The role of the amino-terminal domain in the interaction of unliganded peroxisome proliferator-activated receptor γ-2 with nuclear receptor co-repressor

Journal of Molecular Endocrinology

Volumn 45, Issue 3, 2010, Pages 133-145

  Suzuki, Sadako ^a   Sasaki, Shigekazu ^a   Morita, Hiroshi ^a   Oki, Yutaka ^a   Turiya, Daisuke ^a   Ito, Takeshi ^a   Misawa, Hiroko ^a   Ishizuka, Keiko ^a   Nakamura, Hirotoshi ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; MUTANT PROTEIN; NUCLEAR RECEPTOR COREPRESSOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; THYROID HORMONE RECEPTOR BETA;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; GENE DELETION; GENE SILENCING; IN VITRO STUDY; INSULIN RESISTANCE; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; WILD TYPE;

ANIMALS; CELL LINE; CO-REPRESSOR PROTEINS; GENES, DOMINANT; HUMANS; LIGANDS; MICE; MUTANT PROTEINS; PPAR GAMMA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP; THYROID HORMONE RECEPTORS BETA;

EID: 77957340603     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-10-0007     Document Type: Article

References (72)

1. Adams M, Reginato MJ, Shao D, Lazar MA & Chatterjee VK 1997 Transcriptional activation by peroxisome proliferator-activated receptor gamma is inhibited by phosphorylation at a consensus mitogen-activated protein kinase site. Journal of Biological Chemistry 272 5128-5132. (doi:10.1074/jbc.272.43. 27295)
2. Agostini M, Gurnell M, Savage DB, Wood EM, Smith AG, Rajanayagam O, Garnes KT, Levinson SH, Xu HE, Schwabe JW et al. 2004 Tyrosine agonists reverse the molecular defects associated with dominant-negative mutations in human peroxisome proliferator-activated receptor gamma. Endocrinology 145 1527-1538. (doi:10.1210/en.2003-1271)
3. Armoni M, Kritz N, Harel C, Bar-Yoseph F, Chen H, Quon MJ & Karnieli E 2003 Peroxisome proliferator-activated receptor-gamma represses GLUT4 promoter activity in primary adipocytes, and rosiglitazone alleviates this effect. Journal of Biological Chemistry 278 30614-30623. (doi:10.1074/jbc.M304654200)
4. Barroso I, Gurnell M, Crowley VE, Agostini M, Schwabe JW, Soos MA, Maslen GL, Williams TD, Lewis H, Schafer AJ et al. 1999 Dominant negative mutations in human PPARgamma associated with severe insulin resistance, diabetes mellitus and hypertension. Nature 402 880-883. (doi:10.1038/47254)
5. van Beekum O, Brenkman AB, Grøntved L, Hamers N, van den Broek NJ, Berger R, Mandrup S & Kalkhoven E 2008 The adipogenic acetyltransferase Tip60 targets activation function 1 of peroxisome proliferator-activated receptor gamma. Endocrinology 149 1840-1849. (doi:10.1210/en.2007-0977)
6. Bugge A, Grøntved L, Aagaard MM, Borup R & Mandrup S 2009 The PPARgamma2 A/B-domain plays a gene-specific role in transactivation and cofactor recruitment. Molecular Endocrinology 23 794-808. (doi:10.1210/me.2008-0236)
7. Camp HS & Tafuri SR 1997 Regulation of peroxisome proliferator-activated receptor gamma activity by mitogen-activated protein kinase. Journal of Biological Chemistry 272 10811-10816. (doi:10.1074/jbc.272. 16.10811)
8. Camp HS, Chaudhry A & Leff T 2001 A novel potent antagonist of peroxisome proliferator-activated receptor gamma blocks adipocyte differentiation but does not revert the phenotype of terminally differentiated adipocytes. Endocrinology 142 3207-3213. (doi:10.1210/en.142.7.3207) (Pubitemid 32575558)
9. Chatterjee VK 2001 Resistance to thyroid hormone, and peroxisome-proliferator-activated receptor gamma resistance. Biochemical Society Transactions 29 227-231. (doi:10.1042/BST0290227)
10. Cheng S, Brzostek S, Lee SR, Hollenberg AN & Balk SP 2002 Inhibition of the dihydrotestosterone-activated androgen receptor by nuclear receptor corepressor. Molecular Endocrinology 16 1492-1501. (doi:10.1210/me.16.7.1492)
11. Chui PC, Guan HP, Lehrke M & Lazar MA 2005 PPARgamma regulates adipocyte cholesterol metabolism via oxidized LDL receptor 1. Journal of Clinical Investigation 115 2244-2256. (doi:10.1172/JCI24130)
12. Deeb SS, Fajas L, Nemoto M, Pihlajamaki J, Mykkanen L, Kuusisto J, Laakso M, Fujimoto W & Auwerx J 1998 A Pro12Ala substitution in PPARgamma2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nature Genetics 20 284-287. (doi:10.1038/3099)
13. Desvergne B & Wahli W 1999 Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocrine Reviews 20 649-688. (doi:10.1210/er.20.5.649)
14. DiRenzo J, Soderstrom M, Kurokawa R, Ogliastro MH, Ricote M, Ingrey S, Horlein A, Rosenfeld MG & Glass CK 1997 Peroxisome proliferator-activated receptors and retinoic acid receptors differentially control the interactions of retinoid X receptor heterodimers with ligands, coactivators, and corepressors. Molecular and Cellular Biology 17 2166-2176.
15. Freedman B, Lee E, Park Y & Jameson J 2005 A dominant negative peroxisome proliferator-activated receptor-gamma knock-in mouse exhibits features of the metabolic syndrome. Journal of Biological Chemistry 280 17118-17125. (doi:10.1074/jbc.M407539200) (Pubitemid 41389176)
16. Ge K, Guermah M, Yuan CX, Ito M, Wallberg AE, Spiegelman BM & Roeder RG 2002 Transcription coactivator TRAP220 is required for PPAR gamma 2-stimulated adipogenesis. Nature 417 563-567. (doi:10.1038/417563a)
17. Gelman L, Zhou G, Fajas L, Raspe E, Fruchart JC & Auwerx J 1999 p300 interacts with the N- and C-terminal part of PPARgamma2 in a ligand-independent and -dependent manner, respectively. Journal of Biological Chemistry 274 7681-7688. (doi:10.1074/jbc.274.12.7681)
18. Guan HP, Ishizuka T, Chui PC, Lehrke M & Lazar MA 2005 Corepressors selectively control the transcriptional activity of PPARgamma in adipocytes. Genes and Development 19 453-461. (doi:10.1101/gad.1263305) (Pubitemid 40256277)
19. Gurnell M, Wentworth JM, Agostini M, Adams M, Collingwood TN, Provenzano C, Browne PO, Rajanayagam O, Burris TP, Schwabe JW et al. 2000 A dominant-negative peroxisome proliferator-activated receptor gamma (PPARgamma) mutant is a constitutive repressor and inhibits PPARgamma-mediated adipogenesis. Journal of Biological Chemistry 275 5754-5759. (doi:10.1074/jbc.275.8.5754)
20. Gurnell M, Savage DB, Chatterjee VK & O'Rahilly S 2003 The metabolic syndrome: peroxisome proliferator-activated receptor gamma and its therapeutic modulation. Journal of Clinical Endocrinology and Metabolism 88 2412-2421. (doi:10.1210/jc.2003-030435)
21. He B & Wilson EM 2002 The NH(2)-terminal and carboxylterminal interaction in the human androgen receptor. Molecular Genetics and Metabolism 75 293-298. (doi:10.1016/S1096-7192(02)00009-4) (Pubitemid 34971578)
22. Hollenberg AN, Monden T, Madura JP, Lee K & Wondisford FE 1996 Function of nuclear co-repressor protein on thyroid hormone response elements is regulated by the receptor A/B domain. Journal of Biological Chemistry 271 28516-28520. (doi:10.1074/jbc.271.45.28516)
23. Horlein AJ, Naar AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Soderstrom M, Glass CK et al. 1995 Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377 397-404. (doi:10.1038/377397a0)
24. Hu E, Kim JB, Sarraf P & Spiegelman BM 1996 Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARgamma. Science 274 2100-2103. (doi:10.1126/science.274.5295.2100)
25. Hummasti S & Tontonoz P 2006 The peroxisome proliferator-activated receptor N-terminal domain controls isotype-selective gene expression and adipogenesis. Molecular Endocrinology 20 1261-1275. (doi:10.1210/me.2006-0025) (Pubitemid 43804815)
26. Hunter J, Kassam A, Winrow CJ, Rachubinski RA & Capone JP 1996 Crosstalk between the thyroid hormone and peroxisome proliferator-activated receptors in regulating peroxisome proliferator-responsive genes. Molecular and Cellular Endocrinology 116 213-221. (doi:10.1016/0303-7207(95)03717-9)
27. Juge-Aubry CE, Gorla-Bajszczak A, Pernin A, Lemberger T, Wahli W, Burger AG & Meier CA 1995 Peroxisome proliferator-activated receptor mediates cross-talk with thyroid hormone receptor by competition for retinoid X receptor. Possible role of a leucine zipper-like heptad repeat. Journal of Biological Chemistry 270 18117-18122. (doi:10.1074/jbc.270.30.18117)
28. Juge-Aubry CE, Hammar E, Siegrist-Kaiser C, Pernin A, Takeshita A, Chin WW, Burger AG & Meier CA 1999 Regulation of the transcriptional activity of the peroxisome proliferator-activated receptor alpha by phosphorylation of a ligand-independent trans-activating domain. Journal of Biological Chemistry 274 10505-10510. (doi:10.1074/jbc.274.15.10505)
29. Kallenberger BC, Love JD, Chatterjee VK & Schwabe JW 2003 A dynamic mechanism of nuclear receptor activation and its perturbation in a human disease. Nature Structural Biology 10 136-140. (doi:10.1038/nsb892)
30. Kawai K, Sasaki S, Morita H, Ito T, Suzuki S, Misawa H & Nakamura H 2004 Unliganded thyroid hormone receptor beta1 represses liver X receptor alpha/oxysterol-dependent transactivation. Endocrinology 145 5515-5524. (doi:10.1210/en.2004-0382)
31. Kim JB, Wright HM, Wright M & Spiegelman BM 1998 ADD1/SREBP1 activates PPARgamma through the production of endogenous ligand. PNAS 95 4333-4337. (doi:10.1073/pnas.95.8.4333) (Pubitemid 28207912)
32. Krogsdam AM, Nielsen CA, Neve S, Holst D, Helledie T, Thomsen B, Bendixen C, Mandrup S & Kristiansen K 2002 Nuclear receptor corepressor-dependent repression of peroxisome-proliferator activated receptor delta-mediated transactivation. Biochemical Journal 363 157-165. (doi:10.1042/0264-6021: 3630157)
33. Kumar R & Thompson EB 2003 Transactivation functions of the N-terminal domains of nuclear hormone receptors: protein folding and coactivator interactions. Molecular Endocrinology 17 1-10. (doi:10.1210/me.2002-0258)
34. Kurokawa R, Yu VC, Naar A, Kyakumoto S, Han Z, Silverman S, Rosenfeld MG & Glass CK 1993 Differential orientations of the DNA-binding domain and carboxy-terminal dimerization interface regulate binding site selection by nuclear receptor heterodimers. Genes and Development 7 1423-1435. (doi:10.1101/gad.7.7b.1423)
35. Lee G, Elwood F, McNally J, Weiszmann J, Lindstrom M, Amaral K, Nakamura M, Miao S, Cao P, Learned RM et al. 2002 T0070907, a selective ligand for peroxisome proliferator-activated receptor gamma, functions as an antagonist of biochemical and cellular activities. Journal of Biological Chemistry 277 19649-19657. (doi:10.1074/jbc.M200743200)
36. Liao G, Chen LY, Zhang A, Godavarthy A, Xia F, Ghosh JC, Li H & Chen JD 2003 Regulation of androgen receptor activity by the nuclear receptor corepressor SMRT. Journal of Biological Chemistry 278 5052-5061. (doi:10.1074/jbc.M206374200)
37. Lu C & Cheng SY 2010 Thyroid hormone receptors regulate adipogenesis and carcinogenesis via cross-talk signaling with peroxisome proliferator- activated receptors. Journal of Molecular Endocrinology 44 143-154. (doi:10.1677/JME-09-0107)
38. Madsen L, Petersen RK, Sorensen MB, Jorgensen C, Hallenborg P, Pridal L, Fleckner J, Amri E, Krieg P, Furstenberger G et al. 2003 Adipocyte differentiation of 3T3-L1 preadipocytes is dependent on lipoxygenase activity during the initial stages of the differentiation process. Biochemical Journal 375 539-549. (doi:10.1042/BJ20030503)
39. Marimuthu A, Feng W, Tagami T, Nguyen H, Jameson JL, Fletterick RJ, Baxter JD & West BL 2002 TR surfaces and conformations required to bind nuclear receptor corepressor. Molecular Endocrinology 16 271-286. (doi:10.1210/me.16.2.271)
40. Masugi J, Tamori Y, Mori H, Koike T & Kasuga M 2000 Inhibitory effect of a proline-to-alanine substitution at codon 12 of peroxisome proliferator-activated receptor-gamma 2 on thiazolidinedione-induced adipogenesis. Biochemical and Biophysical Research Communications 268 178-182. (doi:10.1006/bbrc.2000.2096) (Pubitemid 30116630)
41. Metivier R, Petit FG, Valotaire Y & Pakdel F 2000 Function of N-terminal transactivation domain of the estrogen receptor requires a potential alpha-helical structure and is negatively regulated by the A domain. Molecular Endocrinology 14 1849-1871. (doi:10.1210/me.14.11.1849)
42. Metivier R, Penot G, Flouriot G & Pakdel F 2001 Synergism between ERalpha transactivation function 1 (AF-1) and AF-2 mediated by steroid receptor coactivator protein-1: requirement for the AF-1 alpha-helical core and for a direct interaction between the N- and C-terminal domains. Molecular Endocrinology 15 1953-1970. (doi:10.1210/me.15.11.1953)
43. Michalik L, Auwerx J, Berger JP, Chatterjee VK, Glass CK, Gonzalez FJ, Grimaldi PA, Kadowaki T, Lazar MA, O'Rahilly S et al. 2006 International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacological Reviews 58 726-741. (doi:10.1124/pr.58.4.5)
44. Nugent C, Prins JB, Whitehead JP, Savage D, Wentworth JM, Chatterjee VK & O'Rahilly S 2001 Potentiation of glucose uptake in 3T3-L1 adipocytes by PPAR gamma agonists is maintained in cells expressing a PPAR gamma dominant-negative mutant: evidence for selectivity in the downstream responses to PPAR gamma activation. Molecular Endocrinology 15 1729-1738. (doi:10.1210/me.15.10.1729)
45. Ohshima T, Koga H & Shimotohno K 2004 Transcriptional activity of peroxisome proliferator-activated receptor gamma is modulated by SUMO-1 modification. Journal of Biological Chemistry 279 29551-29557. (doi:10.1074/jbc.M403866200) (Pubitemid 38915836)
46. Park Y, Freedman BD, Lee EJ, Park S & Jameson JL 2003 A dominant negative PPARgamma mutant shows altered cofactor recruitment and inhibits adipogenesis in 3T3-L1 cells. Diabetologia 46 365-377. (doi:10.1007/s00125-003- 1177-6)
47. Perissi V & Rosenfeld MG 2005 Controlling nuclear receptors: the circular logic of cofactor cycles. Nature Reviews. Molecular Cell Biology 6 542-554. (doi:10.1038/nrm1680) (Pubitemid 40943045)
48. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Leid M, McBurney MW & Guarente L 2004 Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429 771-776. (doi:10.1038/nature02583)
49. Pippal JB & Fuller PJ 2008 Structure-function relationships in the mineralocorticoid receptor. Journal of Molecular Endocrinology 41 405-413. (doi:10.1677/JME-08-0093)
50. Rangwala SM, Rhoades B, Shapiro JS, Rich AS, Kim JK, Shulman GI, Kaestner KH & Lazar MA 2003 Genetic modulation of PPARgamma phosphorylation regulates insulin sensitivity. Developmental Cell 5 657-663. (doi:10.1016/S1534-5807(03)00274-0)
51. Refetoff S, Weiss RE & Usala SJ 1993 The syndromes of resistance to thyroid hormone. Endocrine Reviews 14 348-399. (doi:10.1210/edrv-14-3-348)
52. Samuels HH, Stanley F & Casanova J 1979 Depletion of L-3,5,3′-triiodothyronine and L-thyroxine in euthyroid calf serum for use in cell culture studies of the action of thyroid hormone. Endocrinology 105 80-85. (doi:10.1210/endo-105-1-80)
53. Sasaki S, Nakamura H, Tagami T, Miyoshi Y & Nakao K 1995 Functional properties of a mutant T3 receptor beta (R338W) identified in a subject with pituitary resistance to thyroid hormone. Molecular and Cellular Endocrinology 113 109-117. (doi:10.1016/0303-7207(95)03621-D)
54. Sasaki S, Lesoon-Wood LA, Dey A, Kuwata T, Weintraub BD, Humphrey G, Yang WM, Seto E, Yen PM, Howard BH et al. 1999 Ligand-induced recruitment of a histone deacetylase in the negative-feedback regulation of the thyrotropin beta gene. EMBO Journal 18 5389-5398. (doi:10.1093/emboj/18.19.5389)
55. Savage DB, Tan GD, Acerini CL, Jebb SA, Agostini M, Gurnell M, Williams RL, Umpleby AM, Thomas EL, Bell JD et al. 2003 Human metabolic syndrome resulting from dominant-negative mutations in the nuclear receptor peroxisome proliferator-activated receptor-gamma. Diabetes 52 910-917. (doi:10.2337/ diabetes.52.4.910)
56. Semple RK, Chatterjee VK & O'Rahilly S 2006 PPARgamma and human metabolic disease. Journal of Clinical Investigation 116 581-589. (doi:10.1172/JCI28003)
57. Shao D, Rangwala SM, Bailey ST, Krakow SL, Reginato MJ & Lazar MA 1998 Interdomain communication regulating ligand binding by PPAR-gamma. Nature 396 377-380. (doi:10.1038/24634) (Pubitemid 28557399)
58. Shi Y, Hon M & Evans RM 2002 The peroxisome proliferator-activated receptor delta, an integrator of transcriptional repression and nuclear receptor signaling. PNAS 99 2613-2618. (doi:10.1073/pnas.052707099)
59. Stanley TB, Leesnitzer LM, Montana VG, Galardi CM, Lambert MH, Holt JA, Xu HE, Moore LB, Blanchard SG & Stimmel JB 2003 Subtype specific effects of peroxisome proliferator-activated receptor ligands on corepressor affinity. Biochemistry 42 9278-9287. (doi:10.1021/bi034472c)
60. Tachibana K, Kobayashi Y, Tanaka T, Tagami M, Sugiyama A, Katayama T, Ueda C, Yamasaki D, Ishimoto K, Sumitomo M et al. 2005 Gene expression profiling of potential peroxisome proliferator-activated receptor (PPAR) target genes in human hepatoblastoma cell lines inducibly expressing different PPAR isoforms. Nuclear Receptor 3 3. (doi:10.1186/1478-1336-3-3)
61. Tzameli I, Fang H, Ollero M, Shi H, Hamm JK, Kievit P, Hollenberg AN & Flier JS 2004 Regulated production of a peroxisome proliferator-activated receptor-gamma ligand during an early phase of adipocyte differentiation in 3T3-L1 adipocytes. Journal of Biological Chemistry 279 36093-36102. (doi:10.1074/jbc.M405346200)
62. Wang LH, Yang XY, Zhang X, Huang J, Hou J, Li J, Xiong H, Mihalic K, Zhu H, Xiao W et al. 2004 Transcriptional inactivation of STAT3 by PPARgamma suppresses IL-6-responsive multiple myeloma cells. Immunity 20 205-218. (doi:10.1016/S1074-7613(04)00030-5)
63. Werman A, Hollenberg A, Solanes G, Bjorbaek C, Vidal-Puig AJ & Flier JS 1997 Ligand-independent activation domain in the N terminus of peroxisome proliferator-activated receptor gamma (PPARgamma). Differential activity of PPARgamma1 and -2 isoforms and influence of insulin. Journal of Biological Chemistry 272 20230-20235. (doi:10.1074/jbc.272.32.20230)
64. Winrow CJ, Kassam A, Miyata KS, Marcus SL, Hunter J, Capone JP & Rachubinski RA 1996 Interplay of the peroxisome proliferator-activated receptor and the thyroid hormone receptorsignaling pathways in regulating peroxisome proliferator-responsive genes. Annals of the New York Academy of Sciences 804 214-230. (doi:10.1111/j.1749-6632.1996.tb18618.x)
65. Xu HE, Stanley TB, Montana VG, Lambert MH, Shearer BG, Cobb JE, McKee DD, Galardi CM, Plunket KD, Nolte RT et al. 2002 Structural basis for antagonist-mediated recruitment of nuclear co-repressors by PPARalpha. Nature 415 813-817. (doi:10.1038/415813a)
66. Yamashita D, Yamaguchi T, Shimizu M, Nakata N, Hirose F & Osumi T 2004 The transactivating function of peroxisome proliferator-activated receptor gamma is negatively regulated by SUMO conjugation in the amino-terminal domain. Genes to Cells 9 1017-1029. (doi:10.1111/j.1365-2443.2004.00786.x) (Pubitemid 39467975)
67. Yang Z, Hong SH & Privalsky ML 1999 Transcriptional antirepression. Thyroid hormone receptor beta-2 recruits SMRT corepressor but interferes with subsequent assembly of a functional corepressor complex. Journal of Biological Chemistry 274 37131-37138. (doi:10.1074/jbc.274.52.37131) (Pubitemid 129513894)
68. Yano M, Matsumura T, Senokuchi T, Ishii N, Murata Y, Taketa K, Motoshima H, Taguchi T, Sonoda K, Kukidome D et al. 2007 Statins activate peroxisome proliferator-activated receptor gamma through extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase-dependent cyclooxygenase-2 expression in macrophages. Circulation Research 100 1442-1451. (doi:10.1161/01.RES.0000268411.49545.9c)
69. Yoh SM, Chatterjee VK & Privalsky ML 1997 Thyroid hormone resistance syndrome manifests as an aberrant interaction between mutant T3 receptors and transcriptional corepressors. Molecular Endocrinology 11 470-480. (doi:10.1210/me.11.4.470)
70. Yu C, Markan K, Temple KA, Deplewski D, Brady MJ & Cohen RN 2005 The nuclear receptor corepressors NCoR and SMRT decrease peroxisome proliferator-activated receptor gamma transcriptional activity and repress 3T3-L1 adipogenesis. Journal of Biological Chemistry 280 13600-13605. (doi:10.1074/jbc.M409468200) (Pubitemid 40517253)
71. Zamir I, Zhang J & Lazar MA 1997 Stoichiometric and steric principles governing repression by nuclear hormone receptors. Genes and Development 11 835-846. (doi:10.1101/gad.11.7.835)
72. Zhang J, Hu X & Lazar MA 1999 A novel role for helix 12 of retinoid X receptor in regulating repression. Molecular and Cellular Biology 19 6448-6457. (Pubitemid 29399348)