-2 related anti-inflammatory therapy after status epilepticus. Neurobiol. Dis. 2015, 76, 126–136. [Google Scholar] [CrossRef] [Green Version]
- Minghetti, L. Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. J. Neuropathol. Exp. Neurol. 2004, 63, 901–910. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rojas, A.; Chen, D.; Ganesh, T.; Varvel, N.H.; Dingledine, R. The COX-2/prostanoid signaling cascades in seizure disorders. Expert Opin. Ther. Targets 2019, 23, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Serrano, G.E.; Lelutiu, N.; Rojas, A.; Cochi, S.; Shaw, R.; Makinson, C.D.; Wang, D.; FitzGerald, G.A.; Dingledine, R. Ablation of cyclooxygenase-2 in forebrain neurons is neuroprotective and dampens brain inflammation after status epilepticus. J. Neurosci. 2011, 31, 14850–14860. [Google Scholar] [CrossRef]
- Rawat, C.; Kukal, S.; Dahiya, U.R.; Kukreti, R. Cyclooxygenase-2 (COX-2) inhibitors: Future therapeutic strategies for epilepsy management. J. Neuroinflammation 2019, 16, 197. [Google Scholar] [CrossRef] [Green Version]
- Rojas, A.; Jiang, J.; Ganesh, T.; Yang, M.S.; Lelutiu, N.; Gueorguieva, P.; Dingledine, R. Cyclooxygenase-2 in epilepsy. Epilepsia 2014, 55, 17–25. [Google Scholar] [CrossRef] [PubMed]
- Radu, B.M.; Epureanu, F.B.; Radu, M.; Fabene, P.F.; Bertini, G. Nonsteroidal anti-inflammatory drugs in clinical and experimental epilepsy. Epilepsy Res. 2017, 131, 15–27. [Google Scholar] [CrossRef]
- Jiang, J.; Quan, Y.; Ganesh, T.; Pouliot, W.A.; Dudek, F.E.; Dingledine, R. Inhibition of the prostaglandin receptor EP2 following status epilepticus reduces delayed mortality and brain inflammation. Proc. Natl. Acad. Sci. USA 2013, 110, 3591–3596. [Google Scholar] [CrossRef] [Green Version]
- Rojas, A.; Ganesh, T.; Manji, Z.; O’Neill, T.; Dingledine, R. Inhibition of the prostaglandin E2 receptor EP2 prevents status epilepticus-induced deficits in the novel object recognition task in rats. Neuropharmacology 2016, 110, 419–430. [Google Scholar] [CrossRef] [Green Version]
- Rojas, A.; Ganesh, T.; Lelutiu, N.; Gueorguieva, P.; Dingledine, R. Inhibition of the prostaglandin EP2 receptor is neuroprotective and accelerates functional recovery in a rat model of organophosphorus induced status epilepticus. Neuropharmacology 2015, 93, 15–27. [Google Scholar] [CrossRef] [Green Version]
- Rojas, A.; Amaradhi, R.; Banik, A.; Jiang, C.; Abreu-Melon, J.; Wang, S.; Dingledine, R.; Ganesh, T. A Novel Second-Generation EP2 Receptor Antagonist Reduces Neuroinflammation and Gliosis After Status Epilepticus in Rats. Neurotherapeutics 2021, 18, 1207–1225. [Google Scholar] [CrossRef]
- Sanz, P.; Garcia-Gimeno, M.A. Reactive Glia Inflammatory Signaling Pathways and Epilepsy. Int. J. Mol. Sci. 2020, 21. [Google Scholar] [CrossRef]
- Schartz, N.D.; Herr, S.A.; Madsen, L.; Butts, S.J.; Torres, C.; Mendez, L.B.; Brewster, A.L. Spatiotemporal profile of Map2 and microglial changes in the hippocampal CA1 region following pilocarpine-induced status epilepticus. Sci. Rep. 2016, 6, 24988. [Google Scholar] [CrossRef] [Green Version]
- Wyatt-Johnson, S.K.; Herr, S.A.; Brewster, A.L. Status Epilepticus Triggers Time-Dependent Alterations in Microglia Abundance and Morphological Phenotypes in the Hippocampus. Front. Neurol 2017, 8, 700. [Google Scholar] [CrossRef] [Green Version]
- Sano, F.; Shigetomi, E.; Shinozaki, Y.; Tsuzukiyama, H.; Saito, K.; Mikoshiba, K.; Horiuchi, H.; Cheung, D.L.; Nabekura, J.; Sugita, K.; et al. Reactive astrocyte-driven epileptogenesis is induced by microglia initially activated following status epilepticus. JCI Insight 2021, 6. [Google Scholar] [CrossRef]
- Morin-Brureau, M.; Milior, G.; Royer, J.; Chali, F.; Le Duigou, C.; Savary, E.; Blugeon, C.; Jourdren, L.; Akbar, D.; Dupont, S.; et al. Microglial phenotypes in the human epileptic temporal lobe. Brain 2018, 141, 3343–3360. [Google Scholar] [CrossRef]
- Altmann, A.; Ryten, M.; Di Nunzio, M.; Ravizza, T.; Tolomeo, D.; Reynolds, R.H.; Somani, A.; Bacigaluppi, M.; Iori, V.; Micotti, E.; et al. A systems-level analysis highlights microglial activation as a modifying factor in common epilepsies. Neuropathol. Appl. Neurobiol. 2021. [Google Scholar] [CrossRef]
- Wetherington, J.; Serrano, G.; Dingledine, R. Astrocytes in the epileptic brain. Neuron 2008, 58, 168–178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aronica, E.; Ravizza, T.; Zurolo, E.; Vezzani, A. Astrocyte immune responses in epilepsy. Glia 2012, 60, 1258–1268. [Google Scholar] [CrossRef] [PubMed]
- Devinsky, O.; Vezzani, A.; Najjar, S.; De Lanerolle, N.C.; Rogawski, M.A. Glia and epilepsy: Excitability and inflammation. Trends Neurosci. 2013, 36, 174–184. [Google Scholar] [CrossRef]
- Barker-Haliski, M.; White, H.S. Glutamatergic Mechanisms Associated with Seizures and Epilepsy. Cold Spring Harb. Perspect. Med. 2015, 5, a022863. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kinoshita, S.; Koyama, R. Pro-and anti-epileptic roles of microglia. Neural. Regen. Res. 2021, 16, 1369–1371. [Google Scholar] [CrossRef]
- Wu, W.; Li, Y.; Wei, Y.; Bosco, D.B.; Xie, M.; Zhao, M.G.; Richardson, J.R.; Wu, L.J. Microglial depletion aggravates the severity of acute and chronic seizures in mice. Brain Behav. Immun. 2020, 89, 245–255. [Google Scholar] [CrossRef]
- Di Nunzio, M.; Di Sapia, R.; Sorrentino, D.; Kebede, V.; Cerovic, M.; Gullotta, G.S.; Bacigaluppi, M.; Audinat, E.; Marchi, N.; Ravizza, T.; et al. Microglia proliferation plays distinct roles in acquired epilepsy depending on disease stages. Epilepsia 2021, 62, 1931–1945. [Google Scholar] [CrossRef]
- Zhao, X.F.; Liao, Y.; Alam, M.M.; Mathur, R.; Feustel, P.; Mazurkiewicz, J.E.; Adamo, M.A.; Zhu, X.C.; Huang, Y. Microglial mTOR is Neuronal Protective and Antiepileptogenic in the Pilocarpine Model of Temporal Lobe Epilepsy. J. Neurosci. 2020, 40, 7593–7608. [Google Scholar] [CrossRef] [PubMed]
- Alam, M.M.; Zhao, X.F.; Liao, Y.; Mathur, R.; McCallum, S.E.; Mazurkiewicz, J.E.; Adamo, M.A.; Feustel, P.; Belin, S.; Poitelon, Y.; et al. Deficiency of Microglial Autophagy Increases the Density of Oligodendrocytes and Susceptibility to Severe Forms of Seizures. eNeuro 2021, 8. [Google Scholar] [CrossRef]
- Liddelow, S.A.; Barres, B.A. Reactive Astrocytes: Production, Function, and Therapeutic Potential. Immunity 2017, 46, 957–967. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Daneman, R.; Prat, A. The blood-brain barrier. Cold Spring Harb. Perspect. Biol. 2015, 7, a020412. [Google Scholar] [CrossRef] [Green Version]
- Marchi, N.; Granata, T.; Ghosh, C.; Janigro, D. Blood-brain barrier dysfunction and epilepsy: Pathophysiologic role and therapeutic approaches. Epilepsia 2012, 53, 1877–1886. [Google Scholar] [CrossRef] [Green Version]
- van Vliet, E.A.; da Costa Araújo, S.; Redeker, S.; van Schaik, R.; Aronica, E.; Gorter, J.A. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007, 130, 521–534. [Google Scholar] [CrossRef] [Green Version]
- Ivens, S.; Kaufer, D.; Flores, L.P.; Bechmann, I.; Zumsteg, D.; Tomkins, O.; Seiffert, E.; Heinemann, U.; Friedman, A. TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 2007, 130, 535–547. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rustenhoven, J.; Aalderink, M.; Scotter, E.L.; Oldfield, R.L.; Bergin, P.S.; Mee, E.W.; Graham, E.S.; Faull, R.L.; Curtis, M.A.; Park, T.I.; et al. TGF-beta1 regulates human brain pericyte inflammatory processes involved in neurovasculature function. J. Neuroinflammation 2016, 13, 37. [Google Scholar] [CrossRef] [Green Version]
- Yamanaka, G.; Takata, F.; Kataoka, Y.; Kanou, K.; Morichi, S.; Dohgu, S.; Kawashima, H. The Neuroinflammatory Role of Pericytes in Epilepsy. Biomedicines 2021, 9, 759. [Google Scholar] [CrossRef]
- Varvel, N.H.; Neher, J.J.; Bosch, A.; Wang, W.; Ransohoff, R.M.; Miller, R.J.; Dingledine, R. Infiltrating monocytes promote brain inflammation and exacerbate neuronal damage after status epilepticus. Proc. Natl. Acad. Sci. USA 2016, 113, E5665–E5674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zattoni, M.; Mura, M.L.; Deprez, F.; Schwendener, R.A.; Engelhardt, B.; Frei, K.; Fritschy, J.M. Brain infiltration of leukocytes contributes to the pathophysiology of temporal lobe epilepsy. J. Neurosci. 2011, 31, 4037–4050. [Google Scholar] [CrossRef] [Green Version]
- Varvel, N.H.; Espinosa-Garcia, C.; Hunter-Chang, S.; Chen, D.; Biegel, A.; Hsieh, A.; Blackmer-Raynolds, L.; Ganesh, T.; Dingledine, R. Peripheral Myeloid Cell EP2 Activation Contributes to the Deleterious Consequences of Status Epilepticus. J. Neurosci. 2021, 41, 1105–1117. [Google Scholar] [CrossRef]
- Brennan, G.P.; Henshall, D.C. MicroRNAs as regulators of brain function and targets for treatment of epilepsy. Nat. Rev. Neurol. 2020, 16, 506–519. [Google Scholar] [CrossRef]
- Aronica, E.; Fluiter, K.; Iyer, A.; Zurolo, E.; Vreijling, J.; van Vliet, E.A.; Baayen, J.C.; Gorter, J.A. Expression pattern of miR-146a, an inflammation-associated microRNA, in experimental and human temporal lobe epilepsy. Eur. J. Neurosci. 2010, 31, 1100–1107. [Google Scholar] [CrossRef]
- Zhang, H.; Qu, Y.; Wang, A. Antagonist targeting microRNA-146a protects against lithium-pilocarpine-induced status epilepticus in rats by nuclear factor-kappaB pathway. Mol. Med. Rep. 2018, 17, 5356–5361. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zheng, P.; Bin, H.; Chen, W. Inhibition of microRNA-103a inhibits the activation of astrocytes in hippocampus tissues and improves the pathological injury of neurons of epilepsy rats by regulating BDNF. Cancer Cell Int. 2019, 19, 109. [Google Scholar] [CrossRef]
- Lu, J.; Zhou, N.; Yang, P.; Deng, L.; Liu, G. MicroRNA-27a-3p Downregulation Inhibits Inflammatory Response and Hippocampal Neuronal Cell Apoptosis by Upregulating Mitogen-Activated Protein Kinase 4 (MAP2K4) Expression in Epilepsy: In Vivo and In Vitro Studies. Med. Sci. Monit. 2019, 25, 8499–8508. [Google Scholar] [CrossRef] [PubMed]
- Fu, M.; Tao, J.; Wang, D.; Zhang, Z.; Wang, X.; Ji, Y.; Li, Z. Downregulation of MicroRNA-34c-5p facilitated neuroinflammation in drug-resistant epilepsy. Brain Res. 2020, 1749, 147130. [Google Scholar] [CrossRef]
- van Stuijvenberg, M.; Derksen-Lubsen, G.; Steyerberg, E.W.; Habbema, J.D.; Moll, H.A. Randomized, controlled trial of ibuprofen syrup administered during febrile illnesses to prevent febrile seizure recurrences. Pediatrics 1998, 102, E51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marchi, N.; Granata, T.; Freri, E.; Ciusani, E.; Ragona, F.; Puvenna, V.; Teng, Q.; Alexopolous, A.; Janigro, D. Efficacy of anti-inflammatory therapy in a model of acute seizures and in a population of pediatric drug resistant epileptics. PLoS ONE 2011, 6, e18200. [Google Scholar] [CrossRef]
- Chen, J.; Cai, F.; Jiang, L.; Hu, Y.; Feng, C. A prospective study of dexamethasone therapy in refractory epileptic encephalopathy with continuous spike-and-wave during sleep. Epilepsy Behav. 2016, 55, 1–5. [Google Scholar] [CrossRef]
- Nowak, M.; Strzelczyk, A.; Reif, P.S.; Schorlemmer, K.; Bauer, S.; Norwood, B.A.; Oertel, W.H.; Rosenow, F.; Strik, H.; Hamer, H.M. Minocycline as potent anticonvulsant in a patient with astrocytoma and drug resistant epilepsy. Seizure 2012, 21, 227–228. [Google Scholar] [CrossRef] [Green Version]
- Godfred, R.M.; Parikh, M.S.; Haltiner, A.M.; Caylor, L.M.; Sepkuty, J.P.; Doherty, M.J. Does aspirin use make it harder to collect seizures during elective video-EEG telemetry? Epilepsy Behav. 2013, 27, 115–117. [Google Scholar] [CrossRef] [PubMed]
- Jyonouchi, H.; Geng, L. Intractable Epilepsy (IE) and Responses to Anakinra, a Human RecombinantIL-1 Receptor Agonist (IL-1ra): Case Reports. J. Clin. Cell Immunol. 2016, 7. [Google Scholar] [CrossRef] [Green Version]
- Jun, J.S.; Lee, S.T.; Kim, R.; Chu, K.; Lee, S.K. Tocilizumab treatment for new onset refractory status epilepticus. Ann. Neurol. 2018, 84, 940–945. [Google Scholar] [CrossRef]
- Vossler, D.G. Remarkably High Efficacy of Cenobamate in Adults With Focal-Onset Seizures: A Double-Blind, Randomized, Placebo-Controlled Trial. Epilepsy Curr. 2020, 20, 85–87. [Google Scholar] [CrossRef] [Green Version]
- Latimer, D.R.; Edinoff, A.N.; Ruff, R.D.; Rooney, K.C.; Penny, K.M.; Patel, S.B.; Sabbenahalli, S.; Kaye, A.M.; Cornett, E.M.; Viswanath, O.; et al. Cenobamate, a Sodium Channel Inhibitor and Positive Allosteric Modulator of GABAA Ion Channels, for Partial Onset Seizures in Adults: A Comprehensive Review and Clinical Implications. Neurol. Int. 2021, 13, 252–265. [Google Scholar] [CrossRef] [PubMed]
- Herzog, A.G.; Frye, C.A.; Progesterone Trial Study, G. Allopregnanolone levels and seizure frequency in progesterone-treated women with epilepsy. Neurology 2014, 83, 345–348. [Google Scholar] [CrossRef] [Green Version]
- Wu, Y.V.; Burnham, W.M. The anti-seizure effects of IV 5alpha-dihydroprogesterone on amygdala-kindled seizures in rats. Epilepsy Res. 2018, 146, 132–136. [Google Scholar] [CrossRef]
- Lattanzi, S.; Riva, A.; Striano, P. Ganaxolone treatment for epilepsy patients: From pharmacology to place in therapy. Expert Rev. Neurother. 2021, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Bough, K.J.; Rho, J.M. Anticonvulsant mechanisms of the ketogenic diet. Epilepsia 2007, 48, 43–58. [Google Scholar] [CrossRef]
- Neal, E.G.; Chaffe, H.; Schwartz, R.H.; Lawson, M.S.; Edwards, N.; Fitzsimmons, G.; Whitney, A.; Cross, J.H. The ketogenic diet for the treatment of childhood epilepsy: A randomised controlled trial. Lancet Neurol. 2008, 7, 500–506. [Google Scholar] [CrossRef]
- Groomes, L.B.; Pyzik, P.L.; Turner, Z.; Dorward, J.L.; Goode, V.H.; Kossoff, E.H. Do patients with absence epilepsy respond to ketogenic diets? J. Child. Neurol. 2011, 26, 160–165. [Google Scholar] [CrossRef]
- Liu, H.; Yang, Y.; Wang, Y.; Tang, H.; Zhang, F.; Zhang, Y.; Zhao, Y. Ketogenic diet for treatment of intractable epilepsy in adults: A meta-analysis of observational studies. Epilepsia Open 2018, 3, 9–17. [Google Scholar] [CrossRef]
- Cervenka, M.; Pascual, J.M.; Rho, J.M.; Thiele, E.; Yellen, G.; Whittemore, V.; Hartman, A.L. Metabolism-based therapies for epilepsy: New directions for future cures. Ann. Clin. Transl. Neurol. 2021, 8, 1730–1737. [Google Scholar] [CrossRef]
- Jung, K.H.; Chu, K.; Lee, S.T.; Kim, J.; Sinn, D.I.; Kim, J.M.; Park, D.K.; Lee, J.J.; Kim, S.U.; Kim, M.; et al. Cyclooxygenase-2 inhibitor, celecoxib, inhibits the altered hippocampal neurogenesis with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Neurobiol. Dis. 2006, 23, 237–246. [Google Scholar] [CrossRef] [PubMed]
- Alsaegh, H.; Eweis, H.; Kamal, F.; Alrafiah, A. Celecoxib Decrease Seizures Susceptibility in a Rat Model of Inflammation by Inhibiting HMGB1 Translocation. Pharmaceuticals 2021, 14, 380. [Google Scholar] [CrossRef] [PubMed]
- Vieira, M.J.; Perosa, S.R.; Argaaaraz, G.A.; Silva, J.A., Jr.; Cavalheiro, E.A.; Graca Naffah-Mazzacoratti, M. Indomethacin can downregulate the levels of inflammatory mediators in the hippocampus of rats submitted to pilocarpine-induced status epilepticus. Clinics 2014, 69, 621–626. [Google Scholar] [CrossRef]
- Ma, L.; Cui, X.L.; Wang, Y.; Li, X.W.; Yang, F.; Wei, D.; Jiang, W. Aspirin attenuates spontaneous recurrent seizures and inhibits hippocampal neuronal loss, mossy fiber sprouting and aberrant neurogenesis following pilocarpine-induced status epilepticus in rats. Brain Res. 2012, 1469, 103–113. [Google Scholar] [CrossRef] [PubMed]
- Zhu, K.; Hu, M.; Yuan, B.; Liu, J.X.; Liu, Y. Aspirin attenuates spontaneous recurrent seizures in the chronically epileptic mice. Neurol. Res. 2017, 39, 744–757. [Google Scholar] [CrossRef] [PubMed]
- Peng, J.; Wu, S.; Guo, C.; Guo, K.; Zhang, W.; Liu, R.; Li, J.; Hu, Z. Effect of Ibuprofen on Autophagy of Astrocytes During Pentylenetetrazol-Induced Epilepsy and its Significance: An Experimental Study. Neurochem. Res. 2019, 44, 2566–2576. [Google Scholar] [CrossRef] [PubMed]
- Gao, F.; Liu, Y.; Li, X.; Wang, Y.; Wei, D.; Jiang, W. Fingolimod (FTY720) inhibits neuroinflammation and attenuates spontaneous convulsions in lithium-pilocarpine induced status epilepticus in rat model. Pharmacol. Biochem. Behav. 2012, 103, 187–196. [Google Scholar] [CrossRef]
- Cipriani, R.; Chara, J.C.; Rodriguez-Antiguedad, A.; Matute, C. FTY720 attenuates excitotoxicity and neuroinflammation. J. Neuroinflammation 2015, 12, 86. [Google Scholar] [CrossRef] [Green Version]
- Vizuete, A.F.K.; Hansen, F.; Negri, E.; Leite, M.C.; de Oliveira, D.L.; Goncalves, C.A. Effects of dexamethasone on the Li-pilocarpine model of epilepsy: Protection against hippocampal inflammation and astrogliosis. J. Neuroinflammation 2018, 15, 68. [Google Scholar] [CrossRef] [Green Version]
- Jiang, J.; Yu, Y.; Kinjo, E.R.; Du, Y.; Nguyen, H.P.; Dingledine, R. Suppressing pro-inflammatory prostaglandin signaling attenuates excitotoxicity-associated neuronal inflammation and injury. Neuropharmacology 2019, 149, 149–160. [Google Scholar] [CrossRef]
- Reddy, D.S. Neurosteroid replacement therapy for catamenial epilepsy, postpartum depression and neuroendocrine disorders in women. J. Neuroendocrinol. 2021, e13028. [Google Scholar] [CrossRef]
- Lucchi, C.; Costa, A.M.; Rustichelli, C.; Biagini, G. Allopregnanolone and Pregnanolone Are Reduced in the Hippocampus of Epileptic Rats, but Only Allopregnanolone Correlates with Seizure Frequency. Neuroendocrinology 2021, 111, 536–541. [Google Scholar] [CrossRef]
- Sayeed, I.; Stein, D.G. Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog. Brain Res. 2009, 175, 219–237. [Google Scholar] [CrossRef]
- Stein, D.G.; Sayeed, I. Repurposing and repositioning neurosteroids in the treatment of traumatic brain injury: A report from the trenches. Neuropharmacology 2019, 147, 66–73. [Google Scholar] [CrossRef]
- Yilmaz, C.; Karali, K.; Fodelianaki, G.; Gravanis, A.; Chavakis, T.; Charalampopoulos, I.; Alexaki, V.I. Neurosteroids as regulators of neuroinflammation. Front. Neuroendocrinol. 2019, 55, 100788. [Google Scholar] [CrossRef] [PubMed]
- Guennoun, R.; Labombarda, F.; Gonzalez Deniselle, M.C.; Liere, P.; De Nicola, A.F.; Schumacher, M. Progesterone and allopregnanolone in the central nervous system: Response to injury and implication for neuroprotection. J. Steroid Biochem. Mol. Biol. 2015, 146, 48–61. [Google Scholar] [CrossRef] [PubMed]
- Guennoun, R. Progesterone in the Brain: Hormone, Neurosteroid and Neuroprotectant. Int. J. Mol. Sci. 2020, 21, 5271. [Google Scholar] [CrossRef] [PubMed]
- Massieu, L.; Haces, M.L.; Montiel, T.; Hernandez-Fonseca, K. Acetoacetate protects hippocampal neurons against glutamate-mediated neuronal damage during glycolysis inhibition. Neuroscience 2003, 120, 365–378. [Google Scholar] [CrossRef]
- Gasior, M.; Rogawski, M.A.; Hartman, A.L. Neuroprotective and disease-modifying effects of the ketogenic diet. Behav Pharmacol. 2006, 17, 431–439. [Google Scholar] [CrossRef] [Green Version]
- D’Andrea Meira, I.; Romão, T.T.; Pires do Prado, H.J.; Krüger, L.T.; Pires, M.E.P.; da Conceição, P.O. Ketogenic Diet and Epilepsy: What We Know So Far. Front. Neurosci. 2019, 13, 5. [Google Scholar] [CrossRef] [Green Version]
- Dupuis, N.; Curatolo, N.; Benoist, J.F.; Auvin, S. Ketogenic diet exhibits anti-inflammatory properties. Epilepsia 2015, 56, e95–e98. [Google Scholar] [CrossRef]
- Shen, Y.; Kapfhamer, D.; Minnella, A.M.; Kim, J.E.; Won, S.J.; Chen, Y.; Huang, Y.; Low, L.H.; Massa, S.M.; Swanson, R.A. Bioenergetic state regulates innate inflammatory responses through the transcriptional co-repressor CtBP. Nat. Commun. 2017, 8, 624. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zheng, Y.Q.; Jin, M.F.; Suo, G.H.; Wu, Y.J.; Sun, Y.X.; Ni, H. Proteomics for Studying the Effects of Ketogenic Diet Against Lithium Chloride/Pilocarpine Induced Epilepsy in Rats. Front. Neurosci. 2020, 14, 562853. [Google Scholar] [CrossRef]
- Hirotsu, C.; Matos, G.; Tufik, S.; Andersen, M.L. Changes in gene expression in the frontal cortex of rats with pilocarpine-induced status epilepticus after sleep deprivation. Epilepsy Behav. 2013, 27, 378–384. [Google Scholar] [CrossRef]
- Matos, G.; Scorza, F.A.; Mazzotti, D.R.; Guindalini, C.; Cavalheiro, E.A.; Tufik, S.; Andersen, M.L. The effects of sleep deprivation on microRNA expression in rats submitted to pilocarpine-induced status epilepticus. Prog. Neuropsychopharmacol. Biol. Psychiatry 2014, 51, 159–165. [Google Scholar] [CrossRef]
- Huang, T.R.; Jou, S.B.; Chou, Y.J.; Yi, P.L.; Chen, C.J.; Chang, F.C. Interleukin-1 receptor (IL-1R) mediates epilepsy-induced sleep disruption. BMC Neurosci. 2016, 17, 74. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohammed, H.S.; Khadrawy, Y.A. Electrophysiological and neurochemical evaluation of the adverse effects of REM sleep deprivation and epileptic seizures on rat’s brain. Life Sci. 2021, 273, 119303. [Google Scholar] [CrossRef]
- Aboul Ezz, H.S.; Noor, A.E.; Mourad, I.M.; Fahmy, H.; Khadrawy, Y.A. Neurochemical effects of sleep deprivation in the hippocampus of the pilocarpine-induced rat model of epilepsy. Iran. J. Basic Med. Sci. 2021, 24, 85–91. [Google Scholar] [CrossRef] [PubMed]
- Somani, A.; El-Hachami, H.; Patodia, S.; Sisodiya, S.; Thom, M. Regional microglial populations in central autonomic brain regions in SUDEP. Epilepsia 2021, 62, 1318–1328. [Google Scholar] [CrossRef] [PubMed]
- Carrion, M.J.; Nunes, M.L.; Martinez, J.V.; Portuguez, M.W.; da Costa, J.C. Evaluation of sleep quality in patients with refractory seizures who undergo epilepsy surgery. Epilepsy Behav. 2010, 17, 120–123. [Google Scholar] [CrossRef]
- Serafini, A.; Kuate, C.; Gelisse, P.; Velizarova, R.; Gigli, G.L.; Coubes, P.; Crespel, A. Sleep before and after temporal lobe epilepsy surgery. Seizure 2012, 21, 260–265. [Google Scholar] [CrossRef] [Green Version]
- Zanzmera, P.; Shukla, G.; Gupta, A.; Goyal, V.; Srivastava, A.; Garg, A.; Bal, C.S.; Suri, A.; Behari, M. Effect of successful epilepsy surgery on subjective and objective sleep parameters--a prospective study. Sleep Med. 2013, 14, 333–338. [Google Scholar] [CrossRef]
- Hallbook, T.; Lundgren, J.; Rosen, I. Ketogenic diet improves sleep quality in children with therapy-resistant epilepsy. Epilepsia 2007, 48, 59–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McCarter, A.R.; Timm, P.C.; Shepard, P.W.; Sandness, D.J.; Luu, T.; McCarter, S.J.; Dueffert, L.; Dresow, M.; Feemster, J.C.; Cascino, G.D.; et al. Obstructive sleep apnea in refractory epilepsy: A pilot study investigating frequency, clinical features, and association with risk of sudden unexpected death in epilepsy. Epilepsia 2018, 59, 1973–1981. [Google Scholar] [CrossRef] [Green Version]
- Soontornpun, A.; Andrews, N.; Bena, J.; Grigg-Damberger, M.; Foldvary-Schaefer, N. 797 Obstructive Sleep Apnea is a Risk Factor for Sudden Unexplained Death in Epilepsy (SUDEP). Sleep 2021, 44, A310. [Google Scholar] [CrossRef]
- Malow, B.A.; Foldvary-Schaefer, N.; Vaughn, B.V.; Selwa, L.M.; Chervin, R.D.; Weatherwax, K.J.; Wang, L.; Song, Y. Treating obstructive sleep apnea in adults with epilepsy: A randomized pilot trial. Neurology 2008, 71, 572–577. [Google Scholar] [CrossRef] [PubMed]
- Malow, B.A.; Weatherwax, K.J.; Chervin, R.D.; Hoban, T.F.; Marzec, M.L.; Martin, C.; Binns, L.A. Identification and treatment of obstructive sleep apnea in adults and children with epilepsy: A prospective pilot study. Sleep Med. 2003, 4, 509–515. [Google Scholar] [CrossRef]
- Hollinger, P.; Khatami, R.; Gugger, M.; Hess, C.W.; Bassetti, C.L. Epilepsy and obstructive sleep apnea. Eur. Neurol. 2006, 55, 74–79. [Google Scholar] [CrossRef]
- Vendrame, M.; Auerbach, S.; Loddenkemper, T.; Kothare, S.; Montouris, G. Effect of continuous positive airway pressure treatment on seizure control in patients with obstructive sleep apnea and epilepsy. Epilepsia 2011, 52, e168–e171. [Google Scholar] [CrossRef] [PubMed]
- Li, P.; Ghadersohi, S.; Jafari, B.; Teter, B.; Sazgar, M. Characteristics of refractory vs. medically controlled epilepsy patients with obstructive sleep apnea and their response to CPAP treatment. Seizure 2012, 21, 717–721. [Google Scholar] [CrossRef] [Green Version]
- Pornsriniyom, D.; Kim, H.; Bena, J.; Andrews, N.D.; Moul, D.; Foldvary-Schaefer, N. Effect of positive airway pressure therapy on seizure control in patients with epilepsy and obstructive sleep apnea. Epilepsy Behav. 2014, 37, 270–275. [Google Scholar] [CrossRef]
- Segal, E.; Vendrame, M.; Gregas, M.; Loddenkemper, T.; Kothare, S.V. Effect of treatment of obstructive sleep apnea on seizure outcomes in children with epilepsy. Pediatr. Neurol. 2012, 46, 359–362. [Google Scholar] [CrossRef]
- Latreille, V.; Bubrick, E.J.; Pavlova, M. Positive Airway Pressure Therapy Is Challenging for Patients With Epilepsy. J. Clin. Sleep Med. 2018, 14, 1153–1159. [Google Scholar] [CrossRef]
- Şenel, G.B.; Karadeniz, D. Factors determining the long-term compliance with PAP therapy in patients with sleep-related epilepsy. Clin. Neurol. Neurosurg. 2021, 202, 106498. [Google Scholar] [CrossRef]
- Virk, J.S.; Kotecha, B. When continuous positive airway pressure (CPAP) fails. J. Thorac. Dis. 2016, 8, E1112. [Google Scholar] [CrossRef] [Green Version]
- Esposito, S.; Laino, D.; D’Alonzo, R.; Mencarelli, A.; Di Genova, L.; Fattorusso, A.; Argentiero, A.; Mencaroni, E. Pediatric sleep disturbances and treatment with melatonin. J. Transl. Med. 2019, 17, 77. [Google Scholar] [CrossRef]
- Khan, S.; Khurana, M.; Vyas, P.; Vohora, D. The role of melatonin and its analogues in epilepsy. Rev. Neurosci. 2020, 32, 49–67. [Google Scholar] [CrossRef] [PubMed]
- Elkhayat, H.A.; Hassanein, S.M.; Tomoum, H.Y.; Abd-Elhamid, I.A.; Asaad, T.; Elwakkad, A.S. Melatonin and sleep-related problems in children with intractable epilepsy. Pediatr. Neurol. 2010, 42, 249–254. [Google Scholar] [CrossRef]
- Goldberg-Stern, H.; Oren, H.; Peled, N.; Garty, B.Z. Effect of melatonin on seizure frequency in intractable epilepsy: A pilot study. J. Child. Neurol. 2012, 27, 1524–1528. [Google Scholar] [CrossRef] [PubMed]
- Jain, S.V.; Horn, P.S.; Simakajornboon, N.; Beebe, D.W.; Holland, K.; Byars, A.W.; Glauser, T.A. Melatonin improves sleep in children with epilepsy: A randomized, double-blind, crossover study. Sleep Med. 2015, 16, 637–644. [Google Scholar] [CrossRef] [Green Version]
- Akyuz, E.; Kullu, I.; Arulsamy, A.; Shaikh, M.F. Melatonin as an Antiepileptic Molecule: Therapeutic Implications via Neuroprotective and Inflammatory Mechanisms. ACS Chem. Neurosci. 2021, 12, 1281–1292. [Google Scholar] [CrossRef] [PubMed]
- Stanley, D.; Talathi, S.; Carney, P. Chronotherapy in the treatment of epilepsy. ChronoPhysiology Ther. 2014, 109–123. [Google Scholar] [CrossRef] [Green Version]
- Potruch, A.; Khoury, S.T.; Ilan, Y. The role of chronobiology in drug-resistance epilepsy: The potential use of a variability and chronotherapy-based individualized platform for improving the response to anti-seizure drugs. Seizure 2020, 80, 201–211. [Google Scholar] [CrossRef]
- Peng, W.; Ding, J.; Wang, X. The Management and Alternative Therapies for Comorbid Sleep Disorders in Epilepsy. Curr. Neuropharmacol. 2021, 19, 1264–1272. [Google Scholar] [CrossRef]
- Leeman-Markowski, B.A.; Schachter, S.C. Cognitive and Behavioral Interventions in Epilepsy. Curr. Neurol. Neurosci. Rep. 2017, 17, 42. [Google Scholar] [CrossRef]
- Ahorsu, D.K.; Lin, C.-Y.; Imani, V.; Carlbring, P.; Nygårdh, A.; Broströmd, A.; Hamilton, K.; Pakpourd, A.H. Testing an app-based intervention to improve insomnia in patients with epilepsy: A randomized controlled trial. Epilepsy Behav. 2020, 112, 107371. [Google Scholar] [CrossRef]
- Paardekooper, D.; Thayer, Z.; Miller, L.; Nikpour, A.; Gascoigne, M.B. Group-based cognitive behavioral therapy program for improving poor sleep quality and quality of life in people with epilepsy: A pilot study. Epilepsy Behav. 2020, 104, 106884. [Google Scholar] [CrossRef]
- Jain, S.V.; Glauser, T.A. Effects of epilepsy treatments on sleep architecture and daytime sleepiness: An evidence-based review of objective sleep metrics. Epilepsia 2014, 55, 26–37. [Google Scholar] [CrossRef] [PubMed]
- Reddy, D.S.; Chuang, S.H.; Hunn, D.; Crepeau, A.Z.; Maganti, R. Neuroendocrine aspects of improving sleep in epilepsy. Epilepsy Res. 2018, 147, 32–41. [Google Scholar] [CrossRef]
- Moore, J.L.; Carvalho, D.Z.; St Louis, E.K.; Bazil, C. Sleep and Epilepsy: A Focused Review of Pathophysiology, Clinical Syndromes, Co-morbidities, and Therapy. Neurotherapeutics 2021, 18, 170–180. [Google Scholar] [CrossRef] [PubMed]
- Shvarts, V.; Chung, S. Epilepsy, antiseizure therapy, and sleep cycle parameters. Epilepsy Res. Treat. 2013, 2013, 670682. [Google Scholar] [CrossRef] [PubMed] [Green Version]
(A) Clinical studies | ||||
Drug | Mechanism/Target | Pathology | Outcome | Ref |
Ibuprofen | COX-2 inhibitor | Febrile seizures | Reduced recurrence of a febrile seizure This study lacks inflammation analysis | [249,285] |
Dexamethasone | Glucocorticoid with anti-inflammatory and immunosuppressant properties | Drug-resistant pediatric epilepsy Epileptic encephalopathy with continuous spike-and-wave during sleep | Reduced number of seizures Common side effects: increased body weight, anxiety, and insomnia | [286,287] |
Minocycline | Suppresses microglial activation and reduces pro-inflammatory cytokine release | Astrocytoma and drug-resistant epilepsy | Reduced seizure frequency This study lacks inflammation analysis | [288] |
Aspirin | COX-2 inhibitor | Partial epilepsy | Reduced seizure frequency This study lacks inflammation analysis | [249,289] |
Anakinra | IL-1 receptor agonist | Intractable seizures | Reduced number of seizures Changes in IL-1β/IL-10 ratio produced by peripheral blood monocytes | [290] |
Tocilizumab | IL-6 receptor inhibitor | New onset refractory status epilepticus | No recurrence of status epilepticus IL-6 levels were normalized 2 out of 7 patients experienced severe adverse events related to infection | [291] |
Cenobamate | Sodium channel inhibitor and positive allosteric modulator of GABAA ion channels | Uncontrolled focal (partial)-onset epilepsy | Reduced seizure frequency This study lacks inflammation analysis | [292,293] |
Neurosteroids | Pleiotropic actions, including modulation of neuronal excitability and anti-inflammatory properties | Catamenial epilepsy Tuberous Sclerosis Complex | Progesterone was beneficial in reducing seizures in women with perimenstrual exacerbation; its anti-epileptic effects are mainly mediated by allopregnanolone (ALLO), which interacts with the GABAA receptor Ganaxolone (GNX), a synthetic analog of ALLO, reduced seizure frequency These studies lack inflammation analyses | [294,295,296] |
Ketogenic diet | Pleiotropic actions, including modulation of neuronal excitability | Absence epilepsy Drug-resistant epilepsy | Reduced seizures These studies lack inflammation analyses | [297,298,299,300,301] |
(B) Pre-clinical studies | ||||
Celecoxib | COX-2 inhibitor | Pilocarpine | Delayed latency to seizure onset Prevented neuronal death and microglia activation in the hippocampus Decreased in hippocampal levels of pro-inflammatory cytokines, oxidative stress markers, and suppressed MGB1 translocation | [223,302,303] |
Indomethacin | COX-2 inhibitor | Pilocarpine | Decreased IL-1β and TNF-α expression | [304] |
Aspirin | COX-2 inhibitor | Pilocarpine | Reduced spontaneous recurrent seizures, memory loss, and aberrant neurogenesis These studies lack inflammation analyses | [249,305,306] |
Ibuprofen | COX-2 inhibitor | Pentylenetetrazol | Increased latency to seizure and reduced seizure duration Reduced proliferation of astrocytes by increasing autophagy | [307] |
Fingolimod (FTY720) | Immunosuppression via modulation of sphingosine-1-phosphate receptors | Lithium–Pilocarpine Excitotoxicity in vitro Kainic acid | Inhibited neuroinflammation, reduced neuronal loss, activation of microglia and astrocytes, and attenuated spontaneous seizures | [308,309] |
Dexamethasone | Glucocorticoid with anti-inflammatory and immunosuppressant properties | Pilocarpine Lithium–Pilocarpine | Reduced SE severity and abolished mortality Decreased number of circulating T-cells Reduced BBB damage Reduced hippocampal inflammatory cytokines, prostaglandin E2, and cyclooxygenases Attenuated astrogliosis markers | [286,310] |
TG6-10-1 | EP2 receptor antagonist | Organophosphorus-induced SE Kainate | Reduced hippocampal neurodegeneration, blunted the inflammatory cytokine burst, and reduced microglial activation | [252,311] |
TG8-260 | EP2 receptor antagonist | Pilocarpine | Reduced hippocampal neuroinflammation and gliosis, but no effect on neuronal injury nor BBB breakdown | [253] |
Neurosteroids | Pleiotropic actions, including modulation of neuronal excitability and anti-inflammatory properties | Pentylenetetrazol Amygdala kindling Kainic acid | Reduced levels of ALLO in the hippocampus correlates with seizure frequency Exogenous treatment with progesterone, ALLO, and GNX suppressed seizures Progesterone and ALLO inhibit inflammatory signaling pathway TLR4/NFκB and NLRP3 inflammasome activation and pro-inflammatory cytokine production in multiple models of brain injury | [295,312,313,314,315,316,317,318] |
Ketogenic diet | Pleiotropic actions, including reduction of reactive oxygen species and neuronal excitability, and enhanced production of high-energy molecules | Excitotoxicity in vitro Lithium–Pilocarpine LPS | Improved neuronal survival in vitro Reduced glutamate and enhanced GABA synthesis in the brain, suppressing seizures Reduced levels of pro-inflammatory cytokines in blood and brain after LPS injection Regulated NF-κB activation and pro-inflammatory gene expression in macrophages and microglia | [297,319,320,321,322,323,324] |
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Bonilla-Jaime, H.; Zeleke, H.; Rojas, A.; Espinosa-Garcia, C. Sleep Disruption Worsens Seizures: Neuroinflammation as a Potential Mechanistic Link. Int. J. Mol. Sci. 2021, 22, 12531. https://doi.org/10.3390/ijms222212531
Bonilla-Jaime H, Zeleke H, Rojas A, Espinosa-Garcia C. Sleep Disruption Worsens Seizures: Neuroinflammation as a Potential Mechanistic Link. International Journal of Molecular Sciences. 2021; 22(22):12531. https://doi.org/10.3390/ijms222212531
Chicago/Turabian StyleBonilla-Jaime, Herlinda, Helena Zeleke, Asheebo Rojas, and Claudia Espinosa-Garcia. 2021. "Sleep Disruption Worsens Seizures: Neuroinflammation as a Potential Mechanistic Link" International Journal of Molecular Sciences 22, no. 22: 12531. https://doi.org/10.3390/ijms222212531