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Differential control of lipogenesis and lipolysis during development of ovine preadipocytes in vitro

Published online by Cambridge University Press:  09 March 2007

B. Soret ,
S. E. Melrose ,
E. Finley  and
R. G. Vernon
E. Finley
Affiliation:
Hannah Research Institute, Ayr KA6 5HL, UK
R. G. Vernon
Affiliation:
Hannah Research Institute, Ayr KA6 5HL, UK
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Abstract

The stromovascular fraction of adipose tissue from sheep, like that of other species, contains preadipocytes which can be induced to differentiate in culture, providing a potentially useful system for studying adipocyte development. Differentiation of ruminant preadipocytes has only been partly characterized previously so we have investigated the factors regulating the development of lipogenesis and lipolysis in sheep cells. Insulin, rosiglitazone (a peroxisome proliferation activated receptor-γ agonist) and either dexamethasone or a lipid suplement are required during differentiation for maximum rates of lipogenesis, whereas all four components are required to achieve maximum rates of catecholamine-stimulated lipolysis. Tri-iodothyronine had no effect on the development of lipogenesis but resulted in a reduced rate of catecholamine-stimulated lipolysis. Lipogenesis and lipolysis also differed in that the rate of lipogenesis increased to a maximum at about 10 days of differentiation and then fell, whereas the rate of lipolysis reached a plateau at about 10 days. By contrast to catecholamine-stimulated lipolysis, there is little or no evidence for development of the adenosine-based antilipolytic system; this may be because response to adenosine develops very late during preadipocyte differentiation or additional, unidentified factors are required to induce this antilipolytic system. Lipogenesis in differentiated preadipocytes responded to both insulin and growth hormone. These studies show that the development of lipogenesis and lipolysis are under distinct control systems. Furthermore, while preadipocytes differentiated in vitro show many of the characteristics of adipocytes differentiated in vivo, there are still significant differences.

Keywords

adipocytescell culture, lipogenesislipolysissheep
Type
Research Article
Information
Animal Science , Volume 82 , Issue 4 , August 2006 , pp. 517 - 525
Copyright
Copyright © British Society of Animal Science 2006

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References

Ailhaud, G., Grimaldi, P. and Négrel, R. (1992) Cellular and molecular aspects of adipose tissue development. Annual Review of Nutrition 12: 207–233.CrossRefGoogle ScholarPubMed
Arana, A., Vernon, R. G., Eguinoa, P., Soret, B., Mendizábal, J. A. and Purroy, A. (2002) Differentiation in vitro of omental and subcutaneous preadipocytes from Spanish Lacha and Rasa Aragonesa sheep. Animal Science 74: 469–476.CrossRefGoogle Scholar
Aso, H., Abe, H., Nakajima, I., Ozutsumi, K., Yamaguchi, T., Takamori, Y., Kodama, A., Hoshino, F. B. and Takano, S. (1995) A preadipocytes clonal line from bovine intramuscular adipose tissue: nonexpression of GLUT-4 protein during adipocyte differentiation. Biochemical and Biophysical Research Communications 213: 369–375.CrossRefGoogle ScholarPubMed
Boone, C., Grégoire, F. and Remacle, C. (2000) Culture of porcine stromal-vascular cells in serum-free medium: differential action of various hormonal agents on adipose conversion. Journal of Animal Science 78: 885–895.CrossRefGoogle ScholarPubMed
Børglum, J. D., Vassaux, G., Richelsen, B., Gaillard, D., Darimont, C., Ailhaud, G. and Negrel, R. (1996) Changes in adenosine A 1 - and A 2 - receptor expression during adipose cell differentiation. Molecular and Cellular Endocrinology 117: 17–25.CrossRefGoogle Scholar
Bowen, W. P., Flint, D. J. and Vernon, R. G. (1992) Regional and interspecific differences in the ligand binding properties of β-adrenergic receptors of individual white adipose tissue depots in the sheep and rat. Biochemical Pharmacology 44: 681–686.CrossRefGoogle ScholarPubMed
Broad, T. E. and Ham, R. G., (1983) Growth and adipose differentiation of sheep preadipocyte fibroblasts in serum-free medium. European Journal of Biochemistry 135: 33–39.CrossRefGoogle ScholarPubMed
Butterwith, S. C. (1994) Molecular events in adipocyte development. Pharmacology and Therapeutics 61: 399–411.CrossRefGoogle ScholarPubMed
Casteilla, L., Muzzin, P., Revelli, J.-P., Ricquier, D. and Giacobino, J.-P. (1994). Expression of β 1 - and β 3 -adrenergic-receptor messages and adenylate cyclase β-adrenergic response in bovine perirenal adipose tissue during its transformation from brown into white fat. Biochemical Journal 297: 93–97.CrossRefGoogle ScholarPubMed
Casteilla, L., Nouguès, J., Reyne, Y. and Ricquier, D. (1991). Differentiation of ovine brown adipocyte precursor cells in a chemically defined serum-free medium. European Journal of Biochemistry 198: 195–199.CrossRefGoogle Scholar
Chen, N. X., Hausman, G. J. and Wright, J. T. (1996) Hormonal regulation of insulin-like growth factor binding proteins and insulin-like growth factor 1 (IGF-1) secretion in porcine stromal-vascular cultures. Journal of Animal Science 74: 2369–2375.CrossRefGoogle ScholarPubMed
Darimont, C., Gaillard, D., Ailhaud, G. and Negrel, R. (1993) Terminal differentiation of mouse preadipocytes cells: adipogenic and antimitogenic role of triiodothyronine. Molecular and Cellular Endocrinology 98: 67–73.CrossRefGoogle ScholarPubMed
Deslex, S., Negrel, R. and Ailhaud, G. (1987) Development of a chemically defined serum-free medium for differentiation of rat adipose precursor cells. Experimental Cell Research 186: 15–30.CrossRefGoogle Scholar
Ferlay, A., Charret, C., Galitzky, J., Berlan, M. and Chilliard, Y. (2001) Effects of the perfusion of β-, β2-, or β3-adrenergic agonists or epinephrine on in situ adipose tissue lipolysis measured by microdialysis in underfed ewes. Journal of Animal Science 79: 453–462.CrossRefGoogle ScholarPubMed
Flint, D. J. and Vernon, R. G. (1993) Hormones and adipose tissue growth. In Vertebrate endocrinology: fundamentals and biomedical implications (ed. Schreibman, M. P., Scanes, C. G. and Pang, P. K. T.), pp. 469–494. Academic Press, Orlando.CrossRefGoogle Scholar
Folch, J., Lees, M. and Stanley, G. H. S. (1957) A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226: 497–509.CrossRefGoogle ScholarPubMed
Gate, J. J., Clarke, L., Bird, J. A., Lomax, M. A. and Symonds, M. E. (2000) Effect of feeding level and thyroxine on adipose tissue development and growth in postnatal lambs. Experimental Physiology 85: 439–444.CrossRefGoogle ScholarPubMed
Grégoire, F. M., Smas, C. M. and Sul, H. S. (1998) Understanding adipocyte differentiation. Physiological Reviews 78: 783–809.CrossRefGoogle ScholarPubMed
Halvorsen, Y.-D. C., Bond, A., Sen, A., Franklin, D. M., Lea-Currie, Y. R., Sujkowski, D., Ellis, P. N., Wilkison, W. O. and Gimble, J. M. (2001) Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: biochemical, cellular, and molecular analysis. Metabolism 50: 407–413.CrossRefGoogle ScholarPubMed
Hausman, D. B., Hausman, G. J. and Martin, R. J. (1999) Endocrine regulation of fetal adipose tissue development in the pig: interaction of porcine growth hormone and thyroxine. Obesity Research 7: 76–82.CrossRefGoogle ScholarPubMed
Hausman, D. B., Hausman, G. J. and Martin, R. J. (1996) Endocrine regulation of fetal adipose tissue metabolism in the pig: ontogeny of thyroxine influence. Biology of the Neonate 70: 41–51.CrossRefGoogle ScholarPubMed
Hausman, G. J. (1989) The influence of insulin and triiodothyronine (T 3) and insulin-like growth factor-1 (IGF-1) on the differentiation of preadipocytes in serum-free cultures of pig stromal-vascular cells. Journal of Animal Science 67: 3136–3143.CrossRefGoogle Scholar
Hausman, G. J. (1992) The influence of thyroxine on the differentiation of adipose tissue and skin during fetal development. Pediatric Research 32: 204–211.CrossRefGoogle ScholarPubMed
Klaus, S., Ely, M., Encke, D. and Heldmaier, G. (1995) Functional assessment of white and brown adipocyte development and energy metabolism in cell culture. Dissociation of terminal differentiation and thermogenesis in brown adipocytes. Journal of Cell Science 108: 3171–3180.CrossRefGoogle Scholar
Krebs, H. A. and Henseleit, K. (1933) Urea formation in the animal body. Hoppe-Seyler's Zeitschift für Physiologische Chemie 210: 33–66.CrossRefGoogle Scholar
Labarca, C. and Paigen, K. (1980) A simple rapid and sensitive DNA assay procedure. Analytical Biochemistry 102: 344–352.CrossRefGoogle ScholarPubMed
Malbon, C. C., Rapiejko, P. J. and Watkins, D. C. (1988) Permissive hormone regulation of hormone-sensitive effector systems. Trends in Pharmacological Science 9: 33–36.CrossRefGoogle ScholarPubMed
Mersmann, H. J., Carey, G. B. and O'Brian Smith, E. (1997a) Adipose tissue β-adrenergic and A 1 adenosine receptors in suckling pigs. Journal of Animal Science 75: 3161–3168.CrossRefGoogle Scholar
Mersmann, H. J., Carey, G. B. and O'Brian Smith, E. (1997b) Influence of nutritional weaning on porcine adipocyte β-adrenergic and adenosine-A 1 receptors. Journal of Animal Science 75: 2368–2377.CrossRefGoogle Scholar
Moulin, K., Truel, N., André, M., Arnauld, E., Nibbelink, M., Cousin, B., Dani, C., Pénicaud, L. and Casteilla, L. (2001) Emergence during development of the white-adipocyte cell phenotype is independent of the brown-adipocyte cell phenotype. Biochemical Journal 356: 659–664.CrossRefGoogle ScholarPubMed
Nedergaard, J., Connolly, E. and Cannon, B. (1986) Brown adipose tissuein the mammalian neonate. In Brown adipose tissue (ed. Trayhurn, P. and Nicholls, D. G.), pp. 152–213.E.Arnold, London.Google Scholar
Nouguès, J., Reyne, Y., Champigny, O., Holloway, B., Casteilla, L. and Ricquier, D. (1993) The β3-adrenoceptor agonist ICI-D7114 is not as efficient on reinduction of uncoupling protein mRNA in sheep as it is in dogs and smaller species. Journal of Animal Science 71: 2388–2394.CrossRefGoogle Scholar
Ohyama, M., Matsuda, K., Torii, S., Matsui, T., Yano, H., Kawada, T. and Ishihara, T. (1998) The interaction between vitamin A and thiazolidinedione on bovine adipocyte differentiation in primary culture. Journal of Animal Science 76: 61–65.CrossRefGoogle ScholarPubMed
Patel, N. G., Holder, J. C., Smith, S. A., Kumar, S. and Eggo, M. C. (2003) Differential regulation of lipogenesis and leptin production by independent signalling pathways and rosiglitazone during human adipocyte differentiation. Diabetes 52: 43–50.CrossRefGoogle ScholarPubMed
Patterson, H. D. and Thompson, R. (1971) Recovery of inter-block information when block sizes are unequal. Biometrika 58: 545–554.CrossRefGoogle Scholar
Piétri-Rouxel, F., Lenzen, G., Kapoor, A., Drumare, M.-F., Archimbaud, P.Strosberg, A. D., Manning, B. and St, J. (1995) Molecular cloning and pharmacological characterization of the bovine β3-adrenergic receptor. European Journal of Biochemistry 230: 350–358.CrossRefGoogle Scholar
Plested, C. P., Taylor, E., Brindley, D. N. and Vernon, R. G. (1987) Interactions of insulin and dexamethasone in the control of pyruvate kinase activity and glucose metabolism in sheep adipose tissue. Biochemical Journal 247: 459–465.CrossRefGoogle ScholarPubMed
Ramsay, T. G., Rao, S. V. and Wolverton, C. K. (1992) In vitro systems for the analysis of the development of adipose tissue in domestic animals. Journal of Nutrition 122: 806–817.CrossRefGoogle ScholarPubMed
Rubio, M., Raasmaja, A. and Enrique Silva, J. (1995) Thyroid hormone and norepinephrine signalling in brown adipose tissue: differential effects of thyroid hormone on β 3 -adrenergic receptors in brown and white adipose tissue. Endocrinology 136: 3277–3284.CrossRefGoogle ScholarPubMed
Saulnier-Blanche, J. S., Dauzats, M., Daviaud, D., Gaillard, D., Ailhaud, G., Négrel, R. and Lafontan, M. (1991) Late expression of α2-adrenergic-mediated antilipolysis during differentiation of hamster preadipocytes. Journal of Lipid Research 32: 1489–1499.CrossRefGoogle Scholar
Smith, S. B., Carstens, G. E., Randerl, R. D., Mersmann, H. J. and Lunt, D. K. (2004) Brown adipose tissue development and metabolism in ruminants. Journal of Animal Science 82: 942–954.CrossRefGoogle ScholarPubMed
Sonnenfeld, M. C., Karpe, B., Bolme, P. and Arner, P. (1989) Inhibition of lipolysis by agents acting via adenylate cyclase in fat cells from infants and adults. Pediatrics Research 26: 255–259.Google Scholar
Soret, B., Lee, H.-J., Finley, E., Lee, S. C. and Vernon, R. G. (1999) Regulation of differentiation of sheep subcutaneous and abdominal preadipocytes in culture. Journal of Endocrinology 161: 517–524.CrossRefGoogle ScholarPubMed
Suryawan, A., Swanson, L. V. and Hu, C. Y. (1997) Insulin and hydrocortisone, but not triiodothyronine, are required for the differentiation of pig preadipocytes in primary culture. Journal of Animal Science 75: 105–111.CrossRefGoogle ScholarPubMed
Sztalryd, C., Levacher, C. and Picon, L. (1989) Acceleration by triiodothyronine of adipose conversion of rat preadipocytes from two adipose localisations. Cellular and Molecular Biology 35: 81–88.Google Scholar
Travers, M. T., Vallance, A. J., Gourlay, H. T., Gill, G. A., Klein, I., Bottema, C. B. K. and Barber, M. C. (2001) Promoter 1 of the ovine acetyl-CoA carboxylase-α gene: an E-box motif at -114 in the proximal promoter binds upstream stimulatory factor (USF)-1 and USF-2 and acts as an insulin-response sequence in differentiating adipocytes. Biochemical Journal 359: 273–284.CrossRefGoogle ScholarPubMed
Van de Venter, M., Litthauer, D. and Oelofsen, W. (1994) Catecholamine stimulated lipolysis in differentiated human preadipocytes in a serum-free, defined medium. Journal of Cellular Biochemistry 54: 1–10.CrossRefGoogle Scholar
Vassaux, G., Gaillard, D., Mari, B., Ailhaud, G. and Negrel, R. (1993) Differential expression of adenosine A 1 and A 2 receptors in preadipocytes and adipocytes. Biochemical and Biophysical Research Communications 193: 1123–1130.CrossRefGoogle Scholar
Vernon, R. G. (1992) Control of lipogenesis and lipolysis. In The control of fat and lean deposition (ed. Boorman, K. N., Buttery, P. J. and Lindsay, D. B.), pp. 59–81. Butterworth Heinemann, Oxford.CrossRefGoogle Scholar
Vernon, R. G. and Taylor, E. (1986) Acetyl CoA carboxylase of sheep adipose tissue: problems of the assay and adaptation during fetal development. Journal of Animal Science 63: 1119–1125.CrossRefGoogle ScholarPubMed
Vierck, J. L., McNamara, J. P. and Dodson, M. V. (1996) Proliferation and differentiation of progeny of ovine unilocular fat cells (adipofibroblasts). In Vitro Cellular and Developmental Biology 32: 564–572.CrossRefGoogle ScholarPubMed
Wise, L. S. and Green, H. (1979) Participation of one isozyme of cytosolic glycerolphosphate dehydrogenase in the adipose conversion of 3T3 cells. Journal of Biological Chemistry 254: 273–275.CrossRefGoogle Scholar
Wrutniak, C. and Cabello, G. (1986) Influence of hypothyroidism on the lipolytic activity of norepinephrine in the newborn lamb. Journal of Endocrinology 108: 451–454.CrossRefGoogle ScholarPubMed
Wu, P., Sato, K., Suzuta, F., Hikasa, Y. and Kagota, K. (2000) Effects of lipid-related factors on adipocyte differentiation of bovine stromal-vascular cells in primary culture. Journal of Veterinary Medicinal Science 62: 933–939.CrossRefGoogle ScholarPubMed