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Nutritional status induces divergent variations of GLUT4 protein content, but not lipoprotein lipase activity, between adipose tissues and muscles in adult cattle

Published online by Cambridge University Press:  09 March 2007

Muriel Bonnet ,
Yannick Faulconnier ,
Jean-François Hocquette ,
François Bocquier ,
Christine Leroux ,
Patrice Martin  and
Yves Chilliard
Muriel Bonnet
Affiliation:
INRA, Unité de Recherches sur les Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
Yannick Faulconnier
Affiliation:
INRA, Unité de Recherches sur les Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
Jean-François Hocquette
Affiliation:
INRA, Unité de Recherches sur les Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
François Bocquier
Affiliation:
INRA, Unité de Recherches sur les Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
Christine Leroux
Affiliation:
INRA, Unité de Recherches sur les Herbivores, Theix, 63122 Saint-Genès-Champanelle, France INRA, Laboratoire de Génétique Biochimique et de Cytogénétique, Domaine de Vilvert, 78352 Jouy-en-Josas, France
Patrice Martin
Affiliation:
INRA, Laboratoire de Génétique Biochimique et de Cytogénétique, Domaine de Vilvert, 78352 Jouy-en-Josas, France
Yves Chilliard*
Affiliation:
INRA, Unité de Recherches sur les Herbivores, Theix, 63122 Saint-Genès-Champanelle, France
*
*Corresponding author: Dr Y. Chilliard, fax +33 473 62 45 19, email [email protected]
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Abstract

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Metabolic adaptations to variations in food supply are incompletely understood in ruminant animal adipose tissue (AT) and muscle. To explore this, we studied lipid metabolism and glucose transport potential in one internal and one external AT, as well as in one oxidative and one glycolytic muscle from control, 7 d underfed and 21 d refed adult cows. Refeeding increased (+79 to +307 %) the activities of enzymes involved in de novo lipogenesis (fatty acid synthase, malic enzyme, glucose-6-phosphate dehydrogenase) in perirenal and subcutaneous AT; underfeeding did not modify these variables. Underfeeding decreased the activities of lipoprotein lipase (LPL) in perirenal AT (−70 %) and cardiac muscle (−67 %), but did not modify the activities in subcutaneous AT and longissimus thoracis. Refeeding increased LPL activities in all tissues (+40 to +553 %) to levels comparable with (cardiac muscle) or greater than (AT, longissimus thoracis) those observed in control cows. Such variations in perirenal and cardiac muscle LPL activities did not result from variations in LPL mRNA levels, but suggest a post-transcriptional regulation of LPL in these nutritional conditions. Underfeeding did not modify GLUT4 contents in perirenal AT and muscles, while refeeding increased it only in perirenal AT (+250 %). Our present results contrast with previous results in rats, where LPL is regulated in opposite directions in AT and muscles, and GLUT4 is generally increased by fasting and decreased by refeeding in skeletal muscles. The present results highlight the bovine specificity of the response, which probably arises in part from peculiarities of ruminant animals for nutrient digestion and absorption.

Keywords

LipogenesisGLUT4Adipose tissueMuscleAdult cattle
Type
Research Article
Information
British Journal of Nutrition , Volume 92 , Issue 4 , October 2004 , pp. 617 - 625
Copyright
Copyright © The Nutrition Society 2004

References

Balage, M, Hocquette, JF, Graulet, B, Ferré, P & Grizard, J (1997) Skeletal muscle glucose transporter (GLUT-4) protein is decreased in lactating goats. Anim Sci 65, 257–265CrossRefGoogle Scholar
Barnouin, J, El Idilbi, N, Chilliard, Y, Chacornac, JP, & Lefaivre, R (1986) Micro-dosage automatisé sans déprotéinisation du 3-hydroxybutyrate plasmatique chez les bovins (An automated micro-method for the determination of 3-hydroxybutyrate in bovine plasma without acid precipitation). Ann Rech Vet 17, 129–139Google Scholar
Bell, AW & Bauman, DE (1997) Adaptations of glucose metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 2, 265–278CrossRefGoogle ScholarPubMed
Bergö, M, Olivecrona, G & Olivecrona, T (1996 a) Diurnal rhythms and effects of fasting and refeeding on rat adipose tissue lipoprotein lipase. Am J Physiol 271, E1092–E1097Google ScholarPubMed
Bergö, M, Olivecrona, G & Olivecrona, T (1996 b) Forms of lipoprotein lipase in rat tissues: in adipose tissue the proportion of inactive lipase increases on fasting. Biochem J 313, 893–898CrossRefGoogle ScholarPubMed
Björntorp, P, Edström, S, Kral, JG, Lundholm, K, Presta, E, Walks, D & Yang, MU (1982) Refeeding after fasting in the rat: energy substrate fluxes and replenishment of energy stores. Am J Clin Nutr 36, 450–456CrossRefGoogle ScholarPubMed
Bocquier, F, Bonnet, M, Faulconnier, Y, Guerre-Millo, M, Martin, P & Chilliard, Y (1998) Effects of photoperiod and feeding level on perirenal adipose tissue metabolic activity and leptin synthesis in the ovariectomized ewe. Reprod Nutr Dev 38, 489–498CrossRefGoogle ScholarPubMed
Bonnet, M, Faulconnier, Y, Fléchet, J, Hoquette, JF, Levoux, C, Langin, D, Martin, P & Chilliard, Y (1998) Messenger RNAs encoding lipoprotein lipase, fatty acid synthase and hormone-sensitive lipase in the adipose tissue of underfed-refed ewes and cows. Reprod Nutr Dev 38, 297–307CrossRefGoogle ScholarPubMed
Bonnet, M, Leroux, C, Faulconnier, Y, Hocquette, JF, Bocquier, F, Martin, P & Chilliard, Y (2000) Lipoprotein lipase activity and mRNA are up-regulated by refeeding in adipose tissue and cardiac muscle of sheep. J Nutr 130, 749–756CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254CrossRefGoogle ScholarPubMed
Chilliard, Y, Doreau, M, Bocquier, F & Lobley, GE (1995) Recent developments in nutrition of herbivores. In Proceedings of the IVth International Symposium on the Nutrition of Herbivores, pp. 329–360 [Journet, M, Grenet, E, Farce, MH, Thériez, M and Demarquilly, C, editors]. Paris: INRA Editions.Google Scholar
Chilliard, Y, Ferlay, A, Faulconnier, Y, Bonnet, M, Rouel, J & Bocquier, F (2000) Adipose tissue metabolism and its role in adaptations to undernutrition in ruminants. Proc Nutr Soc 59, 127–134CrossRefGoogle ScholarPubMed
Chilliard, Y, Gagliostro, G, Fléchet, J, Lefaivre, R & Sebastian, I (1991) Duodenal rapeseed oil infusion in early and midlactation cows. 5. Milk fatty acid and adipose tissue lipogenic activities. J Dairy Sci 74, 1844–1854CrossRefGoogle ScholarPubMed
Chilliard, Y, Sauvant, D, Morand-Fehr, P (1979) Goat mammary, adipose and milk lipoprotein lipases. Ann Rech Vet 10, 401–403Google ScholarPubMed
Delavaud, C, Ferlay, A, Faulconnier, Y, Bocquier, F, Kann, G & Chilliard, Y (2002) Plasma leptin concentration in adult cattle: effects of breed, adiposity, feeding level, and meal intake. J Anim Sci 80, 1317–1328CrossRefGoogle ScholarPubMed
DiMarco, NM, Bietz, DC & Whitehurst, GB (1981) Effect of fasting on free fatty acid, glycerol and cholesterol concentrations in blood plasma and lipoprotein lipase activity in adipose tissue of cattle. J Anim Sci 52, 75–82CrossRefGoogle ScholarPubMed
Faulconnier, Y, Bonnet, M, Bocquier, F, Leroux, C & Chilliard, Y (2001) Effects of photoperiod and feeding level on adipose tissue and muscle lipoprotein lipase activity and mRNA level in dry non-pregnant sheep. Br J Nutr 85, 299–306CrossRefGoogle ScholarPubMed
Faulconnier, Y, Thévenet, M, Fléchet, J & Chilliard, Y (1994) Lipoprotein lipase and metabolic activities in incubated bovine adipose tissue explants: effects of insulin, dexamethasone, and fetal bovine serum. J Anim Sci 72, 184–191CrossRefGoogle ScholarPubMed
Ferlay, A & Chilliard, Y (1999) Effects of the infusion of non-selective beta-, and selective beta1- or beta2-adrenergic agonists, on body fat mobilisation in underfed or overfed non-pregnant heifers. Reprod Nutr Dev 39, 409–421CrossRefGoogle ScholarPubMed
Hocquette, JF & Abe, H (2000) Facilitative glucose transporters in livestock species. Reprod Nutr Dev 40, 517–533CrossRefGoogle ScholarPubMed
Hocquette, JF, Bornes, F, Balage, M, Ferre, P, Grizard, J & Vermorel, M (1995) Glucose-transporter (GLUT4) protein content in oxidative and glycolytic skeletal muscles from calf and goat. Biochem J 305, 465–470CrossRefGoogle ScholarPubMed
Hocquette, JF, Graulet, B & Olivecrona, T (1998) Lipoprotein lipase activity and mRNA levels in bovine tissues. Comp Biochem Physiol 121, 85–96CrossRefGoogle ScholarPubMed
Hocquette, JF, Graulet, B, Vermorel, M & Bauchart, D (2001) Weaning affects lipoprotein lipase activity and gene expression in adipose tissues and in masseter but not in other muscles of the calf. Br J Nutr 86, 433–441CrossRefGoogle Scholar
Ingle, DL, Bauman, DE, Mellenberger, RW & Johnson, DE (1973) Lipogenesis in the ruminant: effect of fasting and refeeding on fatty acid synthesis and enzymatic activity of sheep adipose tissue. J Nutr 103, 1479–1488CrossRefGoogle ScholarPubMed
Institut National, de la Recherche Agronomique (1989) Ruminant Nutrition, Recommended Allowances and Feed Tables [Jarrige, R, editor]. Paris: John Libley Eurotext.Google Scholar
James, DE, Strube, M & Mueckler, M (1989) Molecular cloning and characterization of an insulin-regulatable glucose transporter. Nature 338, 83–87CrossRefGoogle ScholarPubMed
Kahn, BB (1994) Dietary regulation of glucose transporter gene expression: tissue specific effects in adipose cells and muscle. J Nutr 124 1289S–1295S.CrossRefGoogle ScholarPubMed
Labarca, C & Paigen, KA (1980) Simple, rapid, sensitive DNA assay procedure. Anal Biochem 102, 344–352CrossRefGoogle ScholarPubMed
Ladu, MJ, Kapsas, H & Palmer, WK (1991) Regulation of lipoprotein lipase in adipose and muscle tissues during fasting. Am J Physiol 260, R953–R959Google ScholarPubMed
Lee, JJ, Smith, JP & Fried, SK (1998) Mechanisms of decreased lipoprotein lipase activity in adipocytes of starved rats depend on duration of starvation. J Nutr 128, 940–946CrossRefGoogle ScholarPubMed
Martin, RJ, Wilson, LL, Cowan, RL & Sink, JD (1973) Effects of fasting and diet on enzyme profiles in ovine liver and adipose tissue. J Anim Sci 36, 101–106CrossRefGoogle ScholarPubMed
Pethick, DW (1984) Energy metabolism of skeletal muscle. In Proceedings of the Symposium on Ruminant Physiology: Concepts and Consequences, pp. 277–287 [Baker, SK, Gawthorne, JM, Mackintosh, JB, Purser, DB, editors]. Nedlands: University of Western Australia.Google Scholar
Pothoven, MA & Beitz, DC (1975) Changes in fatty acid synthesis and lipogenic enzymes in adipose tissue from fasted and fasted–refed steers. J Nutr 105, 1055–1061CrossRefGoogle ScholarPubMed
Pothoven, MA & Beitz, DC (1973) Effect of adipose tissue site, animal weight, and long-term fasting on lipogenesis in the bovine. J Nutr 103, 468–475CrossRefGoogle ScholarPubMed
Quig, DW, Layman, DK, Bechtel, PJ & Hackler, LR (1983) The influence of starvation and refeeding on the lipoprotein lipase activity of skeletal muscle and adipose tissue of lean and obese Zucker rats. J Nutr 113, 1150–1156CrossRefGoogle ScholarPubMed
Robelin, J (1981) Cellularity of bovine adipose tissue: developmental changes from 15 to 65 percent mature weight. J Lipid Res 22, 452–457CrossRefGoogle ScholarPubMed
Smith, SB, Prior, RL & Mersmann, HJ (1983) Interrelationships between insulin and lipid metabolism in normal and alloxan-diabetic cattle. J Nutr 113, 1002–1015CrossRefGoogle ScholarPubMed
Sugden, MC, Holness, MJ & Howard, RM (1993) Changes in lipoprotein lipase activities in adipose tissue, heart and skeletal muscle during continuous or interrupted feeding. Biochem J 292, 113–119CrossRefGoogle ScholarPubMed
Tume, RK, Thornton, RF & Johnson, GW (1983) Lipoprotein lipase of sheep and rat adipose tissues. Aust J Biol Sci 36, 41–48CrossRefGoogle ScholarPubMed
Vernon, RG (1980) Lipid metabolism in the adipose tissue of ruminant animals. Prog Lipid Res 19, 23–106CrossRefGoogle ScholarPubMed
Woloschak, M, Shen-Orr, Z, LeRoith, D, Roberts, CT Jr (1993) Nutritional regulation of insulin-sensitive glucose transporter gene expression in rat cardiac muscle. Proc Soc Exp Biol Med 203, 172–174CrossRefGoogle ScholarPubMed
Young, JW, Thorp, SL, De Lumen, HZ (1969) Activity of selected gluconeogenic and lipogenic enzymes in bovine rumen mucosa, liver and adipose tissue. Biochem J 114, 83–88CrossRefGoogle ScholarPubMed