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Weaning marginally affects glucose transporter (GLUT4) expression in calf muscles and adipose tissues

Published online by Cambridge University Press:  09 March 2007

Jean-François Hocquette
Affiliation:
INRA, Laboratoire Croissance et Métabolismes des Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
Carole Castiglia-Delavaud
Affiliation:
INRA, Laboratoire Croissance et Métabolismes des Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
Benoît Graulet
Affiliation:
INRA, Laboratoire Croissance et Métabolismes des Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
Pascal Ferré*
Affiliation:
INSERM U342, Hôpital Saint Vincent de Paul, 75014 Paris, France
Brigitte Picard
Affiliation:
INRA, Laboratoire Croissance et Métabolismes des Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
Michel Vermorel
Affiliation:
INRA, Laboratoire Croissance et Métabolismes des Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
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Abstract

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The nutritional regulation of glucose transporter GLUT4 was studied in eight muscles and four adipose tissues from two groups of preruminant (PR) or ruminant (R) calves of similar age (170d), empty body weight (194kg) at slaughter, and level of net energy intake from birth onwards. Isocitrate dehydrogenase (EC 1.1.1.41) activity in muscles was not different between PR and R except in masseter muscle from the cheek (+71 % in R; P<0·003), which becomes almost constantly active at weaning for food chewing. Basal and maximally-insulin-stimulated glucose transport rate (GTR) per g tissue wet weight in rectus abdominis muscle were significantly higher in R calves (+31 and 41 % respectively; P<0·05). GLUT4 protein contents did not differ in muscles from PR and R except in masseter (+74 % in R; P<0·05) indicating that the increased GTR in rectus ubdominis cannot be accounted for by an enhanced GLUT4 expression. GLUT4 mRNAlevels did not differ between the two groups of animals in all muscles suggesting a regulation of GLUT4 at the protein level in masseter. GLUT4 number expressed on a per cell basis was lower in adipose tissue from R calves (-39 % P<0·05) and higher in internal than in peripheral adipose tissues. In summary, the regulation of GLUT4 in calves at weaning differs markedly from that previously described in rodents (for review, see Girard et al. 1992). Furthermore, significant inter-individual variations were shown for metabolic activities in muscle and for biochemical variables in adipose tissue.

Type
Animal Nutrition
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Andersen, P. H., Lund, S., Schmitz, O., Junker, S., Kahn, B. B. & Pedersen, O. (1993 a). Increased insulin-stimulated glucose uptake in athletes - the importance of GLUT4 mRNA, GLUT4 protein and fibre type composition of skeletal muscle. Acta Physiologica Scandinavica 149, 393404.CrossRefGoogle ScholarPubMed
Andersen, P. H., Lund, S., Vestergaard, H., Junker, S., Kahn, B. B. & Pedersen, O. (1993 b). Expression of the major insulin regulatable glucose transporter (GLUT4) in skeletal muscle of non-insulin-dependent diabetic patients and healthy subjects before and after insulin infusion. Journal of Clinical Endocrinology and Metabolism 77, 2732.Google Scholar
Bauchart, D., Ortigues, I., Hocquette, J. F., Gruffat, D. & Durand, D. (1996). Energy and fat metab-olism of the liver, the digestive tract and muscles: transport, processing, energy consumption, fixation by tissues. In Veal, Perspectives to the Year 2000, Proceedings of the International Symposium, Le Mans, France, pp. 255290 [The French Federation of Veal Producers, editor]. Le Mans: Presse de Jouve.Google Scholar
Colvin, H. W. Jr, Attebery, J. T. & Daniels, L. B. (1967). Effect of diet on glucose tolerance of dairy calves one to thirteen weeks old. Journal of Dairy Science 50, 362370.CrossRefGoogle ScholarPubMed
Cousin, B., Casteilla, L., Dani, C., Muzzin, P., Revelli, J. P. & Pénicaud, L. (1993). Adipose tissues from various anatomical sites are characterized by different patterns of gene expression and regulation. Biochemical Journal 292, 873876.CrossRefGoogle ScholarPubMed
De la Hoz, L. & Vernon, R. G. (1993). Endocrine control of sheep adipose tissue fatty acid synthesis - depot specific differences in response to lactation. Hormone and Metabolic Research 25, 214218.CrossRefGoogle ScholarPubMed
Doppenberg, J. & Palmquist, D. L. (1991). Effect of dietary fat level on feed intake, growth, plasma metabolites and hormones of calves fed dry or liquid diets. Livestock Production Science 29, 151166.CrossRefGoogle Scholar
Etgen, G. J., Brozinick, J. T., Kang, H. Y. & Ivy, J. L. (1993). Effects of exercise training on skeletal muscle glucose uptake and transport. American Journal of Physiology 264, C727C733.CrossRefGoogle ScholarPubMed
Fabres-Machado, U. & Saito, M. (1995). The effect of adipose cell size on the measurement of GLUT4 in white adipose tissue of obese mice. Brazilian Journal of Medical and Biological Research 28, 369376.Google Scholar
Girard, J., Ferré, P., Pégorier, J. P. & Duée, P. H. (1992). Adaptations of glucose and fatty acid metabolism during perinatal period and suckling-weaning transition. Physiological Reviews 72, 507562.CrossRefGoogle ScholarPubMed
Hocquette, J. F., Balage, M. & Ferré, P. (1996 a). Facilitative glucose transporters in ruminants. Proceedings of the Nutrition Society 55, 221236.CrossRefGoogle ScholarPubMed
Hocquette, J. F., Bornes, F., Balage, M.Ferré, P., Grizard, J. & 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. & Ferré, P. (1996 b). Insulin-sensitive glucose transporter transcript levels in calf muscles assessed with a bovine GLUT4 cDNA fragment. International Journal of Biochemistry and Cell Biology 28, 795806.CrossRefGoogle ScholarPubMed
Hostettler-Allen, R. L., Tappy, L. & Blum, J. W. (1994). Insulin resistance, hyperglycemia, and glucosuria in intensively milk-fed calves. Journal of Animal Science 72, 160173.CrossRefGoogle ScholarPubMed
Houmard, J. A., Weidner, M. D., Dolan, P. L., Leggett-Frazier, N., Gavigan, K. E., Rickey, M. S., Tyndall, G. E., Zhen, D. H., Alshami, A. & Dohm, G. L. (1995). Skeletal muscle GLUT4 protein concentration and aging in humans. Diabetes 44, 555560.CrossRefGoogle ScholarPubMed
Jarrett, I. G., Jones, G. B. & Potter, B. J. (1964). Changes in glucose utilization during development of the lamb. Biochemical Journal 90, 189194.CrossRefGoogle ScholarPubMed
Johnson, M. A., Polgar, J., Weightman, D. & Appleton, D. (1973). Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. Journal of Neurology Science 18, 111129.CrossRefGoogle ScholarPubMed
Jouany, J. P. (1982). Volatile fatty acid and alcohol determination in digestive contents, silage, juices, bacterial cultures and anaerobic fermentor contents. Science des Aliments 2, 131144.Google Scholar
Kaestner, K. H., Flores-Riveros, J. R., McLenithan, J. C., Janicot, M. & Lane, D. (1991). Transcriptional repression of the mouse insulin-responsive glucose transporter (GLUT4) gene by cAMP. Proceedings of the National Academy of Sciences USA 88, 19331937.CrossRefGoogle ScholarPubMed
Kahn, B. B. (1992). Facilitative glucose transporters - regulatory mechanisms and dysregulation in diabetes. Journal of Clinical Investigation 89, 13671374.CrossRefGoogle ScholarPubMed
Karlstrom, K., Essen-Gustavsson, B. & Lindholm, A. (1994). Fibre type distribution, capillarization and enzymatic profile of locomotor and nonlocomotor muscles of horses and steers. Acta Anatomica 151, 97106.CrossRefGoogle ScholarPubMed
Klip, A., Tsakiridis, T., Marette, A. & Ortiz, P. A. (1994). Regulation of expression of glucose transporters by glucose - A review of studies in vivo and in cell cultures. FASEB Journal 8, 4353.CrossRefGoogle ScholarPubMed
Kouame, K. G., Troccon, J. L., Patureau-Mirand, P., Journet, M. & Pion, R. (1984). Nutrition des veaux au cours du sevrage. I. Evolution de la consommation d'aliments et des concentrations sanguines de divers métabolites énergétiques (Calf nutrition during the weaning period. I. Variations in feed intake and blood levels of energy metabolites). Annales de Zootechnie 33, 427444.CrossRefGoogle Scholar
Le Marchand-Brustel, Y., Olichon-Berthe, C., Grémaux, T., Tanti, J. F., Rochet, N. & Van Obberghen, E. (1990). Glucose transport in insulin sensitive tissues of lean and obese mice. Effect of the thermogenic agent BRL 26830A. Endocrinology 127, 26872695.CrossRefGoogle ScholarPubMed
McGowan, K. M., Long, S. D. & Pekala, P. H. (1995). Glucose transporter gene expression: regulation of transcription and mRNA stability. Pharmacology and Therapeutics 66, 465505.CrossRefGoogle ScholarPubMed
Maher, F. & Harrison, L. C. (1991). Stimulation of glucose transporter (GLUT1) mRNA and protein expression by inhibitors of glycosylation. Biochimica et Biophysica Acta 1089, 2732.CrossRefGoogle ScholarPubMed
Manchester, J., Kong, X., Nerbonne, J., Lowry, O. H. & Lawrence, J. C. Jr (1994). Glucose transport and phosphorylation in single cardiac myocytes: rate-limiting steps in glucose metabolism. American Journal of Physiology 266, E326–E333.Google ScholarPubMed
Megeney, L. A., Neufer, P. D., Dohm, G. L., Tan, M. H., Blewett, C. A., Elder, G. C. B. & Bonen, A. (1993). Effects of muscle activity and fibre composition on glucose transport and GLUT4. American Journal of Physiology 264, E583–E593.Google ScholarPubMed
Palmquist, D. L., Doppenberg, J. D., Roehrig, K. L. & Kinsey, D. J. (1992). Glucose and insulin metabolism in ruminating and veal calves fed high and low fat diets. Domestic Animal Endocrinology 9, 233241.CrossRefGoogle ScholarPubMed
Pénicaud, L., Ferré, P., Assimacopoulos-Jeannet, F., Perdereau, D., Leturque, A., Jeanrenaud, B., Picon, L. & Girard, J. (1991). Increased gene expression of lipogenic enzymes and glucose transporter in white adipose tissue of suckling and weaned obese Zucker rats. Biochemical Journal 279, 303308.CrossRefGoogle ScholarPubMed
Picard, B., Gagniere, H., Geay, Y., Hocquette, J. F. & Robelin, J. (1995). Study of the influence of age and weaning on the contractile and metabolic characteristics of bovine muscle. Reproduction Nutrition Development 35, 7184.CrossRefGoogle ScholarPubMed
Robelin, J. (1986). Growth of adipose tissues in cattle; partitioning between depots, chemical composition and cellularity. A review. Livestock Production Science 14, 349364.CrossRefGoogle Scholar
Robinson, K. A., Sens, D. A. & Buse, M. G. (1993). Pre-exposure to glucosamine induces insulin resistance of glucose transport and glycogen synthesis in isolated rat skeletal muscles - study of mechanisms in muscle and in rat-1 fibroblasts overexpressing the human insulin receptor. Diabetes 42, 13331346.CrossRefGoogle ScholarPubMed
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, 457461.CrossRefGoogle ScholarPubMed
Smith, S. B. (1983). Contribution of the pentose cycle to lipogenesis in bovine adipose tissue. Archives of Biochemistry and Biophysics 221, 4656.CrossRefGoogle ScholarPubMed
Statistical Analysis Systems (1987). SAS/STAT® Guide for Personal Computers. Version 6. Cary, NC: SAS Institute Inc.Google Scholar
Tordjman, K. M., Leingang, K. A. & Mueckler, M. (1990). Differential regulation of the HepG2 and adipocyte/muscle glucose transporters in 3T3L1 adipocytes - effect of chronic glucose deprivation. Biochemical Journal 271, 201207.CrossRefGoogle ScholarPubMed
Vermorel, M. (1978). Energie (Energy). In Alimentation des Ruminants, pp. 4788 [Jarrige, R. editor]. Versailles, France: INRA Publications.Google Scholar
Webb, D. W., Head, H. H. & Wilcox, C. J. (1969). Effect of age and diet on fasting blood and plasma glucose levels, plasma nonesterified fatty acid levels, and glucose tolerance in dairy calves. Journal of Dairy Science 52, 20072013.CrossRefGoogle ScholarPubMed
Yki-Järvinen, H. (1992). Glucose toxicity. Endocrine Reviews 13, 415431.Google ScholarPubMed
Zierath, J. R. (1995). In vitro studies of human skeletal muscle: hormonal and metabolic regulation of glucose transport introduction. Acta Physiologica Scandinavica 155, 1196.Google Scholar