Expression of mitochondrial biogenesis-signaling factors in brown adipocytes is influenced specifically by 17β-estradiol, testosterone, and progesterone

American Journal of Physiology - Endocrinology and Metabolism

Volumn 292, Issue 1, 2007, Pages

  Rodriguez Cuenca S ^a,c   Monjo, M ^b   Gianotti, M ^a   Proenza, A M ^a   Roca, P ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b UNIVERSITY OF OSLO   (Norway)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Brown adipose tissue; Mitochondriogenesis program signaling; Nuclear and mitochondrial transcription factors; Sex steroids

Indexed keywords

DNA BINDING PROTEIN; ESTRADIOL; MESSENGER RNA; MITOCHONDRIAL PROTEIN; NUCLEAR FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROGESTERONE; PROTEIN INHIBITOR; PROTEIN KINASE B; PROTEIN TFAM; STEROID HORMONE; TESTOSTERONE; TRANSCRIPTION FACTOR NRF1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; BROWN ADIPOSE TISSUE; CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; FEMALE; GENE EXPRESSION; IN VITRO STUDY; MALE; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENCE; THERMOGENESIS;

ADIPOCYTES, BROWN; ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; FEMALE; GENE EXPRESSION; MALE; MICE; MITOCHONDRIA; PROGESTERONE; RATS; RATS, WISTAR; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; TESTOSTERONE; THERMOGENESIS;

EID: 33845991136     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00175.2006     Document Type: Article

References (47)

1. Barbera MJ, Schluter A, Pedraza N, Iglesias R, Villarroya F, Giralt M. Peroxisome proliferator-activated receptor alpha 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, 2001.
2. Belanger C, Luu-The V, Dupont P, Tchernof A. Adipose tissue intracrinology: potential importance of local androgen/estrogen metabolism in the regulation of adiposity. Horm Metab Res 34: 737-745, 2002.
3. Butow RA, Bahassi EM. Adaptive thermogenesis: orchestrating mitochondrial biogenesis. Curr Biol 9: R767-R769, 1999.
4. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359, 2004.
5. Cannon B, Nedergaard J. Respiratory and thermogenic capacities of cells and mitochondria from brown and white adipose tissue. Methods Mol Biol 155: 295-303, 2001.
6. Chen JQ, Delannoy M, Cooke C, Yager JD. Mitochondrial localization of ERα and ERβ in human MCF7 cells. Am J Physiol Endocrinol Metab 286: E1011-E1022, 2004.
7. Chen JQ, Eshete M, Alworth WL, Yager JD. Binding of MCF-7 cell mitochondrial proteins and recombinant human estrogen receptors alpha and beta to human mitochondrial DNA estrogen response elements. J Cell Biochem 93: 358-373, 2004.
8. Chen JQ, Yager JD. Estrogen's effects on mitochondrial gene expression: mechanisms and potential contributions to estrogen carcinogenesis. Ann NY Acad Sci 1028: 258-272, 2004.
9. Dairaghi DJ, Shadel GS, Clayton DA. Human mitochondrial transcription factor A and promoter spacing integrity are required for transcription initiation. Biochim Biophys Acta 1271: 127-134, 1995.
10. el-Migdadi F, Alfano J, Brownie AC, Gallant S. Cytochrome c oxidase in rat adrenal and liver: effects of anti-androgen treatment and studies in testicular feminized rats. Endocr Res 22: 59-75, 1996.
11. Falkenberg M, Gaspari M, Rantanen A, Trifunovic A, Larsson NG, Gustafsson CM. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat Genet 31: 289-294, 2002.
12. Goffart S, Wiesner RJ. Regulation and co-ordination of nuclear gene expression during mitochondrial biogenesis. Exp Physiol 88: 33-40, 2003.
13. Gomez-Ambrosi J, Fruhbeck G, Aguado M, Milagro FI, Margareto J, Martinez AJ. Divergent effects of an alpha2-adrenergic antagonist on lipolysis and thermogenesis: interactions with a beta3-adrenergic agonist in rats. Int J Mol Med 8: 103-109, 2001.
14. Guzeloglu-Kayisli O, Kayisli UA, Al-Rejjal R, Zheng W, Luleci G, Arici A. Regulation of PTEN (phosphatase and tensin homolog deleted on chromosome 10) expression by estradiol and progesterone in human endometrium. J Clin Endocrinol Metab 88: 5017-5026, 2003.
15. Himms-Hagen J. Brown adipose tissue thermogenesis: role in thermoregulation, energy regulation and obesity. In: Thermoregulation: Physiology and Biochemistry, edited by Schönbaum EaL, P. New York: Pergamon, 1990, p. 327-414.
16. Kelly DP, Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18: 357-368, 2004.
17. Kressler D, Schreiber SN, Knutti D, Kralli A. The PGC-1-related protein PERC is a selective coactivator of estrogen receptor alpha. J Biol Chem 277: 13918-13925, 2002.
18. Kurlawalla-Martinez C, Stiles B, Wang Y, Devaskar SU, Kahn BB, Wu H. Insulin hypersensitivity and resistance to streptozotocin-induced diabetes in mice lacking PTEN in adipose tissue. Mol Cell Biol 25: 2498-2510, 2005.
19. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18: 231-236, 1998.
20. Lee HC, Wei YH. Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int J Biochem Cell Biol 37: 822-834, 2005.
21. Lindgren EM, Nielsen R, Petrovic N, Jacobsson A, Mandrup S, Cannon B, Nedergaard J. Noradrenaline represses PPAR (peroxisome-proliferator- activated receptor) gamma2 gene expression in brown adipocytes: intracellular signalling and effects on PPARgamma2 and PPARgamma1 protein levels. Biochem J 382: 597-606, 2004.
22. Lombardi G, Zarrilli S, Colao A, Paesano L, Di Somma C, Rossi F, De Rosa M. Estrogens and health in males. Mol Cell Endocrinol 178: 51-55, 2001.
23. Matthias A, Ohlson KB, Fredriksson JM, Jacobsson A, Nedergaard J, Cannon B. Thermogenic responses in brown-fat cells are fully UCP1-dependent. UCP2 or UCP3 cannot substitute for UCP1 in adrenergically or fatty-acid induced thermogenesis. J Biol Chem 275: 25073-25081, 2000.
24. Monjo M, Rodriguez AM, Palou A, Roca P. Direct effects of testosterone, 17 beta-estradiol, and progesterone on adrenergic regulation in cultured brown adipocytes: potential mechanism for gender-dependent thermogenesis. Endocrinology 144: 4923-4930, 2003.
25. Mootha VK, Handschin C, Arlow D, Xie X, St Pierre J, Sihag S, Yang W, Altshuler D, Puigserver P, Patterson N, Willy PJ, Schulman IG, Heyman RA, Lander ES, Spiegelman BM. Erralpha and Gabpa/b specify PGC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA 101: 6570-6575, 2004.
26. Nechad M, Kuusela P, Carneheim C, Bjorntorp 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 149: 105-118, 1983.
27. Nedergaard J, Petrovic N, Lindgren EM, Jacobsson A, Cannon B. PPARgamma in the control of brown adipocyte differentiation. Biochim Biophys Acta 1740: 293-304, 2005.
28. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36, 2002.
29. Piantadosi CA, Suliman HB. Mitochondrial transcription factor A induction by redox activation of nuclear respiratory factor 1. J Biol Chem 281: 324-333, 2006.
30. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839, 1998.
31. Quevedo S, Roca P, Pico C, Palou A. Sex-associated differences in cold-induced UCP1 synthesis in rodent brown adipose tissue. Pflügers Arch 436: 689-695, 1998.
32. Ricquier D, Bouillaud F. The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 345: 161-179, 2000.
33. Roca P, Rodriguez AM, Oliver P, Bonet ML, Quevedo S, Pico C, Palou A. Brown adipose tissue response to cafeteria diet-feeding involves induction of the UCP2 gene and is impaired in female rats as compared to males. Pflügers Arch 438: 628-634, 1999.
34. Rodriguez AM, Monjo M, Roca P, Palou A. Opposite actions of testosterone and progesterone on UCP1 mRNA expression in cultured brown adipocytes. Cell Mol Life Sci 59: 1714-1723, 2002.
35. Rodriguez E, Monjo M, Rodriguez-Cuenca S, Pujol E, Amengual B, Roca P, Palou A. Sexual dimorphism in the adrenergic control of rat brown adipose tissue response to overfeeding. Pflügers Arch 442: 396-403, 2001.
36. Rodriguez-Cuenca S, Pujol E, Justo R, Frontera M, Oliver J, Gianotti M, Roca P. Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem 277: 42958-42963., 2002.
37. Scarpulla RC. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14, 2002.
38. Sears IB, MacGinnitie MA, Kovacs LG, Graves RA. Differentiation-dependent expression of the brown adipocyte uncoupling protein gene: regulation by peroxisome proliferator-activated receptor gamma. Mol Cell Biol 16: 3410-3419, 1996.
39. Silva JE. Thermogenic mechanisms and their hormonal regulation. Physiol Rev 86: 435-464, 2006.
40. Staub NL, De Beer M. The role of androgens in female vertebrates. Gen Comp Endocrinol 108: 1-24, 1997.
41. Suliman HB, Carraway MS, Welty-Wolf KE, Whorton AR, Piantadosi CA. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. J Biol Chem 278: 41510-41518, 2003.
42. Tai TA, Jennermann C, Brown KK, Oliver BB, MacGinnitie MA, Wilkison WO, Brown HR, Lehmann JM, Kliewer SA, Morris DC, Graves RA. Activation of the nuclear receptor peroxisome proliferator-activated receptor gamma promotes brown adipocyte differentiation. J Biol Chem 271: 29909-29914, 1996.
43. Uldry M, Yang W, St-Pierre J, Lin J, Seale P, Spiegelman BM. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab 3: 333-341, 2006.
44. Valverde AM, Arribas M, Mur C, Navarro P, Pons S, Cassard-Doulcier AM, Kahn CR, Benito M. Insulin-induced up-regulated uncoupling protein-1 expression is mediated by insulin receptor substrate 1 through the phosphatidylinositol 3-kinase/Akt signaling pathway in fetal brown adipocytes. J Biol Chem 278: 10221-10231, 2003.
45. Van Itallie CM, Dannies PS. Estrogen induces accumulation of the mitochondrial ribonucleic acid for subunit II of cytochrome oxidase in pituitary tumor cells. Mol Endocrinol 2: 332-337, 1988.
46. Vega RB, Huss JM, Kelly DP. The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 20: 1868-1876, 2000.
47. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999.