Differential regulation of Igf1 and Igf2 mRNA levels in tilapia hepatocytes: Effects of insulin and cortisol on GH sensitivity

Journal of Endocrinology

Volumn 211, Issue 2, 2011, Pages 201-210

  Pierce, Andrew L ^a   Breves, Jason P ^a   Moriyama, Shunsuke ^b   Hirano, Tetsuya ^a   Grau, E Gordon ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b KITASATO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH HORMONE; HYDROCORTISONE; INSULIN; MESSENGER RNA; SOMATOMEDIN B; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; FETUS GROWTH; HORMONE SENSITIVITY; INSULIN RESPONSE; LIVER CELL; MALE; NONHUMAN; NUTRITIONAL STATUS; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; REPRODUCTION; TILAPIA;

EID: 83455211573     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-10-0456     Document Type: Article

References (77)

1. Ayson FG, de Jesus-Ayson EG & Takemura A 2007 mRNA expression patterns for GH, PRL, SL, IGF-I and IGF-II during altered feeding status in rabbitfish, Siganus guttatus. General and Comparative Endocrinology 150 196-204.
2. Balm PH, Pepels P, Helfrich S, Hovens ML & Bonga SE 1994 Adrenocorticotropic hormone in relation to interrenal function during stress in tilapia (Oreochromis mossambicus). General and Comparative Endocrinology 96 347-360.
3. Banos N, Planas JV, Gutierrez J & Navarro I 1999 Regulation of plasma insulin-like growth factor-I levels in brown trout (Salmo trutta). Comparative Biochemistry and Physiology 124C 33-40.
4. Beauloye V, Ketelslegers JM, Moreau B & Thissen JP 1999 Dexamethasone inhibits both growth hormone (GH)-induction of insulin-like growth factor-I (IGF-I) mRNA and GH receptor (GHR) mRNA levels in rat primary cultured hepatocytes. Growth Hormone and IGF Research 9 205-211.
5. Boni-Schnetzler M, Schmid C, Meier PJ & Froesch ER 1991 Insulin regulates insulin-like growth factor I mRNA in rat hepatocytes. American Journal of Physiology 260 E846-E851.
6. Brameld JM, Weller PA, Saunders JC, Buttery PJ & Gilmour RS 1995 Hormonal control of insulin-like growth factor-I and growth hormone receptor mRNA expression by porcine hepatocytes in culture. Journal of Endocrinology 146 239-245.
7. Breves JP, Hirano T & Grau EG 2010 Ionoregulatory and endocrine responses to disturbed salt and water balance in Mozambique tilapia exposed to confinement and handling stress. Comparative Biochemistry and Physiology 155A 294-300.
8. Butler ST, Marr AL, Pelton SH, Radcliff RP, Lucy MC & Butler WR 2003 Insulin restoresGHresponsiveness during lactation-induced negative energy balance in dairy cattle: effects on expression of IGF-I and GH receptor 1A. Journal of Endocrinology 176 205-217.
9. Carnevali O, Cardinali M, Maradonna F, Parisi M, Olivotto I, Polzonetti-Magni AM, Mosconi G & Funkenstein B 2005 Hormonal regulation of hepatic IGF-I and IGF-II gene expression in the marine teleost Sparus aurata. Molecular Reproduction and Development 71 12-18.
10. Chen J-Y, Chen J-C, Chang C-Y, Shen S-C, Chen M-S & Wu J-L 2000 Expression of recombinant tilapia insulin-like growth factor-I and stimulation of juvenile tilapia growth by injection of recombinant IGFs polypeptides. Aquaculture 181 347-360.
11. Chia DJ, Varco-Merth B & Rotwein P 2010 Dispersed chromosomal Stat5bbinding elements mediate growth hormone-activated insulin-like growth factor-I gene transcription. Journal of Biological Chemistry 285 17636-17647.
12. Codina M, Garcia de la serrana D, Sanchez-Gurmaches J, Montserrat N, Chistyakova O, Navarro I & Gutierrez J 2008 Metabolic and mitogenic effects of IGF-II in rainbow trout (Oncorhynchus mykiss) myocytes in culture and the role of IGF-II in the PI3K/Akt and MAPK signalling pathways. General and Comparative Endocrinology 157 116-124.
13. Denver RJ & Nicoll CS 1994 Pancreatic hormones differentially regulate insulin-like growth factor (IGF)-I and IGF-binding protein production by primary rat hepatocytes. Journal of Endocrinology 142 299-310.
14. Devlin RH, Sakhrani D, Tymchuk WE, Rise ML & Goh B 2009 Domestication and growth hormone transgenesis cause similar changes in gene expression in coho salmon (Oncorhynchus kisutch). PNAS 106 3047-3052.
15. Dickhoff WW, Beckman BR, Larsen DA, Duan C & Moriyama S 1997 The role of growth in endocrine regulation of salmonid smoltification. Fish Physiology and Biochemistry 17 231-236.
16. Eppler E, Berishvili G, Mazel P, Caelers A, Hwang G, Maclean N & Reinecke M 2010 Distinct organ-specific up- and down-regulation of IGF-I and IGF-II mRNA in various organs of a GH-overexpressing transgenic Nile tilapia. Transgenic Research 19 231-240.
17. Fox BK, Breves JP, Hirano T & Grau EG 2009 Effects of short- and long-term fasting on plasma and stomach ghrelin, and the growth hormone/insulinlike growth factor I axis in the tilapia, Oreochromis mossambicus. Domestic Animal Endocrinology 37 1-11.
18. Fruchtman S, Jackson L & Borski R 2000 Insulin-like growth factor I disparately regulates prolactin and growth hormone synthesis and secretion: studies using the teleost pituitary model. Endocrinology 141 2886-2894.
19. Gabillard JC, Kamangar BB & Montserrat N 2006 Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). Journal of Endocrinology 191 15-24.
20. Gahr SA, Vallejo RL, Weber GM, Shepherd BS, Silverstein JT & Rexroad CE III 2008 Effects of short-term growth hormone treatment on liver and muscle transcriptomes in rainbow trout (Oncorhynchus mykiss). Physiological Genomics 32 380-392.
21. Goya L, de la Puente A, Ramos S, Martin MA, Escriva F & Pascual-Leone AM 1999 Regulation of insulin-like growth factor-I and -II by glucose in primary cultures of fetal rat hepatocytes. Journal of Biological Chemistry 274 24633-24640.
22. Griffen SC, Russell SM, Katz LS & Nicoll CS 1987 Insulin exerts metabolic and growth-promoting effects by a direct action on the liver in vivo: clarification of the functional significance of the portal vascular link between the beta cells of the pancreatic islets and the liver. PNAS 84 7300-7304.
23. Haig D 1993 Genetic conflicts in human pregnancy. Quarterly Review of Biology 68 495-532.
24. Holly JMP 1998 Editorial: the IGF-II enigma. Growth Hormone and IGF Research 8 183-184.
25. vonHornH, EkstromC, Ellis E, OlivecronaH, EinarssonC, TallyM&Ekstrom TJ 2002 GH is a regulator of IGF2 promoter-specific transcription in human liver. Journal of Endocrinology 172 457-465.
26. Houston B & O'Neill IE 1991 Insulin and growth hormone act synergistically to stimulate insulin-like growth factor-I production by cultured chicken hepatocytes. Journal of Endocrinology 128 389-393.
27. Humbel RE 1990 Insulin-like growth factors I and II. European Journal of Biochemistry 190 445-462.
28. Jones JI & Clemmons DR 1995 Insulin-like growth factors and their binding proteins: biological actions. Endocrine Reviews 16 3-34.
29. Kajimura S, Uchida K, Yada T, Riley LG, Byatt JC, Collier RJ, Aida K, Hirano T & Grau EG 2001 Stimulation of insulin-like growth factor-I production by recombinant bovine growth hormone in Mozambique tilapia, Oreochromis mossambicus. Fish Physiology and Biochemistry 25 221-230.
30. Kajimura S, Hirano T, Visitacion N, Moriyama S, Aida K & Grau EG 2003 Dual mode of cortisol action on GH/IGF-I/IGF binding proteins in the tilapia, Oreochromis mossambicus. Journal of Endocrinology 178 91-99.
31. Leung LY, Kwong AK, Man AK & Woo NY 2008 Direct actions of cortisol, thyroxine and growth hormone on IGF-I mRNA expression in sea bream hepatocytes. Comparative Biochemistry and Physiology 151A 705-710.
32. Lo JH & Chen TT 2010 CCAAT/enhancer binding protein beta 2 is involved in growth hormone-regulated insulin-like growth factor-II gene expression in the liver of rainbow trout (Oncorhynchus mykiss). Endocrinology 151 2128-2139.
33. Lo JH, Chiou PP, Lin CM & Chen TT 2007Molecular cloning and expression analysis of rainbow trout (Oncorhynchus mykiss) CCAAT/enhancer binding protein genes and their responses to induction by GH in vitro and in vivo. Journal of Endocrinology 194 393-406.
34. Luckenbach JA, Dickey JT & Swanson P 2010 Regulation of pituitary GnRH receptor and gonadotropin subunits by IGF1 and GnRH in prepubertal male coho salmon. General and Comparative Endocrinology 167 387-396.
35. Meton I, Boot EP, Sussenbach JS & Steenbergh PH 1999 Growth hormone induces insulin-like growth factor-I gene transcription by a synergistic action of STAT5 and HNF-1 alpha. FEBS Letters 444 155-159.
36. Mommsen TP & Plisetskaya EM 1991 Insulin in fishes and agnathans: history, structure, and metabolic regulation. Reviews in Aquatic Sciences 4 225-259.
37. Moriyama S, Oda M, Yamazaki T, Yamaguchi K, Amiya N, Takahashi A, Amano M, Goto T, Nozaki M, Meguro H et al. 2008a Gene structure and functional characterization of growth hormone in dogfish, Squalus acanthias. Zoological Science 25 604-613.
38. Moriyama S, Yamaguchi K, Takasawa T, Chiba H & Kawauchi H 2008b Identification of two insulin-like growth factor IIs in the Japanese eel, Anguilla japonica: cloning, tissue distribution, and expression after growth hormone treatment and seawater acclimation. Comparative Biochemistry and Physiology 149B 47-57.
39. Olivecrona H, Hilding A, Ekstrom C, Barle H, Nyberg B, Moller C, Delhanty PJ, Baxter RC, Angelin B, Ekstrom TJ et al. 1999 Acute and short-term effects of growth hormone on insulin-like growth factors and their binding proteins: serum levels and hepatic messenger ribonucleic acid responses in humans. Journal of Clinical Endocrinology and Metabolism 84 553-560.
40. O'Neill MJ, Lawton BR, Mateos M, Carone DM, Ferreri GC, Hrbek T, Meredith RW, Reznick DN & O'Neill RJ 2007 Ancient and continuing Darwinian selection on insulin-like growth factor II in placental fishes. PNAS 104 12404-12409.
41. Palamarchuk AY, Kavsan VM, Sussenbach JS & Holthuizen PE 2001 The chum salmon insulin-like growth factor II promoter requires Sp1 for its activation by C/EBPbeta. Molecular and Cellular Endocrinology 172 57-67.
42. Peterson BC & Waldbieser GC 2009 Effects of fasting on IGF-I, IGF-II, and IGF-binding protein mRNA concentrations in channel catfish (Ictalurus punctatus). Domestic Animal Endocrinology 37 74-83.
43. Peterson BC, Waldbieser GC & Bilodeau L 2004 IGF-I and IGF-II mRNA expression in slow and fast growing families of USDA103 channel catfish (Ictalurus punctatus). Comparative Biochemistry and Physiology 139A 317-323.
44. Peterson BC, Waldbieser GC & Bilodeau L 2005 Effects of recombinant bovine somatotropin on growth and abundance of mRNA for IGF-I and IGF-II in channel catfish (Ictalurus punctatus). Journal of Animal Science 83 816-824.
45. Phillips LS, Pao CI & Villafuerte BC 1998 Molecular regulation of insulin-like growth factor-I and its principal binding protein, IGFBP-3. Progress in Nucleic Acid Research and Molecular Biology 60 195-265.
46. Picha ME, Turano MJ, Beckman BR & Borski RJ 2008a Endocrine biomarkers of growth and applications to aquaculture: a minireview of growth hormone, insulin-like growth factor (IGF)-I, and IGF-binding proteins as potential growth indicators in fish. North American Journal of Aquaculture 70 196-211.
47. Picha ME, Turano MJ, Tipsmark CK & Borski RJ 2008b Regulation of endocrine and paracrine sources of Igfs and GH receptor during compensatory growth in hybrid striped bass (Morone chrysops!Morone saxatilis). Journal of Endocrinology 199 81-94.
48. Pierce AL, Dickey JT, Larsen DA, Fukada H, Swanson P & Dickhoff WW 2004 A quantitative real-time RT-PCR assay for salmon IGF-I mRNA, and its application in the study of GH regulation of IGF-I gene expression in primary culture of salmon hepatocytes. General and Comparative Endocrinology 135 401-411.
49. Pierce AL, Fukada H & Dickhoff WW 2005 Metabolic hormones modulate the effect of growth hormone (GH) on insulin-like growth factor-I (IGF-I) mRNA level in primary culture of salmon hepatocytes. Journal of Endocrinology 184 341-349.
50. Pierce AL, Fox BK, Davis LK, Visitacion N, Kitahashi T, Hirano T & Grau EG 2007 Prolactin receptor, growth hormone receptor, and putative somatolactin receptor in Mozambique tilapia: tissue specific expression and differential regulation by salinity and fasting. General and Comparative Endocrinology 154 31-40.
51. Pierce AL, Dickey JT, Felli L, Swanson P & Dickhoff WW 2010 Metabolic hormones regulate basal and growth hormone-dependent igf2 mRNA level in primary cultured coho salmon hepatocytes: effects of insulin, glucagon, dexamethasone, and triiodothyronine. Journal of Endocrinology 204 331-339.
52. Plisetskaya EM&Sullivan CV 1989 Pancreatic and thyroid hormones in rainbow trout (Salmo gairdneri): what concentration does the liver see? General and Comparative Endocrinology 75 310-315
53. Ponce M, InfanteC, Funes V & ManchadoM 2008 Molecular characterization and gene expression analysis of insulin-like growth factors I and II in the redbanded seabream, Pagrus auriga: transcriptional regulation by growth hormone. Comparative Biochemistry and Physiology 150B 418-426.
54. Pozios KC, Ding J, Degger B, Upton Z & Duan C 2001 IGFs stimulate zebrafish cell proliferation by activating MAP kinase and PI3-kinasesignaling pathways. American Journal of Physiology 280 R1230-R1239.
55. Reinecke M & Collet C 1998 The phylogeny of the insulin-like growth factors. International Review of Cytology 183 1-94.
56. Rodgers BD, Lau AO & Nicoll CS 1994 Hypophysectomy or adrenalectomy of rats with insulin-dependent diabetes mellitus partially restores their responsiveness to growth hormone. Proceedings of the Society for Experimental Biology and Medicine 207 220-226.
57. Rosenfeld RG & Hwa V 2009 The growth hormone cascade and its role in mammalian growth. Hormone Research 71 36-40.
58. Schmid AC, Reinecke M & Kloas W 2000 Primary cultured hepatocytes of the bony fish, Oreochromis mossambicus, the tilapia: a valid tool for physiological studies on IGF-I expression in liver. Journal of Endocrinology 166 265-273.
59. Shamblott MJ, Cheng CM, Bolt D & Chen TT 1995 Appearance of insulinlike growth factor mRNA in the liver and pyloric ceca of a teleost in response to exogenous growth hormone. PNAS 92 6943-6946.
60. Shamblott MJ, Leung S, Greene MW & Chen TT 1998 Characterization of a teleost insulin-like growth factor II (IGF-II) gene: evidence for promoter CCAAT/enhancer-binding protein (C/EBP) sites, and the presence of hepatic C/EBP. Molecular Marine Biology and Biotechnology 7 181-190.
61. Specker JL, King DS, Nishioka RS, Shirahata K, Yamaguchi K & Bern HA 1985 Isolation and partial characterization of a pair of prolactins released in vitro by the pituitary of a cichlid fish, Oreochromis mossambicus. PNAS 82 7490-7494.
62. Stratikopoulos E, Szabolcs M, Dragatsis I, Klinakis A & Efstratiadis A 2008 The hormonal action of IGF1 in postnatal mouse growth. PNAS 105 19378-19383.
63. TatarM, Bartke A & Antebi A 2003 The endocrine regulation of aging by insulin-like signals. Science 299 1346-1351.
64. TerovaG, Rimoldi S, ChiniV, Gornati R, Bernardini G & Saroglia M 2007 Cloning and expression analysis of insulin-like growth factor I and II in liver and muscle of sea bass (Dicentrarchus labrax, L.) during long-termfasting and refeeding. Journal of Fish Biology 70 219-233.
65. Thissen JP, Ketelslegers JM & Underwood LE 1994 Nutritional regulation of the insulin-like growth factors. Endocrine Reviews 15 80-101.
66. Thissen JP, Underwood LE & Ketelslegers JM1999 Regulation of insulin-like growth factor-I in starvation and injury. Nutrition Reviews 57 167-176.
67. Tollet P, Enberg B & Mode A 1990 Growth hormone (GH) regulation of cytochrome P-450IIC12, insulin-like growth factor-I (IGF-I), and GH receptor messenger RNA expression in primary rat hepatocytes: a hormonal interplay with insulin, IGF-I, and thyroid hormone. Molecular Endocrinology 4 1934-1942.
68. Tse MC, Vong QP, Cheng CH & Chan KM 2002 PCR-cloning and gene expression studies in common carp (Cyprinus carpio) insulin-like growth factor-II. Biochimica et Biophysica Acta 1575 63-74.
69. Tse MC, Chan KM & Cheng CH 2008 Cloning, characterization and promoter analysis of the common carp IGF-II gene. Gene 412 26-38.
70. Uchida K, Kajimura S, Riley LG, Hirano T, Aida K & Grau EG 2003 Effects of fasting on growth hormone/insulin-like growth factor I axis in the tilapia, Oreochromis mossambicus. Comparative Biochemistry and Physiology 134A 429-439.
71. Villafuerte BC, Phillips LS, Rane MJ & Zhao W 2004 Insulin-response element-binding protein 1: a novel Akt substrate involved in transcriptional action of insulin. Journal of Biological Chemistry 279 36650-36659.
72. Vong QP, Chan KM & Cheng CH 2003a Quantification of common carp (Cyprinus carpio) IGF-I and IGF-II mRNA by real-time PCR: differential regulation of expression by GH. Journal of Endocrinology 178 513-521.
73. Vong QP, Chan KM, Leung K & Cheng CH 2003b Common carp insulinlike growth factor-I gene: complete nucleotide sequence and functional characterization of the 50-flanking region. Gene 322 145-156.
74. Weber GM & Grau EG 1999 Changes in serum concentrations and pituitary content of the two prolactins and growth hormone during the reproductive cycle in female tilapia, Oreochromis mossambicus, compared with changes during fasting. Comparative Biochemistry and Physiology 124 323-335.
75. White YA, Kyle JT &Wood AW2009 Targeted gene knockdown in zebrafish reveals distinct intraembryonic functions for insulin-like growth factor II signaling. Endocrinology 150 4366-4375.
76. Wilkinson RJ, Porter M, Woolcott H, Longland R & Carragher JF 2006 Effects of aquaculture related stressors and nutritional restriction on circulating growth factors (GH, IGF-I and IGF-II) in Atlantic salmon and rainbow trout. Comparative Biochemistry and Physiology 145 214-224.
77. Wood AW, Duan C & Bern HA 2005 Insulin-like growth factor signaling in fish. International Review of Cytology 243 215-285.