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Seasonal variations of cellular stress response of the gilthead sea bream (Sparus aurata)

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Abstract

The present study aimed to investigate the seasonal cellular stress response in vital organs, like the heart, the liver, the whole blood and the skeletal (red and white) muscles of the Mediterranean fish Sparus aurata during a 1-year acclimatization period in the field, in two examined depths (0–2 m and 10–12 m). Processes studied included heat shock protein expression and protein kinase activation. Molecular responses were addressed through the expression of Hsp70 and Hsp90, the phosphorylation of stress-activated protein kinases and particularly p38 mitogen-activated protein kinase (p38 MAPK), the extracellular signal-regulated kinases (ERK-1/2) and c-Jun N-terminal kinases (JNK1/2/3). The induction of Hsp70 and Hsp90 and the phosphorylation of p38 MAPK, JNKs and ERKs in the examined five tissues of the gilthead sea bream indicated a cellular stress response under the prism of a seasonal pattern which was characterized by distinct tissue specificity. Specifically, Hsp induction and MAPK activation occurred before peak summer water temperatures, with no further increases in their levels despite increases in water temperatures. Moreover, although water temperature did not vary significantly with depth of immersion, significant effects of depth on cellular stress response were observed, probably caused by different light regime. The expression and the activation of these certain proteins can be used as tools to define the extreme thermal limits of the gilthead sea bream.

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References

  • Adams SM (1990) Status and use of bioindicators for evaluating effects of chronic stress on fish. Am Fish Soc Sym 8:1–8

    Google Scholar 

  • Ali KS, Dorgai L, Abraham M, Hermesz E (2003) Tissue- and stressor-specific differential expression of two hsc70 genes in carp. Biochem Biophys Res Comm 307:503–509

    Article  PubMed  CAS  Google Scholar 

  • Anestis A, Pörtner HO, Lazou A, Michaelidis B (2008) Metabolic and molecular stress responses of sublittoral bearded horse mussel Modiolus barbatus to warming sea water: implications for vertical zonation. J Exp Biol 211:2889–2898

    Article  PubMed  CAS  Google Scholar 

  • Arias A (1976) Sobre la biología de la dorada, Sparus aurata L., de los esteros de la provincia de Cádiz Inv Pesq 40:201–222

  • Balm PHM, Pepels P, Helfrich S, Hovens MLM, Wendelaar Bonga SE (1994) Adrenocorticotropic hormone in relation to interrenal function during stress in tilapia (Oreochromis mossambicus). Gen Comp Endocrinol 96:347–360

    Article  PubMed  CAS  Google Scholar 

  • Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama KG (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183

    Article  PubMed  CAS  Google Scholar 

  • Bayarri MJ, Madrid JA, Sanchez-Vazquez FJ (2002) Influence of light intensity, spectrum and orientation on sea bass plasma and ocular melatonin. J Pineal Res 32:34–40

    Article  PubMed  CAS  Google Scholar 

  • Blazer VS (2002) Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 26:85–101

    Article  CAS  Google Scholar 

  • Boulcott PD, Walton K, Braithwaite VA (2005) The role of ultraviolet wavelengths in the mate-choice decisions of female threespined sticklebacks. J Exp Biol 208:1453–1458

    Article  PubMed  CAS  Google Scholar 

  • Bovo G, Olesen NJ, Jorgensen PEV, Ahne W, Winton JR (1995) Characterization of a rhabdovirus isolated from carpione Salmo trutta carpio in Italy. Dis Aquat Org 21(2):115–122

    Article  Google Scholar 

  • Buckley BA, Hofmann GE (2002) Thermal acclimation changes DNA-binding activity of heat shock factor (HSF1) in the goby Gillichthys mirabilis: implications for plasticity in the heat-shock response in natural populations. J Exp Biol 205:3231–3240

    PubMed  CAS  Google Scholar 

  • Buckley BA, Hofmann EG (2004) Magnitude and duration of thermal stress determine kinetics of hsp gene regulation in the goby Gillicthys mirabilis. Physiol Biochem Zool 77(4):570–581

    Article  PubMed  CAS  Google Scholar 

  • Calvo N, Marsh DR (2011) The combined effects of ENSO and the 11 year solar cycle on the Northern Hemisphere polar stratosphere. J Geoph Res 116:1–14

    Google Scholar 

  • Cano E, Mahadevan LC (1995) Parallel signal processing among mammalian MAPKs. Trend Biochem Sci 20:117–122

    Article  PubMed  CAS  Google Scholar 

  • Currie S, Tufts BL (1997) Synthesis of stress protein 70 in rainbow trout (Onkorhynchus mykiss) red blood cells. J Exp Biol 200:607–614

    PubMed  CAS  Google Scholar 

  • Currie S, Moyes CD, Tufts BL (2000) The effects of heat shock and acclimation temperature on hsp70 and hsp30 mRNA expression in rainbow trout: in vivo and in vitro comparisons. J Fish Biol 56:398–408

    Article  CAS  Google Scholar 

  • Currie S, Reddin K, McGinn P, McConnell T, Perry S (2008) Adrenergic stimulation enhances the heat-shock response in fish. Physiol Biochem Zool 81:414–425

    Article  PubMed  CAS  Google Scholar 

  • Davis RJ (1994) MAPKs: new JNK expands the group. Trend Biochem Sci 19:470–473

    Article  PubMed  CAS  Google Scholar 

  • Deane EE, Woo NYS (2003) Ontogeny of thyroid hormones, cortisol, hsp70 and hsp90 during silver sea bream larval development. Life Sci 72:805–818

    Article  PubMed  CAS  Google Scholar 

  • Dietz T (1994) Acclimation of the threshold induction temperatures for hsp 70 and hsp 90 in the fish Gillicthys mirabilis. J Exp Biol 188:333–338

    PubMed  CAS  Google Scholar 

  • Dietz T, Somero GN (1992) The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). Proc Natl Acad Sci USA 89:3389–3393

    Article  PubMed  CAS  Google Scholar 

  • Doimi M (1996) A new winter disease in sea bream (Sparus aurata): a preliminary report. Bull Eur Assoc Fish Pathol 16:17–18

    Google Scholar 

  • Downing G (2002) Impact of spectral composition on larval haddock, Melanogrammus aeglefinus L., growth and survival. Aquacult Res 33:251–259

    Article  Google Scholar 

  • Downing G, Litvak MK (2001) The effect of light intensity and spectrum on the incidence of first feeding by larval haddock. J Fish Biol 59:1566–1578

    Article  Google Scholar 

  • Egan SE, Weinberg RA (1993) The pathway to signal achievement. Nature 365:781–783

    Article  PubMed  CAS  Google Scholar 

  • Fader S, Yu Z, Spotila JR (1994) Seasonal variation in heat shock proteins (Hsp70) in stream fish under natural conditions. J Therm Biol 19(5):335–341

    Article  CAS  Google Scholar 

  • Feidantsis K, Pörtner HO, Lazou A, Kostoglou B, Michaelidis B (2009) Metabolic and molecular stress responses of the gilthead sea bream Sparus aurata during long term exposure to increasing temperatures. Mar Biol 156:797–809

    Article  CAS  Google Scholar 

  • Feidantsis K, Pörtner HO, Markou T, Lazou A, Michaelidis B (2012) Involvement of p38 MAPK in the induction of Hsp70 during acute thermal stress in red blood cells of the gilthead sea bream, Sparus aurata. J Exp Zool Part A 317:303–310

    Article  CAS  Google Scholar 

  • Fujii R, Yamashita S, Hibi M, Hirano T (2000) Asymmetric p38 activation in zebrafish: its possible role in symmetric and synchronous cleavage. J Cell Biol 150:1335–1348

    Article  PubMed  CAS  Google Scholar 

  • Gambaiani DD, Mayol P, Isaac SJ, Simmonds MP (2009) Potential impacts of climate change and greenhouse gas emissions on Mediterranean marine ecosystems and cetaceans. J Mar Biol Assoc UK 89(1):179–201

    Article  CAS  Google Scholar 

  • Giri SS, Sahoo SK, Sahu BB, Sahu AK, Mohanty SN, Mukhopadhyay PK, Ayyappan S (2002) Larval survival and growth in Wallagoattu (Bloch and Schneider): effects of light, photoperiod and feeding regimes. Aquaculture 213:151–161

    Article  Google Scholar 

  • Goldman D, Sapru MK, Stewart S, Plotkin J, Libermann TA, Wasylyk B, Guan K (1998) Cloning and characterization of GETS-1, a goldfish Ets family member that functions as a transcriptional repressor in muscle. Biochem J 335(Pt 2):267–275

    PubMed  CAS  Google Scholar 

  • Gornati R, Papis E, Rimoldi S, Terova G, Saroglia M, Bernardini G (2004) Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax L.). Gene 341:111–118

    Article  PubMed  CAS  Google Scholar 

  • Grad I, Picard D (2007) The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol 275:2–12

    Article  PubMed  CAS  Google Scholar 

  • Greenway SC, Storey KB (2000) Activation of mitogen-activated protein kinases during natural freezing and thawing in the wood frog. Mol Cell Biochem 209:29–37

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto H, Matsuo Y, Yokoyama Y, Toyohara H, Sakaguchi M (1997) Structure and expression of carp mitogen-activated protein kinases homologous to mammalian JNK/SAPK. J Biochem (Tokyo) 122:381–386

    Article  CAS  Google Scholar 

  • Hashimoto H, Yokoyama Y, Matsuo Y, Toyohara H, Kohno M, Sakaguchi M (1998) Existence of two isoforms of extracellular signal regulated kinase in fish. J Biochem (Tokyo) 123:1031–1035

    Article  CAS  Google Scholar 

  • Hashimoto H, Fukuda M, Matsuo Y, Yokoyama Y, Nishida E, Toyohara H, Sakaguchi M (2000) Identification of a nuclear export signal of MKK6, an activator of the carp p38 mitogen activated protein kinases. Eur J Biochem 267:4362–4371

    Article  PubMed  CAS  Google Scholar 

  • Head AB, Malison JA (2000) Effects of lighting spectrum and disturbance level on the growth and stress responses of yellow perch Perca flavescens. J World Aquacult Soc 31:73–80

    Article  Google Scholar 

  • Helmuth B (2009) From cells to coastlines: how can we use physiology to forecast the impacts of climate change? J Exp Biol 212:753–760

    Article  PubMed  Google Scholar 

  • Helmuth B, Broitman BR, Yamane L, Gilman SE, Mach K, Mislan KAS, Denny MW (2010) Organismal climatology: analyzing environmental variability at scales relevant to physiological stress. J Exp Biol 213:955–1003

    Article  Google Scholar 

  • Hermes-Lima M, Storey KB (1996) Relationship between anoxia exposure and antioxidant status in the frog Rana pipiens. Am J Physiol 271:R918–R925

    PubMed  CAS  Google Scholar 

  • Hermes-Lima M, Storey KB (1998) Role of antioxidant defences in the tolerance of severe dehydration by anurans. The case of the leopard frog Rana pipiens. Mol Cell Biochem 189:79–89

    Article  PubMed  CAS  Google Scholar 

  • Hoffman J, Katz U (1997) Salt and water balance in the toad Bufo viridis during recovery from two different osmotically stressful conditions. Comp Biochem Physiol A 117(1):147–154

    Article  CAS  Google Scholar 

  • Hofmann GE (2005) Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255

    Article  PubMed  CAS  Google Scholar 

  • Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Ann Rev Physiol 72:127–145

    Article  CAS  Google Scholar 

  • Ibarz J, Fernαndez-Borrΰs J, Blasco MA, Gallardo G, Sanchez J (2003) Oxygen consumption and feeding rates of gilthead sea bream (Sparus aurata) reveal lack of acclimation to cold. Fish Physiol Biochem 29:313–321

    Article  CAS  Google Scholar 

  • Ibarz A, Martin-Perez M, Blasco J, Bellido D, de Oliveira E, Fernandez-Borras J (2010a) Gilthead sea bream liver proteome altered at low temperatures by oxidative stress. Proteomics 10(5):963–975

    PubMed  CAS  Google Scholar 

  • Ibarz A, Padros F, Gallardo MA, Fernandez-Borras J, Blasco J, Tort L (2010b) Low-temperature challenges to gilthead sea bream culture: review of cold-induced alterations and ‘Winter Syndrome’. Rev Fish Biol Fisher 20(4):539–556

    Article  Google Scholar 

  • Iwama GK (1999) Stress in fish. Stress of life: from molecules to man. Ann NY Acad Sci 851:304–310

    Article  Google Scholar 

  • Iwama KG, Thomas TP, Forsyth BR, Vijayan MM (1998) Heat shock expression in fish. Rev Fish Biol Fish 8:35–56

    Article  Google Scholar 

  • Ju Z, Dunham RA, Liu Z (2002) Differential gene expression in the brain of channel catfish (Ictalurus punctatus) in response to cold acclimation. Mol Gen Genomics 268(1):87–95

    Article  CAS  Google Scholar 

  • Kassahn KS, Crozier RS, Pörtner HO, Caley MJ (2009) Animal performance and stress responses and tolerance limits at different levels of biological organisation. Biol Rev 84:277–292

    Article  PubMed  Google Scholar 

  • Kultz D, Avila K (2001) Mitogen activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp Biochem Physiol B 129:821–829

    Article  PubMed  CAS  Google Scholar 

  • Kyprianou TD, Pörtner HO, Anestis A, Kostoglou B, Feidantsis K, Michaelidis B (2010) Metabolic and molecular stress responses of gilthead seam bream Sparus aurata during exposure to low ambient temperature: an analysis of mechanisms underlying the winter syndrome. J Comp Physiol B 180:1005–1018

    Article  PubMed  CAS  Google Scholar 

  • Kyriakis JM, Avruch J (2001) Mammalian mitogen activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869

    PubMed  CAS  Google Scholar 

  • LeBlanc S, Höglund E, Gilmour KM, Currie S (2012) Hormonal modulation of the heat shock response: insights from fish with divergent cortisol stress responses. Am J Physiol Regul Integr Comp Physiol 302:R184–R192

    Article  PubMed  CAS  Google Scholar 

  • Lewis TS, Shapiro PS, Ahn NG (1998) Signal transduction through MAP kinase cascades. Adv Cancer Res 74:49–139

    Article  PubMed  CAS  Google Scholar 

  • Logan CA, Somero GN (2010) Transcriptional responses to thermal acclimation in the eurythermal fish Gillichthys mirabilis (Cooper 1864). Am J Physiol Regul Integr Comp Physiol 299:R843–R852

    Article  PubMed  CAS  Google Scholar 

  • MacDougal KG, Merickob PA, Burnett KG (1984) Antigen receptor-mediated activation of extracellular related kinase (ERK) in B lymphocytes of teleost fishes. BBA 783:137–143

    Article  Google Scholar 

  • Marchesan M, Spoto M, Verginella L, Ferrero EA (2005) Behavioural effects of artificial light on fish species of commercial interest. Fish Res 73:171–185

    Article  Google Scholar 

  • Mazeaud MM, Mazeaud F, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data with a general review. Trans Am Fish Soc 106:201–212

    Article  CAS  Google Scholar 

  • Mehanna SF (2007) A preliminary assessment and management of gilthead bream Sparus aurata in the Port Said Fishery, the Southeastern Mediterranean, Egypt. Turk J Fish Aquat Sci 7:123–130

    Google Scholar 

  • Murphy SJ, Song D, Welsh FA, Wilson DF, Pastuszko A (1996) The effect of hypoxia and catecholamines on regional expression of heat-shock protein-72 mRNA in neonatal piglet brain. Brain Res 727:145–152

    Article  PubMed  CAS  Google Scholar 

  • Naor A, Segev N, Bressler K, Peduel A, Hadas E, Ron B (2003) The influence of the pineal organ and melatonin on the reproductive system and of light intensity and wavelength on melatonin in the gilthead sea bream (Sparus aurata). Isr J Aquacult 55:230

    Google Scholar 

  • Nicholls RJ, Hoozemans FMJ (1996) The Mediterranean: vulnerability to coastal implication of climate change. Ocean Coast Manage 31(2–3):105–132

    Article  Google Scholar 

  • Nishida E, Gotoh Y (1993) The MAP kinase cascade is essential for diverse signal transduction pathways. Trend Biochem Sci 18:128–131

    Article  PubMed  CAS  Google Scholar 

  • Nolan M, Jobling S, Brighty G, Sumpter JP, Tyler CR (2001) A histological description of intersexuality in the roach. J Fish Biol 58:160–176

    Article  Google Scholar 

  • Paroo Z, Noble EG (1999) Isoproteronol potentiates exercise-induction of Hsp70 in cardiac and skeletal muscle. Cell Stress Chap 4:199–204

    CAS  Google Scholar 

  • Piñeiro C, Cañas B, Carrera M (2010) The role of proteomics in the study of the influence of climate change on seafood products. Food Res Int 43:1791–1802

    Article  Google Scholar 

  • Place SP, Hofmann GE (2005) Function and expression of the molecular chaperone HSP70 in Antarctic fishes. FASEB J 19:A214–A214

    Google Scholar 

  • Place SP, Zippay ML, Hofmann GE (2004) Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fishes. Am J Physiol Regul Integr Comp Physiol 287:R429–R436

    Article  PubMed  CAS  Google Scholar 

  • Pörtner HO (2001) Climate change and temperature dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Article  PubMed  Google Scholar 

  • Pörtner HO (2002a) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761

    Google Scholar 

  • Pörtner HO (2002b) Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J Exp Biol 205:2217–2230

    PubMed  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692

    Article  PubMed  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the Oxygen Limitation of Thermal Tolerance. Science 315:95–97

    Article  PubMed  Google Scholar 

  • Pörtner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779

    Article  PubMed  Google Scholar 

  • Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122–132

    Article  PubMed  CAS  Google Scholar 

  • Presnell JK, Schreibman MP (1997) Humason’s animal tissue techniques. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Ruchin AB (2001) Some peculiarities of the fish young growth under light-gradient conditions. J Evol Biochem Physiol 37:312–313

    Article  Google Scholar 

  • Ruchin AB (2004) Influence of colored light on growth rate of juveniles of fish. Fish Physiol Biochem 30:175–178

    Article  CAS  Google Scholar 

  • Smith LS, Bell GR (1964) A technique for prolonged blood sampling in free-swimming salmon. J Fish Res Board Can 21(4):711

    Article  Google Scholar 

  • Snaar-Jagalska BE, Krens SF, Robina I, Wang LX, Spaink HP (2003) Specific activation of ERK pathways by chitin oligosaccharides in embryonic zebrafish cell lines. Glycobiology 13:725–732

    Article  PubMed  CAS  Google Scholar 

  • Somero GN (1997) Temperature relationships from molecules to biogeography. Hopkins Marine Station, Stanford University, Pacific Grove, California. In: Handbook of Physiology, vol 2, section 13. Comparative Physiology, chapter 19. Oxford University Press, Oxford, pp 1392–1444

  • Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789

    Article  PubMed  Google Scholar 

  • Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920

    Article  PubMed  CAS  Google Scholar 

  • Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annu Rev Mar Sci 4:39–61

    Article  Google Scholar 

  • Szisch V, Van der Salm AL, Wendelaar Bonga SE, Pavlidis M (2002) Physiological colour changes in the red porgy, Pagrus pagrus, following adaptation to blue lighting spectrum. Fish Physiol Biochem 27:1–8

    Article  CAS  Google Scholar 

  • Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species’ biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971–979

    Article  PubMed  CAS  Google Scholar 

  • Tomanek L (2012) Environmental proteomics of the mussel Mytilus: implications for tolerance to stress and change in limits of biogeographical ranges in response to climate change. Integr Comp Biol 52(5):648–664

    Article  PubMed  CAS  Google Scholar 

  • Tort L, Rotllant J, Rovira L (1998) Immunological suppression in gilthead sea bream Sparus aurata of the North-West Mediterranean at low temperatures. Comp Biochem Physiol A 120(1):175–179

    Google Scholar 

  • Tsikliras CA, Torre M, Stergiou IK (2005) Feeding habits and trophic level of round sardinella (Sardinella aurita) in the northeastern Mediterranean (Aegean Sea, Greece). J Biol Res 3:67–75

    Google Scholar 

  • Udelsman R, Blake MJ, Stagg CA, Li DG, Putney J, Holbrook NJ (1993) Vascular heat shock protein expression in response to stress. Endocrine and autonomic regulation of this age-dependent response. J Clin Invest 91:465–473

    Article  PubMed  CAS  Google Scholar 

  • Volpato GL, Barreto RE (2001) Environmental blue light prevents stress in the Nile tilapia. Braz J Med Biol Res 34:1041–1045

    Article  PubMed  CAS  Google Scholar 

  • Wedemeyer GA, Barton BA, McLeay DJ (1990) Stress and acclimation. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 451–489

  • Yamashita M, Yabu T, Ojima N (2010) Stress Protein HSP70 in Fish. ABSM 3(4):111–141

    Google Scholar 

  • Μarshall WS, Ossum CG, Hoffmann EK (2005) Hypotonic shock mediation by p38 MAPK, JNK, PKC, FAK, OSR1 and SPAK in osmosensing chloride secreting cells of killifish opercular epithelium. J Exp Biol 208:1063–1077

    Article  Google Scholar 

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Feidantsis, K., Antonopoulou, E., Lazou, A. et al. Seasonal variations of cellular stress response of the gilthead sea bream (Sparus aurata). J Comp Physiol B 183, 625–639 (2013). https://doi.org/10.1007/s00360-012-0735-y

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