Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T13:47:27.489Z Has data issue: false hasContentIssue false

Ontogenic study of insulin-like growth factor-1 and growth hormone receptor mRNA expression in porcine liver and skeletal muscle

Published online by Cambridge University Press:  02 September 2010

J. M. Brameld
Affiliation:
Department of Applied Biochemistry and Food Science, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD
P. A. Weller
Affiliation:
Department of Applied Biochemistry and Food Science, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD
J. M. Pell
Affiliation:
Department of Cellular Physiology, The Babraham Institute, Babraham, Cambridge CB2 4AT
P. J. Buttery
Affiliation:
Department of Applied Biochemistry and Food Science, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD
R. S. Gilmour
Affiliation:
Department of Cellular Physiology, The Babraham Institute, Babraham, Cambridge CB2 4AT
Get access

Abstract

The growth hormone-insulin-like growth factor (GH-IGF) axis is involved in the control of postnatal growth in all animals studied to date. At birth, blood levels of IGF-1 are low, although levels of GH are high. Thus a switching occurs during the postnatal period, which involves an increase in liver GH-receptors (GHR). This study investigates the changes in serum IGF-1 and IGF-1 and GHR mRNA in liver and skeletal muscle of growing pigs. The period from birth to 20 days of age showed a gradual increase in both IGF-1 and GHR mRNA expression by the liver, thus accounting for the gradual increase in serum IGF-1. The IGF-1 mRNA expressed was found to be predominantly class 1 transcripts with very few class 2 transcripts. There was a plateau of liver IGF-1 mRNA levels after 20 days and up to 140 days, even though the expression of GHR mRNA continued to increase. The levels of expression of the two genes were found to correlate in the first 20-day period (r = 0·76, P < 0·005), but not in the later period (r = 0·44, P > 0·05).

Levels of expression of both genes in the LD muscle were highly variable, with no age related changes being observed. However, a significant negative correlation of expression of the two genes was observed (R = 0·60, P < 0·001), with the correlation still being significant in the two age periods.

The data are consistent with a likely initial dependence for postnatal growth upon GH-stimulated IGF-1 mRNA expression by the liver, up to 20 days of age. After this time, hepatic expression of IGF-1 mRNA reaches a plateau, even though the serum IGF-1 and hepatic GHR mRNA levels continue to rise. A possible explanation for this could be an increase in either turn-over or stability of IGF-1 mRNA, giving rise to increased levels of peptide with no apparent change in mRNA level. Another possibility is that an increased expression/production of the IGF-binding proteins leads to an increase in the half-life of the peptide in the circulation.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamo, M., Lowe, W. L., LeRoith, D. and Roberts, C. T. 1989. Insulin-like growth factor-I messenger ribonucleic acids with alternative 5'-untranslated regions are differentially expressed during development in the rat. Endocrinology 124: 27372744.CrossRefGoogle ScholarPubMed
Ambler, G. R., Breier, B. H., Surus, A., Blair, H. T., McCutcheon, S. N., Silbergeld, A. and Gluckman, P. D. 1992. The interrelationship between and the regulation of hepatic growth hormone receptors and circulating GH binding protein in the pig. Acta Endocrinologica 126: 155161.Google ScholarPubMed
Baumbach, W. R., Horner, D. L. and Logan, J. S. 1989. The growth hormone-binding protein in rat serum is an alternatively spliced form of the rat growth hormone receptor. Genes and Development 3: 11991205.CrossRefGoogle ScholarPubMed
Bichell, D. P., Kikuchi, K. and Rotwein, P. 1992. Growth hormone rapidly activates insulin-like growth factor-I gene transcription in vivo. Molecular Endocrinology 6: 18991908.Google ScholarPubMed
Brameld, J. M., Weller, P. A., Saunders, J. C., Buttery, P. J. and Gilmour, R. S. 1995. Hormonal control of insulin-like growth factor-1 and growth hormone receptor mRNA expression by porcine hepatocytes in culture, journal of Endocrinology 146: 239245.CrossRefGoogle ScholarPubMed
Breier, B. H., Gluckman, P. D., Blair, H. T. and McCutcheon, S. N. 1989. Somatotrophic receptors in hepatic tissue of the developing male pig. journal of Endocrinology 123: 2531.CrossRefGoogle ScholarPubMed
Buonomo, F. C. and Klindt, J. 1993. Ontogeny of growth hormone (GH), insulin-like growth factors (IGF-I and IGFII) and IGF binding protein-2 (IGFBP-2) in genetically lean and obese swine. Domestic Animal Endocrinology 10: 257265.CrossRefGoogle ScholarPubMed
Chomczynski, P. and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162: 156159.CrossRefGoogle ScholarPubMed
Daughaday, W. H., Hall, K., Raben, M. S., Salmon, W. D., Van den Brande, J. L. and Van Wyk, J. I. 1972. Somatomedin: a proposed designation for the ‘sulfation factor’. Nature, London 235: 107108.CrossRefGoogle Scholar
Dauncey, M. J., Burton, K. A., White, P., Harrison, A. P., Gilmour, R. S., Duchamp, C. and Cattaneo, D. 1994. Nutritional regulation of growth hormone receptor gene expression. FASEB Journal 8: 8188.CrossRefGoogle ScholarPubMed
D'Ercole, A. I., Stiles, A. D. and Underwood, L. E. 1984. Tissue concentration of somatomedin-C: further evidence for multiple sites of synthesis and paracrine or autocrine mechanisms of action. Proceedings of the National Academy Sciences USA 81: 935939.CrossRefGoogle ScholarPubMed
Dickson, M. C., Saunders, J. C. and Gilmour, R. S. 1991. The ovine insulin-like growth factor-I gene: characterization, expression and identification of a putative promoter, journal of Molecular Endocrinology 6: 1731.CrossRefGoogle ScholarPubMed
Foyt, H. L., Lanau, F., Woloschak, M., LeRoith, D. and Roberts, C. T. 1992. Effect of growth hormone on levels of differentially processed insulin-like growth factor I mRNAs in total and polysomal mRNA populations. Molecular Endocrinology 6: 18811888.Google ScholarPubMed
Kikuchi, K., Buonomo, F. C., Kajimoto, Y. and Rotwein, P. 1991. Expression of insulin-like growth factor-I during chicken development. Endocrinology 128: 13231328.CrossRefGoogle ScholarPubMed
Lee, C. Y., Bazer, F. W., Etherton, T. D. and Simmen, F. A. 1991. Ontogeny of insulin-like growth factors (IGF-I and IGF-II) and IGF-binding proteins in porcine serum during fetal and postnatal development. Endocrinology 128: 23362344.CrossRefGoogle ScholarPubMed
Lee, C. Y., Chung, C. S. and Simmen, F. A. 1993. Ontogeny of the porcine insulin-like growth factor system. Molecular and Cellular Endocrinology 93: 7180.CrossRefGoogle ScholarPubMed
Louveau, I., Bonneau, M. and Salter, D. N. 1991. Agerelated changes in plasma porcine growth hormone (GH)profiles and insulin-like growth factor-I (IGF-I) concentrations in Large White and Meishan pigs. Reproduction Nutrition Development 31: 205216.CrossRefGoogle ScholarPubMed
Louveau, I. and Etherton, T. D. 1992. Partial purification of somatotropin receptors from pig liver: they arise from a single somatotropin receptor messenger RNA transcript. journal of Animal Science 70: 34213428.CrossRefGoogle ScholarPubMed
Lund, P. K., Moats-Staats, B. M., Hynes, M. A., Simmons, J. G., Jansen, M., D'Ercole, A. J. and Van Wyk, J. J. 1986. Somatomedin-C/insulin-like growth factor-I and insulinlike growth factor-H mRNAs in rat fetal and adult tissues. Journal of Biological Chemistry 261: 45394544.CrossRefGoogle Scholar
Owens, P. C., Conlon, M. A., Campbell, R. G., Johnson, R. J., King, R. and Ballard, F. J. 1991. Developmental changes in growth hormone, insulin-like growth factors (IGF-I and IGF-II) and IGF-binding proteins in plasma of young growing pigs. Journal of Endocrinology 128: 439447.CrossRefGoogle ScholarPubMed
Pell, J. M., Saunders, J. C. and Gilmour, R. S. 1993. Differential regulation of transcription initiation from insulin-like growth factor-I (IGF-I) leader exons and of tissue IGF-I expression in response to changed growth hormone and nutritional status in sheep. Endocrinology 132: 17971807.CrossRefGoogle ScholarPubMed
Saunders, J. C., Dickson, M. C., Pell, J. M. and Gilmour, R. S. 1991. Expression of a growth hormone-responsive exon of the ovine insulin-like growth factor-I gene. Journal of Molecular Endocrinology 7: 233240.CrossRefGoogle ScholarPubMed
Singh, J. S., Rail, L. B. and Styne, D. M. 1991. Insulin-like growth factor-I and factor-II gene expression in BALB/cmouse liver during postnatal development. Biology of the Neonate 60: 718.CrossRefGoogle Scholar
Straus, D. S. 1994. Nutritional regulation of hormones and growth-factors that control mammalian growth. FASEB Journal 8: 612.CrossRefGoogle ScholarPubMed
Trivedi, B. and Daughaday, W. H. 1988. Release of growth hormone binding protein from IM-9 lymphocytes by endopeptidase is dependent on sulfydryl group inactivation. Endocrinology 123: 2201–206.CrossRefGoogle Scholar
Weller, P. A., Dauncey, M. J., Bates, P. C., Brameld, J. M., Buttery, P. J. and Gilmour, R. S. 1994. Regulation of porcine insulin-like growth factor-I and growth hormone receptor mRNA expression by energy status. American Journal of Physiology 266: E776–E785.Google ScholarPubMed
Weller, P. A., Dickson, M. C., Huskisson, N. S., Dauncey, M. J., Buttery, P. J. and Gilmour, R. S. 1993. The porcine insulin-like growth factor-I gene: characterization and expression of alternate transcription sites, journal of Molecular Endocrinology 11: 201211.CrossRefGoogle ScholarPubMed