Noradrenaline represses PPAR (peroxisome-proliferator-activated receptor) γ2 gene expression in brown adipocytes: Intracellular signalling and effects on PPARγ2 and PPARγ1 protein levels

Biochemical Journal

Volumn 382, Issue 2, 2004, Pages 597-606

  Lindgren, Eva M ^a   Nielsen, Ronni ^b   Petrovic, Natasa ^a   Jacobsson, Anders ^a   Mandrup, Susanne ^b   Cannon, Barbara ^a   Nedergaard, Jan ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Brown adipocyte; cAMP; Cycloheximide; Noradrenaline; Peroxisome proliferator activated receptor 2 (PPAR 2); Protein kinase A

Indexed keywords

ENZYMES; PROBABILITY; RNA; SIGNAL THEORY; SIGNALING; TISSUE;

DIFFERENTIATING CELLS; GENE EXPRESSION; PROLIFERATION;

GENES;

BETA ADRENERGIC RECEPTOR; CYCLIC AMP; CYCLOHEXIMIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NORADRENALIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL PROLIFERATION; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TIME;

ADIPOCYTES; ADIPOSE TISSUE, BROWN; ANIMALS; CELLS, CULTURED; GENE EXPRESSION REGULATION; INTRACELLULAR SPACE; MALE; MICE; MICE, INBRED STRAINS; NOREPINEPHRINE; PPAR GAMMA; RNA, MESSENGER; SIGNAL TRANSDUCTION;

ANIMALIA; EUKARYOTA;

EID: 4644222981     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031622     Document Type: Article

References (49)

1. Kliewer, S. A., Forman, B. M., Blumberg, B., Ong, E. S., Borgmeyer, U., Mangelsdorf, D. J., Umesono, K. and Evans, R. M. (1994) Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc. Natl. Acad. Sci. U.S.A. 91, 7355-7359
2. Tontonoz, P., Hu, E., Graves, R. A., Budavari, A. I. and Spiegelman, B. M. (1994) mPPARγ2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8, 1224-1234
3. 2a Zhu, Y., Qi, C., Korenberg, J. R., Chen, X. N., Noya, D., Rao, M. S. and Reddy, J. K. (1995) Structural organization of mouse peroxisome proliferator-activated receptor γ (mPPARγ) gene: alternative promoter use and different splicing yield two mPPARγ isoforms. Proc. Natl. Acad. Sci. U.S.A. 92, 7921-7925
4. Tontonoz, P., Hu, E. and Spiegelman, B. M. (1994) Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor. Cell 79, 1147-1156
5. Kliewer, S. A., Umesono, K., Noonan, D. J., Heyman, R. A. and Evans, R. M. (1992) Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature (London) 358, 771-774
6. Berger, J. and Moller, D. E. (2002) The mechanisms of action of PPARs. Annu. Rev. Med. 53, 409-435
7. Sears, I. B., MacGinnitie, M. A., Kovacs, L. G. and Graves, R. A. (1996) Differentiation-dependent expression of the brown adipocyte uncoupling protein gene: regulation by peroxisome proliferator-activated receptor γ. Mol. Cell. Biol. 16, 3410-3419
8. Barbera, M. J., Schluter, A., Pedraza, N., Iglesias, R., Villarroya, F. and Giralt, M. (2001) Peroxisome proliferator-activated receptor α activates transcription of the brown fat uncoupling protein-1 gene: a link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J. Biol. Chem. 276, 1486-1493
9. Rosen, E. D. and Spiegelman, B. M. (2001) PPARγ: a nuclear regulator of metabolism, differentiation, and cell growth. J. Biol. Chem. 276, 37731-37734
10. Koeffler, H. P. (2003) Peroxisome proliferator-activated receptor γ and cancers. Clin. Cancer Res. 9, 1-9
11. Nedergaard, J., Herron, D., Jacobsson, A., Rehnmark, S. and Cannon, B. (1995) Norepinephrine as a morphogen?: its unique interaction with brown adipose tissue. Int. J. Dev. Biol. 39, 827-837
12. Rehnmark, S., Néchad, M., Herron, D., Cannon, B. and Nedergaard, J. (1990) α- and β-adrenergic induction of the expression of the uncoupling protein thermogenin in brown adipocytes differentiated in culture. J. Biol. Chem. 265, 16464-16471
13. Hansen, J. B., Petersen, R. K., Larsen, B. M., Bartkova, J., Alsner, J. and Kristiansen, K. (1999) Activation of peroxisome proliferator-activated receptor γ bypasses the function of the retinoblastoma protein in adipocyte differentiation. J. Biol. Chem. 274, 2386-2393
14. Valmaseda, A., Carmona, M. C., Barbera, M. J., Vinas, O., Mampel, T., Iglesias, R., Villarroya, F. and Giralt, M. (1999) Opposite regulation of PPAR-α and -γ gene expression by both their ligands and retinoic acid in brown adipocytes. Mol. Cell. Endocrinol. 154, 101-109
15. 3 switch in control of cAMP during brown adipocyte development explains distinct β-adrenoceptor subtype mediation of proliferation and differentiation. Endocrinology 140, 4185-4197
16. Rehnmark, S., Antonson, P., Xanthopoulos, K. G. and Jacobsson, A. (1993) Differential adrenergic regulation of C/EBPα and C/EBPβ in brown adipose tissue. FEBS Lett. 318, 235-241
17. Rodriguez, E., Ribot, J. and Palou, A. (2002) Trans-10, cis-12, but not cis-9, trans-11 CLA isomer, inhibits brown adipocyte thermogenic capacity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R1789-R1797
18. Fredriksson, J. M., Lindquist, J. M., Bronnikov, G. E. and Nedergaard, J. (2000) Norepinephrine induces vascular endothelial growth factor gene expression in brown adipocytes through a β-adrenoreceptor/cAMP/protein kinase A pathway involving Src but independently of Erk1/2. J. Biol. Chem. 275, 13802-13811
19. Fredriksson, J. M. and Nedergaard, J. (2002) Norepinephrine specifically stimulates ribonucleotide reductase subunit R2 gene expression in proliferating brown adipocytes: mediation via a cAMP/PKA pathway involving src and Erk1/2 kinases. Exp. Cell Res. 274, 207-215
20. Bengtsson, T., Nedergaard, J. and Cannon, B. (2000) Differential regulation of the gene expression of β-adrenoceptor subtypes in brown adipocytes. Biochem. J. 347, 643-651
21. 3-adrenoreceptor gene expression in brown fat cells is transient and recovery is dependent upon a short-lived protein factor. J. Biol. Chem. 271 33366-33375
22. Thuillier, P., Baillie, R., Sha, X. and Clarke, S. D. (1998) Cytosolic and nuclear distribution of PPARγ2 in differentiating 3T3-L1 preadipocytes. J. Lipid Res. 39, 2329-2338
23. Escher, P., Braissant, O., Basu-Modak, S., Michalik, L., Wahli, W. and Desvergne, B. (2001) Rat PPARs: quantitative analysis in adult rat tissues and regulation in fasting and refeeding. Endocrinology 142, 4195-4202
24. Kozak, M. (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234, 187-208
25. Picó, C., Herron, D., Palou, A., Jacobsson, A., Cannon, B. and Nedergaard, J. (1994) 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. 302, 81-86
26. 2+ levels in brown adipocytes. Biochem. Biophys. Res. Commun. 163, 292-300
27. 1-and β-adrenoreceptors synergistically to maximally induce c-fos expression in brown adipocytes. J. Biol. Chem. 269, 33179-33186
28. Barge, R. M., Mills, I., Silva, E. and Larsen, P. R. (1988) Phorbol esters, protein kinase C, and thyroxine 5′-deiodinase in brown adipocytes. Am. J. Physiol. 254, E323-E327
29. Pappone, P. A. and Lee, S. C. (1995) α-Adrenergic stimulation activates a calcium-sensitive chloride current in brown fat cells. J. Gen. Physiol. 106, 231-258
30. Gerhardt, C. C., Gros, J., Strosberg, A. D. and Issad, T. (1999) Stimulation of the extracellular signal-regulated kinase 1/2 pathway by human β-3 adrenergic receptor: new pharmacological profile and mechanism of activation. Mol. Pharmacol. 55, 255-262
31. i-dependent mechanism. J. Biol. Chem. 274, 12017-12022
32. 3- adrenoceptors through a cAMP, PKA and PI3-kinase-dependent pathway stimulating conventional and novel PKCs. Endocrinology 145, 269-280
33. 3-adrenoceptor antagonism by H89. Biochim. Biophys. Acta 1538, 206-217
34. i-mediated in brown adipocytes. J. Biol. Chem. 275, 22670-22677
35. Lindquist, J. M. and Rehnmark, S. (1998) Ambient temperature regulation of apoptosis in brown adipose tissue: Erk 1/2 promotes norepinephrine-dependent cell survival. J. Biol. Chem. 273, 30147-30156
36. Hu, E., Kim, J. B., Sarraf, P. and Spiegelman, B. M. (1996) Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARγ. Science 274, 2100-2103
37. Cao, W., Medvedev, A. V., Daniel, K. W. and Collins, S. (2001) β-Adrenergic activation of p38 MAP kinase in adipocytes: cAMP induction of the uncoupling protein 1 (UCP1) gene requires p38 MAP kinase. J. Biol. Chem. 276, 27077-27082
38. Puigserver, P., Herron, D., Gianotti, M., Palou, A., Cannon, B. and Nedergaard, J. (1992) Induction and degradation of the uncoupling protein thermogenin in brown adipocytes in vitro and in vivo: evidence for a rapidly degradable pool. Biochem. J. 284, 393-398
39. 2 in visceral and subcutaneous adipose tissue of obese women. Diabetes 52, 1673-1676
40. Vidal-Puig, A., Jimenez-Linan, M., Lowell, B. B., Hamann, A., Hu, E., Spiegelman, B., Flier, J. S. and Moller, D. E. (1996) Regulation of PPARγ gene expression by nutrition and obesity in rodents. J. Clin. Invest. 97, 2553-2561
41. Auboeuf, D., Rieusset, J., Fajas, L., Vallier, P., Frering, V., Riou, J. P., Staels, B., Auwerx, J., Laville, M. and Vidal, H. (1997) Tissue distribution and quantification of the expression of mRNAs of peroxisome proliferator-activated receptors and liver X receptor-α in humans: no alteration in adipose tissue of obese and NIDDM patients. Diabetes 46, 1319-1327
42. Guardiola-Diaz, H. M., Rehnmark, S., Usuda, N., Albrektsen, T., Feltkamp, D., Gustafsson, J.-Å, and Alexson, S. E. H. (1999) Rat petoxisome proliferator-activated receptors and brown adipose tissue function during cold acclimatization. J. Biol. Chem. 274, 23368-23377
43. Yu, X. X., Lewin, D. A., Forrest, W. and Adams, S. H. (2002) Cold elicits the simultaneous induction of fatty acid synthesis and β-oxidation in murine brown adipose tissue: prediction from differential gene expression and confirmation in vivo. FASEB J. 16, 155-168
44. 3 receptors. J. Biol. Chem. 267, 2006-2013
45. 1 expression is induced during cyclic adenosine monophosphate-stimulated differentiation of alveolar type II pneumonocytes. Endocrinology 138, 3695-3703
46. Chaudhry, A. and Granneman, J. G. (1999) Differential regulation of functional responses by β-adrenergic receptor subtypes in brown adipocytes. Am. J. Physiol. 277, R147-R153
47. 1-adrenoceptors and protein kinase C activation. Biochem. J. 364, 73-79
48. Reusch, J. E. B., Colton, L. A. and Klemm, D. J. (2000) CREB activation induces adipogenesis in 3T3-L1 cells. Mol. Cell. Biol. 20, 1008-1020
49. Ross, J. (1997) A hypothesis to explain why translation inhibitors stabilize mRNAs in mammalian cells: mRNA stability and mitosis. Bioessays 19, 527-529