Metabolic molecular indicators of chronic stress in gilthead seabream (Sparus aurata) using comparative proteomics

Aquaculture

Volumn 299, Issue 1-4, 2010, Pages 57-66

  Alves, Ricardo N ^a   Cordeiro, Odete ^a   Silva, Tomé S ^a   Richard, Nadège ^a   de Vareilles, Mahaut ^a   Marino, Giovanna ^b   Di Marco, Patrizia ^b   Rodrigues, Pedro M ^a   Conceição, Luís E C ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b INSTITUTE FOR ENVIRONMENTAL PROTECTION AND RESEARCH ISPRA   (Italy)

Author keywords

Biomarkers; Chronic stress; Fish welfare; Proteomics; Sparus aurata

Indexed keywords

ENZYME ACTIVITY; GENETIC MARKER; IMMUNOASSAY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PERCIFORM; PLASMA; POLYMERASE CHAIN REACTION; PROTEIN; PROTEOMICS; REARING; STATISTICAL ANALYSIS; STOCKING DENSITY;

ARCHOSARGUS RHOMBOIDALIS; SPARUS AURATA;

EID: 73749084022     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2009.11.014     Document Type: Article

References (83)

1. Acerete L., Balasch J.C., Espinosa E., Josa A., and Tort L. Physiological responses in Eurasian perch (Perca fluviatilis, L.) subjected to stress by transport and handling. Aquaculture 237 (2004) 167-178
2. Ali K.S., Dorgai L., Ábrahám M., and Hermesz E. Tissue- and stressor-specific differential expression of two hsc70 genes in carp. Biochem. Biophys. Res. Commun. 307 (2003) 503-509
3. Anderson P.M., Broderius M.A., Fong K.C., Tsui K.N.T., Chew S.F., and Ip Y.K. Glutamine synthetase expression in liver, muscle, stomach and intestine of Bostrichthys sinensis in response to exposure to a high exogenous ammonia concentration. J. Exp. Biol. 205 (2002) 2053-2065
4. Arends R.J., Mancera J.M., Muñoz J.L., Wendelaar Bonga S.E., and Flik G. The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J. Endocrinol. 163 (1999) 149-157
5. Ashley P.J. Fish welfare: current issues in aquaculture. Appl. Anim. Behav. Sci. 104 (2007) 199-235
6. Barton B.A. Stress in finfish: past, present and future - a historical perspective. In: Iwama G.K., Pickering A.D., Sumpter J.P., and Schreck C.B. (Eds). Fish Stress and Health in Aquaculture. Society for Experimental Biology Seminar Series vol. 62 (1997), Cambridge University Press, Cambridge, U.K. 1-33
7. Barton B.A. Stress in fish: a diversity of response with particular reference to changes in circulating corticosteroids. Integ. Comp. Biol. 42 (2002) 517-525
8. Barton B.A., Ribas L., Acerete L., and Tort L. Effects of chronic confinement on physiological responses of juvenile gilthead sea bream, Sparus aurata L., to acute handling. Aquac. Res. 36 (2005) 172-179
9. Basu N., Nakano T., Grau E.G., and Iwama G.K. The effects of cortisol on heat shock protein 70 levels in two fish species. Gen. Comp. Endocrinol. 124 (2001) 97-105
10. Bernlohr D.A., Simpson M.A., Hertzel A.V., and Banaszak L.J. Intracellular lipid-binding proteins and their genes. Annu. Rev. Nutr. 17 (1997) 277-303
11. Biron M., and Benfey T.J. Cortisol, glucose and hematocrit changes during acute stress, cohort sampling, and the diel cycle in diploid and triploid brook trout (Salvelinus fontinalis Mitchell). Fish Phys. Biochem. 13 (1994) 153-160
12. Bollen M., Keppens S., and Stalmans W. Specific features of glycogen metabolism in the liver. Biochem. J. 336 (1998) 19-31
13. Bone Q., Marshall N.B., and Blaxter J.H.S. Biology of Fishes. Second ed (1996), Chapman & Hall, London
14. Boone A.N., and Vijayan M.M. Glucocorticoid-mediated attenuation of the hsp70 response in trout hepatocytes involves the proteasome. Am. J. Reg. Int. Comp. Phys. 283 (2002) 680-687
15. Boone A.N., and Vijayan M.M. Constitutive heat shock protein 70 (HSC 70) expression in rainbow trout hepatocytes: effect of heat shock and heavy metal exposure. Comp. Biochem. Physiol. C 132 (2002) 223-233
16. In: Branson E.J. (Ed). Fish Welfare (2008), Blackwell Publishing Ltd., Oxford, UK 300 pp.
17. Cairs M.T., Johnson M.C., Talbot A.T., Pemmasani J.K., McNeill R.E., Houeix B., Sangrador-Vegas A., and Pottinger T.G. A cDNA microarray assessment of gene expression in the liver of rainbow trout (Oncorhynchus mykiss) in response to a handling and confinement stressor. Comp. Biochem. Physiol. D 3 (2008) 51-66
18. Cockram M.S. Criteria and potential reasons for maximum journey times for farm animals destined for slaughter. Appl. Anim. Behav. Sci. 106 (2007) 234-243
19. Conte F.S. Stress and welfare of cultured fish. Appl. Anim. Behav. Sci. 86 (2004) 205-223
20. Cowan M.L., and Vera J. Proteomics: advances in biomarker discovery. Expert Rev. Proteomic 5 (2008) 21-23
21. Deane E.E., Kelly S.P., Lo C.K.M., and Woo N.Y.S. Effects of GH, prolactin and cortisol on hepatic heat shock protein 70 expression in a marine teleost Sparus sarba. J. Endocrinol. 161 (1999) 413-421
22. EFSA. 2008. Scientific report of EFSA on animal welfare aspects of husbandry systems for farmed European sea bass and Gilthead sea bream. (Question No EFSA-Q-2006-149). Annex I to the EFSA Journal 844, 1-89.
23. Erol E., Kumar L.S., Cline G.W., Shulman G.I., Kelly D.P., and Binas B. Liver fatty acid binding protein is required for high rates of hepatic fatty acid oxidation but not for the action of PPAR-α in fasting mice. FASEB J. 18 (2004) 347-349
24. Feder M.E., and Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61 (1999) 243-282
25. Friedberg F., and Rhoads A.R. Multiple calmodulin genes in fish. Mol. Biol. Rep. 29 (2002) 377-382
26. Gornati R., Terova G., Vigetti D., Prati M., Saroglia M., and Bernardini G. Effects of population density on sea bass (Dicentrarchus labrax) gene expression. Aquaculture 230 (2004) 229-239
27. Gornati R., Papis E., Rimoldi S., Terova G., Saroglia M., and Bernardini G. Rearing density influences the expression of stress-related genes in sea bass (Dicentrarchus labrax, L.). Gene 341 (2004) 111-118
28. Guzmán M., Velasco G., and Geelen M.J.H. Do cytoskeletal components control fatty acid translocation into liver mitochondria?. TEM 11 (2000) 49-53
29. Han J.Z., and Wang Y.B. Proteomics: present and future in food science and technology. Trends Food Sci. Technol. 19 (2007) 26-30
30. Haukenes A.H., and Barton B.A. Characterization of the cortisol response following an acute challenge with lipopolysaccharide in the yellow perch and the influence of rearing density. J. Fish Biol. 64 (2004) 851-862
31. Haunerland N.H., and Spener F. Properties and physiological significance of fatty acid binding proteins. Adv. Mol. Cell Biol. 33 (2004) 99-123
32. Her G.M., Chiang C., Chen W., and Wu J. In vivo studies of liver-type fatty acid binding protein (l-FABP) gene expression in liver of transgenic zebrafish (Danio rerio). FEBS Lett. 538 (2003) 125-133
33. Hertzel A.V., and Bernlohr A.E. The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrinol. Metab. 11 (2000) 175-180
34. Hopkins T.E., Wood C.M., and Walsh P.J. Interactions of cortisol and nitrogen metabolism in the ureogenic gulf toadfish Opsanus beta. J. Exp. Biol. 198 (1995) 2229-2235
35. Hung D.Y., Burczynski F.J., Chang P., Lewis A., Masci P.P., Siebert G.A., Anissimov Y.G., and Roberts M.S. Fatty acid binding protein is a major determinant of hepatic pharmacokinetics of palmitate and its metabolites. Am. J. Physiol. Gastrointest. Liver Physiol. 284 (2003) 423-433
36. Huntingford F.A., and Kadri S. Welfare and fish. In: Branson E.J. (Ed). Fish Welfare (2008), Blackwell Publishing 19-31
37. Huntingford F.A., Adams C., Braithwaite V.A., Kadri S., Pottinger T.G., Sandoee P., and Turnbull J.F. Review paper: current issues in fish welfare. J. Fish Biol. 68 (2006) 332-372
38. Ip Y.K., Chew S.F., and Randall D.J. Ammonia toxicity, tolerance, and excretion. In: Hoar W.S., Randall D.J., and Farrell A.P. (Eds). Fish Physiology vol. 20 (2001), Academic Press, San Diego
39. Iwama G.K. The welfare of fish. Dis. Aquat. Org. 75 (2007) 155-158
40. Iwama G.K., Thomas P.T., Forsyth R.B., and Vijayan M.M. Heat shock protein expression in fish. Rev. Fish Biol. 8 (1998) 35-56
41. Iwama G.K., Vijayan M.M., Forsyth R.B., and Ackerman P.A. Heat shock proteins and physiological stress in fish. Am. Zool. 39 (1999) 901-909
42. Iwama G.K., Afonso L.O.B., Todgham A., Ackerman P., and Nakano K. Are hsps suitable for indicating stressed states in fish?. J. Exp. Biol. 207 (2004) 15-19
43. Kerner J., and Hoppel C. Fatty acid into mitochondria. Biochim. Biophys. Acta 1486 (2000) 1-17
44. Krasnov A., Koskinen H., Pehkonen P., Rexroad C.E., Afanasyev S., and Mölsä H. Gene expression in the brain and kidney of rainbow trout in response to handling stress. BMC Genomics 6 (2005) 3
45. Kumada Y., Benson D.R., Hillemann D., Hosted T.J., Rochefort D.A., Thompson C.J., Wohlleben W., and Tateno Y. Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 3009-3013
46. Lopez J.L. Two-dimensional electrophoresis in proteome expression analysis. J. Chromatogr. B 849 (2007) 190-202
47. McGarry J.D., and Brown N.F. The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analyses. Eur. J. Biochem. 224 (1997) 1-14
48. Mommsen T.P., Vijayan M.M., and Moon T.W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fish 9 (1999) 211-268
49. Momoda T.S., Schwindt A.R., Feist G.W., Gerwick L., Bayne C.J., and Schreck C.B. Gene expression in the liver of rainbow trout, Oncorhynchus mykiss, during the stress response. Comp. Biochem. Physiol. D 2 (2007) 303-315
50. Montero D., Izquierdo M.S., Tort L., Robaina L., and Vergara J.M. High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles. Fish Physiol. Biochem. 20 (1999) 53-60
51. Montero D., Tort L., Robaina L., Vergara J.M., and Izquierdo M.S. Low vitamin E in diet reduces stress resistance of gilthead seabream (Sparus aurata) juveniles. Fish Shellfish Immunol. 11 (2001) 473-490
52. Moyle P.B., and Cech J.J. Fishes - An Introduction to Ichtyology. Third ed (1996), Prentice Hall, New Jersey
53. Mugnier C., Fostier A., Guezou S., Gaigon J.L., and Quemener L. Effect of some repetitive factors on turbot stress response. Aquac. Int. 6 (1998) 33-45
54. Ortunõ J., Esteban M.A., and Meseguer J. Effects of short-term crowding stress on the gilthead seabream (Sparus aurata L) innate immune response. Fish Shellfish Immunol. 11 (2001) 187-197
55. Pagés T., Gomez E., Suner O., Viscor G., and Tort L. Effects of daily management stress on haematology and blood rheology of the gilthead seabream. J. Fish Biol. 46 (1995) 775-786
56. Papoutsoglou S.E., Miliou H., Chadio S., Karakatsoulia N., and Zarkadaa A. Studies on stress responses and recovery from removal in gilthead sea bream Sparus aurata (L.) using recirculated seawater system. Aquacult. Eng. 21 (1999) 19-32
57. Poltronieri C., Maccatrozzo L., Simontacchi C., Bertotto D., Funkenstein B., Patruno M., and Radaelli G. Quantitative RT-PCR analysis and immunohistochemical localization of HSP70 in sea bass Dicentrarchus labrax exposed to transport stress. Eur. J. Histochem. 51 (2007) 125-136
58. Pottinger T.G. The stress response in fish - mechanisms, effects and measurement. In: Branson E.J. (Ed). Fish Welfare (2008), Blackwell Publishing 32-48
59. Procarione L.S., Barry T.P., and Malison J.A. Effects of high rearing densities and loading rates on the growth and stress responses of juvenile rainbow trout. North Am. J. Aquacult. 61 (1999) 91-96
60. Randall D., Burggren W., French K., and Fernald R. Eckert - Animal Physiology - Mechanisms and Adaptations (1997), W.H. Freeman and Company, New York
61. Ribas L., Planas J.V., Barton B., Monetti C., Bernardini G., Saroglia M., Tort L., and MacKenzie S. A differentially expressed enolase gene isolated from the gilthead seabream (Sparus aurata) under high-density conditions is up-regulated in brain after in vivo lipopolysaccharide challenge. Aquaculture 241 (2004) 195-206
62. Roche H., and Bogé G. Fish blood parameters as a potential tool for identification of stress caused by environmental factors and chemical intoxication. Mar. Environ. Res. 41 (1996) 27-43
63. Roncarati A., Melotti P., Dees A., Mordenti O., and Angellotti L. Welfare status of cultured sea bass (Dicentrarchus labrax L.) and sea bream (Sparus aurata L.) assessed by blood parameters and tissue characteristics. J. Appl. Ichthyol. 22 (2006) 225-234
64. Rotllant J., Balm P.H.M., Ruane N.M., Pérez-Sánchez J., Wendelaar Bonga S.E., and Tort L. Pituitary proopiomelanocortin-derived peptides and hypothalamuspituitary-interrenal axis activity in gilthead sea bream (Sparus aurata) during prolonged crowding stress: differential regulation of adrenocorticotropin hormone and melanocyte-stimulating hormone release by corticotropin-releasing hormone and thyrotropin-releasing hormone. Gen. Comp. Endocrinol. 119 2 (2000) 152-163
65. Rotllant J., Balm P.H.M., Pérez-Sanchez J., Wendelaar Bonga S.E., and Tort L. Pituitary and interrenal function in gilthead sea bream (Sparus aurata L., Teleostei) after handling and confinement stress. Gen. Comp. Endocrinol. 121 (2001) 333-342
66. Sangiao-Alvarellos S., Guzman J.M., Laiz-Carrion R., Míguez J.M., del Río M.P.M., Mancera J.M., and Soengas J.L. Interactive effects of high stocking density and food deprivation on carbohydrate metabolism in several tissues of gilthead sea bream Sparus auratus. J. Exp. Zool. A 303 (2005) 761-775
67. Smulders D., Verbeke G., Mormède P., and Geers R. Validation of a behavioral observation tool to assess pig welfare. Physiol. Behav. 89 (2006) 438-447
68. Tort L., Montero D., Robaina L., Fernandez-Palacios H., and Izquierdo M.S. Consistency of stress response to repeated handling in the gilthead sea bream Sparus aurata Linnaeus, 1758. Aquac. Res. 32 (2001) 593-598
69. Tovar M.A.A., and Giraldo J.D.V. Considerations on ethics and animal welfare in extensive pig production: breeding and fattening Iberian pigs. Livest. Sci. 103 (2006) 237-242
70. Turkaly P., Kerner J., and Hoppel C. A 22 kDa polyanion inhibits carnitine-dependent fatty acid oxidation in rat liver. FEBS Lett. 460 (1999) 241-245
71. Turnbull J.F., and Kadri S. Safeguarding the many guises of farmed fish welfare. Dis. Aquat. Org. 75 (2007) 173-182
72. Vats P., Mukherjee A.K., Kumria M.M.L., Singh S.N., Patil S.K.B., Rangnathan S., and Sridharan K. Changes in the activity levels of glutamine synthetase, glutaminase and glycogen synthetase in rats subjected to hypoxic stress. Int. J. Biometeorol. 42 (1999) 205-209
73. Veissier I., Butterworth A., Bock B., and Roe E. European approaches to ensure good animal welfare. Appl. Anim. Behav. Sci. 113 (2008) 279-297
74. Velasco G., Sánchez C., Geelen M.J.H., and Guzmán M. Are cytoskeletal components involved in the control of hepatic carnitine palmitoyltransferase I activity?. Biochim. Biophys. Res. Commun. 224 (1996) 754-759
75. Velasco G., Geelen M.J.H., Pulgar T.G., and Guzmán M. Malonyl-CoA-independent acute control of hepatic carnitine palmitolytransferase I activity. J. Biol. Chem. 273 (1998) 21497-21504
76. Vijayan M.M., Ballantyne J.S., and Leatherland J.F. High stocking density alters the energy metabolism of brook charr, Salvelinus fontinalis. Aquaculture 88 (1990) 371-381
77. Voet D., and Voet J.G. Biochemistry. Second ed. (2005), John Wiley & Sons, Inc., New York
78. Yamashita M., Hirayoshi K., and Nagata. Characterization of multiple members of the HSP70 family in platfish cultured cells: molecular evolution of stress protein HSP70 in vertebrates. Gene 336 (2004) 207-218
79. Yildiz H.Y. Reference biochemical values for three cultured Sparid fish: striped sea bream, Lithognathus mormyrus; common dentex, Dentex dentex; and gilthead sea bream, Sparus aurata. Comp. Clin. Path (2008) 10.1007/s00580-008-0743-1
80. Wang G., Gong Y., Anderson J., Sun D., Minuk G., Roberts M.S., and Burczynski F.J. Antioxidative function of L-FABP in L-FABP stably transfected Chang liver cells. Hepatology 42 (2005) 871-879
81. 2+-binding and structural dynamics in the functions of calmodulin. Annu. Rev. Physiol. 56 (1994) 213-236
82. Wendelaar Bonga S.E. The stress response in fish. Physiol. Rev. 77 (1997) 591-625
83. Westermeier R., Naven T., and Höpker H. Proteomics in Practice: A Guide to Successful Experimental Design. Second ed. (2008), Wiley-VCH, Federal Republic of Germany