Whole body cortisol and expression of HSP70, IGF-I and MSTN in early development of sea bass subjected to heat shock

General and Comparative Endocrinology

Volumn 174, Issue 1, 2011, Pages 44-50

  Bertotto, Daniela ^a   Poltronieri, Carlo ^a   Negrato, Elena ^a   Richard, Jacopo ^b   Pascoli, Francesco ^a   Simontacchi, Claudia ^a   Radaelli, Giuseppe ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b Veneto Agricoltura   (Italy)

Author keywords

Cortisol; Heat shock protein 70; Insulin growth factor I; Myostatin; Sea bass larvae

Indexed keywords

HEAT SHOCK PROTEIN 70; HYDROCORTISONE; MYOSTATIN; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEVELOPMENT; EUROPEAN SEA BASS; GENE EXPRESSION; HATCHING; HEAT SHOCK; HYPOTHALAMIC PITUITARY INTERRENAL AXIS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LARVA; LARVAL STAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RADIOIMMUNOASSAY; REAL TIME POLYMERASE CHAIN REACTION;

EID: 80052778747     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.08.003     Document Type: Article

References (92)

1. Alderman S.L., Bernier N.J. Ontogeny of the corticotropin-releasing factor system in zebrafish. Gen. Comp. Endocrinol. 2009, 164:61-69.
2. Andersen D.E., Reis S.D., Moon T.W., Perry S.F. Metabolic effects associated with chronically elevated cortisol in rainbow trout (Oncorhynchus mykiss). Can. J. Fish. Aquat. Sci. 1991, 48:1811-1817.
3. Applebaum S.L., Wilson C.A., Holt G.J., Nunez B.S. The onset of cortisol synthesis and the stress response is independent of changes in CYP11B or CYP21 mRNA levels in larval red drum (Sciaenops ocellatus). Gen. Comp. Endocrinol. 2010, 165:269-276.
4. Applied Biosystems, Chemistry Guide 7500 Real Time PCR Systems, Applied Biosystems, USA (2004) 61pp.
5. Auperin B., Geslin M. Plasma cortisol response to stress in juvenile rainbow trout is influenced by their life history during early development and by egg cortisol content. Gen. Comp. Endocrinol. 2010, 158:234-239.
6. Ayson F.G., de Jesus E.G., Moriyama S., Hyodo S., Funkenstein B., Gertler A., Kawauchi H. Differential expression of insulin-like growth factor I and II mRNAs during embryogenesis and early development in rabbitfish, Siganus guttatus. Gen. Comp. Endocrinol. 2002, 126:165-174.
7. Barry T.P., Malison J.A., Held J.A., Parrish J.J. Ontogeny of the cortisol stress response in larval rainbow trout. Gen. Comp. Endocrinol. 1995, 97:57-65.
8. Barry T.P., Ochiai M., Malison J.A. In vitro effects of ACTH on interrenal corticosteroidogenesis during early larval development in rainbow trout. Gen. Comp. Endocrinol. 1995, 99:382-387.
9. Barton B.A., Iwama G.K. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann. Rev. Fish Dis. 1991, 1:3-26.
10. Barton B.A., Schreck C.B., Barton L.D. Effects of chronic cortisol administration and daily acute stress on growth, physiological condition and stress response in juvenile rainbow trout. Dis. Aquat. Organ. 1987, 2:173-185.
11. Berishvili G., Shved N., Eppler E., Clota F., Baroiller J.F., Reinecke F. Organ-specific expression of IGF-I during early development of bony fish as revealed in the tilapia, Oreochromis niloticus, by in situ hybridization and immunohistochemistry: indication for the particular importance of local IGF-I. Cell Tissue Res. 2006, 325:287-301.
12. Breves J.P., Hirano T., Grau E.G. Ionoregulatory and endocrine responses to disturbed salt and water balance in Mozambique tilapia exposed to confinement and handling stress. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2010, 155:294-300.
13. Cao Y.B., Chen X.Q., Wang S., Chen X.C., Wang Y.X., Chang J.P., Du J.Z. Growth hormone and insulin-like growth factor of naked carp (Gymnocypris przewalskii) in Lake Qinghai: expression in different water environments. Gen. Comp. Endocrinol. 2009, 161:400-406.
14. Chauvigne F., Gabillard J.C., Weil C., Rescan P.Y. Effect of refeeding on IGF-I, IGF-II, IGF receptors, FGF2, FGF6, and myostatin mRNA expression in rainbow trout myotomal muscle. Gen. Comp. Endocrinol. 2003, 132:209-215.
15. Colombo L., Barbaro A., Libertini A., Benedetti P., Francescon A., Lombardo I. Artificial fertilization and induction of triploidy and meiogynogenesis in the European sea bass, Dicentrarchus labrax L. J. Appl. Ichthyol. 1995, 11:118-125.
16. Davis K.B., Peterson B.C. The effect of temperature, stress, and cortisol on plasma IGF-I and IGFBPs in sunshine bass. Gen. Comp. Endocrinol. 2006, 149:219-225.
17. De Jesus E.G., Hirano T. Changes in whole body concentrations of cortisol, thyroid hormones, and sex steroids during early development of the chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol. 1992, 85:55-61.
18. De Jesus E.G., Hirano T., Inui Y. Changes in cortisol and thyroid hormone concentrations during early development and metamorphosis in the Japanese flounder, Paralichthys olivaceus. Gen. Comp. Endocrinol. 1991, 82:369-376.
19. Dietz T.J. Acclimation of the threshold induction temperatures for the 70-kDa and 90-kDa heat shock proteins in the fish Gillichthys mirabilis. J. Exp. Biol. 1994, 188:333-338.
20. Duan C. Nutritional and developmental regulation of insulin-like growth factor in fish. J. Nutr. 1998, 128:306S-314S.
21. Duguay S.J., Lai-Zhang J., Steiner D.F., Funkenstein B., Chan S.J. Developmental and tissue-regulated expression of IGF-I and IGF-II mRNAs in Sparus aurata. J. Mol. Endocrinol. 1996, 16:123-132.
22. Duval H., Rousseau K., Elies G., Le Bail P.Y., Dufour S., Boeuf G., Boujard D. Cloning, characterization, and comparative activity of turbot IGF-I and IGF-II. Gen. Comp. Endocrinol. 2002, 126:269-278.
23. Eder K.J., Köhler H.R., Werner J. Pesticide and pathogen: heat shock protein expression and acetylcholinesterase inhibition in juvenile Chinook salmon in response to multiple stressors. Environ. Toxicol. Chem. 2007, 26:1233-1242.
24. Feder M.E., Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Ann. Rev. Physiol. 1999, 61:243-282.
25. Gabillard J.C., Kamangar B.B., Montserrat N. Coordinated regulation of the GH-IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J. Endocrinol. 2006, 191:15-24.
26. Garikipati D.K., Gahr S.A., Rodgers B.D. Identification, characterization, and quantitative expression analysis of rainbow trout myostatin-1a and myostatin-1b genes. J. Endocrinol. 2006, 190:879-888.
27. Garikipati D.K., Gahr S.A., Roalson E.H., Rodgers B.D. Characterization of rainbow trout myostatin-2 genes (rtMSTN-2a and -2b): genomic organization, differential expression, and pseudogenization. Endocrinology 2007, 148:2106-2115.
28. 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.
29. Gornati R., Papis E., Rimoldi S., Chini V., Trova G., Prati M., Saroglia M., Bernardini G. Molecular markers for animal biotechnology: sea bass (Dicentrarchus labrax L.) HMG-CoA reductase mRNA. Gene 2005, 344:299-305.
30. Greene M.W., Chen T.T. Temporal expression pattern of insulin-like growth factor mRNA during embryonic development in a teleost, rainbow trout (Onchorynchus mykiss). Mol. Mar. Biol. Biotechnol. 1997, 6:144-151.
31. Greene M.W., Chen T.T. Quantitation of IGF-I, IGF-II, and multiple insulin receptor family member messenger RNAs during embryonic development in rainbow trout. Mol. Reprod. Dev. 1999, 54:348-361.
32. Gregory D.J., Waldbieser G.C., Bosworth B.G. Cloning and characterization of myogenic regulatory genes in three Ictalurid species. Anim. Genet. 2004, 35:425-430.
33. Hagen Ø., Fernandes J.M.O., Solberg C., Johnston I.A. Expression of growth-related genes in muscle during fasting and refeeding of juvenile Atlantic halibut, Hippoglossus hippoglossus L. Comp. Biochem. Physiol. 2009, 152:47-53.
34. Hansen B.H., Ganno O.A., Olsvik P.A., Andersen R.A. Gill metal binding and stress gene transcription in brown trout (Salmo trutta) exposed to metal environments: the effect of pre-exposure in natural populations. Environ. Toxicol. Chem. 2007, 26:944-953.
35. Helterline D.L., Garikipati D., Stenkamp D.L., Rodgers B.D. Embryonic and tissue-specific regulation of myostatin-1 and -2 gene expression in zebrafish. Gen. Comp. Endocrinol. 2007, 151:90-97.
36. Hwang P.P., Wu S.M., Lin J.H., Wu L.S. Cortisol content of eggs and larvae of teleosts. Gen. Comp. Endocrinol. 1992, 86:189-196.
37. Iwama G.K., Thomas P.T., Forsyth R.B., Vijayan M.M. Heat shock protein expression in fish. Rev. Fish Biol. Fish. 1998, 8:35-56.
38. Jentoft S., Held J.A., Malison J.A., Barry T.P. Ontogeny of the cortisol stress response in yellow perch (Perca flavescens). Fish Physiol. Biochem. 2002, 26:371-378.
39. Jonsson H., Schiedek D., Goksøyr A. Expression of cytoskeletal proteins, cross-reacting with anti-CYP1A, in Mytilus sp. Exposed to organic contaminants. Aquat. Toxicol. 2006, 78:42-48.
40. Ko C.F., Chiou T.T., Chen T.T., Wu J.L., Chen J.C., Lu J.K. Molecular cloning of myostatin gene and characterization of tissue-specific and developmental stage-specific expression of the gene in orange spotted grouper, Epinephelus coioides. Mar. Biotechnol. 2007, 9:20-32.
41. Kocabas A.M., Kucuktas H., Dunham R.A., Liu Z. Molecular characterization and differential expression of the myostatin gene in channel catfish (Ictalurus punctatus). Biochim. Biophys. Acta 2002, 1575:99-107.
42. Lang C.H., Silvis C., Nystrom G., Frost R.A. Regulation of myostatin by glucocorticoids after thermal injury. FASEB J. 2001, 15:1807-1809.
43. Larsen D.A., Beckman B.R., Dickhoff W.W. The effect of low temperature and fasting during the winter on metabolic stores and endocrine physiology (insulin, insulin-like growth factor-1, and thyroxine) of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 2001, 123:308-323.
44. Liebert A.M., Schreck C.B. Effects of acute stress on osmoregulation, feed intake, IGF-I, and cortisol in yearling steelhead trout (Oncorhynchus mykiss) during seawater adaptation. Gen. Comp. Endocrinol. 2006, 148:195-202.
45. Ma K., Mallidis C., Bhasin S., Mahabadi V., Artaza J., Cadavid N.G., Arias J., Salehian B. Glucocorticoid-induced skeletal muscle atrophy is associated with upregulation of myostatin gene expression. Am. J. Physiol. Endocrinol. Metab. 2003, 285:363-371.
46. Maccatrozzo L., Bargelloni L., Cardazzo B., Rizzo G., Patarnello T. A novel second myostatin gene is present in teleost fish. FEBS Lett. 2001, 509:36-40.
47. Maccatrozzo L., Bargelloni L., Radaelli G., Mascarello F., Patarnello T. Characterization of the myostatin gene in the gilthead sea bream (Sparus aurata): sequence, genomic structure, and expression pattern. Mar. Biotechnol. 2001, 3:224-230.
48. Maradonna F., Carnevali O. Vitellogenin, zona radiate protein, cathepsin D and heat shock protein 70 as biomarkers of response to xenobiotics. Biomarkers 2007, 12:240-255.
49. McPherron A.C., Lawler A.M., Lee S.J. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997, 387:83-90.
50. Mesa M.G., Weiland L.K., Wagner P. Effects of acute thermal stress on the survival, predator avoidance, and physiology of juvenile fall Chinook salmon. Northwest Sci. 2002, 76:118-128.
51. Mommsen T.P., Vijayan M.M., Moon T.W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fish. 1999, 9:211-268.
52. Montserrat N., Gabillard J.C., Capilal E., Navarro M.I., Gutiérrez J. Role of insulin, insulin-like growth factors, and muscle regulatory factors in the compensatory growth of the trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 2007, 150:462-472.
53. Morimoto R.I., Tissieres A., Georgopoulos C. Stress Proteins in Biology and Medicine 1990, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
54. Moriyama S., Ayson F.G., Kawauchi H. Growth regulation by insulin-like growth factor-I in fish. Biosci. Biotech. Biochem. 2000, 64:1553-1562.
55. Murtha J.M., Keller E.T. Characterization of the heat shock response in mature zebrafish (Danio rerio). Exp. Gerontol. 2003, 38:683-691.
56. Nakano K., Takemura A., Nakamura S., Nakano Y., Ywama G.K. Changes in the cellular and organismal stress responses of the subtropical fish, the Indo-Pacific sergeant, Abudefduf vaigiensis, due to the 1997-1998 El Nino/Southern Oscillation. Environ. Biol. Fish 2004, 70:321-329.
57. Østbye T.K., Falck Galloway T., Nielsen C., Gabestad I., Bardal T., Andersen Ø. The two myostatin genes of Atlantic salmon (Salmo salar) are expressed in a variety of tissues. Eur. J. Biochem. 2001, 268:5249-5257.
58. Patruno M., Maccatrozzo L., Funkenstein B., Radaelli G. Cloning and expression of insulin-like growth factors I and II in the SHI drum (Umbrina cirrosa). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2006, 137:137-151.
59. Patruno M., Sivieri S., Poltronieri C., Sacchetto R., Maccatrozzo L., Martinello T., Funkenstein B., Radaelli G. Real-time polymerase chain reaction, in situ hybridization and immunohistochemical localization of insulin-like growth factor-I and myostatin during development of Dicentrarchus labrax (Pisces: Osteichthyes). Cell Tissue Res. 2008, 331:643-658.
60. Pavlidis M., Karantzali E., Fanouraki E., Barsakis C., Kollias S., Papandroulakis N. Onset of the primary stress in European sea bass Dicentrarchus labrax, as indicated by whole body cortisol in relation to glucocorticoid receptor during early development. Aquaculture 2010, 10.1016/j.aquaculture.2010.09.013.
61. Perrot V., Moiseeva E.B., Gozes Y., Chan S.J., Ingleton P., Funkenstein B. Ontogeny of the insulin-like growth factor system (IGF-I, IGF-II, and IGF-IR) in gilthead seabream (Sparus aurata): expression and cellular localization. Gen. Comp. Endocrinol. 1999, 116:445-460.
62. Pickering A.D., Pottinger T.G., Christie P. Recovery of the brown trout, Salmo trutta L., from acute handling stress: a time-course study. J. Fish Biol. 1982, 20:229-244.
63. Podrabsky J.E., Somero G.N. An inducible 70kDa-class heat shock protein is constitutively expressed during early development and diapause in the annual killifish Austrofundulus limnaeus. Cell Stress Chaperon. 2007, 12:199-204.
64. Poltronieri C., Maccatrozzo L., Simontacchi C., Bertotto D., Funkenstein B., Radaelli G. Quantitative RT-PCR analysis and immunohistochemical localization of HSP70 in sea bass Dicentrarchus labrax exposed to transport stress. Eur. J. Histochem. 2007, 51:125-136.
65. Poltronieri C., Negrato E., Bertotto D., Majolini D., Simontacchi C., Radaelli G. Immunohistochemical localization of constitutive and inducible heat shock protein 70 in carp (Cyprinus carpio) and trout (Oncorhynchus mykiss) exposed to transport stress. Eur. J. Histochem. 2008, 52:191-198.
66. Råbergh C.M.I., Airaksinen S., Soitamo A., Björklund H.V., Johansson T., Nikinmaa M., Sistonen L. Tissue-specific expression of zebrafish (Danio rerio) heat shock factor 1 mRNAs in response to heat stress. J. Exp. Biol. 2000, 203:1817-1824.
67. Radaelli G., Rowlerson A., Mascarello F., Patruno M., Funkenstein B. Myostatin precursor is present in several tissues in teleost fish: a comparative immunolocalization study. Cell Tissue Res. 2003, 311:239-250.
68. Rasmussen R. Quantification on the LightCycler. Methods and Applications 2001, 21-34. Springer Press, Heidelberg. S. Meuer, C. Wittwer, K. Nakagawara (Eds.).
69. Reinecke M., Collet C. The phylogeny of the insulin-like growth factors. Int. Rev. Cytol. 1998, 183:1-94.
70. Reinecke M., Björnsson B.T., Dickhoff W.W., McCormick S.D., Navarro I., Power D.M., Gutiérrez J. Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen. Comp. Endocrinol. 2005, 142:20-24.
71. Reinecke M., Schmid A., Ermatinger R., Loffin-Cueni D. Insulin-like growth factor I in the teleost Oreochromis mossambicus, the tilapia: gene sequence, tissue expression, and cellular localization. Endocrinology 1997, 138:3613-3619.
72. Rescan P.Y., Jutel I., Ralliere C. Two myostatin genes are differentially expressed in myotomal muscles of the trout (Oncorhynchus mykiss). J. Exp. Biol. 2001, 204:3523-3529.
73. Roberts S.B., Goetz F.W. Differential skeletal muscle expression of myostatin across teleost species, and the isolation of multiple myostatin isoforms. FEBS Lett. 2001, 491:212-216.
74. Rodgers B.D., Weber G.M., Kelley K.M., Levine M.A. Prolonged fasting and cortisol reduce myostatin mRNA levels in tilapia larvae; short-therm fasting elevates. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 284:1277-1286.
75. Rotllant J., Tort L. Cortisol and glucose responses after acute stress by net handling in the sparid red porgy previously subjected to crowding stress. J. Fish Biol. 1997, 51:21-28.
76. Roy S., Bhattacharya S. Arsenic-induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus. Ecotoxicol. Environ. Saf. 2006, 65:218-229.
77. Saera-Vila A., Calduch-Giner J.A., Prunet P., Pérez-Sánchez J. Dynamics of liver GH/IGF axis and selected stress markers in juvenile gilthead sea bream (Sparus aurata) exposed to acute confinement: differential stress response of growth hormone receptors. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2009, 154:197-203.
78. Sampath-Kumar R., Byers R.E., Munro A.D., Lam T.J. Profile of cortisol during the ontogeny of the Asian seabass, Lates calcarifer. Aquaculture 1995, 132:349-359.
79. Sampath-Kumar R., Lee S.T.L., Tan C.H., Munro A.D., Lam T.J. Biosynthesis in vivo and excretion of cortisol by fish larvae. J. Exp. Zool. 1997, 277:337-344.
80. Simontacchi C., Negrato E., Pazzaglia M., Bertotto D., Poltronieri C., Radaelli G. Whole-body concentrations of cortisol and sex steroids in white sturgeon (Acipenser transmontanus, Richardson 1836) during early development and stress response. Aquacult. Int. 2009, 17:7-14.
81. Terova G., Bernardini G., Binelli G., Gornati R., Saroglia M. CDNA encoding sequences for myostatin and FGF6 in sea bass (Dicentrarchus labrax L.) and the effect of fasting and refeeding on their abundance levels. Domest. Anim. Endocrinol. 2006, 30:304-319.
82. Tomas F.M., Munro H.N., Young V.R. Effect of glucocorticoid administration on the rate of muscle protein breakdown in vivo in rats as measured by urinary excretion Ntau-methylh-istidine. Biochem. J. 1979, 179:139-146.
83. Van Raaij M.T.M., Pit D.S.S., Balm P.H.M., Steffens A.B., Van den Thillart G.E.E.J.M. Behavioral strategy and the physiological stress response in rainbow trout exposed to severe hypoxia. Horm. Behav. 1996, 30:85-92.
84. Vianello S., Brazzoduro L., Dalla Valle L., Belvedere P., Colombo L. Myostatin expression during development and chronic stress in zebrafish (Danio rerio). J. Endocrinol. 2003, 176:47-59.
85. Vijayan M.M., Pereira C., Grau E.G., Iwama G.K. Metabolic responses associated with confinement stress in tilapia: the role of cortisol. Comp. Biochem. Physiol. C 1997, 116:89-95.
86. Wada H. Glucocorticoids: mediators of vertebrate ontogenetic transitions. Gen. Comp. Endocrinol. 2008, 156:441-453.
87. Wang Y., Xu J., Sheng L., Zheng Y. Field and laboratory investigations of the thermal influence on tissue-specific HSP70 levels in common carp (Cyprinus carpio). Comp. Biochem. Physiol. 2007, 148:821-827.
88. Weber T.E., Small B.C., Bosworth B.G. Lipopolysaccaride regulates myostatin and MyoD independently of an increase in plasma cortisol in channel catfish (Ictalurus punctatus). Domest. Anim. Endocrinol. 2005, 28:64-73.
89. Wendelaar Bonga S.E. The stress response in fish. Physiol. Rev. 1997, 77:591-625.
90. Wilkinson R.J., Porter M., Woolcott H., Longland R., Carragher J.F. Effects of aquaculture related stressors and nutritional restriction on circulating growth factors (GH, IGF-I and IGF-II) in Atlantic salmon and rainbow trout. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2006, 145:214-224.
91. Wood A.W., Duan C., Bern H.A. Insulin-like growth factor signaling in fish. Int. Rev. Cytol. 2005, 243:215-285.
92. Zakhartsev M., De Wachter B., Johansen T., Portner H.O., Blus R. HSP70 is not a sensitive indicator of thermal limitation in Gadus morhua. J. Fish Biol. 2005, 67:767-778.