Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1993 Jun 15;292(Pt 3):873–876. doi: 10.1042/bj2920873

Adipose tissues from various anatomical sites are characterized by different patterns of gene expression and regulation.

B Cousin 1, L Casteilla 1, C Dani 1, P Muzzin 1, J P Revelli 1, L Penicaud 1
PMCID: PMC1134195  PMID: 8318015

Abstract

We have shown previously the presence of brown adipocytes among white fat pads, and proposed the existence of a spectrum of adipose depots according to the abundance of brown fat cells [Cousin, Cinti, Morroni, Raimbault, Ricquier, Pénicaud and Casteilla (1992) J. Cell Sci. 103, 931-942]. In this study, we tried to characterize this spectrum better. We determined in several adipose depots (i) the richness of pre-adipose cells, as assessed by A2COL6 mRNA levels; (ii) whether a fat pad was characterized by a pattern of mRNA expression; (iii) whether this pattern was close related to abundance of brown adipocytes, and (iv) whether the regulation of this pattern by catecholamines under cold exposure or beta-agonist treatment was similar in the different pads. This was achieved by studying proteins involved in glucose and lipid metabolism such as insulin-sensitive glucose transporter (GLUT4), fatty acid synthase, lipoprotein lipase and fatty acid binding protein aP2, as well as beta 3-adrenergic-receptor expression. Among white adipose depots, the periovarian fat pad was characterized by the highest content of pre-adipocytes and of brown adipocytes, and inguinal fat by the highest lipogenic activity potential. There was no close correlation between beta 3-adrenergic-receptor expression and brown adipocyte content in the tissues, as measured by the degree of uncoupling protein (UCP) gene expression. However, in pads expressing UCP mRNA, mRNA levels of beta 3-adrenergic receptor and other markers were increased in parallel. Under cold exposure or beta 3-agonist treatment, a specific up-regulation of GLUT4 expression was observed in interscapular brown adipose tissue. The regional difference described in this study, could participate in preferential fat-pad growth under physiological conditions as well as in pathological situations.

Full text

PDF

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Assimacopoulos-Jeannet F., Greco-Perotto R., Terrettaz J., Meier M. K., Jeanrenaud B. Effect of a beta-adrenergic agonist on glucose transport and insulin-responsive glucose transporters (GLUT4) in brown adipose tissue of control and obese fa/fa rats. Pflugers Arch. 1992 May;421(1):52–58. doi: 10.1007/BF00374733. [DOI] [PubMed] [Google Scholar]
  2. Bouillaud F., Ricquier D., Thibault J., Weissenbach J. Molecular approach to thermogenesis in brown adipose tissue: cDNA cloning of the mitochondrial uncoupling protein. Proc Natl Acad Sci U S A. 1985 Jan;82(2):445–448. doi: 10.1073/pnas.82.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carneheim C., Nedergaard J., Cannon B. Beta-adrenergic stimulation of lipoprotein lipase in rat brown adipose tissue during acclimation to cold. Am J Physiol. 1984 Apr;246(4 Pt 1):E327–E333. doi: 10.1152/ajpendo.1984.246.4.E327. [DOI] [PubMed] [Google Scholar]
  4. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  5. Cousin B., Agou K., Leturque A., Ferre P., Girard J., Pénicaud L. Molecular and metabolic changes in white adipose tissue of the rat during development of ventromedial hypothalamic obesity. Eur J Biochem. 1992 Jul 1;207(1):377–382. doi: 10.1111/j.1432-1033.1992.tb17060.x. [DOI] [PubMed] [Google Scholar]
  6. Cousin B., Cinti S., Morroni M., Raimbault S., Ricquier D., Pénicaud L., Casteilla L. Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J Cell Sci. 1992 Dec;103(Pt 4):931–942. doi: 10.1242/jcs.103.4.931. [DOI] [PubMed] [Google Scholar]
  7. Fève B., Emorine L. J., Lasnier F., Blin N., Baude B., Nahmias C., Strosberg A. D., Pairault J. Atypical beta-adrenergic receptor in 3T3-F442A adipocytes. Pharmacological and molecular relationship with the human beta 3-adrenergic receptor. J Biol Chem. 1991 Oct 25;266(30):20329–20336. [PubMed] [Google Scholar]
  8. Himms-Hagen J. Brown adipose tissue thermogenesis: interdisciplinary studies. FASEB J. 1990 Aug;4(11):2890–2898. [PubMed] [Google Scholar]
  9. Ibrahimi A., Bertrand B., Bardon S., Amri E. Z., Grimaldi P., Ailhaud G., Dani C. Cloning of alpha 2 chain of type VI collagen and expression during mouse development. Biochem J. 1993 Jan 1;289(Pt 1):141–147. doi: 10.1042/bj2890141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. James D. E., Strube M., Mueckler M. Molecular cloning and characterization of an insulin-regulatable glucose transporter. Nature. 1989 Mar 2;338(6210):83–87. doi: 10.1038/338083a0. [DOI] [PubMed] [Google Scholar]
  11. Johnson P. R., Zucker L. M., Cruce J. A., Hirsch J. Cellularity of adipose depots in the genetically obese Zucker rat. J Lipid Res. 1971 Nov;12(6):706–714. [PubMed] [Google Scholar]
  12. Kashiwagi A., Foley J. E. Opposite effects of a beta-adrenergic agonist and a phosphodiesterase inhibitor on glucose transport in isolated human adipocytes: isoproterenol increases Vmax and IBMX increases Ks. Biochem Biophys Res Commun. 1982 Aug;107(3):1151–1157. doi: 10.1016/0006-291x(82)90642-8. [DOI] [PubMed] [Google Scholar]
  13. Kirchgessner T. G., Svenson K. L., Lusis A. J., Schotz M. C. The sequence of cDNA encoding lipoprotein lipase. A member of a lipase gene family. J Biol Chem. 1987 Jun 25;262(18):8463–8466. [PubMed] [Google Scholar]
  14. Lafontan M., Dang-Tran L., Berlan M. Alpha-adrenergic antilipolytic effect of adrenaline in human fat cells of the thigh: comparison with adrenaline responsiveness of different fat deposits. Eur J Clin Invest. 1979 Aug;9(4):261–266. doi: 10.1111/j.1365-2362.1979.tb00883.x. [DOI] [PubMed] [Google Scholar]
  15. Loncar D. Convertible adipose tissue in mice. Cell Tissue Res. 1991 Oct;266(1):149–161. doi: 10.1007/BF00678721. [DOI] [PubMed] [Google Scholar]
  16. Marette A., Bukowiecki L. J. Stimulation of glucose transport by insulin and norepinephrine in isolated rat brown adipocytes. Am J Physiol. 1989 Oct;257(4 Pt 1):C714–C721. doi: 10.1152/ajpcell.1989.257.4.C714. [DOI] [PubMed] [Google Scholar]
  17. Nahmias C., Blin N., Elalouf J. M., Mattei M. G., Strosberg A. D., Emorine L. J. Molecular characterization of the mouse beta 3-adrenergic receptor: relationship with the atypical receptor of adipocytes. EMBO J. 1991 Dec;10(12):3721–3727. doi: 10.1002/j.1460-2075.1991.tb04940.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nikami H., Shimizu Y., Endoh D., Yano H., Saito M. Cold exposure increases glucose utilization and glucose transporter expression in brown adipose tissue. Biochem Biophys Res Commun. 1992 Jun 30;185(3):1078–1082. doi: 10.1016/0006-291x(92)91736-a. [DOI] [PubMed] [Google Scholar]
  19. Olichon-Berthe C., Van Obberghen E., Le Marchand-Brustel Y. Effect of cold acclimation on the expression of glucose transporter Glut 4. Mol Cell Endocrinol. 1992 Nov;89(1-2):11–18. doi: 10.1016/0303-7207(92)90205-k. [DOI] [PubMed] [Google Scholar]
  20. Pond C. M., Mattacks C. A. The effects of noradrenaline and insulin on lipolysis in adipocytes isolated from nine different adipose depots of guinea-pigs. Int J Obes. 1991 Sep;15(9):609–618. [PubMed] [Google Scholar]
  21. Rebuffé-Scrive M. Neuroregulation of adipose tissue: molecular and hormonal mechanisms. Int J Obes. 1991 Sep;15 (Suppl 2):83–86. [PubMed] [Google Scholar]
  22. Ricquier D., Casteilla L., Bouillaud F. Molecular studies of the uncoupling protein. FASEB J. 1991 Jun;5(9):2237–2242. doi: 10.1096/fasebj.5.9.1860614. [DOI] [PubMed] [Google Scholar]
  23. Santos R. F., Sztalryd C., Reaven G. Effect of anatomical site on insulin action and insulin receptor phosphorylation in isolated rat adipocytes. Int J Obes. 1991 Nov;15(11):755–762. [PubMed] [Google Scholar]
  24. Shimizu Y., Nikami H., Saito M. Sympathetic activation of glucose utilization in brown adipose tissue in rats. J Biochem. 1991 Nov;110(5):688–692. doi: 10.1093/oxfordjournals.jbchem.a123642. [DOI] [PubMed] [Google Scholar]
  25. Sivitz W. I., DeSautel S. L., Kayano T., Bell G. I., Pessin J. E. Regulation of glucose transporter messenger RNA levels in rat adipose tissue by insulin. Mol Endocrinol. 1990 Apr;4(4):583–588. doi: 10.1210/mend-4-4-583. [DOI] [PubMed] [Google Scholar]
  26. Smith O. L. Insulin response in rats acutely exposed to cold. Can J Physiol Pharmacol. 1984 Aug;62(8):924–927. doi: 10.1139/y84-154. [DOI] [PubMed] [Google Scholar]
  27. Smith U., Kuroda M., Simpson I. A. Counter-regulation of insulin-stimulated glucose transport by catecholamines in the isolated rat adipose cell. J Biol Chem. 1984 Jul 25;259(14):8758–8763. [PubMed] [Google Scholar]
  28. Sztalryd C., Azhar S., Reaven G. M. Differences in insulin action as a function of original anatomical site of newly differentiated adipocytes obtained in primary culture. J Clin Invest. 1991 Nov;88(5):1629–1635. doi: 10.1172/JCI115476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Trayhurn P. Fatty acid synthesis in vivo in brown adipose tissue, liver and white adipose tissue of the cold-acclimated rat. FEBS Lett. 1979 Aug 1;104(1):13–16. doi: 10.1016/0014-5793(79)81075-3. [DOI] [PubMed] [Google Scholar]
  30. Vallerand A. L., Lupien J., Bukowiecki L. J. Interactions of cold exposure and starvation on glucose tolerance and insulin response. Am J Physiol. 1983 Dec;245(6):E575–E581. doi: 10.1152/ajpendo.1983.245.6.E575. [DOI] [PubMed] [Google Scholar]
  31. Wang H., Kirkland J. L., Hollenberg C. H. Varying capacities for replication of rat adipocyte precursor clones and adipose tissue growth. J Clin Invest. 1989 May;83(5):1741–1746. doi: 10.1172/JCI114075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Young J. B., Saville E., Rothwell N. J., Stock M. J., Landsberg L. Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue of the rat. J Clin Invest. 1982 May;69(5):1061–1071. doi: 10.1172/JCI110541. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES