Starvation and re-feeding affect Hsp expression, MAPK activation and antioxidant enzymes activity of European Sea Bass (Dicentrarchus labrax)

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 165, Issue 1, 2013, Pages 79-88

  Antonopoulou, Efthimia ^a   Kentepozidou, Elissavet ^a   Feidantsis, Konstantinos ^a   Roufidou, Chrysoula ^a   Despoti, Smaragda ^a   Chatzifotis, Stavros ^b  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b INSTITUTE OF OCEANOGRAPHY   (Greece)

Author keywords

Antioxidant defenses; HSPs; Intestine; Liver; MAPKs; Re feeding; Red and white muscle; Starvation

Indexed keywords

CATALASE; GLUTATHIONE PEROXIDASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ENZYME ACTIVITY; EUROPEAN SEA BASS; FAST MUSCLE; FEEDING BEHAVIOR; FISH; INTESTINE; LIVER; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SLOW MUSCLE; STARVATION; STRESS;

EID: 84875044904     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2013.02.019     Document Type: Article

References (94)

1. Barcellos L.J.G., Marqueze A., Trapp M., Quevedo R.M., Ferreira D. The effects of fasting on cortisol, blood glucose and liver and muscle glycogen in adult jundiá Rhamdia quelen. Aquaculture 2010, 300:231-236.
2. Basu N., Todgham P.A., Ackerman P.A., Bibeau M.R., Nakano K., Schulte P.M., Iwama K.G. Heat shock protein genes and their functional significance in fish. Gene 2002, 295:173-183.
3. Bayir A., Sirkecioglu A., Bayir M., Haliloglu H.I., Kocaman E.M., Aras N.M. Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: Oxidative stress and antioxidant defenses. Comp. Biochem. Physiol. B 2012, 159:191-196.
4. Beamish F.W.H. Influence of starvation on standard and routine oxygen consumption. Trans. Am. Fish. Soc. 1964, 93:103-107.
5. Bilden W.N., Wang Z., Iserovich P., Reinach P.S. Hypertonically induced p38 MAPK activation elicits recovery of corneal epithelial cell volume and layer integrity. J. Membr. Biol. 2003, 193:1-13.
6. Bonamusa L., García de Frutos P., Fernandez F., Baanante I.V. Nutritional effects on key glycolitic-gluconeogenic enzyme activities and metabolite levels in the liver of the teleost fish Sparus aurata. Mol. Mar. Biol. Biotechnol. 1992, 1:113-125.
7. Boujard T., Gelineau A., Corraze G. Time of a single daily meal influences growth performance in rainbow trout (Oncorhynchus mykiss). Aquacult. Res. 1995, 26:341-349.
8. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Meth. Enzymol. 1978, 52:302-310.
9. Cano E., Mahadevan L.C. Parallel signal processing among mammalian MAPKs. Trends Biochem. Sci. 1995, 20:117-122.
10. Cara J.B., Aluru N., Moyano F.J., Vijayan M.M. Food deprivation induces hsp70 and hsp90 protein expression in larval gilthead sea bream and rainbow trout. Comp. Biochem. Physiol. B 2005, 142:426-431.
11. Caruso G., Maricchiolo G., Micale V., Genovese L., Caruso R., Denaro M.G. Physiological responses to starvation in the European eel (Anguilla anguilla): effects on haematological, biochemical, non-specific immune parameters and skin structures. Fish Physiol. Biochem. 2010, 36:71-83.
12. Chang H., Siegel B.Z., Siegel S.M. Salinity induced changes in isoperoxidase in taro, Colocasia esculenta. Phytochemistry 1984, 23:233-235.
13. Chatzifots S., Papadaki M., Despoti S., Roufidou C., Antonopoulou E. Effect of starvation and re-feeding on reproductive induces, body weight, plasma metabolites and oxidative enzymes of sea bass (Dicentrarchus labrax). Aquaculture 2011, 316:53-59.
14. Cohen G., Dembiec D., Marcus J. Measurement of catalase activity in tissue extracts. Anal. Biochem. 1970, 34:30.
15. Cook J.T., Sutterlin A.M., McNiven M.A. Effect of food deprivation on oxygen consumption and body composition of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture 2000, 188:47-63.
16. Currie S., Tufts B.L. Synthesis of stress protein 70 in rainbow trout (Onkorhynchus mykiss) red blood cells. J. Exp. Biol. 1997, 200:607-614.
17. Currie S., Moyes C.D., Tufts B. The effects of heat shock and acclimation temperature on hsp 70 and hsp30 mRNA expression in rainbow trout: in vivo and in vitro comparisons. J. Fish Biol. 2000, 56:398-408.
18. Davies K.J.A. Protein damage and degredation by oxygen radicals I. General aspects. Biol. Chem. 1987, 262:9895-9901.
19. Davis R.J. MAPKs: New JNK expands the group. Trends Biochem. Sci. 1994, 19:470-473.
20. Deane E.E., Woo N.Y.S. Ontogeny of thyroid hormones, cortisol, hsp70 and hsp90 during silver sea bream larval development. Life Sci. 2003, 72:805-818.
21. Deng D.F., Wang C.F., Lee S.H., Bai S.C., Hung S.S.O. Feeding rates affect heat shock protein levels in liver of larval white sturgeon (Acipenser transmontanus). Aquaculture 2009, 287:223-226.
22. Dietz T. Acclimation of the threshold induction temperatures for hsp 70 and hsp 90 in the fish Gyllicthys mirabilis. J. Exp. Biol. 1994, 188:333-338.
23. Domenicali M., Caraceni P., Vendemiale G., Grattagliano I., Nardo B., Dall'Agata M., Santoni B., Trevisani F., Cavallari A., Altomare E., Bernardi M. Food deprivation exacerbates mitochondrial oxidative stress in rat liver exposed to ischemia-reperfusion injury. J. Nutr. 2001, 131:105-110.
24. Echevarria G., Zarauz N., Lopez R.J., Zamora S. Study of nitrogen excretion in the gilthead seabream (Sparus aurata L.): influence of nutritional state. Comp. Biochem. Physiol. A 1995, 105:17-19.
25. Egan S.E., Weinberg R.A. The pathway to signal achievement. Nature 1993, 365:781-783.
26. Feder M.E., Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response. Annu. Rev. Physiol. 1999, 61:243-282.
27. Feidantsis K., Pörtner H.O., Lazou A., Kostoglou B., Michaelidis B. Metabolic and molecular stress responses of the gilthead sea bream Sparus aurata during long term exposure to increasing temperatures. Mar. Biol. 2009, 156:797-809.
28. Feidantsis K., Antonopoulou E., Lazou A., Pörtner H.O., Michaelidis B. Seasonal variations of cellular stress response of the gilthead sea bream (Sparus aurata). J. Comp. Physiol. B 2012, 10.1007/s00360-012-0735-y.
29. Feidantsis K., Pörtner H.O., Markou T., Lazou A., Michaelidis B. 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. A 2012, 317:303-310.
30. Feidantsis, K., Kaitetzidou, E., Mavrogiannis, N., Michaelidis, B., Kotzamanis, Y., Antonopoulou, E., submitted for publication. Effect of taurine enriched diets on the Hsp expression, MAPK activation and the antioxidant defences of the European Sea Bass (Dicentrarchus labrax). Aquac. Nutr.
31. Fridovich I. Biological effects of the superoxide radical. Arch. Biochem. Biophys. 1986, 247:1-11.
32. Fujii R., Yamashita S., Hibi M., Hirano T. Asymmetric p38 activation in zebrafish: its possible role in symmetric and synchronous cleavage. J. Cell Biol. 2000, 150:1335-1348.
33. Furné M., García-Gallego M., Hidalgo M.C., Morales A.E., Domezain A., Domezain J., Sanz A. Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquacult. Nutr. 2009, 15:587-595.
34. García de Frutos P., Bonamusa L., Fernandez F., Baanante I.V. Fructose 2,6-biphosphatase in liver of Sparus aurata: influence of nutritional state. Comp. Biochem. Physiol. B 1990, 96:63-65.
35. Glass N.R. The effect of time of food deprivation on the routine oxygen consumption of largemouth black bass (Micropterus salmoides). Ecology 1968, 49:340-343.
36. Goldman D., Sapru M.K., Stewart S., Plotkin J., Libermann T.A., Wasylyk B., Guan K. Cloning and characterization of GETS-1, a goldfish Ets family member that functions as a transcriptional repressor in muscle. Biochem. J. 1998, 335:267-275.
37. Gornati R., Papis E., Rimoldi S., Terova G., Saroglia M., Bernardini G. Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax L.). Gene 2004, 341:111-118.
38. Guderley H., Lapointe D., Bédarda M., Jean-Denis Dutil J.-D. Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp. Biochem. Physiol. A 2003, 135:347-356.
39. Han D., Huang S.S.Y., Wang W.-F., Deng D.-F., Hung S.S.O. Starvation reduces the heat shock protein responses in white sturgeon larvae. Environ. Biol. Fish. 2012, 93:333-342.
40. Hashimoto H., Matsuo Y., Yokoyama Y., Toyohara H., Sakaguchi M. Structure and expression of carp mitogen-activated protein kinases homologous to mammalian JNK/SAPK. J. Biochem. (Tokyo) 1997, 122:381-386.
41. Hashimoto H., Yokoyama Y., Matsuo Y., Toyohara H., Kohno M., Sakaguchi M. Existence of two isoforms of extracellular signal regulated kinase in fish. J. Biochem. (Tokyo) 1998, 123:1031-1035.
42. Hashimoto H., Fukuda M., Matsuo Y., Yokoyama Y., Nishida E., Toyohara H., Sakaguchi M. Identification of a nuclear export signal of MKK6, an activator of the carp p38 mitogen activated protein kinases. Eur. J. Biochem. 2000, 267:4362-4371.
43. Heydari A.R., Wu B., Takahashi R., Strong R., Richardson A. Expression of heat shock protein 70 is altered by age and diet at the level of transcription. Mol. Cell. Biol. 1993, 13:2909-2918.
44. Heydari A.R., Conrad C.C., Richardson A. Expression of heat shock genes in hepatocytes is affected by age and food restriction in rats. J. Nutr. 1995, 125:410-418.
45. Hidalgo M.C., Expósito A., Palma J.M., de la Higuera M. Oxidative stress generated by dietary Zn-deficiency: studies in rainbow trout (Oncorhynchus mykiss). Int. J. Biochem. Cell Biol. 2002, 34:183-193.
46. Ibarz A., Martin-Perez M., Blasco J., Bellido D., de Oliveira E., Fernandez-Borras J. Gilthead sea bream liver proteome altered at low temperatures by oxidative stress. Proteomics 2010, 10:963-975.
47. Imlay J.A., Linn S. DNA damage and oxygen radical toxicity. Science 1988, 240:1302-1309.
48. Iwama G.K., Thomas P., Vijayan M.M., Forsyth R.B. Stress proteins expression in fish. Rev. Fish Biol. Fish. 1998, 8:35-56.
49. Iwama K.G., Afonso O.B.L., Todgham A., Ackerman P., Nakano K. Are hsp's suitable for indicating stressed states in fish?. J. Exp. Biol. 2003, 207:15-19.
50. Jürss K., Bittorf Th., Vökler Th., Wacke R. Effects of temperature, food deprivation and salinity on growth, RNA/DNA ratio certain enzyme activities in rainbow trout (Salmo gairdnieri Richardson). Comp. Biochem. Physiol. B 1987, 87:241-253.
51. Kassahn K.S., Crozier R.S., Pörtner H.O., Caley M.J. Animal performance and stress responses and tolerance limits at different levels of biological organisation. Biol. Rev. 2009, 84:277-292.
52. Kultz D., Avila K. Mitogen activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp. Biochem. Physiol. B 2001, 129:821-829.
53. Leal B.R., Ribeiro J.S., Posser T., Cordova M.F., Rigon P.A., Filho Z.E., Bainy D.C.A. Modulation of ERK1/2 and p38MAPK by lead in the cerebellum of Brazilian catfish Rhamdia quelen. Aquat. Toxicol. 2006, 77:98-104.
54. Liu P.T., Ioannides C., Shavila J., Symons A.M., Parke D.V. Effects of ether anesthesia and fasting on various cytochromes P450 of rat liver and kidney. Biochem. Pharmacol. 1993, 45:871-877.
55. MacDougal K.G., Merickob P.A., Burnett K.G. Antigen receptor-mediated activation of extracellular related kinase (ERK) in B lymphocytes of teleost fishes. Biochim. Biophys. Acta 1984, 783:137-143.
56. Madrid J.A., Boujard T., Sanchez-Vazquez F.J. Feeding rhythms. Food intake in fish 2001, 189-215. Blackwell Science, UK. D. Houlihan, T. Boujard, M. Jobling (Eds.).
57. Marshall W.S., Ossum C.G., Hoffmann E.K. Hypotonic shock mediation by p38 MAPK, JNK, PKC, FAK, OSR1 and SPAK in osmosensing chloride secreting cells of killifish opercular epithelium. J. Exp. Biol. 2005, 208:1063-1077.
58. Mazeaud M.M., Mazeaud F., Donaldson E.M. Primary and secondary effects of stress in fish: some new data with a general review. Trans. Am. Fish. Soc. 1977, 106:201-212.
59. Metón I., Fernández F., Baanant I.V. Short- and long-term effects of refeeding on key enzyme activities in glycolysis-gluconeogenesis in the liver of gilthead seabream (Sparus aurata). Aquaculture 2003, 225:99-107.
60. Moody C.S., Hassan H.M. Anaerobic biosynthesis of the manganese-containing superoxide dismutase in Escherichia coli. J. Biol. Chem. 1984, 259:12821-12825.
61. Morales A.E., Pérez-Jiménez A., Hidalgo M.C., Abellan E., Cardenete G. Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp. Biochem. Physiol. C 2004, 139:153-161.
62. Nishida E., Gotoh Y. The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci. 1993, 18:128-131.
63. Olsen R.E., Sundell K., Ringø E., Myklebust R., Hemre G.-I., Hansen T., Karlsen Ø. The acute stress response in fed and food deprived Atlantic cod, Gadus morhua L. Aquaculture 2008, 280:232-241.
64. Paglia D.E., Valentin W.N. Studies on quantitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 1967, 70(1):158.
65. Pannevis M.C., Houlihan D.F. The energetic cost of protein synthesis in isolated hepatocytes of rainbow trout (Oncorhynchus mykiss). J. Comp. Physiol. B 1992, 162:393-400.
66. Paoletti F., Mocali A. Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Meth. Enzymol. 1990, 186:209-220.
67. Pascual P., Pedrajas J.R., Toribio F., Lopez-Barea J., Peinado J. Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem. Biol. Interact. 2003, 145:191-199.
68. Paterson P.G., Lyon A.W., Kamencic H., Andersen L.B., Juurlink B.H. Sulfur amino acid deficiency depresses brain glutathione concentration. Nutr. Neurosci. 2001, 4:213-222.
69. Pérez-Jiménez A., Guedes M.J., Morales A.E., Oliva-Teles A. Metabolic responses to short starvation and refeeding in Dicentrarchus labrax. Effect of dietary composition. Aquaculture 2007, 265:325-335.
70. Pérez-Jiménez A., Cardenete G., Hidalgo M.C., García-Alcázar A., Abellán E., Morales A.E. Metabolic adjustments of Dentex dentex to prolonged starvation and refeeding. Fish Physiol. Biochem. 2012, 38:1145-1157.
71. Pörtner H.O. Climate change and temperature dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 2001, 88:137-146.
72. Pörtner H.O. Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp. Biochem. Physiol. A 2002, 132:739-761.
73. Pörtner H.O., Farrell A.P. Ecology: physiology and climate change. Science 2008, 322:690-692.
74. Rios F.S., Kalinin A.L., Rantin F.T. The effects of long-term food deprivation on respiration and haematology of the neotropical fish Hoplias malabaricus. J. Fish Biol. 2002, 61:85-95.
75. Robinson M.K., Rustum R.R., Chambers E.A., Rounds J.D., Wilmore D.W., Jacobs D.O. Starvation enhances hepatic free radical release following endotoxemia. J. Surg. Res. 1997, 69:325-330.
76. Ronnestad I., Conceicao L.E., Aragao C., Dinis M.T. Free amino acids are absorbed faster and assimilated more efficiently than protein in post larval Senegal sole (Solea senegalensis). J. Nutr. 1999, 130:2809-2812.
77. Salach J.I. Preparation of monoamine oxidase from beef liver mitochondria. Meth. Enzymol. 1978, 53:495-501.
78. Sanders B.M. Stress protein in aquatic organisms: an environmental perspective. Crit. Rev. Toxicol. 1993, 23:49-75.
79. Sheridan M.A., Mommsen T.P. Effects of nutritional state on vivo lipid and carbohydrate metabolism of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 1991, 81:473-483.
80. Snaar-Jagalska B.E., Krens S.F., Robina I., Wang L.X., Spaink H.P. Specific activation of ERK pathways by chitin oligosaccharides in embryonic zebrafish cell lines. Glycobiology 2003, 13:725-732.
81. Stead D., Park S.F. Roles of Fe superoxide dismutase and catalase in resistance of Campylobacter coli to freeze-thaw stress. Appl. Environ. Microbiol. 2000, 66:3110-3112.
82. Encyclopedia of Aquaculture 2000, John Wiley & Sons, Inc., Toronto, Canada, (1063 pp.). R.R. Stickney (Ed.).
83. Tripathi G., Priyanka V. Scaling effects on metabolism of a teleost. J. Exp. Zool. 2004, 301A:718-726.
84. Tuckey N., Davison W. Mode of locomotion places selective pressures on Antarctic and temperate labriform swimming fish. Comp. Biochem. Physiol. A 2004, 138:391-398.
85. Valavanidis A., Vlahogianni T., Dassenakis M., Scoullos M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol. Environ. Saf. 2006, 64:178-189.
86. Vijayan M.M., Aluru N., Maule A.G., Jørgensen E.V. Fasting augments PCB impact on liver metabolism in anadromous arctic char. Toxicol. Sci. 2006, 91:431-439.
87. Vogt B.L., Richie J.P. Fasting-induced depletion of glutathione in the aging mouse. Biochem. Pharmacol. 1993, 46:257-263.
88. Weatherly A.H., Gill H.S. The Biology of Fish Growth 1981, Academic Press, London.
89. Weber T.E., Bosworth B.G. Effects of 28day exposure to cold temperature or feed restriction on growth, body composition, and expression of genes related to muscle growth and metabolism in channel catfish. Aquaculture 2005, 246:483-492.
90. Wedemeyer G.A., Barton B.A., McLeay D.J. Stress and acclimation. Methods for Fish Biology 1990, 451-489. American Fisheries Society, Bethesda, MD. C.B. Schreck, P.B. Moyle (Eds.).
91. Wright C.E., Talan H.H., Lin Y.Y., Coaull G.E. Taurine: biological update. Annu. Rev. Biochem. 1986, 55:427-453.
92. Yengkokpam S., Pal A.K., Sahu N.P., Jain K.K., Dalvi R., Misra S., Debnath D. Metabolic modulation in Labeo rohita fingerlings during starvation: Hsp70 expression and oxygen consumption. Aquaculture 2008, 285:234-237.
93. Yokoyama M., Nakazoe J.-I. Effects of dietary protein levels on free amino acid and glutathione contents in the tissues of rainbow trout. Comp. Biochem. Physiol. A 1991, 99:203-206.
94. Zarate J., Bradley T.M. Heat shock proteins are not sensitive indicators of hatchery stress in salmon. Aquaculture 2003, 223:175-187.