Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T05:45:16.089Z Has data issue: false hasContentIssue false

Skeletal muscle glucose transporter (GLUT-4) protein is decreased in lactating goats

Published online by Cambridge University Press:  02 September 2010

M. Balage
Affiliation:
INRA, Unité d'Etudé du Métabolisme Azoté, Theix, 63122 Saint-Genés Champanelle, France
J. F. Hocquette
Affiliation:
INRA, Laboratoire Croissance et Métabolismes des Herbivores, Theix, 63122 Saint-Genes Champanelle, France
B. Graulet
Affiliation:
INRA, Laboratoire Croissance et Métabolismes des Herbivores, Theix, 63122 Saint-Genes Champanelle, France
P. Ferre
Affiliation:
INSERM U342, Hôpital Saint-Vincent de Paul, 75014 Paris, France
J. Grizard
Affiliation:
INRA, Unité d'Etudé du Métabolisme Azoté, Theix, 63122 Saint-Genés Champanelle, France
Get access

Abstract

Lactation in goats is associated with an insulin resistance manifested by an impairment of the ability of insulin maximally to stimulate skeletal muscle glucose utilization. The mechanism responsible for this modification is unknown. Therefore an investigation was made of the insulin-sensitive glucose transporter (GLUT-4) in three skeletal muscles from six lactating (peak of lactation) and six non-lactating goats. GLUT-4 protein content was assessed in crude membrane preparations and Triton X-100 extracts by Western-blot analysis. Lactation resulted in a decrease in GLUT-4 protein content. This decrease was more pronounced in oxidoglycolytic muscles (proportionately -0·40 to -0·60 in m. tensor fasciae latae and longissimus dorsi) than in oxidative muscles (-0·20 in masseter). Down-regulation of the insulin-sensitive glucose transporter (GLUT-4) expression in skeletal muscles from lactating goats may be responsible for the decrease in insulin responsiveness of glucose utilization previously observed in vivo.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 1997

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., Sornet, C. and Grizard, J. 1992. Insulin receptor binding and tyrosine kinase activity in liver and various skeletal muscles of lactating goats. American Journal of Physiology 262: E561–E568.Google ScholarPubMed
Burnol, A. F., Ferre, P., Leturque, A. and Girard, J. 1987. Effect of insulin on in vivo glucose utilization in individual tissues of anesthetized lactating rats. American journal of Physiology 252: E183–E188.Google ScholarPubMed
Champredon, C., Debras, E., Patureau-Mirand, P. and Arnal, M. 1990. Methionine flux and tissue protein synthesis in lactating and dry goats. Journal of Nutrition 20: 10061015.CrossRefGoogle Scholar
Coderre, L., Monfar, M. M., Chen, K. S., Heydrick, S. J., Kurowski, T. G., Ruderman, N. B. and Pilch, P. F. 1992. Alteration in the expression of GLUT-1 and GLUT-4 protein and messenger RNA levels in denervated rat muscles. Endocrinology 131:18211825.CrossRefGoogle ScholarPubMed
Debras, E., Grizard, J., Aina, E., Tesseraud, S., Champredon, C. and Arnal, M. 1989. Insulin sensitivity and responsiveness during lactation and dry period in goats. American Journal of Physiology 256: E295–E302.Google ScholarPubMed
Devaskar, S. U. and Mueckler, M. M. 1992. The mammalian glucose transporters. Pediatric Research 31:113.CrossRefGoogle ScholarPubMed
Ebeling, P., Bourey, R., Koranyi, L., Tuominen, J. A., Groop, L. C, Henriksson, J., Mueckler, M., Sovijarvi, A. and Koivisto, V. A. 1993. Mechanism of enhanced insulin sensitivity in athletes. Increased blood flow, muscle glucose transport protein (GLUT-4) concentration, and glycogen synthase activity. Journal of Clinical Investigation 92: 16231631.CrossRefGoogle ScholarPubMed
Etherton, T. D. and Louveau, I. 1992. Manipulation of adiposity by somatotropin and beta-adrenergic agonists: a comparison of their mechanisms of action. Proceedings of the Nutrition Society 51:419431.CrossRefGoogle ScholarPubMed
Faulkner, A. and Pollock, H. T. 1990. Metabolic responses to euglycaemic hyperinsulinaemia in lactating and nonlactating sheep in vivo. Journal of Endocrinology 124:5966.CrossRefGoogle ScholarPubMed
Garvey, W. T. 1994. GLUT-4 glucose transporters and insulin action in humans. In Molecular biology of diabetes, part II (ed. Draznin, B. and LeRoith, D.), pp. 437471. Humana Press Inc., Totowa, NJ.Google Scholar
Garvey, W. T., Maianu, L., Hancock, J. A., Golichowski, A. M. and Baron, A. 1992. Gene expression of GLUT4 in skeletal muscle from insulin-resistant patients with obesity, IGT, GDM, and NIDDM. Diabetes 41:465475.CrossRefGoogle ScholarPubMed
Gill, R. D. and Hart, I. C. 1980. Properties of insulin and glucagon receptors on sheep hepatocytes: a comparison of hormone binding and plasma hormones and metabolites in lactating and non-lactating ewes. Journal of Endocrinology 84: 237247.CrossRefGoogle ScholarPubMed
Hocquette, J. F., Bornes, F., Balage, M., Ferre, P., Grizard, J. and Vermorel, M. 1995. Glucose-transporter (GLUT4) protein content in oxidative and glycolytic skeletal muscles from calf and goat. Biochemical Journal 305: 465470.CrossRefGoogle ScholarPubMed
Hocquette, J. F., Graulet, B., Castiglia-Delavaud, C, Bornes, F., Lepetit, N. and Ferre, P. 1996. Insulin-sensitive glucose transporter transcript levels in calf muscles assessed with a bovine GLUT-4 cDNA fragment. International Journal of Biochemistry and Cell Biology 28: 795806.CrossRefGoogle Scholar
Hove, K. 1978. Effects of hyperinsulinemia on lactose secretion and glucose uptake by the goat mammary gland. Ada Physiologia Scandinavica 104:422430.CrossRefGoogle ScholarPubMed
James, D. E., Strube, M. and Mueckler, M. 1989. Molecular cloning and characterization of an insulin-regulatable glucose transporter. Nature 338: 8387.CrossRefGoogle ScholarPubMed
Kahn, B. B. 1992. Facultative glucose transporters — regulatory mechanisms and dysregulation in diabetes. Journal of Clinical Investigation 89:13671374.CrossRefGoogle Scholar
Klip, A., Tsakiridis, T., Marette, A. and Ortiz, P. A. 1994. Regulation of expression of glucose transporters by glucose: a review of studies in vivo and cell cultures. FASEB Journal 8:4353.CrossRefGoogle Scholar
Koranyi, L. I., Bourey, R. E., Vuorinenmarkkola, H., Koivisto, V. A., Mueckler, M., Permutt, M. A. and Ykijarvinen, H. 1991. Level of skeletal muscle glucose transporter protein correlates with insulin-stimulated whole body glucose disposal in man. Diabetologia 34: 763765.CrossRefGoogle ScholarPubMed
Laarveld, B., Chaplin, R. K. and Brockman, R. P. 1985. Effects of insulin on the metabolism of acetate, bhydroxybutyrate and triglycerides by the bovine mammary gland. Comparative Biochemistry and Physiology 82B: 265267.Google Scholar
Laarveld, B., Christensen, D. A. and Brockman, R. P. 1981. The effect of insulin on net metabolism of glucose and amino acids by the bovine mammary gland. Endocrinology 108:22172221.CrossRefGoogle ScholarPubMed
Leturque, A., Postic, C, Ferre, P. and Girard, J. 1991. Nutritional regulation of glucose transporter in muscle and adipose tissue of weaned rats. American Journal of Physiology 260: E588–E593.Google ScholarPubMed
Liu, C. Y., Grant, A. L. and Mills, S. E. 1992. Effects of recombinant porcine somatotropin on glucose transporter (GLUT1 and GLUT4) mRNA in pig adipose and skeletal muscle. Journal of Animal Science 70: 285 (abstr.).Google Scholar
Metcalf, J. A., Sutton, J. D., Cockburn, J. E., Napper, D. J. and Beever, D. E. 1991a. The influence of insulin and amino acid supply on amino acid uptake by the lactating bovine mammary gland. Journal of Dairy Science 74:34123420.CrossRefGoogle ScholarPubMed
Metcalf, J. A., Vernon, R. G., Flint, D. J. and Weekes, T. E. C. 1991b. Insulin binding to skeletal muscle microsomes in lactating and dry sheep. Hormone and Metabolic Research 23: 271273.CrossRefGoogle ScholarPubMed
Ploug, T., Stallknecht, B. M., Pedersen, O., Kahn, B. B., Ohkuwa, T., Vinten, J. and Galbo, H. 1990. Effect of endurance training on glucose transport capacity and glucose transporter expression in rat skeletal muscle. American Journal of Physiology 259: E778–E786.Google ScholarPubMed
Postic, C., Leturque, A., Rencurel, F., Printz, R. L., Forest, C, Granner, D. K. and Girard, J. 1993. The effects of hyperinsulinemia and hyperglycemia on GLUT4 and hexokinase-II messenger RNA and protein in rat skeletal muscle and adipose tissue. Diabetes 42:922929.CrossRefGoogle ScholarPubMed
Sinha, M. K., Raineri-maldonado, C, Buchanan, C, Pories, W. J., Carter-Su, C, Pilch, P. F. and Caro, J. F. 1991. Adipose tissue glucose transporters in NIDDM. Decreased levels of muscle/fat isoform. Diabetes 40:472477.CrossRefGoogle ScholarPubMed
Statistical Analysis Systems Institute. 1988. SAS/STAT user's guide, release 6.03 edition. Statistical Analysis Systems Institute Inc., Cary, NC.Google Scholar
Tauveron, I., Larbaud, D., Champredon, C, Debras, E., Tesseraud, S., Bayle, G., Bonnet, Y., Thieblot, P. and Grizard, J. 1994. Effect of hyperinsulinemia and hyperaminoacidemia on muscle and liver protein synthesis in lactating goats. American Journal of Physiology 267: E877–E885.Google ScholarPubMed
Tesseraud, S., Grizard, J., Makarski, B., Debras, E., Bayle, G. and Champredon, C. 1992. Effect of insulin in conjunction with glucose, amino acids and potassium on net metabolism of glucose and amino acids in the goat mammary gland. Journal of Dairy Research 59:135149.CrossRefGoogle ScholarPubMed
Trayhurn, P., Thomas, M. E. A. and Keith, J. S. 1993. Postnatal development of uncoupling protein, uncoupling protein mRNA, and GLUT4 in adipose tissues of goats. American Journal of Physiology 265: R676–R682.Google ScholarPubMed
Vernon, R. G. 1985. The response of tissues to hormones and the partition of nutrients during lactation. Hannah Research Report 1985, pp. 115121.Google Scholar
Vernon, R. G. 1988. The partition of nutrients during the lactation cycle. In Nutrition and lactation in the dairy cow (ed. Garnsworthy, P. C.), pp. 3352. Butterworths, London.Google Scholar
Vernon, R. G. 1989. Endocrine control of metabolic adaptation during lactation. Proceedings of the Nutrition Society 48: 2332.CrossRefGoogle ScholarPubMed
Vernon, R. G., Faulkner, A., Hay, W. W., Calvert, D. T. and Flint, D. J. 1990. Insulin resistance of hind-limb tissues in vivo in lactating sheep. Biochemical Journal 270: 783786.CrossRefGoogle Scholar
Vernon, R. G. and Taylor, E. 1988. Insulin, dexamethasone and their interactions in the control of glucose metabolism in adipose tissue from lactating and non-lactating sheep. Biochemical Journal 256: 509514.CrossRefGoogle Scholar
Zhao, F. Q., Moseley, W. M., Tucker, H. A. and Kennelly, J. J. 1996. Regulation of glucose transporter gene expression in mammary gland, muscle, and fat of lactating cows by administration of bovine growth hormone and bovine growth hormone-releasing factor. Journal of Animal Science 74:183189.CrossRefGoogle ScholarPubMed
Ziel, F. H., Venkatesan, N. and Davidson, M. B. 1988. Glucose transport is rate limiting for skeletal muscle glucose metabolism in normal and STZ-induced diabetic rats. Diabetes 37:885890.CrossRefGoogle ScholarPubMed