Distinct stages in adipogenesis revealed by retinoid inhibition of differentiation after induction of PPARγ

Molecular and Cellular Biology

Volumn 16, Issue 4, 1996, Pages 1567-1575

  Xue, Ji Chun ^a   Schwarz, Emily J ^a   Chawla, Ajay ^a   Lazar, Mitchell A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID; RETINOID X RECEPTOR;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN 3T3; CONTROLLED STUDY; GENE EXPRESSION REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN INDUCTION;

EID: 0029919647     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.16.4.1567     Document Type: Article

References (76)

1. Allegretto, E. A., N. Shevde, A. Zou, S. R. Howell, M. F. Boehm, B. W. Hollis, and J. W. Pike. 1995. Retinoid X receptor acts as a hormone receptor in vivo to induce a key metabolic enzyme for 1,25-dihydroxyvitamin D3. J Biol. Chem. 270:23906-23909.
2. Apfel, C., F. Bauer, M. Crettaz, L. Forni, M. Kamber, F. Kaufmann, P. LeMotte, and M. Klaus. 1992 A retinoic receptor α antagonist selectively counteracts retinoic acid effects. Proc. Natl. Acad. Sci. USA 89:7129-7133.
3. Barettino, D., M. D. M. Vivanco-Ruiz, and H. G. Stunnenberg. 1994. Characterization of the ligand-dependent transactivation domain of thyroid hormone receptor. EMBO J. 13:3039-3049.
4. Boylan, J. F., D. Lohnes, R. Taneja, P. Chambon, and L. J. Gudas. 1993. Loss of retinoic acid receptor γ function in F9 cells by gene disruption results in aberrant Hoxa-1 expression and differentiation upon retinoic acid treatment. Proc. Natl. Acad. Sci USA 90:9601-9605.
5. Cao, Z., R. M. Umek, and S. L. McKnight. 1991. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev. 5:1538-1552.
6. Cavailles, V., S. Dauvois, F. L'Horset, G. Lopez, S. Hoare, P. J. Kushner, and M. G. Parker. 1995. Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J. 14:3741-3751.
7. Chawla, A., and M. A. Lazar. 1993. Induction of Rev-ErbAα, an orphan nuclear receptor encoded on the opposite strand of the α-thyroid hormone receptor gene, during adipocyte differentiation. J. Biol. Chem. 268:16265-16269.
8. Chawla, A., and M. A. Lazar. 1994. Peroxisome proliferator and retinoid signalling pathways coregulate preadipocyte phenotype and survival. Proc. Natl. Acad. Sci. USA 91:1786-1790.
9. Chawla, A., E. J. Schwarz, D. D. Dimaculangan, and M. A. Lazar. 1994 Peroxisome proliferator-activated receptor γ (PPARγ): adipose predominant expression and induction early in adipocyte differentiation. Endocrinology 135:798-800.
10. Chen, F., S. W. Law, and B. W. O'Malley. 1993. Identification of two mPPAR related receptors and evidence for the existence of five subfamily members. Biochem. Biophys. Res Commun. 196:671-677.
11. Chen, J. D., and R. M. Evans. 1995. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature (London) 377:454-457.
12. Christy, R. J., K. H. Faestner, D. E. Geiman, and M. D. Lane. 1991. CCAAT/ enhancer binding protein gene promoter: binding of nuclear factors during differentiation of 3T3-L1 preadipocytes. Proc Natl. Acad. Sci. USA 88: 2593-2597.
13. Christy, R. J., V. W. Yang, J. M. Ntambi, D. E. Geiman, W. H. Landschulz, A. D. Friedman, Y. Nakaheppu, T. J. Kelly, and M. D. Lane. 1989. Differentiation-induced gene expression in 3T3-L1 preadipocytes: CCAAT/enhancer binding protein interacts with and activates the promoters of two adipocyte-specific genes. Genes Dev. 3:1323-1335.
14. Davis, K. D., T. J. Berrodin, J. E. Stelmach, J. D. Winkler, and M. A. Lazar. 1994. Endogenous retinoid X receptors can function as hormone receptors in pituitary cells. Mol. Cell. Biol. 14:7105-7110.
15. Dey, A., S. Minucci, and K. Ozato. 1994. Ligand-dependent occupancy of the retinoic acid receptor β2 promoter in vivo Mol Cell. Biol. 14:8191-8201.
16. Distel, R. J., H.-S. Ro, R. S. Rosen, D. L. Groves, and B. M. Spiegelman. 1987. Nucleoprotein complexes that regulate gene expression in adipocyte differentiation: direct participation of c-fos. Cell 49:835-844.
17. Fawell, S. E., J. A. Lees, R. White, and M. G. Parker. 1990. Characterization and colocalization of steroid binding and dimerization activities in the mouse estrogen receptor. Cell 60:953-962.
18. Forman, B. M., P. Tontonoz, J. Chen, R. P. Brun, B. M. Spiegelman, and R. M. Evans. 1995. 15-Deoxy, delta 12,14-prostaglandin J2 is a ligand for the adipocyte determination factor PPARγ. Cell 83:803-812.
19. Forman, B. M., K. Umesono, J. Chen, and R. M. Evans. 1995. Unique response pathways are established by allosteric interactions among nuclear hormone receptors. Cell 81:541-550
20. Freytag, S. O., D. L. Paielli, and J. D. Gilbert. 1994. Ectopic expression of the CCAAT/enhancer binding protein a promotes the adipogenic program in a variety of mouse fibroblastic cells. Genes Dev. 8:165401663.
21. Gearing, K. L., M. Gottlicher, M. Teboul, E. Widmark, and J.-A. Gustafsson. 1993. Interaction of the peroxisome proliferator-activated-receptor and retinoid X receptor. Proc. Natl. Acad. Sci. USA 90:1440-1444.
22. Giguère, V., M. Shago, R. Zirngibl, P. Tate, J. Rossant, and S. Varmuza. 1990. Identification of a novel isoform of the retinoic acid receptor γ expressed in the mouse embryo. Mol Cell Biol. 10:2335-2340.
23. Green, H., and O. Kehinde. 1975. An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5: 19-27.
24. Green, H., and M. Meuth. 1974. An established pre-adipose cell line and its differentiation in culture. Cell 3:127-133.
25. Halachmi, S., E. Marden, G. Martin, H. MacKay, C. Abbondanza, and M. Brown. 1994 Estrogen receptor-associated proteins; possible mediators of hormone-induced transcription. Science 264:1455-1458.
26. Horlein, A. J., A. M. Naar, T. Heinzel, J. Torchia, B. Gloss, R. Kurokawa, A. Rjan, Y. Kamei, M. Soderstrom, C. K. Glass, and M. G. Rosenfeld. 1995. Ligand-independcnt repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature (London) 377:397-104.
27. Hu, E., P. Tontonoz, and B. M. Spiegelman. 1995 Transdifferentiation of myoblasts by the adipogenic transcription factors PPARγ and C/EBPα. Proc. Natl. Acad. Sci USA 92:9856-9860.
28. Imakado, S., J. R. Bickenbach, D. S. Bundman, J. A. Rothnagel, P. S. Attar, X. J. Wang, V. H. Walezak, S. Wisniewski, J. Pote, J. S. Gordon, R. A. Heyman, R. M. Evans, and D. R. Koop. 1995. Targeting expression of a dominant-negative retinoic acid receptor mutant in the epidermis of transgenic mice results in loss of barrier function. Genes Dev 9:317-329
29. Kamei, Y., T. Kawada, R. Kazuki, and E. Sugimoto. 1993. Retinoic acid receptor γ2 gene expression is up-regulated by retinoic acid in 3T3-L1 preadipocytes Biochem J. 293:807-812.
30. Kamei, Y., T. Kawada, J. Mizukami, and E. Sugimoto. 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-PL312
31. Kastner, P., A. Krust, C. Mendelsohn, J. M. Garnier, A. Zelent, P. Leroy, A. Staub, and P. Chambon, 1990. Murine isoforms of retinoic acid receptor γ with specific patterns of expression. Proc Natl. Acad. Sci. USA 87:2700-2704.
32. Katz, D., and M. A. Lazar. 1993. Dominant negative activity of an endogenous thyroid hormone receptor variant (α2) is due to competition for binding sites on target genes. J. Biol. Chem. 268:20904-20910.
33. Keller, H., C. Dreyer, J. Medin, A. Mahfoudi, K. Ozato, and W. Wahli. 1993. Fatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator activated receptor-retinoid X receptor heterodimers. Proc. Natl. Acad. Sci. USA 90:2160-2164.
34. Kletzien, R. F., S. D. Clarke, and R. G. Ulrich. 1992. Enhancement of adipocyte differentiation by an insulin-sensitizing agent. Mol. Pharmacol 41: 393-398.
35. Kliewer, S. A., B. M. Forman, B. Blumberg, E. S. Ong, U. Borgmeyer, D. J. Mangelsdorf, K. Umesono, and R. M. Evans. 1994 Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc. Natl. Acad Sci. USA 91:7355-7359.
36. Kliewer, S. A., J. M. Lenhard, T. M. Willson, I. Patel, D. C. Morris, and J. M. Lehmann. 1995. A prostaglandin 32 metabolite binds peroxisome proliferator-activated receptor γ and promotes adipocyte differentiation. Cell 83: 813-819
37. Kliewer, S. A., K. Umesono, D. J. Noonan, R. A. Heyman, and R. M. Evans. 1992. Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature (London) 358:771-774.
38. Kuri-Harcuch, W. 1982. Differentiation of 3T3-F442A cells into adipocytes is inhibited by retinoic acid. Differentiation 23:164-169.
39. Kurokawa, R., J. DiRenzo, M. Boehm, J. Sugarman, B. Gloss, M. G. Rosengeld, R. A. Heyman, and C. K. Glass. 1994. Regulation of retinoid signalling by receptor polarity and allosteric control of ligand binding. Nature (London) 371:528-531.
40. Kurokawa, R., M. Soderstrom, A. Horlein, S. Halachmi, M. Brown, M. G. Rosenfeld, and C. K. Glass. 1995. Polarity-specific activities of retinoic acid receptors determined by a co-repressor. Nature (London) 377:451-454.
41. Landau, N. R., and D. R. Littman. 1992. Packaging system for rapid production of murine leukemia virus vectors with variable tropism. J. Virol. 66: 5110-5113.
42. LeDouarin, B., C. Zechel, J.-M. Garnier, Y. Lutz, L. Tora, B. Pierrat, D. Heery, H. Gronemeyer, P. Chambon, and R. Losson. 1995. The N-terminal part of TIF1, a putative mediator of the ligand-dependent activation funciton (AF-2) of nuclear receptors, is fused to B-raf in the oncogenic protein TlS EMBO J. 14:2020-2033.
43. Lehmann, J. M., L. Jong, A. Fanjul, J. F. Cameron, X. P. Lu, P. Haefner, M. I. Dawson, and M. Pfahl, 1992 Retinoids selective for retinoid X receptor pathways. Science 258:1944-1946.
44. Lehmann, J. M., L. B. Moore, T. A. Smith-Oliver, W. O. Wilkison, T. M. Willson, and S. A. Kliewer. 1995. An antidiabetic thiazolidinedione is a high affinity ligand for the nuclear peroxisome proliferator-activated receptor γ (PPARγ). J. Biol. Chem. 270:12953-12956.
45. Leid, M., P. Kastner, and P. Chambon. 1992. Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 17:427-433
46. Lepar, G. J., and D. B. Jump. 1992. Retinoic acid and dexamethasone interact to regulate S14 gene transcription in 3T3-F442A adipocytes. Mol Cell. Endocrinol. 84:65-72.
47. Li, E., H. M. Sucov, K. F. Lee, R. M. Evans, and R. Jaenisch. 1993. Normal development and growth of mice carrying a targeted disruption of the alpha 1 retinoic acid receptor gene. Proc. Natl. Acad. Sci. USA 90:1590-1594.
48. Lin, F.-T., and M. D. Lane. 1992. Antisense CCAAT/enhancer-binding protein RNA suppresses coordinate gene expression and triglyceride accumulation during differentiation of 3T3-L1 preadipocytes. Genes Dev. 6:533-544.
49. Lin, F.-T., and M. D. Lane. 1994. CCAAT/enhancer binding protein alpha is sufficient to initiate the 3T3-L1 adipocyte differentiation program Proc. Natl. Acad Sci USA 91:8757-8761
50. Lohnes, D., P. Kastner, A. Dierich, M. Mark, M. LeMeur, and P. Chambon. 1993. Function of retinoic acid receptor gamma m the mouse. Cell 73: 643-658.
51. Mangelsdorf, D. J., K. Umesono, and R. M. Evans. 1994. The retinoid receptors, p 319-349 In M B. Sporn, A. B. Roberts, and D S. Goodman (ed.), The retinoids: biology, chemistry, and medicine, 2nd ed. Raven Press, Ltd., New York
52. Matsui, T., and S. Sashihara. 1995. Tissue-specific distribution of a novel C-terminal truncation retinoic acid receptor mutant which acts as a negative repressor in a promoter- and cell-type-specific manner Mol. Cell. Biol 15: 1961-1967
53. Miller, A. D., and G. J. Rosman. 1989 Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-990.
54. Nagpal, S., M. Saunders, P. Kastner, B. Durand, H. Nakshatri, and P. Chambon. 1992. Promoter context- and response element-dependent specificity of the transcriptional activation and modulating functions of retinoic acid receptors. Cell 70:1007-1019.
55. Perlmann, T., and L. Jansson. 1995. A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and NURR1. Genes Dev. 9:769-782.
56. Ron, D., and J. F. Habener. 1992. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6:439-453.
57. Sadowski, H. B., T. T. Wheeler, and D. A. Young. 1992. Gene expression during 3T3-L1 adipocyte differentiation. J. Biol. Chem. 266:4722-4731.
58. Safonova, I., U. Reichert, B. Shroot, G. Ailhaud, and P. Grimaldi. 1994. Fatty acids and retinoids act synergistically on adipose cell differentiation. Biochem. Biophys. Res. Commun. 204:498-504.
59. Sato, M., A. Hiragun, and H. Mitsui. 1980. Preadipocytes possess cellular retinoid binding proteins and their differentiation is inhibited by retinoids. Biochem. Biophys. Res. Commun. 95:1839-1845.
60. Schwarz, E. J., and M. A. Lazar. Unpublished results.
61. Spiegelman, B. M., M. Frank, and H. Green. 1983. Molecular cloning of mRNA from 3T3 adipocytes. Regulation of mRNA content for glycerophosphate dehydrogenase and other differentiation-dependent proteins during adipocyte development. J. Biol. Chem. 258:10083-10089.
62. Sporn, M. B., and A. B. Roberts. 1983. Role of retinoids in differentiation and carcinogenesis. Cancer Res. 43:3034-3040.
63. Stone, R. L., and D. A. Bernlohr. 1990. The molecular basis of inhibition of adipose conversion of murine 3T3-L1 cells by retinoic acid. Differentiation 45:119-127.
64. Taneja, R., P. Bouillet, J. F. Boylan, M.-P. Gaub, B. Roy, L. J. Gudas, and P. Chambon. 1995. Reexpression of retinoic acid receptor (RAR) γ or overexpression of RARα or RARβ in RARγ-null F9 cells reveals a partial functional redundancy between the three cell types. Proc. Natl. Acad. Sci USA 92:7854-7858.
65. Tontonoz, P., E. Hu, J. Devine, E. G. Beale, and B. M. Spiegelman. 1995. PPARγ2 regulates adipose expression of the phosphoenolpyruvate carboxykinase gene. Mol. Cell Biol. 15:351-357.
66. - tissue-specific regulator of an adipocyte enhancer. Genes Dev 8:1224-1234.
67. Tontonoz, P., E. Hu, and B. M. Spiegelman. 1994. Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor. Cell 79: 1147-1156.
68. Tontonoz, P., J. B. Kim, R. A. Graves, and B. M. Spiegelman. 1993. ADD1: a novel helix-loop-helix transcription factor associated with adipocyte determination and differentiation. Mol Cell. Biol. 13:4753-4759.
69. Umesono, K., K. K. Murakami, C. C. Thompson, and R. M. Evans. 1991. Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell 65:1255-1266.
70. Vasseur-Cognet, M., and M. D. Lane. 1993. Trans-acting factors involved in adipogenic differentiation. Curr. Opin. Genet Dev 3:238-245
71. Willy, P. J., K. Umesono, E. S. Ong, R. M. Evans, R. A. Heyman, and D. J. Mangelsdorf. 1995. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 9:1033-1045.
72. Wu, Z., N. L. R. Bucher, and S. R. Farmer. 1995. Conditional ectopic expression of C/EBPβ in NIH-3T3 cells induces PPARγ and stimulates adipogenesis. Genes Dev. 9:2350-2363.
73. Xue, J.-C., and M. A. Lazar. Unpublished observations.
74. Yeh, W.-C., Z. Cao, M. Classon, and S. L. McKnight. 1995. Cascade regulation of terminal adipocyre differentiation by three members of the C/EBP family of leucine zipper proteins. Genes Dev 9:168-181
75. Yu, K., W. Bayona, C. B. Kallen, H. P. Harding, C. Ravera, J. McMahon, M. Brown, and M. A. Lazar. 1995. Differential activation of peroxisome proliferator-activated receptors by eicosanoids J. Biol. Chem. 270:23975-23983.
76. Zhu, Y., C. Qi, J. R. Korenberg, X.-N. Chen, D. Noya, M. S. Rao, and J. K. Reddy. 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. USA 92:7921-7925