Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-12T19:40:05.825Z Has data issue: false hasContentIssue false
  • English
  • Français

Tissue-specific differences in insulin binding affinity and insulin receptor concentrations in skeletal muscles, adipose tissue depots and liver of cattle and sheep

Published online by Cambridge University Press:  18 August 2016

P. D. McGrattan ,
A. R. G. Wylie  and
J. Nelson
P. D. McGrattan
Affiliation:
Northern Ireland Regional Genetics Centre, Belfast City Hospital Trust, Belfast BT9 7AB, UK
A. R. G. Wylie
Affiliation:
Department of Agriculture for Northern Ireland (DANI) and School of Agriculture and Food Science, The Queen’s University of Belfast, Newforge Lane, Belfast BT9 5PX, UK
J. Nelson
Affiliation:
School of Biology and Biochemistry, The Queen’s University of Belfast Medical Biology Centre, Lisburn Road, Belfast, BT9 7BL, UK
Get access

Abstract

Differences in insulin binding affinity and in concentrations of insulin receptor, were found in a variety of tissues taken, at slaughter, from mature steers (701 (s.d. 23) kg) and growing lambs (47 (s.d. 2·1) kg). In both species, liver had lower insulin binding affinity than skeletal muscles m. pectineus m. longissimus dorsi and m. rectus capitis (all P < 0·001) and subcutaneous, omental and perirenal adipose depots (all P < 0·001). Site-specific differences in affinity for insulin existed between adipose depots (subcutaneous < omental, P < 0·05; subcutaneous < perirenal, P < 0·001) and between tissue-types (subcutaneous fat < m. pectineus skeletal muscle, P < 0·05; m. rectus capitis < perirenal fat, P < 0·05) in steers. In lambs also, receptor affinity for insulin differed between tissue-type (m. longissimus dorsi < perirenal fat, P < 0·05; m. rectus capitis < subcutaneous fat, P < 0·05 and m. rectus capitis < perirenal fat, P < 0·001) but lambs did not show the adipose depot-specific differences in insulin affinity observed in steers. Insulin receptor concentration differed between adipose depots (subcutaneous < omental, P < 0·05; subcutaneous < perirenal, P < 0·01) and between tissue-type (m. pectineus < perirenal fat P < 0·05) in steers and perirenal and subcutaneous adipose depots of lambs had higher receptor concentrations than m. longissimus dorsi and m. pectineusP < 0·001). This is the first study to demonstrate, in any species, differences in insulin receptor binding affinity and receptor concentration in a wide range of tissues (liver, skeletal muscles and adipose depots) from the same individual. Such differences in meat-producing animals could, through effects on tissue sensitivity and/or responsiveness to insulin, influence nutrient partitioning to tissues and affect overall rates of lipid storage and net protein synthesis.

Keywords

binding affinitycattleinsulinreceptorssheep
Type
Research Article
Information
Animal Science , Volume 71 , Issue 3 , December 2000 , pp. 501 - 508
Copyright
Copyright © British Society of Animal Science 2000

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

Balage, M., Grizard, J. and Manin, M. 1990. Effect of calorie restriction on skeletal muscle and liver insulin binding in growing rat. Hormone and Metabolic Research 22: 207—214.Google Scholar
Balage, M., Sornet, C. and Grizard, J. 1992. Insulin receptor binding and kinase activity in liver and skeletal muscles of lactating goats. American Journal of Physiology 262: E561—E568.Google ScholarPubMed
Boge, A., Sauverwein, H. and Meyer, H. H. D. 1995. IGF-1 and insulin receptors in bovine skeletal muscle: comparison of different developmental ages, two different genotypes and various individual muscles. Experimental and Clinical Endocrinology and Diabetes 103: 99—104.CrossRefGoogle Scholar
Bolinder, J., Kager, L., Östman, J. and Arner, P. 1983. Differences at the receptor and postreceptor levels between human omental and subcutaneous adipose tissue in the action of insulin on lipolysis. Diabetes 32: 117—123.CrossRefGoogle ScholarPubMed
Borkman, M., Storlien, L. H., Pan, D. A., Jenkins, A. B., Chisholm, D. J. and Campbell, L. V. 1993. The relation between insulin sensitivity and the fatty acid composition of skeletal muscle phospholipids. New England Journal of Medicine 328: 238—244.CrossRefGoogle ScholarPubMed
Brockman, R. P. and Laarveld, B. 1986. Hormonal regulation of metabolism in ruminants: a review. Livestock Production Science 14: 313—334.Google Scholar
Camara, M. and Mourot, J. 1996. Number and affinity of subcutaneous insulin receptors during growth in Large White and Meishan pigs. Proceedings of the Nutrition Society 55: 66 (abstr.).Google Scholar
Caro, J. F., Raju, S. M., Sinha, M. K., Goldfine, I. D. and Dohm, L. N. 1988. Heterogeneity of human liver, muscle, and adipose tissue insulin receptor. Biochemical and Biophysical Research Communications 151: 123—129.Google Scholar
Goldstein, B. J. and Dudley, A. L. 1990. The rat insulin receptor: primary structure and conservation of tissue-specific alternative messenger RNA splicing. Molecular Endocrinology 4: 235—244.CrossRefGoogle ScholarPubMed
Greathead, H. M. R., Dawson, J. M., Sessions, V. A., Tye, F. T., Buttery, P. J., McAllan, A. B. and Scollan, N. D. 1996. Fat synthesis in different depots of cattle given grass silage and dried grass at different intakes. Animal Science 62: 656 (abstr.).Google Scholar
Guesnet, M., Massoud, M. J. and Demarne, Y. 1991. Regulation of adipose tissue metabolism during pregnancy and lactation in the ewe: the role of insulin. Journal of Animal Science 69: 2057—2065.Google Scholar
Hocquette, J. F., Bornes, F., Balage, M., Ferré, P., Grizard, J. and Vermorel, M. 1995. Glucose transporter (GLUT 4) protein content in oxidative and glycolytic skeletal muscles from calf and goat. Biochemical Journal 305: 465—470.Google Scholar
Hocquette, J. F., Castiglia, C., Ferré, P. and Vermorel, M. 1996. Variations in GLUT 4 protein content among bovine adipose tissues. Proceedings of the Nutrition Society 55: 21A (abstr.).Google Scholar
Huang, Z., Bodkin, N. L., Ortmeyer, H. K., Hansen, B. C. and Shuldiner, A. R. 1994. Hyperinsulinaemia is associated with altered insulin receptor mRNA splicing in muscle of the spontaneously obese diabetic rhesus monkey. Journal of Clinical Investigation 94: 1289—1296.Google Scholar
Kahn, R. C. 1978. Insulin resistance, insulin insensitivity, and insulin unresponsiveness: a necessary distinction. Metabolism 27: 1893—1902.CrossRefGoogle ScholarPubMed
Kotzke, G., Schutt, M., Missler, U., Moller, D. E., Fehm, H. L. and Klein, H. H. 1995. Binding of human, porcine and bovine insulin to insulin receptors from human brain, muscle and adipocytes and to expressed recombinant alternatively spliced insulin receptor isoforms. Diabetologia 38: 757—763.Google Scholar
Krupp, M. and Lane, M. D. 1981. On the mechanism of ligand-induced down-regulation of the insulin receptor level in the liver cell. Journal of Biological Chemistry 256: 1689—1694.Google Scholar
McClain, D. A. 1991. Different ligand affinities of the two human insulin receptor splice variants are reflected in parallel changes in sensitivity for insulin action. Molecular Endocrinology 5: 734—739.Google Scholar
McGrattan, P. D., Wylie, A. R. G. and Bjourson, A. J. 1998. A partial cDNA sequence of the ovine insulin receptor gene. Evidence for alternative splicing of an exon 11 region and for tissue-specific regulation of receptor isoform expression in sheep muscle, adipose and liver. Journal of Endocrinology 159: 381—387.CrossRefGoogle ScholarPubMed
Magri, K. A., Adamo, M., Leroith, D. and Etherton, T. D. 1990. The inhibition of insulin action and glucose metabolism by porcine growth hormone in porcine adipocytes is not the result of any decrease in insulin binding or insulin receptor kinase activity. Biochemical Journal 266: 107—113.CrossRefGoogle ScholarPubMed
Mosthaf, L., Grako, K., Dull, T. J., Coussens, L., Ullrich, A. and McClain, D. A. 1990. Functionally distinct insulin receptors generated by tissue-specific alternative splicing. EMBO Journal 9: 2409—2413.CrossRefGoogle ScholarPubMed
Munson, P. J. and Rodbard, D. 1980. LIGAND: A versatile computerised approach for characterisation of ligand-binding systems. Analytical Biochemistry 107: 220—239.CrossRefGoogle ScholarPubMed
Numerical Algorithms Group. 1993. GENSTAT reference manual release 5. Oxford Science Publications, Clarendon Press, Oxford.Google Scholar
Östman, J., Arner, P. , Engfeldt, P. and Kager, L. 1979. Regional differences in the control of lipolysis in human adipose tissue. Metabolism 29: 1198—1205.Google Scholar
Reed, M. J., Reaven, G. M., Mondon, C. E. and Azhar, S. 1993. Why does insulin resistance develop during maturation? Journal of Gerontology 48: B139—B144.Google Scholar
Rösen, P., Ehrich, B., Junger, E., Bubenzer, H. J. and Kühn, L. 1979. Binding and degradation of insulin by plasma membranes from bovine liver isolated by a large-scale preparation. Biochimica et Biophysica Acta 587: 593—605.CrossRefGoogle ScholarPubMed
Sasaki, S. 1989. Insulin resistance in ovine skeletal muscle: insulin binding and insulin action. Asian-Australian Journal of Animal Science 2: 218—219.CrossRefGoogle Scholar
Sasaki, S. 1990. Mechanism of insulin resistance in the post receptor events in sheep: 3-o-methylglucose transport in ovine adipocytes. Hormone and Metabolic Research 22: 457—461.Google Scholar
Seino, S. and Bell, G. I. 1989. Alternative splicing of the human insulin receptor mRNA. Biochemical and Biophysical Research Communications 159: 312—316.Google Scholar
Smith, D. H., Palmquist, D. L. and Schanbacher, F. L. 1986. Characterisation of insulin binding to bovine liver and mammary microsomes. Comparative Biochemistry and Physiology 85: 161—169.CrossRefGoogle ScholarPubMed
Vernon, R. G., Finley, E., Taylor, E. and Flint, D. J. 1985. Insulin binding and action on bovine adipocytes. Endocrinology 116: 1195—1199.Google Scholar
Vernon, R. G. and Sasaki, S. 1991. Control of responsiveness of tissues to hormones. In Physiological aspects of digestion and metabolism in ruminants (ed. Tsuda, T., Y., Sasaki and R., Kawashima). Proceedings of the seventh international symposium on ruminant physiology, pp. 155—182. Academic Press, Inc., London.Google Scholar
Wolff, J. E., Dobbie, P. M. and Petrie, D. R. 1989. Anabolic effects of insulin in growing lambs. Quarterly Journal of Experimental Physiology 74: 451—463.Google Scholar
Yamaguchi, Y., Flier, J. S., Yokota, A., Benecke, H., Backer, J. M. and Moller, D. E. 1991. Functional properties of two naturally occurring isoforms of the human insulin receptor in Chinese hamster ovary cells. Endocrinology 129: 2058—2066.CrossRefGoogle ScholarPubMed