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Effects of photoperiod and feeding level on adipose tissue and muscle lipoprotein lipase activity and mRNA level in dry non-pregnant sheep

Published online by Cambridge University Press:  09 March 2007

Y. Faulconnier
Affiliation:
INRA, Equipe Tissu Adipeux et Lipides du Lait, Unité de Recherches sur les Herbivores, Theix, 63122 Saint Genès-Champanelle, France
M. Bonnet
Affiliation:
INRA, Equipe Tissu Adipeux et Lipides du Lait, Unité de Recherches sur les Herbivores, Theix, 63122 Saint Genès-Champanelle, France
F. Bocquier
Affiliation:
INRA, Equipe Tissu Adipeux et Lipides du Lait, Unité de Recherches sur les Herbivores, Theix, 63122 Saint Genès-Champanelle, France
C. Leroux
Affiliation:
INRA, Laboratoire de Génétique biochimique et de Cytogénétique, 78352 Jouy-en-Josas, France
Y. Chilliard*
Affiliation:
INRA, Equipe Tissu Adipeux et Lipides du Lait, Unité de Recherches sur les Herbivores, Theix, 63122 Saint Genès-Champanelle, France
*
Corresponding author: Dr Y. Chilliard, fax +33 473 62 45 19, email Yves.Chilliard@clermont.inra.fr
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Abstract

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The aim of the present study was to investigate the effects of photoperiod and feeding level on lipid metabolism in ovine perirenal and subcutaneous adipose tissues (AT) and in skeletal and cardiac muscles. Twenty dry non-pregnant ovariectomised ewes were divided into two groups and subjected to either 8 h or 16 h light/d, and underfed at 22 % energy requirements for 7 d. Half of the ewes in each group were slaughtered and the remaining ewes were refed at 190 % energy requirements for 14 d, until slaughtering. Refeeding increased (2.6–4.3-fold) malic enzyme (ME), fatty acid synthase (FAS), glucose-6-phosphate dehydrogenase (G6PDH) and glycerol-3-phosphate dehydrogenase (G3PDH) activities in subcutaneous AT as well as lipoprotein lipase (LPL) activity in perirenal (3.5-fold) and subcutaneous (10-fold) AT and to a lesser extent (1.4-fold) in the skeletal longissimus thoracis and cardiac muscles. Moreover, variations of LPL mRNA level followed variations of LPL activity: refeeding increased perirenal AT- and cardiac muscle-mRNA levels (7.4- and 2-fold respectively). The main finding of this study is that, for a given level of food intake, long days (compared with short days) increased the LPL activity in the longissimus thoracis muscle and, in refed ewes, the activities of LPL and ME in subcutaneous AT. Furthermore, long days increased LPL mRNA level in cardiac muscle and perirenal AT. Thus, our results show that there are direct effects of photoperiod on sheep AT lipogenic potential, as well as on muscle LPL activity, which are not caused by changes in nutrient availability.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2001

References

Abbott, MJ, Ullrey, DE, Ku, PK, Schmitt, SM, Romsos, DR & Tucker, HA (1984) Effect of photoperiod on growth and fat accretion in white–tailed doe fawns. Journal of Wild Management 48, 776787.CrossRefGoogle Scholar
Baggen, MG, Jansen, H, Lammers, R, Verschoor, L & Birkenhager, JC (1987) Disparate effects of ACTH (1–24) and corticosterone on lipoprotein lipase in rat adipose tissue. Journal of Endocrinology 114, 369372.CrossRefGoogle ScholarPubMed
Bartness, TJ (1995) Short-day-induced depletion of lipid stores is fat pad- and gender-specific in Siberian hamsters. Physiology and Behaviour 58, 539550.CrossRefGoogle ScholarPubMed
Bartness, TJ, Hamilton, JM, Wade, GN & Goldman, BD (1989) Regional differences in fat pad responses to short days in Siberian hamsters. Integrative Comparative of Physiology 26, R1533R1540.CrossRefGoogle Scholar
BergÖ, M, Olivecrona, G & Olivecrona, T (1996) Diurnal rhythms and effects of fasting and refeeding on rat adipose tissue lipoprotein lipase. American Journal of Physiology 271, E1092E1097.Google ScholarPubMed
Blask, DE, Dauchy, RT & Sauer, LA (1999) Physiological melatonin inhibits lipogenesis and fasting-induced lipolysis in the inguinal fat pad perfused in situ in the rat. Proceedings of the 81st Annual Meeting of the Endocrine Society P2–208 p. 324. San Diego, CA..Google Scholar
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 sheep. Reproduction Nutrition Development 38, 489498.Google Scholar
Bonnet, M, Leroux, C, Faulconnier, Y, Hocquette, JF, Bocquier, F, Martin, P & Chilliard, Y (2000) Lipoprotein lipase activity and messenger RNAs are up-regulated by refeeding in adipose tissue and cardiac muscle of sheep. Journal of Nutrition 30, 749756.CrossRefGoogle Scholar
Borensztajn, J (1987) Heart and skeletal muscle lipoprotein lipase. In Lipoprotein Lipase Chapter 5, 133148.[J, Borensztajn, editor]. Chicago, IL: Evener Publishing.Google Scholar
Chemineau, P, Malpaux, B, Pelletier, J, Leboeuf, P, Delgadillo, JA, Deletang, F, Pobel, T & Brice, G (1996) Emploi des implants de mélatonine et des traitements photopériodiques pour maîtriser la reproduction saisonnière chez les ovins et les caprins (Use of melatonin implants and photoperiodic treatments to control seasonal reproduction in sheep and goats). INRA Production Animale 9, 4560.CrossRefGoogle Scholar
Chiappe, deCingalani, GE, Goers, JW, Giannoti, M & Caldiz, CI (1996) Comparative effects of insulin and isoproterenol on lipoprotein lipase in rat adipose cells. American Journal of Physiology 270, C1461C1467.CrossRefGoogle Scholar
Chilliard, Y (1987) Revue bibliographique: Variations quantitatives et métabolisme des lipides dans les tissus adipeux et le foie au cours du cycle gestation–lactation. 2. Chez la brebis et la vache (Quantitative variations and metabolism of lipids in adipose tissue and liver during gestationlactation cycle. 2. In the ewe and cow) Reproduction Nutrition Development 27, 327398.CrossRefGoogle ScholarPubMed
Chilliard, Y, Bocquier, F & Cronjé, PB (2000) Direct effects of photoperiod on lipid metabolism, leptin synthesis and milk secretion in adult sheep. In Ruminant Physiology: Digestion, Metabolism, Growth and Reproduction, pp. 205223. [Cronjé, PB, editor]. Wallingford: CABI Publishing.Google Scholar
Chilliard, Y, Gagliostro, G, Fléchet, J, Lefaivre, J & Sebastian, I (1991) Duodenal rapeseed oil infusion in early and midlactation cows. 5. Milk fatty acids and adipose tissue lipogenic activities. Journal of Dairy Science 74, 18441854.CrossRefGoogle ScholarPubMed
Chilliard, Y, Sauvant, D, Bas, P, Pascal, G, Morand–Fehr, P & (1981) Importance relative et activités métaboliques des différents tissus adipeux de la chèvre laitière. (Relative importance and metabolic activities of various adipose tissues in dairy goats). In Nutrition et Systèmes d'Alimentation de la Chèvre vol. 1, 8089.Google Scholar
Chilliard, Y, Sauvant, D & Morand–Fehr, P (1979) Goat mammary, adipose and milk lipoprotein lipases. Annales de Recherche Vétérinaire 10, 401403.Google ScholarPubMed
Cruz, ML & Williamson, DH (1992) Refeeding meal–fed rats increases lipoprotein lipase activity and deposition of dietary [14C] lipid in white adipose tissue and decreases oxidation to 14CO2. Biochemical Journal 285, 773778.Google Scholar
DiMarco, NM, Beitz, 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. Journal of Animal Science 52, 7582.Google Scholar
Eckel, RH (1987) Adipose tissue lipoprotein lipase Lipoprotein Lipase, Chapter 4, pp.79–132; [JBorensztajn,editor] Borensztajn,editor]. Chicago, IL: Evener Publishing.Google Scholar
Emane, MN, Delouis, C, Kelly, PA & Djiane, J (1986) Evolution of prolactin and placental lactogen receptors in ewes during pregnancy and lactation. Endocrinology 118, 695700.CrossRefGoogle ScholarPubMed
English, DE, Russel, SM, Kartz, LS & Nicoll, CS (1990) Evidence for a role of the liver in the mammotrophic action of prolactin. Endocrinology 126, 22522256.Google Scholar
Faulconnier, Y, Bonnet, M, Flé#chet, J, Bocquier, F & Chilliard, Y (1999) Nutritional regulation of lipoprotein lipase activity in bovine adipose tissues and muscles. Proceedings of the Nutrition Society 58, 108A.Google Scholar
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. Journal of Animal Science 72, 184191.CrossRefGoogle ScholarPubMed
Hocquette, JF, Graulet, B & Olivecrona, T (1998) Lipoprotein lipase activity and mRNA levels in bovine tissues. Comparative Biochemistry and Physiology Part B 121, 201212.CrossRefGoogle ScholarPubMed
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. Journal of Nutrition 103, 14791488.CrossRefGoogle ScholarPubMed
Institut National de la Recherche Agronomique (1989) Recommended allowances and feed tables Ruminants Nutrition [R, Jarrige, editors]. Paris: John Libley Eurotext.Google Scholar
Ladu, MJ, Kapsas, H & Palmer, WK (1991) Regulation of lipoprotein lipase in adipose and muscle tissues during fasting. American Journal of Physiology 260, R953R959.Google ScholarPubMed
Larsen, TS, Nilsson, Blix, AS (1985) Seasonal changes in lipogenesis in isolated adipocytes from Svalbard and Norwegian reindeer. Acta Physiologica Scandinavica 123, 5359.CrossRefGoogle ScholarPubMed
Larsen, TS, Nilsson, & Schytte Blix, A (1985) Seasonal changes in lipogenesis and lipolysis in isolated adipocytes from Svalbard and Norwegian reindeer. Acta Physiologica Scandinavica 123, 97104.CrossRefGoogle ScholarPubMed
Le #Gouic, S, Atgé, C, Viguerie–#Bascands, N, Haoun, N, Larrouy, D, Ambid, L, Raimbault, S, Ricquier, DP, Gardiola–#Lemaitre, B, Pénicaud, L & Casteilla, L (1997) Characterisation of a melatonin binding site in Siberian hamster brown adipose tissue. European Journal of Pharmacology 339, 271278.CrossRefGoogle ScholarPubMed
Lincoln, GA & Richardson, M (1998) Photo–endocrine control of seasonal cycles in body weight, pelage growth and reproduction: lessons from the HPD sheep model. Comparative Biochemistry and Physiology 119C, 283294.Google Scholar
Meier, AH & Cincotta, AH (1996) Circadian rhythms regulate the expression of the thrifty genotype/phenotype. Diabetes Reviews 4, 464487.Google Scholar
Mercer, JG (1998) Regulation of appetite and body weight in seasonal mammals. Comparative Biochemistry and Physiology 119C, 295303.Google Scholar
Ng, TB & Wong, CM (1986) Effects of pineal indoles and arginine vasotocin on lipolysis and lipogenesis in isolated adipocytes. Journal of Pineal Research 3, 5556.Google Scholar
Ong, JM, Simsolo, RB, Saghizadeh, M, Pauer, A & Kern, PA (1994) Expression of lipoprotein lipase in rat muscle: regulation by feeding and hypothyroidism. Journal of Lipid Research 35, 15421551.Google Scholar
Ortavant, R, Bocquier, F, Pelletier, JP, Ravault, JP, Thimonier, J & Volland–Nail, P (1988) Seasonality of reproduction in sheep and its control by photoperiod. Australian Journal of Biology Science 41, 6985.CrossRefGoogle ScholarPubMed
Pang, CS, Brown, GM, Tang, PL, Cheng, KM & Pang, SF (1993) 2–[125I]iodomelatonin binding sites in the lung and heart: a link between the photoperiodic signal, melatonin, and the cardiopulmonary system. Biological Signals 2, 228236.Google Scholar
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. Journal of Nutrition 113, 11501156.CrossRefGoogle ScholarPubMed
Reimers, E, Ringberg, T & Sorumgaard, R (1982) Body composition of Svalbard reindeer. Canadian Journal of Zoology 60, 18121821.CrossRefGoogle Scholar
Renz, M, Tomlinson, E, Hultgren, B, Levin, N, Gu, Q, Shimkets, RA, Lewin, DA & Stewart, TA (2000) Quantitative expression analysis of genes regulated by both obesity and leptin reveals a regulatory loop between leptin and pituitary–derived ACTH. Journal of Biological Chemistry 275, 1042910436.Google Scholar
Sugden, MC, Holness, MJ & Howard, RM (1993) Changes in lipoprotein lipase activities in adipose tissue, heart and skeletal muscle during continuous or interrupted feeding. Biochemical Journal 292, 113119.CrossRefGoogle ScholarPubMed
Vernon, RG (1989) Endocrine control of metabolic adaptation during lactation. Proceedings of the Nutrition Society 48, 2332.CrossRefGoogle ScholarPubMed
Vernon, RG, Clegg, RA & Flint, DJ (1986) Adipose tissue metabolism in sheep: response to season and its modulation by reproductive state. Hormone Metabolism Research 18, 308312.CrossRefGoogle ScholarPubMed
Vernon, RG & Taylor, E (1986) Enzymes of adenosine metabolism of sheep adipose tissue: changes in activity with season, pregnancy and lactation. Hormone and Metabolic Research 18, 369373.Google Scholar
Wade, N & Bartness, TJ (1984) Effects of photoperiod and gonadectomy on food intake, body weight, and body composition in Siberian hamsters. American Journal of Physiology 246, R26R30.Google ScholarPubMed
Wolden–#Hanson, T, Mitton, DR, McCants, L, Yellon, SM, Wilkinson, CW, Matsumoto, AM & Rasmussen, DD (2000) Daily melatonin administration to middle–aged male rats suppresses body weight, intraabdominal adiposity, and plasma leptin and insulin independent of food intake and total body fat. Endocrinology 141, 487497.CrossRefGoogle ScholarPubMed
Youngstrom, TG & Bartness, TJ (1995) Catecholaminergic innervation of white adipose tissue in Siberian hamsters. American Physiological Society 268, R744R751.Google Scholar