Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Mar 1;90(5):1912–1916. doi: 10.1073/pnas.90.5.1912

Expression of insulin-like growth factor I gene in osmoregulatory organs during seawater adaptation of the salmonid fish: possible mode of osmoregulatory action of growth hormone.

T Sakamoto 1, T Hirano 1
PMCID: PMC45990  PMID: 8446608

Abstract

Growth hormone has been shown to contribute to seawater adaptation of salmonid fishes. The growth influence of growth hormone is mediated largely by hepatic production of insulin-like growth factor I (IGF-I). To study the growth hormone-IGF-I axis in osmoregulation, we measured IGF-I mRNA in the liver, gill, and body kidney from rainbow trout by Northern analysis. The levels of IGF-I mRNA in all tissues increased significantly after injection of growth hormone. Transfer of trout from fresh water to 80% seawater evoked an increase in plasma growth hormone after 1 day. IGF-I mRNA was not altered significantly in the liver, but it was increased in the gill and body kidney after 1 and 8 days, respectively. These observations indicate that the IGF-I gene is expressed differently among these organs during seawater adaptation. Growth hormone may stimulate hypoosmoregulatory ability by inducing local expression of IGF-I in osmoregulatory organs, although the possibility that IGF-I expression might occur in part independently of growth hormone during seawater adaptation cannot be excluded.

Full text

PDF
1914

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arteaga C. L., Kitten L. J., Coronado E. B., Jacobs S., Kull F. C., Jr, Allred D. C., Osborne C. K. Blockade of the type I somatomedin receptor inhibits growth of human breast cancer cells in athymic mice. J Clin Invest. 1989 Nov;84(5):1418–1423. doi: 10.1172/JCI114315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Björnsson B. T., Yamauchi K., Nishioka R. S., Deftos L. J., Bern H. A. Effects of hypophysectomy and subsequent hormonal replacement therapy on hormonal and osmoregulatory status of coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol. 1987 Dec;68(3):421–430. doi: 10.1016/0016-6480(87)90081-5. [DOI] [PubMed] [Google Scholar]
  3. Blazer-Yost B. L., Cox M., Furlanetto R. Insulin and IGF I receptor-mediated Na+ transport in toad urinary bladders. Am J Physiol. 1989 Oct;257(4 Pt 1):C612–C620. doi: 10.1152/ajpcell.1989.257.4.C612. [DOI] [PubMed] [Google Scholar]
  4. Bolton J. P., Collie N. L., Kawauchi H., Hirano T. Osmoregulatory actions of growth hormone in rainbow trout (Salmo gairdneri). J Endocrinol. 1987 Jan;112(1):63–68. doi: 10.1677/joe.0.1120063. [DOI] [PubMed] [Google Scholar]
  5. Bolton J. P., Takahashi A., Kawauchi H., Kubota J., Hirano T. Development and validation of a salmon growth hormone radioimmunoassay. Gen Comp Endocrinol. 1986 May;62(2):230–238. doi: 10.1016/0016-6480(86)90113-9. [DOI] [PubMed] [Google Scholar]
  6. Cao Q. P., Duguay S. J., Plisetskaya E., Steiner D. F., Chan S. J. Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor I mRNA. Mol Endocrinol. 1989 Dec;3(12):2005–2010. doi: 10.1210/mend-3-12-2005. [DOI] [PubMed] [Google Scholar]
  7. Chin E., Zhou J., Bondy C. Anatomical relationships in the patterns of insulin-like growth factor (IGF)-I, IGF binding protein-1, and IGF-I receptor gene expression in the rat kidney. Endocrinology. 1992 Jun;130(6):3237–3245. doi: 10.1210/endo.130.6.1375897. [DOI] [PubMed] [Google Scholar]
  8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  9. Clarke W. C., Farmer S. W., Hartwell K. M. Effect of teleost pituitary growth hormone on growth of Tilapia mossambica and on growth and seawater adaptation of sockeye salmon (Oncorhynchus nerka). Gen Comp Endocrinol. 1977 Oct;33(2):174–178. doi: 10.1016/0016-6480(77)90241-6. [DOI] [PubMed] [Google Scholar]
  10. Daughaday W. H. A personal history of the origin of the somatomedin hypothesis and recent challenges to its validity. Perspect Biol Med. 1989 Winter;32(2):194–211. doi: 10.1353/pbm.1989.0006. [DOI] [PubMed] [Google Scholar]
  11. Daughaday W. H., Rotwein P. Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum, and tissue concentrations. Endocr Rev. 1989 Feb;10(1):68–91. doi: 10.1210/edrv-10-1-68. [DOI] [PubMed] [Google Scholar]
  12. Dickson M. C., Saunders J. C., Gilmour R. S. The ovine insulin-like growth factor-I gene: characterization, expression and identification of a putative promoter. J Mol Endocrinol. 1991 Feb;6(1):17–31. doi: 10.1677/jme.0.0060017. [DOI] [PubMed] [Google Scholar]
  13. Duan C., Hirano T. Effects of insulin-like growth factor-I and insulin on the in-vitro uptake of sulphate by eel branchial cartilage: evidence for the presence of independent hepatic and pancreatic sulphation factors. J Endocrinol. 1992 May;133(2):211–219. doi: 10.1677/joe.0.1330211. [DOI] [PubMed] [Google Scholar]
  14. Fagin J. A., Melmed S. Relative increase in insulin-like growth factor I messenger ribonucleic acid levels in compensatory renal hypertrophy. Endocrinology. 1987 Feb;120(2):718–724. doi: 10.1210/endo-120-2-718. [DOI] [PubMed] [Google Scholar]
  15. Foskett J. K., Bern H. A., Machen T. E., Conner M. Chloride cells and the hormonal control of teleost fish osmoregulation. J Exp Biol. 1983 Sep;106:255–281. doi: 10.1242/jeb.106.1.255. [DOI] [PubMed] [Google Scholar]
  16. Fryer J. N. A radioreceptor assay for purified teleost growth hormone. Gen Comp Endocrinol. 1979 Oct;39(2):123–130. doi: 10.1016/0016-6480(79)90217-x. [DOI] [PubMed] [Google Scholar]
  17. GERSHBERG H., HEINEMANN H. O., STUMPF H. H. Renal function studies and autopsy report in a patient with gigantism and acromegaly. J Clin Endocrinol Metab. 1957 Mar;17(3):377–385. doi: 10.1210/jcem-17-3-377. [DOI] [PubMed] [Google Scholar]
  18. Gray E. S., Kelley K. M. Growth regulation in the gobiid teleost, Gillichthys mirabilis: roles of growth hormone, hepatic growth hormone receptors and insulin-like growth factor-I. J Endocrinol. 1991 Oct;131(1):57–66. doi: 10.1677/joe.0.1310057. [DOI] [PubMed] [Google Scholar]
  19. Gray E. S., Young G., Bern H. A. Radioreceptor assay for growth hormone in coho salmon (Oncorhynchus kisutch) and its application to the study of stunting. J Exp Zool. 1990 Dec;256(3):290–296. doi: 10.1002/jez.1402560308. [DOI] [PubMed] [Google Scholar]
  20. Green H., Morikawa M., Nixon T. A dual effector theory of growth-hormone action. Differentiation. 1985;29(3):195–198. doi: 10.1111/j.1432-0436.1985.tb00316.x. [DOI] [PubMed] [Google Scholar]
  21. Hernandez E. R., Resnick C. E., Svoboda M. E., Van Wyk J. J., Payne D. W., Adashi E. Y. Somatomedin-C/insulin-like growth factor I as an enhancer of androgen biosynthesis by cultured rat ovarian cells. Endocrinology. 1988 Apr;122(4):1603–1612. doi: 10.1210/endo-122-4-1603. [DOI] [PubMed] [Google Scholar]
  22. Hirschberg R., Kopple J. D. Effects of growth hormone and IGF-I on renal function. Kidney Int Suppl. 1989 Nov;27:S20–S26. [PubMed] [Google Scholar]
  23. Kikuchi K., Buonomo F. C., Kajimoto Y., Rotwein P. Expression of insulin-like growth factor-I during chicken development. Endocrinology. 1991 Mar;128(3):1323–1328. doi: 10.1210/endo-128-3-1323. [DOI] [PubMed] [Google Scholar]
  24. Komourdjian M. P., Saunders R. L., Fenwick J. C. The effect of porcine somatotropin on growth, and survival in seawater of Atlantic salmon (Salmo salar) parr. Can J Zool. 1976 Apr;54(4):531–535. doi: 10.1139/z76-060. [DOI] [PubMed] [Google Scholar]
  25. Kopple J. D., Hirschberg R. Physiological effects of growth hormone and insulin-like growth factor I on the kidney. Miner Electrolyte Metab. 1990;16(1):82–88. [PubMed] [Google Scholar]
  26. Kuribayashi K., Hikata M., Hiraoka O., Miyamoto C., Furuichi Y. A rapid and efficient purification of poly(A)-mRNA by oligo(dT)30-Latex. Nucleic Acids Symp Ser. 1988;(19):61–64. [PubMed] [Google Scholar]
  27. Luo J. M., Murphy L. J. Dexamethasone inhibits growth hormone induction of insulin-like growth factor-I (IGF-I) messenger ribonucleic acid (mRNA) in hypophysectomized rats and reduces IGF-I mRNA abundance in the intact rat. Endocrinology. 1989 Jul;125(1):165–171. doi: 10.1210/endo-125-1-165. [DOI] [PubMed] [Google Scholar]
  28. Madsen S. S. The role of cortisol and growth hormone in seawater adaptation and development of hypoosmoregulatory mechanisms in sea trout parr (Salmo trutta trutta). Gen Comp Endocrinol. 1990 Jul;79(1):1–11. doi: 10.1016/0016-6480(90)90082-w. [DOI] [PubMed] [Google Scholar]
  29. McCormick S. D., Bern H. A. In vitro stimulation of Na+-K+-ATPase activity and ouabain binding by cortisol in coho salmon gill. Am J Physiol. 1989 Mar;256(3 Pt 2):R707–R715. doi: 10.1152/ajpregu.1989.256.3.R707. [DOI] [PubMed] [Google Scholar]
  30. McCormick S. D., Sakamoto T., Hasegawa S., Hirano T. Osmoregulatory actions of insulin-like growth factor-I in rainbow trout (Oncorhynchus mykiss). J Endocrinol. 1991 Jul;130(1):87–92. doi: 10.1677/joe.0.1300087. [DOI] [PubMed] [Google Scholar]
  31. Miwa S., Inui Y. Effects of L-thyroxine and ovine growth hormone on smoltification of amago salmon (Oncorhynchus rhodurus). Gen Comp Endocrinol. 1985 Jun;58(3):436–442. doi: 10.1016/0016-6480(85)90116-9. [DOI] [PubMed] [Google Scholar]
  32. Murphy L. J., Murphy L. C., Friesen H. G. Estrogen induces insulin-like growth factor-I expression in the rat uterus. Mol Endocrinol. 1987 Jul;1(7):445–450. doi: 10.1210/mend-1-7-445. [DOI] [PubMed] [Google Scholar]
  33. Richman N. H., 3rd, Zaugg W. S. Effects of cortisol and growth hormone on osmoregulation in pre- and desmoltified coho salmon (Oncorhynchus kisutch). Gen Comp Endocrinol. 1987 Feb;65(2):189–198. doi: 10.1016/0016-6480(87)90165-1. [DOI] [PubMed] [Google Scholar]
  34. Rotwein P., Pollock K. M., Watson M., Milbrandt J. D. Insulin-like growth factor gene expression during rat embryonic development. Endocrinology. 1987 Dec;121(6):2141–2144. doi: 10.1210/endo-121-6-2141. [DOI] [PubMed] [Google Scholar]
  35. Sakamoto T., Hirano T. Growth hormone receptors in the liver and osmoregulatory organs of rainbow trout: characterization and dynamics during adaptation to seawater. J Endocrinol. 1991 Sep;130(3):425–433. doi: 10.1677/joe.0.1300425. [DOI] [PubMed] [Google Scholar]
  36. Sakamoto T., Iwata M., Hirano T. Kinetic studies of growth hormone and prolactin during adaptation of coho salmon, Oncorhynchus kisutch, to different salinities. Gen Comp Endocrinol. 1991 May;82(2):184–191. doi: 10.1016/0016-6480(91)90182-6. [DOI] [PubMed] [Google Scholar]
  37. Sara V. R., Hall K. Insulin-like growth factors and their binding proteins. Physiol Rev. 1990 Jul;70(3):591–614. doi: 10.1152/physrev.1990.70.3.591. [DOI] [PubMed] [Google Scholar]
  38. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  39. Yao K., Niu P. D., Le Gac F., Le Bail P. Y. Presence of specific growth hormone binding sites in rainbow trout (Oncorhynchus mykiss) tissues: characterization of the hepatic receptor. Gen Comp Endocrinol. 1991 Jan;81(1):72–82. doi: 10.1016/0016-6480(91)90126-q. [DOI] [PubMed] [Google Scholar]
  40. Young G. Enhanced response of the interrenal of coho salmon (Oncorhynchus kisutch) to ACTH after growth hormone treatment in vivo and in vitro. Gen Comp Endocrinol. 1988 Jul;71(1):85–92. doi: 10.1016/0016-6480(88)90298-5. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES