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Weaning affects lipoprotein lipase activity and gene expression in adipose tissues and in masseter but not in other muscles of the calf

Published online by Cambridge University Press:  09 March 2007

Jean-François Hocquette ,
Benoît Graulet ,
Michel Vermorel  and
Dominique Bauchart
Jean-François Hocquette*
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique, Centre de Recherches de Clermont Ferrand-Theix, 63122 Saint-Genès-Champanelle, France
Benoît Graulet
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique, Centre de Recherches de Clermont Ferrand-Theix, 63122 Saint-Genès-Champanelle, France
Michel Vermorel
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique, Centre de Recherches de Clermont Ferrand-Theix, 63122 Saint-Genès-Champanelle, France
Dominique Bauchart
Affiliation:
Unité de Recherches sur les Herbivores, Institut National de la Recherche Agronomique, Centre de Recherches de Clermont Ferrand-Theix, 63122 Saint-Genès-Champanelle, France
*
*Corresponding author: Dr Jean-François Hocquette, fax +33 4 73 62 46 39, email hocquet@clermont.inra.fr
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Abstract

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The nutritional and physiological modifications that occur during the weaning period induce adaptations of tissue metabolism in all mammal species. Among the adaptations due to weaning in ruminants, the regulation of lipoprotein lipase (LPL) activity, one of the rate-limiting steps of fatty acid utilization by tissues, was still unknown. The present study aimed at comparing LPL activity and gene expression in the heart, seven skeletal muscles and three adipose tissue sites between two groups of seven preruminant (PR) or ruminant (R) calves having a similar age (170 d), similar empty body weight (194 kg) at slaughter, and similar net energy intake from birth onwards. Triacylglycerol content of adipose tissues was 16 % lower in R than in PR calves, (P<0·01). This could be partly the result from a lower LPL activity (-57 %, P<0·01). LPL mRNA levels were also lower in R calves (-48 % to -68 %, P<0·01) suggesting a pretranslational regulation of LPL activity. Activity and mRNA levels of LPL did not differ significantly in the heart and skeletal muscles except in the masseter in which LPL activity and mRNA levels were higher (+50 % and +120 % respectively, P<0·01) in the R calves. Regulation of LPL in masseter could be explained by the high contractile activity of this muscle after weaning due to solid food chewing. In conclusion, weaning in the calf affects LPL activity and expression in adipose tissues, but not in skeletal muscles except the masseter.

Keywords

Lipoprotein lipaseMuscleAdipose tissueWeaningBovine
Type
Research Article
Information
British Journal of Nutrition , Volume 86 , Issue 4 , October 2001 , pp. 433 - 441
Copyright
Copyright © The Nutrition Society 2001

References

Ailhaud, G, Amri, EZ & Grimaldi, PA (1996) Fatty acids and expression of lipid-related genes in adipose cells. Proceedings of the Nutrition Society 55, 151–154.CrossRefGoogle ScholarPubMed
Amri, EZ, Teboul, L, Vannier, C, Grimaldi, PA & Ailhaud, G (1996) Fatty acids regulate the expression of lipoprotein lipase gene and activity in preadipose and adipose cells. Biochemical Journal 314, 541–546.CrossRefGoogle ScholarPubMed
Auwerx, J, Schoonjans, K, Fruchart, JC & Staels, B (1996) Transcriptional control of triglyceride metabolism: fibrates and fatty acids change the expression of the LPL and apo C-III genes by activating the nuclear receptor PPAR. Atherosclerosis 124 Suppl., S29–S37.CrossRefGoogle ScholarPubMed
Bauchart, D (1993) Lipid absorption and transport in ruminants. Journal of Dairy Science 76, 3864–3881.CrossRefGoogle ScholarPubMed
Bonnet, M, Faulconnier, Y, Fléchet, J, Hocquette, JF, Leroux, 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. Reproduction Nutrition and Development 38, 297–307.CrossRefGoogle ScholarPubMed
Braun, JEA & Severson, DL (1992) Regulation of synthesis, processing and translocation of lipoprotein lipase. Biochemical Journal 287, 337–347.CrossRefGoogle ScholarPubMed
Chilliard, Y & Robelin, J (1985) Activité lipoprotéine-lipasique de différents dépôts adipeux et ses relations avec la taille des adipocytes chez la vache tarie en cours d'engraissement ou en début de lactation (Lipoprotein lipase activity in different adipose tissues and relations with the adipocyte size in the dry cow during fattening or at the beginning of the lactation). Reproduction Nutrition Développement 25, 287–293.CrossRefGoogle Scholar
Cooper, DA, Stein, JC, Strieleman, PJ & Bensadoun, A (1989) Avian adipose lipoprotein lipase: cDNA sequence and reciprocal regulation of mRNA levels in adipose and heart. Biochimica et Biophysica Acta 1008, 92–101.CrossRefGoogle ScholarPubMed
Durand, D & Bauchart, D (1986) Variations nycthémérales de la lipémie et de la glycémie au niveau des voies afférentes et éfférentes du foie chez le veau préruminant (Nycthemeral variations in lipaemia and glycaemia in afferant and efferant hepatic vessels in the preruminant calf). Reproduction Nutrition Development 26, 371–372.CrossRefGoogle Scholar
Faulconnier, Y, Bonnet, M, Bocquier, F, Leroux, C, Hocquette, JF, Martin, P & Chilliard, Y (1999) Régulation du métabolisme lipidique des tissus adipeux et musculaires chez le ruminant. Effet du niveau alimentaire et de la photopériode (Regulation of lipid metabolism of adipose tissue and muscle in ruminants. Effects of feeding level and photoperiod). INRA Productions Animales 12, 287–300.CrossRefGoogle Scholar
Ferré, P (1999) Regulation of gene expression by glucose. Proceedings of the Nutrition Society 58, 621–623.CrossRefGoogle ScholarPubMed
Girard, J, Ferré, P, Pégorier, JP & Duée, PH (1992) Adaptations of glucose and fatty acid metabolism during perinatal period and suckling-weaning transition. Physiological Reviews 72, 507–562.CrossRefGoogle ScholarPubMed
Hamilton, MT, Etienne, J, McClure, W, Pavey, BS & Holloway, AK (1998) Role of local contractile activity and muscle fiber type on LPL regulation during exercise. American Journal of Physiology 275, E1016–E1022.Google ScholarPubMed
Hocquette, JF & Bauchart, D (1999) Intestinal absorption, blood transport and hepatic and muscle metabolism of fatty acids in preruminant and ruminant animals. Reproduction Nutrition Development 39, 27–48.CrossRefGoogle ScholarPubMed
Hocquette, JF, Castiglia-Delavaud, C, Graulet, B, Ferré, P, Picard, B & Vermorel, M (1997) Weaning marginally affects glucose transporter (GLUT4) expression in calf muscles and adipose tissues. British Journal of Nutrition 78, 251–271.CrossRefGoogle ScholarPubMed
Hocquette, JF, Graulet, B, Castiglia-Delavaud, C, Bornes, F, Lepetit, N & Ferré, P (1996) Insulin-sensitive glucose transporter transcript levels in calf muscles assessed with a bovine GLUT4 cDNA fragment. International Journal of Biochemistry and Cell Biology 28, 795–806.CrossRefGoogle ScholarPubMed
Hocquette, JF, Graulet, B & Olivecrona, T (1998 a) Lipoprotein lipase activity and mRNA levels in bovine tissues. Comparative Biochemistry and Physiology B 121, 201–212.CrossRefGoogle ScholarPubMed
Hocquette, JF, Ortigues-Marty, I, Pethick, DW, Herpin, P & Fernandez, X (1998 b) Nutritional and hormonal regulation of energy metabolism in skeletal muscles of meat-producing animals. Livestock Production Science 56, 115–143.CrossRefGoogle Scholar
Hugi, D & Blum, JW (1997) Changes of blood metabolites and hormones in breeding calves associated with weaning. Journal of Veterinary Medecine - Series A 44, 99–108.CrossRefGoogle ScholarPubMed
Jarrige, R (1989) Ruminant Nutrition Recommended Allowances and Feed Tables, Paris: Institut National de la Recherche Agronomique, pp. 389.Google Scholar
Jump, DB & Clarke, SD (1999) Regulation of gene expression by dietary fat. Annual Review of Nutrition 19, 63–90.CrossRefGoogle ScholarPubMed
Kauffman, RG, Habel, RE, Smulders, FJM, Hartman, W & Bergstrom, PL (1990) Recommended terminology for the muscle commonly designated longissimus dorsi. Meat Science 28, 259–265.Google Scholar
Kern, PA, Ranganathan, G, Yukht, A, Ong, JM & Davis, RC (1996) Translational regulation of lipoprotein lipase by thyroid hormone is via a cytoplasmic repressor that interacts with the 3′ untranslated region. Journal of Lipid Research 37, 2332–2340.CrossRefGoogle Scholar
Kirchgessner, TG, Svenson, KL, Lusis, AJ & Schotz, MC (1987) The sequence of cDNA encoding lipoprotein lipase. A member of a lipase gene family. Journal of Biological Chemistry 262, 8463–8466.CrossRefGoogle ScholarPubMed
Kouame, KG, Troccon, JL, 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 energetic metabolites). Annales de Zootechnie 33, 427–444.CrossRefGoogle Scholar
Olivecrona, T, Bengtsson-Olivecrona, G, Chajek-Shaul, T, Carpendier, Y, Deckelbaum, R, Hultin, M, Peterson, J, Patsch, J & Vilaro, S (1991) Lipoprotein lipase. Sites of synthesis and sites of action. Atherosclerosis Review 22, 21–25.Google Scholar
Ong, JM, Kirchgessner, TG, Schotz, MC & Kern, PA (1988) Insulin increases the synthetic rate and messenger RNA level of lipoprotein lipase in isolated rat adipocytes. Journal of Biological Chemistry 263, 12933–12938.CrossRefGoogle ScholarPubMed
Pearce, J & Unsworth, EF (1980) The effects of diet on some hepatic enzyme activities in the pre-ruminant and ruminating calf. Journal of Nutrition 110, 255–261.CrossRefGoogle ScholarPubMed
Pethick, DW & Dunshea, FR (1993) Fat metabolism and turnover. In Quantitative Aspects of Ruminants Digestion and Metabolism, pp. 291–311 [Forbes, JM and France, J, editors]. Wallingford: CAB International.Google Scholar
Picard, B, Gagnière, H & Geay, Y (1996) Contractile differenciation of bovine masseter muscle. Basic and Applied Myology 6, 361–372.Google Scholar
Pykalisto, O, Goldberg, AP & Brunzell, JD (1976) Reversal of decreased human adipose tissue lipoprotein lipase and hypertriglyceridemia after treatment of hypothyroidism. Journal of Clinical Endocrinology and Metabolism 43, 591–600.CrossRefGoogle ScholarPubMed
Quigley, JD, Caldwell, LA, Sinks, GD & Heitmann, RN (1991 a) Changes in blood glucose, nonesterified fatty acids, and ketones in response to weaning and feed intake in young calves. Journal of Dairy Science 74, 250–257.CrossRefGoogle ScholarPubMed
Quigley, JD, Smith, ZP & Heitmann, RN (1991 b) Changes in plasma volatile fatty acids in response to weaning and feed intake in young calves. Journal of Dairy Science 74, 258–263.CrossRefGoogle ScholarPubMed
Raclot, T, Dauzats, M & Langin, D (1998) Regulation of hormone-sensitive lipase expression by glucose in 3T3-F442A adipocytes. Biochemical and Biophysical Research Communications 245, 510–513.CrossRefGoogle ScholarPubMed
Raynolds, MV, Awald, PD, Gordon, DF, Gutierrez-Hartmann, A, Rule, DC, Wood, WM & Eckel, RH (1990) Lipoprotein lipase gene expression in rat adipocytes is regulated by isoprotenerol and insulin through different mechanisms. Molecular Endocrinology 4, 1416–1422.CrossRefGoogle Scholar
Schoonjans, K, Peinado-Onsurbe, J, Lefebvre, AM, Heyman, RA, Briggs, M, Deeb, S, Staels, B & Auwerk, J (1996) PPARα and PPARγ activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO Journal 15, 5336–5348.CrossRefGoogle Scholar
Semenkovich, CF, Chen, SH, Wims, M, Luo, CC, Li, WH & Chan, L (1989 a) Lipoprotein lipase and hepatic lipase mRNA tissue specific expression, developmental regulation and evolution. Journal of Lipid Research 30, 423–431.CrossRefGoogle ScholarPubMed
Semenkovich, CF, Wims, M, Noe, L, Etienne, J & Chan, L (1989 b) Insulin regulation of lipoprotein lipase activity in 3T3-L1 adipocytes is mediated at posttranscriptional and posttranslational levels. Journal of Biological Chemistry 264, 9030–9038.CrossRefGoogle ScholarPubMed
Senda, M, Oka, K, Brown, WV, Qasba, PK & Furuichi, Y (1987) Molecular cloning and sequence of a cDNA coding for bovine lipoprotein lipase. Proceedings of the National Academy of Sciences, USA 84, 4369–4373.CrossRefGoogle ScholarPubMed
Van der Lee, KAJM, Vork, MM, De Vries, JE, Willemsen, PHM, Glatz, JFC, Reneman, RS, Van der Vusse, GJ & Van Bilsen, M (2000) Long-chain fatty acid-induced changes in gene expression in neonatal cardiac myocytes. Journal of Lipid Research 41, 41–47.CrossRefGoogle ScholarPubMed
van Houtert, MFJ (1993) The production and metabolism of volatile fatty acids by ruminants fed roughages: A review. Animal Feed Science and Technology 43, 189–225.CrossRefGoogle Scholar
Vermorel, M, Bouvier, JC, Thivend, P & Toullec, R (1974) Utilisation énergétique des aliments d'allaitement par le veau préruminant á l'engrais á différents poids (Energy utilization of liquid milk replacers by veal calves). In Proceedings of the 6th Symposium on Energy Metabolism, Stuggart (Germany), EAAP Publication no. 14, pp. 143–146 [Menke, KH, Lantzch, H-J and Reichl, JR, editors]. Universitat Hohenheim, Dokumentations-stelle, Stuggart, Germany: EAAP.Google Scholar
Wion, KL, Kirchgessner, TG, Lusis, AJ, Schotz, MC & Lawn, RM (1987) Human lipoprotein lipase complementary DNA sequence. Science 235, 1638–1641.CrossRefGoogle ScholarPubMed