Salinity acclimation affects the somatotropic axis in rainbow trout

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 288, Issue 5 57-5, 2005, Pages

  Shepherd, Brian S ^a,b,e   Drennon, Katherine ^b   Johnson, Jaime ^b   Nichols, Joel W ^c   Playle, Richard C ^c   Singer, Thomas D ^d   Vijayan, Mathilakath M ^d  

^a APPALACHIAN FRUIT RESEARCH STATION   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c WILFRID LAURIER UNIVERSITY   (Canada)

^d UNIVERSITY OF WATERLOO   (Canada)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Growth hormone; Insulin like growth factor binding proteins; Insulin like growth factor I; Rainbow trout; Salinity

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); GROWTH HORMONE; HYDROCORTISONE; SEA WATER; SODIUM; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN C;

ACCLIMATIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GROWTH HORMONE BLOOD LEVEL; HYDROCORTISONE BLOOD LEVEL; NONHUMAN; PRIORITY JOURNAL; RAINBOW TROUT; SALINITY; SALMONID; SODIUM BLOOD LEVEL;

ACCLIMATIZATION; ANIMALS; CALCIUM; CHLORIDES; GENE EXPRESSION REGULATION; GROWTH HORMONE; HYDROCORTISONE; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; INSULIN-LIKE GROWTH FACTOR I; ONCORHYNCHUS MYKISS; SODIUM; SODIUM CHLORIDE; WATER; WATER-ELECTROLYTE BALANCE;

EID: 17844398727     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00443.2004     Document Type: Article

References (97)

1. Alexander JB and Ingram GA. A comparison of five of the methods commonly used to measure protein concentrations in fish sera. J Fish Biol 16: 115-122, 1980.
2. Bauchat JR, Busby WH, Garmong A, Swanson P, Moore J, Lin M, and Duan C. Biochemical and functional analysis of a conserved IGF-binding protein isolated from rainbow trout (Oncorhynchus mykiss) hepatoma cells. J Endocrinol 170: 619-628, 2001.
3. Baxter RC. Inhibition of the insulin-like growth factor (IGF)-IGF-binding protein interaction. Horm Res 55: 68-72, 2001.
4. Beckman BR and Dickhoff WW. Plasticity of smolting in spring chinook salmon: relation to growth and insulin-like growth factor-I. J Fish Biol 53: 808-826, 1998.
5. Beckman BR, Larsen DA, Moriyama SL, Lee-Pawlak B, and Dickhoff WW. Insulin-like growth factor-1 and environmental modulation of growth during smoltification of spring chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol 109: 325-335, 1998.
6. Beckman BR, Shimizu M, Gadberry BA, and Cooper KA. Response of the somatotropic axis of juvenile coho salmon to alterations in plane of nutrition with an analysis of the relationships among growth rate and circulating IGF-I and 41 kDa IGFBP. Gen Comp Endocrinol 135: 334-344, 2004.
7. Biga PR, Schelling GT, Hardy RW, Cain KD, Overturf KE, and Ott TL. The effects of recombinant bovine somatotropin (rbST) on tissue IGF-I, IGF-I receptor, and GH mRNA levels in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 135: 324-333, 2004.
8. Björnsson BT. The biology of salmon growth hormone: from daylight to dominance. Fish Physiol Biochem 17: 9-24, 1997.
9. Björnsson BT, Stefansson GV, Berge ÅI, Hansen T, and Setefansson SO. Circulating growth hormone levels in Atlantic salmon smolts following seawater transfer: effects of photoperiod regime, salinity, duration of exposure and season. Aquaculture 168: 121-137, 1998.
10. Björnsson BT, Tharanger GL, Hansen T, Stefannson SO, and Haux C. The interrelation between photoperiod, growth hormone and sexual maturation of adult Atlantic salmon (Salmo salar). Gen Comp Endocrinol 93: 70-81, 1994.
11. Bolton JP, Collie NL, Kawauchi H, and Hirano T. Osmoregulatory actions of growth hormone in rainbow trout (Salmo gairdneri). J Endocrinol 112: 63-68, 1987.
12. Brown PS and Brown SC. Osmoregulatory actions of prolactin and other adenohypophysial hormones. In: Vertebrate Endocrinology: Fundamentals and Biomedical Implications, edited by Pang PKT, Schreibman MP and Sawyer WH. London: Academic, 1987, p. 45-84.
13. Clemmons DM. Use of mutagenesis to probe IGF-binding protein structure/function relationships. Endocr Rev 22: 800-817, 2001.
14. +-ATPase α1 subunit in the European eel (Anguilla anguilla). Comp Biochem Physiol B 111: 567-573, 1995.
15. +-ATPase in Atlantic salmon smolts: differences in α-mRNA and α-protein levels. Am J Physiol Regul Integr Comp Physiol 278: R101-R110, 2000.
16. Dickhoff WW. Hormones, metamorphosis, and smolting. In: The Endocrinology of Growth, Development, and Metabolism in Vertebrates, edited by Schreibman MP, Scanes CG and Pang PKT. New York: Academic, 1993, p. 519-540.
17. Dickhoff WW, Beckman BR, Larsen DA, Duan C, and Moriyama S. The role of growth hormone in endocrine regulation of salmon smoltification. Fish Physiol Biochem 17: 231-236, 1997.
18. Drennon K, Small B, Silverstein JT, Moriyama S, Kawauchi H, and Shepherd BS. Development of an enzyme-linked immunosorbent assay for the measurement of plasma growth hormone levels in channel catfish (Ictalurus punctatus): assessment of environmental salinity and GH-secretagogues on plasma GH levels. Gen Comp Endocrinol 133: 314-312, 2003.
19. Duan C. The insulin-like growth factor system and its biological actions in fish. Am Zool 37: 491-503, 1997.
20. Duan C, Ding J, Li Q, Tsai W, and Pozios K. Insulin-like growth factor binding protein 2 is a growth inhibitory protein conserved in zebrafish. Proc Natl Acad Sci USA 96: 15274-15279, 1999.
21. Duan C and Plisetskaya E. Nutritional regulation of insulin-like growth factor-I mRNA expression in salmon tissues. J Endocrinol 139: 243-252, 1993.
22. Duan C, Plisetskaya E, and Dickhoff WW. Expression of insulin-like growth factor I in normally and abnormally developing coho salmon (Oncorhynchus mykiss). Endocrinology 136: 446-452, 1995.
23. Eliassen RA, Johnsen HK, Mayer I, and Jobling M. Contrasts in Osmoregulatory capacity of two Arctic charr, Salvelinis alpinus (L.), strains from northern Norway. Aquaculture 168: 255-269, 1998.
24. Fleming IA, Ágústsson T, Finstad B, Johnsson JI, and Björnsson TB. Effect of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 59: 1323-1330, 2002.
25. Fukazawa Y, Siharath K, Iguchi T, and Bern HA. In vitro secretion of insulin-like growth factor-binding proteins from liver of striped bass, Morone saxatilis. Gen Comp Endocrinol 99: 239-247, 1995.
26. Gracey A, Troll J, and Somero G. Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci USA 98: 1993-1998, 2001.
27. Handeland SO, Björnsson TB, Arnesen AM, and Stefansson SO. Seawater adaptation and growth of post-smolt Atlantic salmon (Salmo salar) of wild and farmed strains. Aquaculture 220: 367-384, 2003.
28. Hirano T. The spectrum of prolactin action in teleosts. In: Progress in Clinical And Biological Research: Comparative Endocrinology: Developments and Directions, edited by Ralph CL. New York: Alan R. Liss, 1986, p. 53-74.
29. Hirano T, Ogasawara T, Bolton JP, Collie NL, Hasegawa S, and Iwata M. Osmoregulatory role of prolactin in lower vertebrates. In: Comparative Physiology of Environmental Adaptations, edited by Kirsch R and Lahlou B. Basel: Karger, 1987, p. 112-124.
30. Hirano T, Ogasawara T, Hasegawa S, Iwata M, and Nagahama Y. Changes in plasma hormone levels during loss of hypoosmoregulatory capacity in mature chum salmon (Oncorhynchus keta) kept in seawater. Gen Comp Endocrinol 78: 252-262, 1990.
31. Hoar WS. The physiology of smelting salmonids. In: Fish Physiology, edited by Hoar WW and Randall DJ. San Diego: Academic, 1988, p. 275-343.
32. Johnson J, Silverstein JT, Wolters WR, Shimizu M, Dickhoff WW, and Shepherd B. Disparate regulation of the insulin-like growth factor-binding proteins in a primitive, Ictalurid, teleost (Ictalurus punctatus). Gen Comp Endocrinol 134: 122-130, 2003.
33. Kajimura S, Hirano T, Visitacion N, Moriyama S, Aida K, and Grau EG. Dual mode of cortisol action on GH/IGF-I/IGFBPs in the tilapia, Oreochromis mossambicus. J Endocrinol 178: 91-99, 2003.
34. Kelley KM, Gray ES, Siharath K, Nicoll CS, and Bern HA. Experimental diabetes mellitus in a teleost fish. II. Roles of insulin, growth hormone (GH), insulin-like growth factor-I, and hepatic GH receptors in diabetic growth inhibition in the goby, Gillichthys mirabilis. Endocrinology 132: 2696-2702, 1993.
35. Kelley KM, Haigwood JT, Perez M, and Galima MM. Serum insulin-like growth factor binding proteins (IGFBPs) as markers for anabolic stress/catabolic conditions in fishes. Comp Biochem Physiol B 129: 229-236, 2001.
36. Kelley KM, Oh Y, Gargosky SE, Gucev Z, Matsumoto T, Hwa V, Ng L, Simpson DM, and Rosenfeld RG. Insulin-like growth factor-binding proteins (IGFBPs) and their regulatory dynamics. Int J Biochem Cell Biol 28: 619-637, 1996.
37. Kelley KM, Schmidt KE, Berg L, Sak K, Galima MM, Gillespie C, Balogh L, Hawayek A, Reyes JA, and Jamison M. Comparative endocrinology of the insulin-like growth factor-binding protein. J Endocrinol 175: 3-18, 2002.
38. Kelley KM, Siharath K, and Bern HA. Identification of insulin-like growth factor-binding proteins in the circulation of four teleost fish species. J Exp Zool 263: 220-224, 1992.
39. Larsen DA, Shimizu M, Cooper KA, Swanson P, and Dickhoff WW. Androgen effects on plasma GH, IGF-I and 41-kDa IGFBP in coho salmon (Oncorhynchus kisiitch). Gen Comp Endocrinol 139: 29-37, 2004.
40. +-ATPaSe in the brown trout. Salmo trutta: in vitro modulation by hormones and seawater. Am J Physiol Regul Integr Comp Physiol 269: R1339-R1345, 1995.
41. Mancera JM and McCormick SD. Osmoregulatory actions of the GH/IGF axis in non-salmonid teleosts. Comp Biochem Physiol B Biochem Mol Biol 121: 43-48, 1998.
42. Marshall WS, Emberley TR, Singer TD, Bryson SE, and McCormick SD. Time-course of salinity adaptation in a strongly euryhaline estuarine teleost, Fundulus heteroclitus: a multivariate approach. J Exp Biol 202: 1535-1544, 1999.
43. Maures TJ and Duan C. Structure, developmental expression and physiological regulation of zebrafish IGF binding-protein-I. Endocrinology 143: 2722-2731, 2002.
44. +-ATPaSe in Atlantic salmon (Salmo salar): interaction with cortisol. Gen Comp Endocrinol 101: 3-11, 1996.
45. McCormick SD. Endocrine control of osmoregulation in teleost fish. Am Zool 41: 781-794, 2001.
46. +-ATPase and chloride cell function. In: Fish Physiology: Cellular and Molecular Approaches to Fish Ionic Regulation, edited by Hoar WS, Randall DJ and Farrell AP. Sah Francisco, CA: Academic, 1995, p. 285-315.
47. +-ATPase activity. Can J Fish Aquat Sci 50: 656-658, 1993.
48. McCormick SD. Ontogeny and evolution of salinity tolerance in anadromous salmonids: Hormones and heterochrony. Estuaries 17: 26-33, 1994.
49. McCormick SD, Kelley KM, Young G, Nishioka RS, and Bern HA. Stimulation of coho salmon growth by insulin-like growth factor-I. Gen Comp Endocrinol 86: 398-406, 1992.
50. McCormick SD, O'Dea MF, Moeckel AM, and Björnsson BT. Endocrine and physiological changes in Atlantic salmon smolts following hatchery release. Aquaculture 222: 45-57, 2003.
51. McCormick SD, Sakamoto T, Hasegawa S, and Hirano T. Osmoregulatory actions of insulin-like growth factor-I in rainbow trout (Oncorhynchus mykiss). J Endocrinol 130, 1991.
52. Mommsen TP, Vijayan MM, and Moon TW. Cortisol in teleosts: dynamics, mechanisms of action and metabolic regulation. Rev Fish Biol Fisheries 9: 211-268, 1999.
53. Moriyama S. Increased plasma insulin-like growth factor-I (IGF-I) following oral and intraperitoneal administration of growth hormone to rainbow trout, Oncorhynchus mykiss. Growth Regul 5: 164-167, 1995.
54. Moriyama S, Dickhoff WW, and Plisetskaya EM. Isolation and characterization of insulin-like growth factor-I from rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 99: 221-229, 1995.
55. Moriyama S, Shimma H, Tagawa M, and Kagawa H. Changes in plasma insulin-like growth factor-I levels in the precociously maturing amago salmon, Oncorhynchus masou ishikawai. Fish Physiol Biochem 17: 253-259, 1997.
56. Moriyama S, Swanson P, Nishii M, Takahashi A, Kawauchi H, Dickhoff W, and Plisetskaya E. Development of a homologous radioimmunoassay for coho salmon Insulin-like growth factor I. Gen Comp Endocrinol 96: 149-161, 1994.
57. Nielsen C, Holdensgaard G, Petersen HC, Bjornsson TB, and Madsen SS. Genetic differences in physiology, growth hormone levels and migratory behavior of Atlantic salmon smolts. J Fish Biol 59: 28-44, 2001.
58. Nilsen TO, Ebbesson LOE, and Stefansson SO. Smolting in anadromous and landlocked strains of Atlantic salmon (Salmo salar). Aquaculture 222: 71-82, 2003.
59. Niu PD and Le Bail P.-Y. Presence of insulin-like growth factor binding protein (IGF-BP) in rainbow trout (Oncorhynchus mykiss) serum. J Exp Zool 265: 627-636, 1993.
60. Niu PD, Perez-Sanchez J and Le Bail P.-Y. Development of a protein binding assay for teleost insulin-like growth factor (IGF)-like: relationships between growth hormone (GH) and IGF-like in the blood of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 11: 381-391, 1993.
61. Ogasawara T, Hirano T, Akiyama T, Arai S, and Tagawa M. Changes in plasma prolactin and growth hormone concentrations during freshwater adaptation of juvenile chum salmon (Oncorhynchus keta) reared in sea-water for a prolonged period. Fish Physiol Biochem 1: 309-313, 1989.
62. Park R, Shepherd BS, Nishioka RS, Grau EG, and Bern HA. Effects of homologous pituitary hormone treatment on serum insulin-like growth factor-binding proteins (IGFBPs) in hypophysectomized tilapia, Oreochromis mossambicus, with special reference to a novel 20 kDa IGFBP. Gen Comp Endocrinol 117: 404-412, 2000.
63. Peterson BC, Simpson PR, Cain KD, Hardy RH, Schelling GT, and Ott TL. Effects of administration of somatostatin-14 and immunoneutralization of somatostatin on endocrine and growth responses in rainbow trout. J Fish Biol 63: 1-17, 2003.
64. Pierce AL, Beckman BR, Shearer KD, Larsen DA, and Dickhoff WW. Effects of ration on somatotropic hormones and growth in coho salmon. Comp Biochem Physiol B 128: 255-264, 2001.
65. Prunet P, Avella M, Foster A, Bjornsson B, Boeuf G, and Baux C. Roles of prolactin in salmonids. In: Progress in Comparative Endocrinology, edited by Epple A, Scanes CG, and Stetson MH. New York: Wiley-Liss, 1990, p. 547-552.
66. Prunet P, Bouef G, and Houdebine LM. Plasma and pituitary prolactin levels in rainbow trout during adaptation to different salinities. J Exp Zool 235: 187-196, 1985.
67. Rajaram S, Baylink DJ, and Mohan S. Insulin-like growth factor-binding proteins in serum and other biological fluids: Regulation and functions. Endocr Rev 18: 801-831, 1997.
68. Rechler MM. Insulin-like growth factor binding proteins. Vitam Horm 47: 1-114, 1993.
69. Riley LG, Hirano T, and Grau EG. Disparate effects of gonadal steroid hormones on plasma and liver mRNA levels of insulin-like growth factor-I and vitellogenin in the tilapia, Oreochromis mossambicus. Fish Physiol Biochem 26: 223-230, 2002.
70. Riley LG, Hirano T, and Grau EG. Effects of transfer from seawater to fresh water on the growth hormone/insulin-like growth factor-I axis and prolactin in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol B Biochem Mol Biol 136: 647-655, 2003.
71. Sakamoto T and Hirano T. Expression of insulin-like growth factor 1 gene in osmoregulatory organs during seawater adaptation of the salmonid fish: possible mode of osmoregulatory action of growth hormone. Proc Nail Acad Sci USA 90: 1912-1916, 1993.
72. Sakamoto T and Hirano T. Growth hormone receptors in the liver and osmoregulatory organs of rainbow trout: characterization and dynamics during adaptation to seawater. J Endocrinol 130: 425-433, 1991.
73. Sakamoto T, Iwata M, and Hirano T. Kinetic studies of growth hormone and prolactin during adaptation of coho salmon, Oncorhynchus kisutch, to different salinities. Gen Comp Endocrinol 82, 1991.
74. Sakamoto T, McCormick SD, and Hirano T. Osmoregulatory actions of growth hormone and its mode of action in salmonids: a review. Fish Physiol Biochem 11: 155-164, 1993.
75. Sakamoto T, Ogasawara T, and Hirano T. Growth hormone kinetics during adaptation to a hyperosmotic environment in rainbow trout. J Comp Physiol 160B: 1-6, 1990.
76. Shamblott MI, Cheng CM, Bolt D, and Chen TT. Appearance of insulin-like growth factor mRNA in the liver pyloric ceca of a teleost in response to exogenous growth hormone. Proc Natl Acad Sci USA 92: 6943-6946, 1995.
77. Shepherd BS, Weber GM, Vijayan MM, Seale AP, Kiley LG, Rodriguez MF, Richman NH III, Hirano T, and Grau EG. Control of growth in tilapia: Developments and prospects. In: Tilapias: Culture, Nutrition and Feeding, edited by Webster CD and Lim C. Binghamton, NY: Haworth. In Press.
78. Shimizu M, Hara A, and Dickhoff WW. Development of an RIA for salmon 41 kDa IGF-binding protein. J Endocrinol 178: 275-283, 2003.
79. Shimizu M, Swanson P, and Dickhoff WW. Free and protein-bound insulin-like growth factor-1 (IGF-I) and IGF-binding proteins in plasma of coho salmon, Oncorhynchus mykiss. Gen Comp Endocrinol 115: 398-405, 1999.
80. Shimizu M, Swanson P, Hara A, and Dickhoff WW. Purification of a 41-kDa insulin-like growth factor binding protein from serum of chinook salmon, Onchorhynchus tshawytscha. Gen Comp Endocrinol 132: 103-111, 2003.
81. Shimizu M, Swanson P, Haruhisa F, Hara A, and Bickhoff WW. Comparison of extraction methods and assay validation for salmon insulin-like growth factor using commercially available components. Gen Comp Endocrinol 119: 26-36, 2000.
82. Siharath K, Kelley KM, and Bern HA. A low-molecular-weight (25-kDa) IGF-binding protein is increased with growth inhibition in the fasting striped bass, Morone saxatilis. Gen Comp Endocrinol 102: 307-316, 1996.
83. Siharath K, Nishioka SS, Madsen SS, and Bern HA. Regulation of IGF-binding proteins by growth hormone in the striped bass, Morone saxatilis. Mol Mar Biol Biotechnol 4: 171-178, 1995.
84. Singer TD, Tucker SJ, Marshall WS, and Higgins CF. A divergent CFTR homolog: highly regulated salt transport in the euryhaline teleost F. heteroclitus. Am J Physiol Cell Physiol 274: C715-C723, 1998.
85. Somero G. Unity and diversity: a perspective on the methods, contributions, and future of comparative physiology. Annu Rev Physiol 62: 927-937, 2000.
86. Steele RGD and Torrie JH. Principles and Procedures of Statistics: A. Biometrical Approach. New York: McGraw-Hill, 1980.
87. Thissen JP, Ketelslegers JM, and Underwood LE. Nutritional regulation of the Insulin-like growth factors. Endocr Rev 15: 80-101, 1994.
88. Ugedal O, Finstad B, Damsgård B, and Mortensen A. Seawater tolerance and downstream migration in hatchery-reared and wild brown trout. Aquaculture 168: 395-405, 1998.
89. Varnavsky VS, Sakamoto T, and Hirano T. Effects of premature seawater transfer arid fasting on plasma growth hormone levels of yearling coho salmon (Oncorhynchus kisutch) parr. Aquaculture 135: 141-145, 1995.
90. Vijayan MM, Raptis S, and Sathiyaa R. Cortisol treatment affects glucocorticoid receptor and glucorticoid-responsive genes in the liver of rainbow trout. Gen Comp Endocrinol 132: 256-263, 2003.
91. Vijayan MM, Morgan JD, Sakamoto T, Grau EG, and Iwama GK. Food-deprivation affects seawater acclimation in tilapia: hormonal and metabolic changes. J Exp Biol 199: 2467-2475, 1996.
92. Yada T, Hirano T, and Grau EG. Changes in plasma levels of the two prolactins and growth hormone during adaptation to different salinities in the euryhaline tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 93: 214-223, 1994.
93. Yada T, Kazutaka T, and Hirano T. Seasonal changes in seawater adaptability and plasma levels, of prolactin and growth hormone in land-locked sockeye salmon (Oncorhynchus nerka) and amago salmon (O. rhodurus). Gen Comp Endocrinol 82: 33-44, 1991.
94. Yada T, Kobayashi T, Urano A, and Hirano T. Changes in growth hormone and prolactin messenger ribonucleic acid levels during seawater adaptation of amago salmon (Oncorhynchus rhodurus). J Exp Zool 262: 420-425, 1992.
95. Yada T, Urano A, and Hirano T. Growth hormone and prolactin gene expression and release in the pituitary of rainbow trout in serum-free culture. Endocrinology 129: 1183-1192, 1991.
96. Young G, Bjornsson TB, Prunet P, Lin RJ, and Bern HA. Smoltification and seawater adaptation in coho salmon (Oncorhynchus kisutch): plasma prolactin, growth hormone, thyroid hormones and cortisol. Gen Comp Endocrinol 74: 335-345, 1989.
97. Zydlewski GB, Foott JS, Nichols K, Hamelberg S, Zydlewski J, and Bjornsson BT. Enhanced smolt characteristics of steelhead trout exposed to alternative hatchery conditions during the final months of rearing. Aquaculture 222: 101-117, 2003.