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Adipose tissue metabolism and its role in adaptations to undernutrition in ruminants

Published online by Cambridge University Press:  03 March 2008

Yves Chilliard ,
Anne Ferlay ,
Yannick Faulconnier ,
Muriel Bonnet ,
Jacques Rouel  and
François Bocquier
Yves Chilliard*
Affiliation:
Adipose Tissue and Milk Lipids Team of the Research Unit on Herbivores, INRA – Theix, 63122 St Genès Champanelle, France
Anne Ferlay
Affiliation:
Adipose Tissue and Milk Lipids Team of the Research Unit on Herbivores, INRA – Theix, 63122 St Genès Champanelle, France
Yannick Faulconnier
Affiliation:
Adipose Tissue and Milk Lipids Team of the Research Unit on Herbivores, INRA – Theix, 63122 St Genès Champanelle, France
Muriel Bonnet
Affiliation:
Adipose Tissue and Milk Lipids Team of the Research Unit on Herbivores, INRA – Theix, 63122 St Genès Champanelle, France
Jacques Rouel
Affiliation:
Adipose Tissue and Milk Lipids Team of the Research Unit on Herbivores, INRA – Theix, 63122 St Genès Champanelle, France
François Bocquier
Affiliation:
Adipose Tissue and Milk Lipids Team of the Research Unit on Herbivores, INRA – Theix, 63122 St Genès Champanelle, France
*
*Corresponding author: Yves Chilliard, fax +33 473 62 45 19, email [email protected]
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Abstract

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Changes in the amount and metabolism of adipose tissue (AT) occur in underfed ruminants, and are amplified during lactation, or in fat animals. The fat depot of the tail of some ovine breeds seems to play a particular role in adaptation to undernutrition; this role could be linked to its smaller adipocytes and high sensitivity to the lipolytic effect of catecholamines. Glucocorticoids and growth hormone probably interact to induce teleophoretic changes in the AT responses to adenosine and catecholamines during lactation. Fat mobilization in dry ewes is related both to body fatness and to energy balance. The in vivo β-adrenergic lipolytic potential is primarily related to energy balance, whereas basal postprandial plasma non-esterified fatty acids (NEFA) are related to body fatness, and preprandial plasma NEFA is the best predictor of the actual body lipid loss. Several mechanisms seem to be aimed at avoiding excessive fat mobilization and/or insuring a return to the body fatness homeostatic set point. As well as providing the underfed animal with fatty acids as oxidative fuels, AT acts as an endocrine gland. The yield of leptin by ruminant AT is positively related to body fatness, decreased by underfeeding, β-adrenergic stimulation and short day length, and increased by insulin and glucocorticoids. This finding suggests that the leptin chronic (or acute) decrease in lean (or underfed respectively) ruminants is, as in rodents, a signal for endocrine, metabolic and behavioural adaptations aimed at restoring homeostasis.

Keywords

Ruminant undernutritionAdipose tissueLipogenesisLeptin
Type
Animal Nutrition and Metabolism Group Symposium on ‘Regulation of maternal reserves and effects on lactation and the nutrition of young animals’
Information
Proceedings of the Nutrition Society , Volume 59 , Issue 1 , February 2000 , pp. 127 - 134
Copyright
Copyright © The Nutrition Society 2000

References

Ahima, RS, Prabakaran, D, Mantzoros, C, Qu, D, Lowell, B, Maratos-Flier, E & Flier, JS (1996) Role of leptin in the neuroendocrine response to fasting. Nature 382, 250–252.CrossRefGoogle ScholarPubMed
Atti, N & Bocquier, F (1999) Adaptation des brebis Barbarine à l'alternance de sous-nutrition-réalimentation: effets sur les tissus adipeux (Adaptive capacity of Barbary ewes to underfeeding and refeeding periods: effects on adipose tissues). Annales de Zootechnie 48, 189–198.CrossRefGoogle Scholar
Atti, N, Nefzaoui, A & Bocquier, F (1995) Influence de l'état corporel à la mise bas sur les performances, le bilan énergétique de l'évolution des métabolites sanguins de la brebis Barbarine (Effect of body fatness at lambing on performances, energy balance and blood metabolites in the Barbary ewe). Options Méditerranéennes Série A: Séminaires Méditerranéens no. 27, pp. 25–33.Zaragoza, Spain: Centre International des Haut Etudes Agronomiques Méditerranéenes.Google Scholar
Bauman, DE & Vernon, RG (1993) Effects of exogenous bovine somatotropin on lactation. Annual Review of Nutrition 13, 437–461.CrossRefGoogle ScholarPubMed
Bocquier, F, Atti, N, Purroy, A & Chilliard, Y (2000) The role of body reserves in the metabolic adaptation of different breeds of sheep to food shortage. In Livestock Production and Climatic Uncertainty in the Mediterranean. European Association of Animal Production Publication no. 94 [F, Guessous, editor]. Amsterdam: Wageningen Pers (In the Press).Google Scholar
Bocquier, F, Bonnet, M, Faulconnier, Y, Guerre-Millo, M, Martin, P & Chilliard, Y (1998a) Effects of photoperiod and feeding level on adipose tissue metabolic activity and leptin synthesis in the sheep. Reproduction Nutrition Development 38, 489–498.CrossRefGoogle Scholar
Bocquier, F, Ferlay, A & Chilliard, Y (1998b) Effects of body lipids and energy balance on the response of plasma non-esterified fatty acids to a β-adrenergic challenge in the lactating dairy ewe. In Energy Metabolism of Farm Animals, pp. 167–173 [K, McCracken, EF, Unsworth and ARG, Wylie, editors]. Wallingford, Oxon: CAB International.Google Scholar
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 Development 38, 297–307.CrossRefGoogle ScholarPubMed
Bonnet, M, Faulconnier, Y, Leroux, C, Bocquier, F, Martin, P & Chilliard, Y (1999) Effect of refeeding on two mRNAs species of lipoprotein lipase in adipose and cardiac muscle of sheep. Proceedings of the Nutrition Society 58, 108A.Google Scholar
Cherel, Y, Robin, JP, Heitz, A, Calgari, C & Le, Maho Y (1992) Relationships between lipid availability and protein utilization during prolonged fasting. Journal of Comparative Physiology 162B, 305–313.CrossRefGoogle ScholarPubMed
Chilliard, Y (1986) Variations quantitatives et métabolisme des lipides dans les tissus adipeux et le foie au cours du cycle gestation-lactation. 1 – Chez la ratte (Body composition and lipid metabolism in adipose tissues and liver during pregnancy and lactation. 1 – In the rat). Reproduction Nutrition Development 26, 1057–1103.CrossRefGoogle ScholarPubMed
Chilliard, Y (1987) Variations quantitatives et métabolisme des lipides dans les tissus adipeux et de foie au cours du cycle gestation-lactation. 2 – Chez la brebis et la vache (Body composition and lipid metabolism in adipose tissues and liver during pregnancy and lactation. 2 – In the ewe and the cow). Reproduction Nutrition Development 27, 327–398.CrossRefGoogle Scholar
Chilliard, Y (1992) Physiological constraints to milk production: factors which determine nutrient partitioning, lactation persistency and mobilization of body reserves. World Review of Animal Production 27, 19–26.Google Scholar
Chilliard, Y (1999) Metabolic adaptations and nutrient partitioning in the lactating animal. In Biology of Lactation, pp. 503–552 [Martinet, J, Houdebine, LM and Head, HH, editors]. Paris: INRA Ed.Google Scholar
Chilliard, Y & Bocquier, F (2000) Direct effects of photoperiod on lipid metabolism, leptin synthesis and milk secretion in adult sheep. Proceedings of the IXth International Symposium on Ruminant Physiology (In the Press).Google Scholar
Chilliard, Y, Bocquier, F, Delavaud, C, Guerre-Millo, M, Bonnet, M, Martin, P, Faulconnier, Y & Ferlay, A (1998a) Leptin in ruminants: effects of species, breed, adiposity, photoperiod, beta-agonists and nutritional status. Proceedings of the Cornell Nutrition Conference for Feed Manufacturers, pp. 65–74.Ithaca, NY: Cornell University.Google Scholar
Chilliard, Y, Bocquier, F & Doreau, M (1998b) Digestive and metabolic adaptations of ruminants to undernutrition, and consequences on reproduction. Reproduction Nutrition Development 38, 131–152.CrossRefGoogle ScholarPubMed
Chilliard, Y, Ferlay, A, Despres, L & Bocquier, F (1998c) Plasma non esterified fatty acid response to a beta-adrenergic challenge before or after feeding in energy underfed or overfed, dry or lactating cows. Animal Science 67, 213–223.CrossRefGoogle Scholar
Cowan, RT, Robinson, JJ & McDonald, I (1982) A note on the effects of body fatness and level of food intake on rate of fat loss in lactating ewes. Animal Production 34, 355–357.Google Scholar
Cowan, RT, Robinson, JJ, McDonald, I & Smart, R (1980) Effects of body fatness at lambing and diet in lactation on body tissue loss, feed intake and milk yield of ewes in early lactation. Journal of Agricultural Science, Cambridge 95, 497–514.CrossRefGoogle Scholar
Dunshea, FR, Bell, AW & Trigg, TE (1988) Relations between plasma non-esterified fatty acid metabolism and body tissue mobilization during chronic undernutrition in goats. British Journal of Nutrition 60, 633–644.CrossRefGoogle ScholarPubMed
Dunshea, FR, Bell, AW & Trigg, TE (1990) Non-esterified fatty acid and glycerol kinetics and fatty acid re-esterification in goats during early lactation. British Journal of Nutrition 64, 133–145.CrossRefGoogle ScholarPubMed
Faulconnier, Y, Bonnet, M, Bocquier, F, Leroux, C, Hocquette, JF, Martin, P & Chilliard, Y (1999a) Effet du niveau alimentaire et de la photopériode sur l'expression des gènes contrôlant le métabolisme lipidique tissulaire chez le ruminant (Effect of feeding level and photoperiod on the expression of genes encoding enzymes of tissue lipid metabolism in the ruminant). INRA Productions Animales 12, 287–300.CrossRefGoogle Scholar
Faulconnier, Y, Bonnet, M, Fléchet, J, Bocquier, F & Chilliard, Y (1999b) Nutritional regulation of lipoprotein lipase in bovine adipose tissues and muscles. Proceedings of the Nutrition Society 58, 109A.Google Scholar
Ferlay, A, Charret, C, Galitzky, J, Berlan, M & Chilliard, Y (1998) Effects of the infusion of β-, β2- or β3- adrenergic agonists or epinephrine on in situ lipolysis in ewe subcutaneous adipose tissue. Reproduction Nutrition Development 38, 196–197.CrossRefGoogle Scholar
Ferlay, A & Chilliard, Y (1999) Effects of the infusion of non selective β-, and selective β1- or β2-adrenergic agonists, on body fat mobilisation in underfed or overfed non-pregnant heifers. Reproduction Nutrition Development 39, 409–421.CrossRefGoogle ScholarPubMed
Ferlay, A, Chilliard, Y, Sala, AM, Durier, C & Bocquier, F (1996) Somatotropin treatment does not effect non-esterified fatty acid response to adrenergic injections in underfed or overfed nonlactating cows. Journal of Nutrition 126, 945–954.CrossRefGoogle ScholarPubMed
Friedman, JM & Halaas, JL (1998) Leptin and the regulation of body weight in mammals. Nature 395, 763–770.CrossRefGoogle ScholarPubMed
Gagliostro, G & Chilliard, Y (1991) Duodenal rapeseed oil infusion in early and midlactation cows. 4. In vivo and in vitro adipose tissue lipolytic responses. Journal of Dairy Science 74, 1830–1843.CrossRefGoogle ScholarPubMed
Gilson, TL, Kennedy, AD & Rampersand, T (1996) Effects of breed and adipose depot location on responsiveness and sensitivity to adrenergic stimulation in ovine adipose tissue. Comparative Biochemistry and Physiology 115C, 19–26.Google ScholarPubMed
Heiman, ML, Sloop, KW, Chen, Y & Caro, JF (1999) Extension of neuroendocrine axes to include leptin. Journal of Animal Science 77, Suppl. 3, 33–42.CrossRefGoogle Scholar
Houseknecht, KL & Bauman, DE (1997) Regulation of lipolysis by somatotropin: functional alteration of adrenergic and adenosine signaling in bovine adipose tissue. Journal of Endocrinology 152, 465–475.CrossRefGoogle ScholarPubMed
Houseknecht, KL, Bauman, DE, Carey, GB & Mersmann, HJ (1995) Effect of bovine somatotropin and food deprivation on beta-adrenergic and A1 adenosine receptor binding in adipose tissue of lactating cows. Domestic Animal Endocrinology 12, 325–336.CrossRefGoogle ScholarPubMed
Houseknecht, KL, Portocarrero, CP, Ji, S, Lemenager, RP & Spurlock, ME (1998) Growth hormone regulation of leptin gene expression in bovine adipose tissue: in vitro and in vivo studies. International Journal of Obesity 22, Suppl. 3, S166 Abstr.Google Scholar
Le Houérou, HN (1992) Recherches expérimentales sur la tolérance du mouton barbarin à l'inanition et la restriction alimentaire (Experimental research on the adaptation of Barbary ewes to starvation and underfeeding). In L'Aridité: Contrainte au Développement (Aridity: A Constraint to Development), pp. 369–385 [Le Floc'h, E, Grouzis, M, Cornet, A and Bille, JC, editors]. Bondy, France: ORSTOM éditions.Google Scholar
Mc, Namara (1989) Regulation of bovine adipose tissue metabolism during lactation. 5. Relationships of lipid synthesis and lipolysis with energy intake and utilization. Journal of Dairy Science 72, 407–418.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, 69–85.CrossRefGoogle ScholarPubMed
Panaretto, BA (1964) Body composition in vivo. VI. The composition of ewes during a prolonged undernutrition. Australian Journal of Agricultural Research 15, 771–787.CrossRefGoogle Scholar
Pethick, DW & Dunshea, FR (1993) Fat metabolism and turnover. In Quantitative Aspects of Ruminant Digestion and Metabolism, pp. 291–311 [Forbes, JM and France, J, editors]. Wallingford, Oxon: CAB International.Google Scholar
Pickavance, L, Tadayyon, M, Williams, G & Vernon, RG (1998) Lactation suppresses diurnal rhythm of serum leptin. Biochemical and Biophysical Research Communications 248, 196–199.CrossRefGoogle ScholarPubMed
Teixeira, A, Delfa, R & Colomer-Rocher, F (1989) Relationships between fat depots and body condition score or tail fatness in the Rasa Aragonesa breed. Animal Production 49, 275–280.Google Scholar
Vernon, RG (1992) Effects of diet on lipolysis and its regulation. Proceedings of the Nutrition Society 51, 397–408.CrossRefGoogle ScholarPubMed
Vernon, RG (1998) Homeorhesis. In Yearbook 1998, pp.64–73 [E, Taylor, editor. Ayr, Scotland: Hannah Research Institute.Google Scholar
Vernon, RG, Doris, R, Finley, E, Houslay, MD, Kilgour, E & Linday-Watt, S (1995a) Effects of lactation on the signal transduction systems regulating lipolysis in sheep subcutaneous and omental adipose tissue. Biochemical Journal 308, 291–296.CrossRefGoogle ScholarPubMed
Vernon, RG, Faulkner, A, Finley, E, Watt, PW & Zammit, VA (1995b) Effects of prolonged treatment of lactating goats with bovine somatotropin on aspects of adipose tissue and liver metabolism. Journal of Dairy Research 62, 237–248.CrossRefGoogle ScholarPubMed