A complex retinoic acid response element in the uncoupling protein gene defines a novel role for retinoids in thermogenesis

Endocrinology

Volumn 137, Issue 8, 1996, Pages 3488-3496

  Rabelo, Rogerio ^a   Reyes, Carlos ^a   Schifman, Aria ^a   Silva, J Enrique ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RETINOIC ACID; RETINOID; UNCOUPLING PROTEIN;

ARTICLE; BROWN ADIPOSE TISSUE; DNA BINDING; DNA FOOTPRINTING; HORMONE ACTION; NONHUMAN; PRIORITY JOURNAL; RAT; RNA ANALYSIS; SITE DIRECTED MUTAGENESIS; THERMOGENESIS;

EID: 0030014594     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/endo.137.8.8754778     Document Type: Article

References (64)

1. Foster DO, Frydman ML 1978 Brown adipose tissue: the dominant site of nonshivering thermogenesis in the rat. Exper Suppl 32:147-151
2. Himms-Hagen J 1985 Brown adipose tissue metabolism and thermogenesis. Annu Rev Nutr 5:69-94
3. Nicholls DG, Cunningham SA, Rial E 1986 The bioenergetic mechanisms of brown adipose tissue thermogenesis. In: Trayhurn P, Nicholls DG (eds) Brown Adipose Tissue. Edward Arnold, London, pp 52-85
4. Nicholls DG, Locke RM 1984 Thermogenic mechanisms in brown fat. Physiol Rev 64:1-64
5. Cannon B, Nedergaard J 1985 The biochemistry of an inefficient tissue: brown adipose tissue. Essays Biochem 2:110-164
6. Ricquier D, Mory G, Bouillaud F, Thibault J, Weissenbach J 1984 Rapid increase of mitochondrial uncoupling protein and its mRNA in stimulated brown adipose tissue. FEBS Lett 178:240-244
7. Ricquier D, Bouillaud F, Toumelin P, Mory G, Bazin R, Arch J, Penicaud L 1986 Expression of uncoupling protein mRNA in thermogenic or weakly thermogenic brown adipose tissue. J Biol Chem 261:13905-13910
8. Bianco AC, Sheng X, Silva JE 1988 Triiodothyronine amplifies norepinephrine stimulation of uncoupling protein gene transcription by a mechanism not requiring protein synthesis. J Biol Chem 263:18168-18175
9. Rehnmark S, Bianco AC, Kieffer JD, Silva JE 1992 Transcriptional and posttranscriptional mechanisms in the uncoupling protein mRNA response to cold. Am J Physiol 262:E58-E67
10. Silva JE 1988 Full expression of uncoupling protein gene requires the concurrence of norepinephrine and triiodothyronine. Mol Endocrinol 2:706-713
11. Rabelo R, Schifman A, Rubio A, Sheng X, Silva JE 1995 Delineation of thyroid hormone responsive sequences within a critical enhancer in the rat uncoupling protein gene. Endocrinology 136:1003-1013
12. Rabelo R, Reyes C, Schifman A, Silva JE 1995 Role of RXR on the stimulation of the rat uncoupling protein gene by T3. Thyroid 5(Suppl 1):S-141
13. 3). FASEB J 7:A648
14. Cassard-Doulcier A-M, Gelly C, Fox N, Schrementi J, Raimbault S, Klaus S, Forest C, Bouillaud F, Ricquier D 1993 Tissue-specific and β-adrenergic regulation of the mitochondrial uncoupling protein gene: control by cis-acting elements in the 5′-flanking region. Mol Endocrinol 7:497-506
15. Kozak UC, Kopecky J, Teisinger J, Enerbäck S, Boyer BB, Kozak LP 1994 An upstream enhancer regulating brown-fat specific expression of the mitochondrial uncoupling protein gene. Mol Cell Biol 14:59-67
16. Cassard-Doulcier AM, Larose M, Matamala JC, Champigny O, Bouillaud F, Ricquier D 1494 In vitro interactions between nuclear proteins and uncoupling protein gene promoter reveal several putative transactivating factors including Ets1, retinoid X receptor, thyroid hormone receptor, and a CACCC box-binding protein. J Biol Chem 269:24335-24342
17. Yubero P, Manchado C, Cassard-Doulcier A-M, Mampel T, Viñas O, Iglesias R, Giralt M, Villarroya F 1994 CCAAT/enhancer binding proteins α and β are transcriptional activators of the brown fat uncoupling protein gene promoter. Biochem Biophys Res Commun 198:653-659
18. Manchado C, Yubero P, Vinas O, Iglesias R, Villarroya F, Mampel T, Giralt M 1994 CCAAT/enhancer-binding proteins α and β in brown adipose tissue: evidence for a tissue-specific pattern of expression during development. Biochem J 302:695-700
19. Wang ND, Finegold MJ, Bradley A, Ou CN, Abdelsayed SV, Wilde MD, Taylor LR, Wilson DR, Darlington GJ 1995 Impaired energy homeostasis in C/EBP-alpha knockout mice. Science 269:1108-1112
20. Chambon P 1994 The retinoid signaling pathway: molecular and genetic analyses. [Review]. Semin Cell Biol 5:115-125
21. Leid M, Kastner P, Chambon P 1992 Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem Sci 17:427-433
22. Mendelsohn C, Ruberte E, Chambon P 1992 Retinoid receptors in vertebrate limb development. Dev Biol 152:50-61
23. Mangelsdorf DJ, Kliewer SA, Kakizuka A, Umesono K, Evans RM 1993 Retinoid receptors. Recent Prog Horm Res 48:99-121
24. Giguere V 1994 Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocr Rev 15:61-79
25. Allenby G, Janocha R, Kazmer S, Speck J, Grippo JF, Levin AA 1994 Binding of 9-cis-retinoic acid and all-trans-retinoic acid to retinoic acid receptors alpha, beta, and gamma. Retinoic acid receptor gamma binds all-trans-retinoic acid preferentially over 9-cis-retinoic acid. J Biol Chem 269:16689-16695
26. Safonova I, Darimont C, Amri EZ, Grimaldi P, Ailhaud G, Reichert U, Shroot B 1994 Retinoids are positive effectors of adipose cell differentiation. Mol Cell Endocrinol 104:201-211
27. Safonova I, Reichert U, Shroot B, Ailhaud G, Grimaldi P 1994 Fatty acids and retinoids act synergistically on adipose cell differentiation. Biochem Biophys Res Commun 204:498-504
28. Kamei Y, Kawada T, Mizukami J, Sugimoto E 1994 The prevention of adipose differentiation of 3T3-L1 cells caused by retinoic acid is elicited through retinoic acid receptor alpha. Life Sci 55:PL307-312
29. Kamei Y, Kawada T, Fujita A, Etinne J, Noe L, Sugimoto E 1992 Lipoprotein lipase enzyme expression in 3T3-L1 adipocytes is posttranscriptionally down-regulated by retinoic acid. Biochem Int 26:923-934
30. Murray T, Russell TR 1980 Inhibition of adipose conversion in 3T3-L2 cells by retinoic acid. J Supramol Struct 14:255-266
31. Kuri-Harcuch W 1982 Differentiation of 3T3-F442A cells into adipocytes is inhibited by retinoic acid. Differentiation 23:164-169
32. Alvarez R, de Andres J, Yubero P, Vinas O, Mampel T, Iglesias R, Giralt M, Villarroya F 1995 A novel regulatory pathway of brown fat thermogenesis. Retinoic acid is a transcriptional activator of the mitochondrial uncoupling protein gene. J Biol Chem 270:5666-5673
33. Sjogren S, Hammarstrom LE, Larsson A 1977 14C vitamin A in developing rat teeth and bone. A whole body-autoradiographic study. Acta Odontol Scand 35:311-316
34. Hernandez A, Garcia-Jimenez C, Santisteban P, Obregon MJ 1993 Regulation of malic-enzyme-gene expression by cAMP and retinoic acid in differentiating brown adipocytes. Eur J Biochem 215:285-290
35. Tsutsumi C, Okuno M, Tannous L, Piantedosi R, Allan M, Goodman DS, Blaner WS 1992 Retinoids and retinoid-binding protein expression in rat adipocytes. J Biol Chem 267:1805-1810
36. Prost E, Moore DD 1986 CAT vectors for analysis of eukaryotic promoters and enhancers. Gene 45:107-111
37. de The H, Vivanco-Ruiz MM, Tiollais P, Stunnenberg H, Dejean A 1990 Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature 343:177-180
38. Sucov HM, Murakami KK, Evans RM 1990 Characterization of an autoregulated response element in the mouse retinoic acid receptor type beta gene. Proc Natl Acad Sci USA 87:5392-5396
39. Mangelsdorf DJ, Umesono K, Kliewer SA, Borgmeyer U, Ong ES, Evans RM 1991 A direct repeat in the cellular retinol-binding protein type 11 gene confers differential regulation by RXR and RAR. Cell 66:555-561
40. Ross SR, Choy L, Graves RA, Fox N, Solevjeva V, Klaus S, Ricquier D, Spiegelman BM 1992 Hibernoma formation in transgenic mice and isolation of a brown adipocyte cell line expressing the uncoupling protein gene. Proc Natl Acad Sci USA 89:7561-7565
41. Seed B, Sheen JY 1988 A simple phase-extraction assay for chloramphenicol acetyltransferase activity. Gene 67:271-277
42. Heyman RA, Mangelsdorf DJ, Dyck JA, Stein RB, Eichele G, Evans RM, Thaller C 1992 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68:397-406
43. Jetten AM, Grippo JF, Nervi C 1990 Isolation and binding characteristics of nuclear retinoic acid receptors. Methods Enzymol 189:248-255
44. Levin AA, Sturzenbecker LJ, Kazmer S, Bosakowski T, Huselton C, Allenby G, Speck J, Kratzeisen C, Rosenberger M, Lovey A, Grippo JF 1992 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature 355:359-361
45. Gorski K, Carneiro M, Schibler U 1986 Tissue-specific in vitro transcription from the mouse albumin promoter. Cell 47:767-776
46. Bianco AC, Kieffer JD, Silva JE 1992 Adenosine 3′,5′-monophosphate and thyroid hormone control of uncoupling protein messenger ribonucleic acid in freshly dispersed brown adipocytes. Endocrinology 130:2625-2633
47. Hsu JH, Zavacki AM, Harney JW, Brent GA 1995 Retinoid-X receptor (RXR) differentially augments thyroid hormone response in cell lines as a function of the response element and endogenous RXR content. Endocrinology 136:421-430
48. Mangelsdorf DJ, Ong ES, Dyck JA, Evans RM 1990 Nuclear receptor that identifies a novel retinoic acid response pathway. Nature 345:224-229
49. Tontonoz P, Graves RA, Budavari AI, Erdjument-Bromage H, Lui M, Hu E, Tempst P, Spiegelman BM 1994 Adipocyte-specific transcription factor ARF6 is a heterodimeric complex of two nuclear hormone receptors, PPAR gamma and RXR alpha. Nucleic Acids Res 22:5628-5634
50. Kurokawa R, DiRenzo J, Boehm M, Sugarman J, Gloss B, Rosenfeld MG, Heyman RA, Glass CK 1994 Regulation of retinoid signalling by receptor polarity and allosteric control of ligand binding. Nature 371:528-531
51. Barettino D, Bugge TH, Bartunek P, Vivanco Ruiz MD, Sonntag-Buck V, Beug H, Zenke M, Stunnenberg HG 1993 Unliganded T3R, but not its oncogenic variant, v-erbA, suppresses RAR-dependent transactivation by titrating out RXR. EMBO J 12:1343-1354
52. Glass CK 1994 Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Endocr Rev 15:391-407
53. Richard S, Zingg HH 1991 Identification of a retinoic acid response element in the human oxytocin promoter. J Biol Chem 266:21428-21433
54. Vasios GW, Gold JD, Petkovich M, Chambon P, Gudas LJ 1989 A retinoic acid-responsive element is present in the 5′ flanking region of the laminin B1 gene. Proc Natl Acad Sci USA 86:9099-9103
55. Vasios G, Mader S, Gold JD, Leid M, Lutz Y, Gaub MP, Chambon P, Gudas L 1991 The late retinoic acid induction of laminin B1 gene transcription involves RAR binding to the responsive element. EMBO J 10:1149-1158
56. Zhang XK, Hoffman B, Tran PB, Graupner G, Pfahl M 1992 Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature 355:441-446
57. Kliewer SA, Umesono K, Mangelsdorf DJ, Evans RM 1992 Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signaling. Nature 335:446-449
58. Fisher GJ, Talwar HS, Xiao JH, Datta SC, Reddy AP, Gaub MP, Rochette-Egly C, Chambon P, Voorhees JJ 1994 Immunological identification and functional quantitation of retinoic acid and retinoid X receptor proteins in human skin. J Biol Chem 269:20629-20635
59. Motoyama J, Eto K 1994 Antisense retinoic acid receptor gamma-1 oligonucleotide enhances chondrogenesis of mouse limb mesenchymal cells in vitro. FEBS Lett 338:319-322
60. Seleiro EA, Darling D, Brickell PM 1994 The chicken retinoid-X-receptor-gamma gene gives rise to two distinct species of mRNA with different patterns of expression. Biochem J 301:283-288
61. Wan YJ, Wang L, Wu TC 1992 Detection of retinoic acid receptor mRNA in rat tissues by reverse transcriptase-polymerase chain reaction. J Mol Endocrinol 9:291-294
62. Kamei Y, Kawada T, Kazuki R, Sugimoto E 1993 Retinoic acid receptor gamma 2 gene expression is up-regulated by retinoic acid in 3T3-L1 preadipocytes. Biochem J 293:807-812
63. Haq R, Chytil F 1991 Expression of nuclear retinoic acid receptors in rat adipose tissue. Biochem Biophys Res Commun 176:1539-1544
64. Bouillaud F, Weissenbach J, Ricquier D 1988 The gene for rat uncoupling protein: complete sequence, structure of primary transcript and evolutionary relationships between exons. Biochem Biophys Res Commun 157:783-792