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.
Similar content being viewed by others
References
Adams SM (1990) Status and use of bioindicators for evaluating effects of chronic stress on fish. Am Fish Soc Sym 8:1–8
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
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
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
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
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
Blazer VS (2002) Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 26:85–101
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
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
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
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
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
Cano E, Mahadevan LC (1995) Parallel signal processing among mammalian MAPKs. Trend Biochem Sci 20:117–122
Currie S, Tufts BL (1997) Synthesis of stress protein 70 in rainbow trout (Onkorhynchus mykiss) red blood cells. J Exp Biol 200:607–614
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
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
Davis RJ (1994) MAPKs: new JNK expands the group. Trend Biochem Sci 19:470–473
Deane EE, Woo NYS (2003) Ontogeny of thyroid hormones, cortisol, hsp70 and hsp90 during silver sea bream larval development. Life Sci 72:805–818
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
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
Doimi M (1996) A new winter disease in sea bream (Sparus aurata): a preliminary report. Bull Eur Assoc Fish Pathol 16:17–18
Downing G (2002) Impact of spectral composition on larval haddock, Melanogrammus aeglefinus L., growth and survival. Aquacult Res 33:251–259
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
Egan SE, Weinberg RA (1993) The pathway to signal achievement. Nature 365:781–783
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
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
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
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
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
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
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
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
Grad I, Picard D (2007) The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol 275:2–12
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
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
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
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
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
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
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
Hermes-Lima M, Storey KB (1996) Relationship between anoxia exposure and antioxidant status in the frog Rana pipiens. Am J Physiol 271:R918–R925
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
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
Hofmann GE (2005) Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255
Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Ann Rev Physiol 72:127–145
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
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
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
Iwama GK (1999) Stress in fish. Stress of life: from molecules to man. Ann NY Acad Sci 851:304–310
Iwama KG, Thomas TP, Forsyth BR, Vijayan MM (1998) Heat shock expression in fish. Rev Fish Biol Fish 8:35–56
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
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
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
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
Kyriakis JM, Avruch J (2001) Mammalian mitogen activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869
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
Lewis TS, Shapiro PS, Ahn NG (1998) Signal transduction through MAP kinase cascades. Adv Cancer Res 74:49–139
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
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
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
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
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
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
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
Nicholls RJ, Hoozemans FMJ (1996) The Mediterranean: vulnerability to coastal implication of climate change. Ocean Coast Manage 31(2–3):105–132
Nishida E, Gotoh Y (1993) The MAP kinase cascade is essential for diverse signal transduction pathways. Trend Biochem Sci 18:128–131
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
Paroo Z, Noble EG (1999) Isoproteronol potentiates exercise-induction of Hsp70 in cardiac and skeletal muscle. Cell Stress Chap 4:199–204
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
Place SP, Hofmann GE (2005) Function and expression of the molecular chaperone HSP70 in Antarctic fishes. FASEB J 19:A214–A214
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
Pörtner HO (2001) Climate change and temperature dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146
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
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
Pörtner HO, Farrell AP (2008) Ecology: physiology and climate change. Science 322:690–692
Pörtner HO, Knust R (2007) Climate change affects marine fishes through the Oxygen Limitation of Thermal Tolerance. Science 315:95–97
Pörtner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779
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
Presnell JK, Schreibman MP (1997) Humason’s animal tissue techniques. Johns Hopkins University Press, Baltimore
Ruchin AB (2001) Some peculiarities of the fish young growth under light-gradient conditions. J Evol Biochem Physiol 37:312–313
Ruchin AB (2004) Influence of colored light on growth rate of juveniles of fish. Fish Physiol Biochem 30:175–178
Smith LS, Bell GR (1964) A technique for prolonged blood sampling in free-swimming salmon. J Fish Res Board Can 21(4):711
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
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
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
Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annu Rev Mar Sci 4:39–61
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
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
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
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
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
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
Volpato GL, Barreto RE (2001) Environmental blue light prevents stress in the Nile tilapia. Braz J Med Biol Res 34:1041–1045
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
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
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-012-0735-y