Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1997 Feb 1;321(Pt 3):759–767. doi: 10.1042/bj3210759

Adrenergic stimulation of lipoprotein lipase gene expression in rat brown adipocytes differentiated in culture: mediation via beta3- and alpha1-adrenergic receptors.

P Kuusela 1, S Rehnmark 1, A Jacobsson 1, B Cannon 1, J Nedergaard 1
PMCID: PMC1218133  PMID: 9032464

Abstract

In order to investigate whether the positive effect of adrenergic stimulation on lipoprotein lipase (LPL) gene expression in brown adipose tissue is a direct effect on the brown adipocytes themselves, the expression of the LPL gene was investigated by measuring LPL mRNA levels in brown adipocytes, isolated as precursors from the brown adipose tissue of rats and grown in culture in a fully defined medium before experimentation. Addition of noradrenaline led to an enhancement of LPL gene expression; the mRNA levels increased as a linear function of time for at least 5 h and were finally approx. 3 times higher than in control cells, an increase commensurate with that seen in vivo in both LPL mRNA levels and LPL activity during physiological stimulation. The increase was dependent on transcription. The effect of noradrenaline showed simple Michaelis-Menten kinetics with an EC50 of approx. 11 nM. beta3-Agonists (BRL-37344 and CGP-12177) could mimic the effect of noradrenaline; the beta1-agonist dobutamine and the beta2-agonist salbutamol could not; the alpha1-agonist cirazoline had only a weak effect. The effect of noradrenaline was fully inhibited by the beta-antagonist propranolol and was halved by the alpha1-antagonist prazosin; the alpha2-antagonist yohimbine was without effect. An increase in LPL mRNA level similar to (but not significantly exceeding) that caused by noradrenaline could also be induced by the cAMP-elevating agents forskolin and cholera toxin, and 8-Br-cAMP also increased LPL mRNA levels. The increase in LPL gene expression was not mediated via an increase in the level of an intermediary proteinaceous factor. It is concluded that the physiologically induced increase in LPL gene expression is a direct effect of noradrenaline on the brown adipocytes themselves, mediated via a dominant beta3-adrenergic pathway and an auxiliary alpha1-adrenergic pathway which converge at a regulatory point in transcriptional control.

Full Text

The Full Text of this article is available as a PDF (334.9 KB).

Selected References

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

  1. Abe K., Yoshimura K. Changes in lipoprotein lipase activity in tissues of rats exposed to cold of various durations. Nihon Seirigaku Zasshi. 1972 Feb;34(2):81–82. [PubMed] [Google Scholar]
  2. Ailhaud G., Grimaldi P., Négrel R. Cellular and molecular aspects of adipose tissue development. Annu Rev Nutr. 1992;12:207–233. doi: 10.1146/annurev.nu.12.070192.001231. [DOI] [PubMed] [Google Scholar]
  3. Antras J., Lasnier F., Pairault J. Beta-adrenergic-cyclic AMP signalling pathway modulates cell function at the transcriptional level in 3T3-F442A adipocytes. Mol Cell Endocrinol. 1991 Dec;82(2-3):183–190. doi: 10.1016/0303-7207(91)90030-v. [DOI] [PubMed] [Google Scholar]
  4. Arch J. R., Kaumann A. J. Beta 3 and atypical beta-adrenoceptors. Med Res Rev. 1993 Nov;13(6):663–729. doi: 10.1002/med.2610130604. [DOI] [PubMed] [Google Scholar]
  5. Barcellini-Couget S., Pradines-Figuères A., Roux P., Dani C., Ailhaud G. The regulation by growth hormone of lipoprotein lipase gene expression is mediated by c-fos protooncogene. Endocrinology. 1993 Jan;132(1):53–60. doi: 10.1210/endo.132.1.8419145. [DOI] [PubMed] [Google Scholar]
  6. Barcellini-Couget S., Vassaux G., Negrel R., Ailhaud G. Rise in cytosolic Ca2+ abolishes in preadipose cells the expression of lipoprotein lipase stimulated by growth hormone. Biochem Biophys Res Commun. 1994 Feb 28;199(1):136–143. doi: 10.1006/bbrc.1994.1205. [DOI] [PubMed] [Google Scholar]
  7. Belahsen R., Deshaies Y. Alpha-1 adrenergic blockade interacts with dietary carbohydrates on triacylglycerol metabolism in rats. J Nutr. 1993 Mar;123(3):520–528. doi: 10.1093/jn/123.3.520. [DOI] [PubMed] [Google Scholar]
  8. Ben-Zeev O., Doolittle M. H., Davis R. C., Elovson J., Schotz M. C. Maturation of lipoprotein lipase. Expression of full catalytic activity requires glucose trimming but not translocation to the cis-Golgi compartment. J Biol Chem. 1992 Mar 25;267(9):6219–6227. [PubMed] [Google Scholar]
  9. Bertin R., Triconnet M., Portet R. Effects of cold acclimation on the activity of lipoprotein lipase in adipose tissues of genetically obese Zucker rats. Comp Biochem Physiol B. 1985;81(3):797–801. doi: 10.1016/0305-0491(85)90408-0. [DOI] [PubMed] [Google Scholar]
  10. Carneheim C. M., Alexson S. E. Refeeding and insulin increase lipoprotein lipase activity in rat brown adipose tissue. Am J Physiol. 1989 May;256(5 Pt 1):E645–E650. doi: 10.1152/ajpendo.1989.256.5.E645. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Carneheim C., Nedergaard J., Cannon B. Cold-induced beta-adrenergic recruitment of lipoprotein lipase in brown fat is due to increased transcription. Am J Physiol. 1988 Feb;254(2 Pt 1):E155–E161. doi: 10.1152/ajpendo.1988.254.2.E155. [DOI] [PubMed] [Google Scholar]
  13. Champigny O., Holloway B. R., Ricquier D. Regulation of UCP gene expression in brown adipocytes differentiated in primary culture. Effects of a new beta-adrenoceptor agonist. Mol Cell Endocrinol. 1992 Jul;86(1-2):73–82. doi: 10.1016/0303-7207(92)90177-8. [DOI] [PubMed] [Google Scholar]
  14. Connolly E., Nånberg E., Nedergaard J. Norepinephrine-induced Na+ influx in brown adipocytes is cyclic AMP-mediated. J Biol Chem. 1986 Nov 5;261(31):14377–14385. [PubMed] [Google Scholar]
  15. Desanctis J. B., Varesio L., Radzioch D. Prostaglandins inhibit lipoprotein lipase gene expression in macrophages. Immunology. 1994 Apr;81(4):605–610. [PMC free article] [PubMed] [Google Scholar]
  16. Deshaies Y., Arnold J., Richard D. Lipoprotein lipase in adipose tissues of rats running during cold exposure. J Appl Physiol (1985) 1988 Aug;65(2):549–554. doi: 10.1152/jappl.1988.65.2.549. [DOI] [PubMed] [Google Scholar]
  17. Deshaies Y., Géloën A., Paulin A., Marette A., Bukowiecki L. J. Tissue-specific alterations in lipoprotein lipase activity in the rat after chronic infusion of isoproterenol. Horm Metab Res. 1993 Jan;25(1):13–16. doi: 10.1055/s-2007-1002036. [DOI] [PubMed] [Google Scholar]
  18. Deshaies Y., Martineau M. J., LaLonde J. Chronic alpha 1-adrenergic blockade, serum triacylglycerols, and tissue lipoprotein lipase activity in rats fed diets high in starch or sucrose. Nutrition. 1991 Mar-Apr;7(2):109–116. [PubMed] [Google Scholar]
  19. Deshaies Y., Richard D., Arnold J. Lipoprotein lipase in adipose tissues of exercise-trained, cold-acclimated rats. Am J Physiol. 1986 Sep;251(3 Pt 1):E251–E257. doi: 10.1152/ajpendo.1986.251.3.E251. [DOI] [PubMed] [Google Scholar]
  20. Dicker A., Ohlson K. B., Johnson L., Cannon B., Lindahl S. G., Nedergaard J. Halothane selectively inhibits nonshivering thermogenesis. Possible implications for thermoregulation during anesthesia of infants. Anesthesiology. 1995 Feb;82(2):491–501. doi: 10.1097/00000542-199502000-00019. [DOI] [PubMed] [Google Scholar]
  21. Enerbäck S., Gimble J. M. Lipoprotein lipase gene expression: physiological regulators at the transcriptional and post-transcriptional level. Biochim Biophys Acta. 1993 Aug 11;1169(2):107–125. doi: 10.1016/0005-2760(93)90196-g. [DOI] [PubMed] [Google Scholar]
  22. Enerbäck S., Semb H., Bengtsson-Olivecrona G., Carlsson P., Hermansson M. L., Olivecrona T., Bjursell G. Molecular cloning and sequence analysis of cDNA encoding lipoprotein lipase of guinea pig. Gene. 1987;58(1):1–12. doi: 10.1016/0378-1119(87)90023-0. [DOI] [PubMed] [Google Scholar]
  23. Forest C., Doglio A., Casteilla L., Ricquier D., Ailhaud G. Expression of the mitochondrial uncoupling protein in brown adipocytes. Absence in brown preadipocytes and BFC-1 cells. Modulation by isoproterenol in adipocytes. Exp Cell Res. 1987 Jan;168(1):233–246. doi: 10.1016/0014-4827(87)90431-9. [DOI] [PubMed] [Google Scholar]
  24. Forest C., Doglio A., Ricquier D., Ailhaud G. A preadipocyte clonal line from mouse brown adipose tissue. Short- and long-term responses to insulin and beta-adrenergics. Exp Cell Res. 1987 Jan;168(1):218–232. doi: 10.1016/0014-4827(87)90430-7. [DOI] [PubMed] [Google Scholar]
  25. Friedman G., Ben-Naim M., Halimi O., Etienne J., Stein O., Stein Y. The expression of lipoprotein lipase activity and mRNA in mesenchymal rat heart cell cultures is modulated by bFGF. Biochim Biophys Acta. 1991 Feb 26;1082(1):27–32. doi: 10.1016/0005-2760(91)90295-s. [DOI] [PubMed] [Google Scholar]
  26. Friedman G., Reshef A., Ben-Naim M., Leitersdorf E., Stein O., Stein Y. Regulation of lipoprotein lipase by dibutyryl cAMP, cholera toxin, Hepes and heparin in F1 heart-cell cultures. Biochim Biophys Acta. 1992 Oct 27;1137(2):237–241. doi: 10.1016/0167-4889(92)90207-r. [DOI] [PubMed] [Google Scholar]
  27. Gimble J. M., Hua X., Wanker F., Morgan C., Robinson C., Hill M. R., Nadon N. In vitro and in vivo analysis of murine lipoprotein lipase gene promoter: tissue-specific expression. Am J Physiol. 1995 Feb;268(2 Pt 1):E213–E218. doi: 10.1152/ajpendo.1995.268.2.E213. [DOI] [PubMed] [Google Scholar]
  28. Giralt M., Martin I., Iglesias R., Viñas O., Villarroya F., Mampel T. Ontogeny and perinatal modulation of gene expression in rat brown adipose tissue. Unaltered iodothyronine 5'-deiodinase activity is necessary for the response to environmental temperature at birth. Eur J Biochem. 1990 Oct 5;193(1):297–302. doi: 10.1111/j.1432-1033.1990.tb19336.x. [DOI] [PubMed] [Google Scholar]
  29. Giralt M., Martin I., Vilaró S., Villarroya F., Mampel T., Iglesias R., Viñas O. Lipoprotein lipase mRNA expression in brown adipose tissue: translational and/or posttranslational events are involved in the modulation of enzyme activity. Biochim Biophys Acta. 1990 Apr 6;1048(2-3):270–273. doi: 10.1016/0167-4781(90)90066-b. [DOI] [PubMed] [Google Scholar]
  30. Goubern M., Portet R. Circadian rhythm and hormonal sensitivity of lipoprotein lipase activity in cold acclimated rats. Horm Metab Res. 1981 Feb;13(2):73–77. doi: 10.1055/s-2007-1019177. [DOI] [PubMed] [Google Scholar]
  31. Herron D., Néchad M., Rehnmark S., Nelson B. D., Nedergaard J., Cannon B. Effects of cholera toxin on gene expression in brown preadipocytes differentiating in culture. Am J Physiol. 1989 Nov;257(5 Pt 1):C920–C925. doi: 10.1152/ajpcell.1989.257.5.C920. [DOI] [PubMed] [Google Scholar]
  32. Jacobsson A., Stadler U., Glotzer M. A., Kozak L. P. Mitochondrial uncoupling protein from mouse brown fat. Molecular cloning, genetic mapping, and mRNA expression. J Biol Chem. 1985 Dec 25;260(30):16250–16254. [PubMed] [Google Scholar]
  33. Kessin R. H., Fleischmann R. D., Gottesman M. M., Jastorff B., Van Lookeren Campagne M. M. Use of the yeast low-Km cAMP-phosphodiesterase gene to control cyclic AMP levels in mammalian cells. Adv Second Messenger Phosphoprotein Res. 1992;25:13–27. [PubMed] [Google Scholar]
  34. Kirchgessner T. G., LeBoeuf R. C., Langner C. A., Zollman S., Chang C. H., Taylor B. A., Schotz M. C., Gordon J. I., Lusis A. J. Genetic and developmental regulation of the lipoprotein lipase gene: loci both distal and proximal to the lipoprotein lipase structural gene control enzyme expression. J Biol Chem. 1989 Jan 25;264(3):1473–1482. [PubMed] [Google Scholar]
  35. 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]
  36. Kuusela P., Nedergaard J., Cannon B. Beta-adrenergic stimulation of fatty acid release from brown fat cells differentiated in monolayer culture. Life Sci. 1986 Feb 17;38(7):589–599. doi: 10.1016/0024-3205(86)90052-4. [DOI] [PubMed] [Google Scholar]
  37. LaDu M. J., Palmer W. K. Expression of lipoprotein lipase during differentiation of cultured L6 muscle cells. Can J Physiol Pharmacol. 1994 Mar;72(3):243–247. doi: 10.1139/y94-038. [DOI] [PubMed] [Google Scholar]
  38. Marie V., Dupuy F., Bazin R. Acute injection of beta-adrenoceptor agonist BRL 35135 corrects both impaired uncoupling protein and lipoprotein lipase gene expression but not hypercapacity of lipogenesis in brown adipose tissue of suckling fa/fa rats. Int J Obes Relat Metab Disord. 1994 May;18(5):273–279. [PubMed] [Google Scholar]
  39. Martin-Hidalgo A., Holm C., Belfrage P., Schotz M. C., Herrera E. Lipoprotein lipase and hormone-sensitive lipase activity and mRNA in rat adipose tissue during pregnancy. Am J Physiol. 1994 Jun;266(6 Pt 1):E930–E935. doi: 10.1152/ajpendo.1994.266.6.E930. [DOI] [PubMed] [Google Scholar]
  40. Matsuo T., Suzuki M. Beef tallow diet decreases lipoprotein lipase activities in brown adipose tissue, heart, and soleus muscle by reducing sympathetic activities in rats. J Nutr Sci Vitaminol (Tokyo) 1994 Dec;40(6):569–581. doi: 10.3177/jnsv.40.569. [DOI] [PubMed] [Google Scholar]
  41. Mitchell J. R., Jacobsson A., Kirchgessner T. G., Schotz M. C., Cannon B., Nedergaard J. Regulation of expression of the lipoprotein lipase gene in brown adipose tissue. Am J Physiol. 1992 Sep;263(3 Pt 1):E500–E506. doi: 10.1152/ajpendo.1992.263.3.E500. [DOI] [PubMed] [Google Scholar]
  42. Mohell N., Dicker A. The beta-adrenergic radioligand [3H]CGP-12177, generally classified as an antagonist, is a thermogenic agonist in brown adipose tissue. Biochem J. 1989 Jul 15;261(2):401–405. doi: 10.1042/bj2610401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Mohell N., Nedergaard J. Comparison of the pharmacological profiles of adrenergic drugs (including BRL-agonists) at [3H]prazosin and [3H]CGP-12177 binding sites in brown adipose tissue. Comp Biochem Physiol C. 1989;94(1):229–233. doi: 10.1016/0742-8413(89)90171-0. [DOI] [PubMed] [Google Scholar]
  44. Néchad M., Kuusela P., Carneheim C., Björntorp P., Nedergaard J., Cannon B. Development of brown fat cells in monolayer culture. I. Morphological and biochemical distinction from white fat cells in culture. Exp Cell Res. 1983 Nov;149(1):105–118. doi: 10.1016/0014-4827(83)90384-1. [DOI] [PubMed] [Google Scholar]
  45. Néchad M., Nedergaard J., Cannon B. Noradrenergic stimulation of mitochondriogenesis in brown adipocytes differentiating in culture. Am J Physiol. 1987 Dec;253(6 Pt 1):C889–C894. doi: 10.1152/ajpcell.1987.253.6.C889. [DOI] [PubMed] [Google Scholar]
  46. Obregón M. J., Cannon B., Nedergaard J. Postnatal selective suppression of lipoprotein lipase gene expression in brown adipose tissue (relative to the expression of the gene for the uncoupling protein) is not due to adrenergic insensitivity: a possible specific inhibitory effect of colostrum. Biochem J. 1996 Feb 15;314(Pt 1):261–267. doi: 10.1042/bj3140261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Obregón M. J., Jacobsson A., Kirchgessner T., Schotz M. C., Cannon B., Nedergaard J. Postnatal recruitment of brown adipose tissue is induced by the cold stress experienced by the pups. An analysis of mRNA levels for thermogenin and lipoprotein lipase. Biochem J. 1989 Apr 15;259(2):341–346. doi: 10.1042/bj2590341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Ong J. M., Saffari B., Simsolo R. B., Kern P. A. Epinephrine inhibits lipoprotein lipase gene expression in rat adipocytes through multiple steps in posttranscriptional processing. Mol Endocrinol. 1992 Jan;6(1):61–69. doi: 10.1210/mend.6.1.1738372. [DOI] [PubMed] [Google Scholar]
  49. Ong J. M., Simsolo R. B., Saghizadeh M., Pauer A., Kern P. A. Expression of lipoprotein lipase in rat muscle: regulation by feeding and hypothyroidism. J Lipid Res. 1994 Sep;35(9):1542–1551. [PubMed] [Google Scholar]
  50. Peinado-Onsurbe J., Staels B., Deeb S., Auwerx J. Lipoprotein lipase expression in undifferentiated hepatoma cells is regulated by progesterone and protein kinase A. Biochemistry. 1992 Oct 20;31(41):10121–10128. doi: 10.1021/bi00156a036. [DOI] [PubMed] [Google Scholar]
  51. Picó C., Herron D., Palou A., Jacobsson A., Cannon B., Nedergaard J. Stabilization of the mRNA for the uncoupling protein thermogenin by transcriptional/translational blockade and by noradrenaline in brown adipocytes differentiated in culture: a degradation factor induced by cessation of stimulation? Biochem J. 1994 Aug 15;302(Pt 1):81–86. doi: 10.1042/bj3020081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Pradines-Figueres A., Barcellini-Couget S., Dani C., Baudoin C., Ailhaud G. Inhibition by serum components of the expression of lipoprotein lipase gene upon stimulation by growth hormone. Biochem Biophys Res Commun. 1990 Feb 14;166(3):1118–1125. doi: 10.1016/0006-291x(90)90982-s. [DOI] [PubMed] [Google Scholar]
  53. Puigserver P., Herron D., Gianotti M., Palou A., Cannon B., Nedergaard J. Induction and degradation of the uncoupling protein thermogenin in brown adipocytes in vitro and in vivo. Evidence for a rapidly degradable pool. Biochem J. 1992 Jun 1;284(Pt 2):393–398. doi: 10.1042/bj2840393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Radomski M. W., Orme T. Response of lipoprotein lipase in various tissues to cold exposure. Am J Physiol. 1971 Jun;220(6):1852–1856. doi: 10.1152/ajplegacy.1971.220.6.1852. [DOI] [PubMed] [Google Scholar]
  55. Raynolds M. V., Awald P. D., Gordon D. F., Gutierrez-Hartmann A., Rule D. C., Wood W. M., Eckel R. H. Lipoprotein lipase gene expression in rat adipocytes is regulated by isoproterenol and insulin through different mechanisms. Mol Endocrinol. 1990 Sep;4(9):1416–1422. doi: 10.1210/mend-4-9-1416. [DOI] [PubMed] [Google Scholar]
  56. Rehnmark S., Antonson P., Xanthopoulos K. G., Jacobsson A. Differential adrenergic regulation of C/EBP alpha and C/EBP beta in brown adipose tissue. FEBS Lett. 1993 Mar 8;318(3):235–241. doi: 10.1016/0014-5793(93)80519-z. [DOI] [PubMed] [Google Scholar]
  57. Rehnmark S., Kopecký J., Jacobsson A., Néchad M., Herron D., Nelson B. D., Obregon M. J., Nedergaard J., Cannon B. Brown adipocytes differentiated in vitro can express the gene for the uncoupling protein thermogenin: effects of hypothyroidism and norepinephrine. Exp Cell Res. 1989 May;182(1):75–83. doi: 10.1016/0014-4827(89)90280-2. [DOI] [PubMed] [Google Scholar]
  58. Rehnmark S., Néchad M., Herron D., Cannon B., Nedergaard J. Alpha- and beta-adrenergic induction of the expression of the uncoupling protein thermogenin in brown adipocytes differentiated in culture. J Biol Chem. 1990 Sep 25;265(27):16464–16471. [PubMed] [Google Scholar]
  59. Ross S. R., Choy L., Graves R. A., Fox N., Solevjeva V., Klaus S., Ricquier D., Spiegelman B. M. Hibernoma formation in transgenic mice and isolation of a brown adipocyte cell line expressing the uncoupling protein gene. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7561–7565. doi: 10.1073/pnas.89.16.7561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Senda M., Oka K., Brown W. V., Qasba P. K., Furuichi Y. Molecular cloning and sequence of a cDNA coding for bovine lipoprotein lipase. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4369–4373. doi: 10.1073/pnas.84.13.4369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Shima A., Shinohara Y., Doi K., Terada H. Normal differentiation of rat brown adipocytes in primary culture judged by their expressions of uncoupling protein and the physiological isoform of glucose transporter. Biochim Biophys Acta. 1994 Aug 11;1223(1):1–8. doi: 10.1016/0167-4889(94)90066-3. [DOI] [PubMed] [Google Scholar]
  62. Singh-Bist A., Komaromy M. C., Kraemer F. B. Transcriptional regulation of lipoprotein lipase in the heart during development in the rat. Biochem Biophys Res Commun. 1994 Jul 29;202(2):838–843. doi: 10.1006/bbrc.1994.2006. [DOI] [PubMed] [Google Scholar]
  63. Soteriou A., Cryer A. Distinct immunoreactivities suggest the existence of potential tissue variants in rat lipoprotein lipase. Biochem J. 1994 Apr 15;299(Pt 2):417–423. doi: 10.1042/bj2990417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Thonberg H., Zhang S. J., Tvrdik P., Jacobsson A., Nedergaard J. Norepinephrine utilizes alpha 1- and beta-adrenoreceptors synergistically to maximally induce c-fos expression in brown adipocytes. J Biol Chem. 1994 Dec 30;269(52):33179–33186. [PubMed] [Google Scholar]
  65. Trayhurn P., Duncan J. S., Rayner D. V. Acute cold-induced suppression of ob (obese) gene expression in white adipose tissue of mice: mediation by the sympathetic system. Biochem J. 1995 Nov 1;311(Pt 3):729–733. doi: 10.1042/bj3110729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Wion K. L., Kirchgessner T. G., Lusis A. J., Schotz M. C., Lawn R. M. Human lipoprotein lipase complementary DNA sequence. Science. 1987 Mar 27;235(4796):1638–1641. doi: 10.1126/science.3823907. [DOI] [PubMed] [Google Scholar]
  67. Zhao J., Unelius L., Bengtsson T., Cannon B., Nedergaard J. Coexisting beta-adrenoceptor subtypes: significance for thermogenic process in brown fat cells. Am J Physiol. 1994 Oct;267(4 Pt 1):C969–C979. doi: 10.1152/ajpcell.1994.267.4.C969. [DOI] [PubMed] [Google Scholar]

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

RESOURCES