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Daily ingestion of Akkermansia mucciniphila for one month promotes healthy aging and increases lifespan in old female mice

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Abstract

The ingestion of certain probiotics has been suggested as a promising nutritional strategy to improve aging. The objective of this work was to evaluate the effects of the daily intake, for a month, of a new probiotic Akkermansia muciniphila (AKK) (2 × 108 cfu/100µL PBS) on behavior, as well as function and redox state of immune cells of old female ICR-CD1 mice (OA group). For this, several behavioral tests were performed, and function and oxidative-inflammatory stress parameters of peritoneal leukocytes were analyzed in OA group, in a group of the same age that did not take AKK (old control, OC group) and in another adult control (AC) group. The results showed, in OA group, a significant improvement of several behavioral responses (coordination, balance, neuromuscular vigor, exploratory ability and anxiety like-behaviors), as well as in immune functions (chemotaxis, phagocytosis, NK activity and lymphoproliferation) and in oxidative stress parameters (glutathione peroxidase and reductase activities, oxidized glutathione and lipid oxidation concentrations) of the peritoneal leukocytes in comparison to those observed in OC group. In addition, peritoneal immune cells from the OA group released lower basal concentrations of pro-inflammatory cytokines (IL-2, IL-6 and TNF-α) compared to those from the OC group. The values of parameters in OA were similar to those in AC group. These improvements in the old mice receiving the probiotic were reflected in an increase in their lifespan. In conclusion, our data indicate that AKK supplementation for a short period could be a good nutritional strategy to promote healthy longevity.

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Data Availability

All material used and data generated or analyzed during this study are included in this published article.

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References

  • Akbari E, Asemi Z, Daneshvar Kakhaki R, Bahmani F, Kouchaki E, Tamtaji OR, Hamidi GA, Salami M (2016) Effect of probiotic supplementation on cognitive function and metabolic status in alzheimer’s disease: a randomized, double-blind and controlled trial. Front Aging Neurosci 8:256

    PubMed  PubMed Central  Google Scholar 

  • Alvarado C, Álvarez P, Jiménez L, De la Fuente M (2006) Oxidative stress in leukocytes from young prematurely aging mice is reversed by supplementation with biscuits rich in antioxidants. Dev Comp Immunol 30(12):1168–1180

    CAS  PubMed  Google Scholar 

  • Andersson KE, Axling U, Xu J, Swärd K, Ahrné S, Molin G, Holm C, Hellstrand P (2013) Diverse effects of oats on cholesterol metabolism in C57BL/6 mice correlate with expression of hepatic bile acid-producing enzymes. Eur J Nutr 52:1755–1769

    CAS  PubMed  Google Scholar 

  • Arranz L, De Castro NM, Baeza I, Maté I, Viveros MP, De la Fuente M (2010a) Environmental enrichment improves age-related immune system impairment: long-term exposure since adulthood increases life span in mice. Rejuvenation Res 13(4):415–428

    PubMed  Google Scholar 

  • Arranz L, Camaño JH, Lord JM, De la Fuente M (2010b) Preserved immune functions and controlled leukocyte oxidative stress in naturally long-lived mice: possible role of nuclear factor kappa B. J Gerontol A Biol Sci Med Sci 65(9):941–950

    PubMed  Google Scholar 

  • Baeza I, De Castro NM, Giménez-Llort L, De la Fuente M (2010a) Ovariectomy, a model of menopause in rodents, causes a premature aging of the nervous and immune systems. J Neuroimm 219:90–99

    CAS  Google Scholar 

  • Baeza I, Fernandez-Tresguerres J, Ariznavarreta C, De la Fuente M (2010b) Effects of growth hormone, melatonin, oestrogens and phytoestrogens on the oxidized glutathione (GSSG)/reduced glutathione (GSH) ratio and lipid peroxidation in aged ovariectomized rats. Biogerontol 11:687–701

    CAS  Google Scholar 

  • Bárcena C, Valdés-Mas R, Mayoral P, Garabaya C, Durand S, Rodríguez F, Fernández-García MT, Salazar N, Nogacka AM, Garatachea N, Bossut N, Aprahamian F, Lucia A, Kroemer G, Freije JMP, Quirós PM, López-Otín C (2019) Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice. Nat Med 25(8):1234–1242

    PubMed  Google Scholar 

  • Bauer ME, De la Fuente (2016) The role of oxidative and inflammatory stress and persistent viral infections in immunosenescence. Mech Ageing Dev 158:27–37

    CAS  PubMed  Google Scholar 

  • Berry D, Reinisch W (2013) Intestinal microbiota: a source of novel biomarkers in inflammatory bowel diseases? Best Pract Res Clin Gastroenterol 27(1):47–58

    CAS  PubMed  Google Scholar 

  • Biagi E, Franceschi C, Rampelli S, Severgnini M, Ostan R, Turroni S, Consolandi C, Quercia S, Scurti M, Monti D, Capri M, Brigidi P, Candela M (2016) Gut microbiota and extreme longevity. Curr Biol 26(11):1480–1485

    CAS  PubMed  Google Scholar 

  • Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, Nikkïla J, Monti D, Satokari R, Franceschi C, Brigidi P, De Vos W (2010) Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS ONE 5:e10667

    PubMed  PubMed Central  Google Scholar 

  • Bienenstock J, Kunze W, Forsythe P (2016) The microbiome-gut-brain axis and the consequences of infection and dysbiosis. Am J Gastroenterol Suppl 3:33–40

    CAS  Google Scholar 

  • Boyden SV (1962) The chemotaxis effect of mixtures of antibody and antigen on polymorphonuclear leukocytes. J Exp Med 115:453–466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brenes GA, Penninx BW, Judd PH, Rockwell E, Sewell DD, Wetherell JL (2008) Anxiety, depression and disability across life span. Aging Ment Health 12:158–163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cani PD, de Vos WM (2017) Next-generation beneficial microbes: the case of Akkermansia muciniphila. Front Microbiol 8:1765

    PubMed  PubMed Central  Google Scholar 

  • Chahal H, Drake W (2007) The endocrine system and ageing. Journal Pathol 211(2):173–180

    CAS  Google Scholar 

  • Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S (2007) Intestinal integrity and akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 73:7767–7770

    CAS  PubMed  PubMed Central  Google Scholar 

  • Collado MC, Laitinen K, Salminen S, Isolauri E (2012) Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res 72(1):77–85

    CAS  PubMed  Google Scholar 

  • Davidson SR, Burnett M, Hoffman-Goetz L (2006) Training effects in mice after long-term voluntary exercise. Med Sci Sports Exerc 38:250–255

    PubMed  Google Scholar 

  • De la Fuente M (1985) Changes in the macrophage function with aging. Comp Biochem Physiol A Comp Physiol 81(4):935–938

    Google Scholar 

  • De la Fuente M (2010) Murine models of premature ageing for the study of diet-induced immune changes: improvement of leucocyte functions in two strains of old prematurely ageing mice by dietary supplementation with sulphur-containing antioxidants. Proc Nutr Soc 69(4):651–659

    PubMed  Google Scholar 

  • De la Fuente M (2014) Crosstalk between the nervous and the immune systems in health and sickness. Curr Pharm Des 20(29):4605–4607

    PubMed  Google Scholar 

  • De la Fuente M (2018a) Bio-psycho-social bridge: the psychoneuroimmune system in successful aging. In “Cambridge Handbook of Succesful Aging” Fernández-Ballesteros R, Benetos A, Robine JM (Eds) New York Cambridge University Press Pp: 265–280

  • De la Fuente M (2018b). Oxidation and inflammation in the immune and nervous sytems, a link between aging and anxiety. In : “ Handbook of Immunosenescence“ Fulop T, Franceschi C, Hirokawa K, Pawelec G. (eds) Springer Nature Cham Pp: 1–31

  • De la Fuente M (2021) The role of the microbiota-gut-brain axis in the health and illness condition: a focus on alzheimer’s disease. J Alzheimers Dis 81(4):1345–1360

    PubMed  Google Scholar 

  • De la Fuente M, Cruces J, Hernández O, Ortega E (2011) Strategies to improve the functions and redox state of the immune system in aged subjects. Curr Pharm Des 17(36):3966–3993

    PubMed  Google Scholar 

  • De la Fuente M, Ferrández D, Muñoz F, de Juan E, Miquel J (1993) Stimulation by the antioxidant thioproline of the lymphocyte functions of old mice. Mech Ageing Dev 68(1–3):27–36

    PubMed  Google Scholar 

  • De la Fuente M, Miñano M, Manuel Victor V, Del Rio M, Ferrández MD, Díez A, Miquel J (1998) Relation between exploratory activity and immune function in aged mice: a preliminary study. Mech Ageing Dev 102(2–3):263–277

    PubMed  Google Scholar 

  • De la Fuente M, Miquel J (2009) An update of the oxidation-inflammation theory of aging: the involvement of the immune system in oxi-inflamm-aging. Curr Pharm Des 15(26):3003–3026

    PubMed  Google Scholar 

  • Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM (2008) The Mucin degraderAkkermansia muciniphilais an abundant resident of the human intestinal tract. Appl Environ Microbiol 74:1646–1648

    CAS  PubMed  Google Scholar 

  • Derrien M, Van Baarlen P, Hooiveld G, Norin E, Müller M, de Vos WM (2011) Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front Microbiol 2:1–14

    Google Scholar 

  • Dong H, Rowland I, Thomas LV, Yaqoob P (2013) Immunomodulatory effects of a probiotic drink containing Lactobacillus caseiShirota in healthy older volunteers. Eur J Nutr 52:1853–1863

    CAS  PubMed  Google Scholar 

  • Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V (2012) Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition 28:539–543

    CAS  PubMed  Google Scholar 

  • Ferrández MD, Correa R, Del Rio M, De la Fuente M (1999) Effects in vitro of several antioxidants on the natural killer function of aging mice. Exp Gerontol 34(5):675–685

    PubMed  Google Scholar 

  • Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G (2000) Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 908:244–254

    CAS  PubMed  Google Scholar 

  • Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, Anastasovska J, Ghourab S, Hankir M, Zhang S, Carling D, Swann JR, Gibson G, Viardot A, Morrison D, Louise Thomas E, Bell JD (2014) The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 5:3611

    CAS  PubMed  Google Scholar 

  • Garrido A, Cruces J, Ceprián N, De la Fuente M (2018) Improvements in behavior and immune function and increased lifespan of old mice cohabitating with adult animals. J Gerontol A Biol Sci Med Sci 73(7):873–881

    CAS  PubMed  Google Scholar 

  • Gilad GM, Gilad VH (2000) Accelerated functional recovery and neuroprotection by agmatine after spinal cord ischemia in rats. Neurosci Lett 296(2–3):97–100

    CAS  PubMed  Google Scholar 

  • Grompone G, Martorell P, Llopis S, González N, Genovés S, Mulet AP, Fernández-Calero T, Tiscornia I, Bollati-Fogolín M, Chambaud I, Foligné B, Montserrat A, Ramón D (2012) Antiinflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans. PLoS ONE 7:e52493

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guayerbas N, Puerto M, Víctor VM, Miquel J, De la Fuente M (2002a) Leukocyte function and life span in a murine model of premature immunosenescence. Exp Gerontol 37(2–3):249–256

    CAS  PubMed  Google Scholar 

  • Guayerbas N, Catalán M, Víctor VM, Miquel J, De la Fuente M (2002b) Relation of behaviour and macrophage function to life span in a murine model of premature immunosenescence. Behav Brain Res 134:41–48

    PubMed  Google Scholar 

  • Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514

    PubMed  Google Scholar 

  • Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300

    CAS  PubMed  Google Scholar 

  • Higarza SG, Arboleya S, Arias JL, Gueimonde M, Arias N (2021) Akkermansia muciniphila and environmental enrichment reverse cognitive impairment associated with high-fat high-cholesterol consumption in rats. Gut Microbes 3(1):1–20

    Google Scholar 

  • Hissin PJ, Hilf R (1976) A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 74(1):214–226

    CAS  PubMed  Google Scholar 

  • Hunsche C, Cruces J, De la Fuente M (2019) Improvement of redox state and functions of immune cells as well as of behavior response in aged mice after two weeks supplementation of fermented milk with probiotics. Current Microbiol 76(11):1278–1289

    CAS  PubMed  Google Scholar 

  • Hunsche C, Cruces J, Garrido A, Hernández O, De la Fuente M (2018) Dietary supplementation with fermented milk containing probiotics improves behaviour and immune response of aged mice. J Prob Health 6:1

    Google Scholar 

  • Hunsche C, Martínez de Toda I, Hernández O, Jiménez B, Díaz LE, Marcos A, De la Fuente M (2020) The supplementations with 2-hydroxyoleic acid and n-3 polyunsaturated fatty acids revert oxidative stress in various organs of diet-induced obese mice. Free Radic Res 54(6):455–466

    CAS  PubMed  Google Scholar 

  • Jeong JJ, Kim K, Ahn Y, Sim J, Woo J, Huh C, Kim D (2015) Probiotic mixture KF attenuates age-dependent memory deficit and lipidemia in fischer 344 rats. J Microbiol Biotechnol 25(9):1532–1536

    CAS  PubMed  Google Scholar 

  • Johnson M (2012) Protein quantitation. Mater. Methods 2:115

    Google Scholar 

  • Kong Y, Olejar KJ, On SLW, Chelikani V (2020) The potential of Lactobacillus spp. for Modulating Oxidative Stress in the Gastrointestinal Tract. Antioxidants (Basel) 9(7):610

    CAS  Google Scholar 

  • Kimoto Nira H, Suzuki C, Kobayashi M, Sasaki K, Kurisaki J, Mizumachi K (2007) Anti-ageing effect of a Lactococcal strain: analysis using senescence-accelerated mice. Br J Nutr 98:1178–1186

    CAS  PubMed  Google Scholar 

  • Krampe RT (2002) Aging, expertise and fine motor movement. Neurosci Biobehav Rev 26:769–776

    PubMed  Google Scholar 

  • Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbial 72:215–224

    CAS  Google Scholar 

  • Kumar M, Kumar A, Nagpal R, Mohania D, Behare P, Verma V, Kumar P, Poddar D, Aggarwal PK, Henry CJ, Jain S, Yadav H (2010) Cancer-preventing attributes of probiotics: an update. Int J Food Sci Nutr 61(5):473–496

    CAS  PubMed  Google Scholar 

  • Landete JM, Gaya P, Rodríguez E, Langa S, Peirotén Á, Medina M, Arqués JL (2017) Probiotic bacteria for healthier aging: immunomodulation and metabolism of phytoestrogens. Biomed Res Int 2017:5939818

    PubMed  PubMed Central  Google Scholar 

  • Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102(31):11070–11075

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47(4):1460–1466

    CAS  PubMed  Google Scholar 

  • Maneerat S, Lehtinen MJ, Childs CE, Forssten SD, Alhoniemi E, Tiphaine M, Yaqoob P, Ouwehand AC, Rastall RA (2014) Consumption of Bifdobacterium lactis Bi-07 by healthy elderly adults enhances phagocytic activity of monocytes and granulocytes. J Nutr Sci 2:e44

    PubMed  PubMed Central  Google Scholar 

  • Martínez de Toda I, Garrido A, Vida C, Gomez-Cabrera MC, Viña J, De la Fuente M (2018) Frailty Quantified by the “Valencia Score” as a Potential Predictor of Lifespan in Mice. J Gerontol A Biol Sci Med Sci 73(10):1323–1329

    PubMed  Google Scholar 

  • Martínez de Toda I, Maté I, Vida C, Cruces J, De la Fuente M (2016) Immune function parameters as markers of biological age and predictors of longevity. Aging 8:3110–3119

    PubMed  Google Scholar 

  • Martínez de Toda I, Vida C, Sanz San Miguel L, De la Fuente M (2019) When will my mouse die? Lifespan prediction based on immune function, redox and behavioral parameters in female mice at the adult age. Mech Ageing Develop 182:111125

    Google Scholar 

  • Martínez de Toda I, Vida C, Garrido A, De la Fuente M (2020) Redox parameters as markers of the rate of aging and predictors of lifespan. J Gerontol A Biol Sci Med Sci 75(4):613–620

    PubMed  Google Scholar 

  • Martínez de Toda I, Vida C, Díaz-Del Cerro E, De la Fuente M (2021) The Immunity Clock. J Gerontol A Biol Sci Med Sci glab 136.

  • Massey V, Williams CH Jr (1965) On the reaction mechanism of yeast glutathione reductase. J Biol Chem 240(11):4470–4480

    CAS  PubMed  Google Scholar 

  • Miquel J, Blasco M (1978) A simple technique for evaluation of vitality loss in aging mice, by testing their muscular coordination and vigor. Exp Gerontol 13(6):389–396

    CAS  PubMed  Google Scholar 

  • Miquel J, Ramírez-Boscá A (2004) Oxidative stress and antioxidant diet supplementation in ageing, atherosclerotic and immune dysfunction processes. Ars Pharm 45(2):91–109

    Google Scholar 

  • Naveed M, Zhou QG, Xu C, Taleb A, Meng F, Ahmed B, Zhang Y, Fukunaga K, Han F (2021) Gut-brain axis: A matter of concern in neuropsychiatric disorders! Prog Neuropsychopharmacol Biol Psychiatry 104:110051

    CAS  PubMed  Google Scholar 

  • Ottman N, Reunanen J, Meijerink M, Pietilä TE, Kainulainen V, Klievink J, Huuskonen L, Aalvink S, Skurnik M, Boeren S, Satokari R, Mercenier A, Palva A, Smidt H, de Vos WM, Belzer C (2017) Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS ONE 12(3):e0173004

    PubMed  PubMed Central  Google Scholar 

  • Pellow S, Chopin P, File SE, Briley M (1985) Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14(3):149–167

    CAS  PubMed  Google Scholar 

  • Puerto M, Guayerbas N, Víctor V, De la Fuente M (2002) Effects of N-acetylcysteine on macrophage and lymphocyte functions in a mouse model of premature ageing. Pharmacol Biochem Behav 73:797–804

    CAS  PubMed  Google Scholar 

  • Salazar N, Arboleya S, Fernández-Navarro T, de Los Reyes-Gavilán CG, Gonzalez S, Gueimonde M (2019) Age-associated changes in gut microbiota and dietary components related with the immune system in adulthood and old age: a cross-sectional study. Nutrients 11(8):1765

    CAS  PubMed Central  Google Scholar 

  • Sharma R, Padwad Y (2020) Probiotic bacteria as modulators of cellular senescence: emerging concepts and opportunities. Gut Microbes 11:335–349

    PubMed  Google Scholar 

  • Shen Q, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of bifidobacterium animalis 01 isolated from centenarians. Curr Microbiol 62:1097–1103

    CAS  PubMed  Google Scholar 

  • Tang W, Xing Z, Li C, Wang J, Wang Y (2017) Molecular mechanisms and in vitro antioxidant effects of Lactobacillus plantarum MA2. Food Chem 221:1642–1649

    CAS  PubMed  Google Scholar 

  • Tappa B, Amao H, Ogasa A, Takahashi KW (1989) Changes in the estrous cycle and number of ovulated and fertilized ova in aging female IVCS mice. Jikken Dobutsu 38(2):115–119

    CAS  PubMed  Google Scholar 

  • Tsai YCh, Cheng LH, Liu YW, Jeng OJ, Lee YK (2021) Gerobiotics: probiotics targeting fundamental aging processes. Biosc Microb Food Health 40:1–11

    CAS  Google Scholar 

  • United Nations Department of Economic and Social Affairs, Population Division (2020) World Population Ageing 2020 Highlights: Living arrangements of older persons (ST/ESA/SER.A/451).

  • van der Lugt B, Rusli F, Lute C, Lamprakis A, Salazar E, Boekschoten MV, Hooiveld GJ, Müller M, Vervoort J, Kersten S, Belzer C, Kok DEG, Steegenga WT (2018) Integrative analysis of gut microbiota composition, host colonic gene expression and intraluminal metabolites in aging C57BL/6J mice. Aging (albany NY) 10(5):930–950

    Google Scholar 

  • Vida C, González EM, De la Fuente M (2014) Increase of oxidation and inflammation in nervous and immune systems with aging and anxiety. Curr Pharm Des 20(29):4656–4678

    CAS  PubMed  Google Scholar 

  • Viveros MP, Arranz L, Hernanz A, Miquel J, De la Fuente M (2007) A model of premature aging in mice based on altered stress-related behavioral response and immunosenescence. NeuroImmunoModulation 14:157–162

    CAS  PubMed  Google Scholar 

  • Zhang L, Qin Q, Liu M, Zhang X, He F, Wang G (2018) Akkermansia muciniphila can reduce the damage of gluco/lipotoxicity, oxidative stress and inflammation, and normalize intestine microbiota in streptozotocin-induced diabetic rats. Pathog Dis. https://doi.org/10.1093/femspd/fty028

    Article  PubMed  Google Scholar 

  • Zhang T, Li Q, Cheng L, Buch H, Zhang F (2019) Akkermansia muciniphila is a promising probiotic. Microb Biotechnol 12(6):1109–1125

    PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Zhao L, Zheng X, Fu T, Guo H, Ren F (2013) Lactobacillus salivarius strain FDB89 induced longevity in Caenorhabditis elegans by dietary restriction. J Microbiol 51:183–188

    PubMed  Google Scholar 

  • Zitka O, Skalickova S, Gumulec J, Masarik M, Adam V, Hubalek J, Trnkova L, Kruseova J, Eckschlager T, Kizek R (2012) Redox status expressed as GSH:GSSG ratio as a marker for oxidative stress in paediatric tumour patients. Oncol Lett 4(6):1247–1253

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would also like to thank Kate Engel for her critical proofreading of the English language of the manuscript.

Funding

This work was supported by the Research Group UCM (910379) to MDLF.

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Authors and Affiliations

  1. Department of Genetics, Physiology and Microbiology (Unity of Animal Physiology), Faculty of Biology, Complutense University of Madrid (UCM), Madrid, Spain

    Estefanía Díaz-Del Cerro, Manuel Lambea, Judith Félix & Mónica De la Fuente

  2. Institute of Investigation 12 de Octubre Hospital (i+12), Madrid, Spain

    Estefanía Díaz-Del Cerro, Judith Félix & Mónica De la Fuente

  3. Department of Microbiology and Biochemistry of Dairy Products, IPLA-CSIC, Diet, Microbiota and Health Group, ISPA, Asturias, Spain

    Nuria Salazar & Miguel Gueimonde

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  1. Estefanía Díaz-Del Cerro
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  2. Manuel Lambea
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  3. Judith Félix
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  4. Nuria Salazar
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  5. Miguel Gueimonde
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Contributions

Conceptualization, MDLF and MG; methodology, EDC, ML, NS and JF; data curation, EDC; writing—original draft preparation, EDC; writing—review and editing, MDLF, MG, EDC and NS. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Mónica De la Fuente.

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The protocol was approved by the Committee on Animal Experimentation of the Complutense University of Madrid, and the animals were treated in accordance with the guidelines of Royal Decree 53/2013 of 1 February 2013 (BOE No. 34) on the protection of animals used for experimentation and other scientific purposes.

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Cerro, E.DD., Lambea, M., Félix, J. et al. Daily ingestion of Akkermansia mucciniphila for one month promotes healthy aging and increases lifespan in old female mice. Biogerontology 23, 35–52 (2022). https://doi.org/10.1007/s10522-021-09943-w

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