Nuclear corepressors mediate the repression of phospholipase A2 group IIa gene transcription by thyroid hormone

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16321-16333

  Sharma, Pragya ^a   Thakran, Shalini ^a   Deng, Xiong ^a,b   Elam, Marshall B ^a,b   Park, Edwards A ^a  

^a UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN IMMUNOPRECIPITATION ASSAY; GENE TRANSCRIPTIONS; INFLAMMATORY RESPONSE; RECRUITMENT MECHANISM; RESPONSE ELEMENTS; RETINOID X RECEPTOR; SECRETORY PHOSPHOLIPASE; THYROID HORMONES;

CLONING; GENES; HORMONES; RATS;

TRANSCRIPTION;

LIOTHYRONINE; LIOTHYRONINE RECEPTOR; RECEPTOR INTERACTING PROTEIN 140; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE REPRESSION; HORMONE ACTION; HUMAN; HUMAN CELL; MALE; MULTICENTER STUDY; NONHUMAN; PHOSPHOLIPASE A2 GROUP 2A GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; RAT; TRANSCRIPTION TERMINATION;

CARNITINE PALMITOYLTRANSFERASE; COREPRESSOR TRANSCRIPTION; LIVER; NUCLEAR RECEPTORS; PHOSPHOLIPASE A; THYROID HORMONE; THYROID HORMONE RECEPTOR; TRANSCRIPTIONAL REGULATION;

ANIMALS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GROUP II PHOSPHOLIPASES A2; HEP G2 CELLS; HEPATOCYTES; HUMANS; LIVER; MALE; RATS; RATS, SPRAGUE-DAWLEY; REPRESSOR PROTEINS; RESPONSE ELEMENTS; RETINOID X RECEPTORS; THYROID HORMONE RECEPTORS BETA; TRANSCRIPTION, GENETIC; TRIIODOTHYRONINE;

RATTUS;

EID: 84878769511     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.445569     Document Type: Article

References (71)

1. 2. Annu. Rev. Biochem. 77, 495-520
2. 2 enzymes. Physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem. Rev. 111, 6130-6185
3. 2 enzymes. Lessons from transgenic and knockout mice. Biochimie 92, 561-582
4. Arsenault, B. J., Boekholdt, S. M., and Kastelein, J. J. (2011) Varespladib. Targeting the inflammatory face of atherosclerosis. Eur. Heart J. 32, 923-926
5. 2 in atherosclerosis. 2. Potential involvement of biologically active oxidized phospholipids. Arterioscler. Thromb. Vasc. Biol. 19, 1291-1298
6. 2 to chemical hypoxic injury in rat hepatocytes. FASEB J. 10, 1319-1325
7. 2 expression in HepG2 cells. Hepatology 41, 896-905
8. 2-IIA levels. PLoS One 7, e41139
9. 2 gene transcription by interleukin-1β. Role of C/EBP factors. J. Biol. Chem. 275, 22686-22694
10. 2 gene expression in human hepatoma cells by mediators of the acute phase response. J. Biol. Chem. 266, 2647-2651
11. 2 promoter in HepG2 cells. Possible role of single-strand binding proteins. Mol. Cell. Biol. 17, 4238-4248
12. 2 gene by cAMP and interleukin-1β in vascular smooth muscle cells. Interplay of the CCAAT/enhancer binding protein (C/EBP), nuclear factor-κ and Ets transcription factors. Biochem. J. 368, 415-424
13. 2 gene transcription involves C/EBP-β and -δ in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 20, 2559-2565
14. Walker, G., Kunz, D., Pignat, W., van den Bosch, H., and Pfeilschifter, J. (1997) Suppression by cyclosporinAof interleukin 1β-induced expression of group II phospholipase A2 in rat renal mesangial cells. Br. J. Pharmacol. 121, 787-793 (Pubitemid 27260785)
15. Ichiki, T. (2010) Thyroid hormone and atherosclerosis. Vascul. Pharmacol. 52, 151-156
16. Kvetny, J., Heldgaard, P. E., Bladbjerg, E. M., and Gram, J. (2004) Subclinical hypothyroidism is associated with a low-grade inflammation, increased triglyceride levels and predicts cardiovascular disease in males below 50 years. Clin. Endocrinol. (Oxf.) 61, 232-238 (Pubitemid 39093119)
17. Crunkhorn, S., and Patti, M. E. (2008) Links between thyroid hormone action, oxidative metabolism, and diabetes risk? Thyroid 18, 227-237 (Pubitemid 351271527)
18. Cappola, A. R., and Ladenson, P. W. (2003) Hypothyroidism and atherosclerosis. J. Clin. Endocrinol. Metab 88, 2438-2444 (Pubitemid 36724408)
19. Yen, P. M. (2001) Physiological and molecular basis of thyroid hormone action. Physiol. Rev. 81, 1097-1142
20. Lazar, M. A. (2003) Thyroid hormone action. A binding contract. J. Clin. Invest. 112, 497-499
21. Cheng, S. Y., Leonard, J. L., and Davis, P. J. (2010) Molecular aspects of thyroid hormone actions. Endocr. Rev. 31, 139-170
22. Flores-Morales, A., Gullberg, H., Fernandez, L., Ståhlberg, N., Lee, N. H., Vennström, B., and Norstedt, G. (2002) Patterns of liver gene expression governed by TRβ. Mol. Endocrinol. 16, 1257-1268 (Pubitemid 34621074)
23. Feng, X., Jiang, Y., Meltzer, P., and Yen, P. M. (2000) Thyroid hormone regulation of hepatic genes in vivo detected by complementary DNA microarray. Mol. Endocrinol. 14, 947-955 (Pubitemid 32250513)
24. Lin, J. Z., Sieglaff, D. H., Yuan, C., Su, J., Arumanayagam, A. S., Firouzbakht, S., Cantu Pompa, J. J., Reynolds, F. D., Zhou, X., Cvoro, A., and Webb, P. (2013) Gene specific actions of thyroid hormone receptor subtypes. PLoS One 8, e52407
25. Weitzel, J. M., Radtke, C., and Seitz, H. J. (2001) Two thyroid hormone-mediated gene expression patterns in vivo identified by cDNA expression arrays in rat. Nucleic Acids Res. 29, 5148-5155 (Pubitemid 34065433)
26. Weitzel, J. M. (2008) To bind or not to bind. How to down-regulate target genes by liganded thyroid hormone receptor? Thyroid Res. 1, 4
27. Santos, G. M., Fairall, L., and Schwabe, J. W. (2011) Negative regulation by nuclear receptors. A plethora of mechanisms. Trends Endocrinol. Metab. 22, 87-93
28. Li, Q. L., Jansen, E., Brent, G. A., and Friedman, T. C. (2001) Regulation of prohormone convertase 1 (PC1) by thyroid hormone. Am. J. Physiol. Endocrinol. Metab. 280, E160-E170
29. Chatterjee, V. K., Lee, J. K., Rentoumis, A., and Jameson, J. L. (1989) Negative regulation of the thyroid-stimulating hormone α gene by thyroid hormone. Receptor interaction adjacent to the TATA box. Proc. Natl. Acad. Sci. U.S.A. 86, 9114-9118 (Pubitemid 20010375)
30. Wondisford, F. E., Farr, E. A., Radovick, S., Steinfelder, H. J., Moates, J. M., McClaskey, J. H., and Weintraub, B. D. (1989) Thyroid hormone inhibition of human thyrotropin β-subunit gene expression is mediated by a cis-acting element located in the first exon. J. Biol. Chem. 264, 14601-14604 (Pubitemid 19237269)
31. Thomas, G., Bertrand, F., and Saunier, B. (2000) The differential regulation of group II(A) and group V low molecular weight phospholipases A2 in cultured rat astrocytes. J. Biol. Chem. 275, 10876-10886 (Pubitemid 30212721)
32. Boone, L. R., Lagor, W. R., Moya Mde, L., Niesen, M. I., Rothblat, G. H., and Ness, G. C. (2011) Thyroid hormone enhances the ability of serum to accept cellular cholesterol via the ABCA1 transporter. Atherosclerosis 218, 77-82
33. Jansen, M. S., Cook, G. A., Song, S., and Park, E. A. (2000) Thyroid hormone regulates carnitine palmitoyltransferase Iα gene expression through elements in the promoter and first intron. J. Biol. Chem. 275, 34989 -34997
34. Attia, R. R., Connnaughton, S., Boone, L. R., Wang, F., Elam, M. B., Ness, G. C., Cook, G. A., and Park, E. A. (2010) Regulation of pyruvate dehydrogenase kinase 4 (PDK4) by thyroid hormone. Role of the peroxisome pro-liferator- activated receptor γ coactivator (PGC-1α). J. Biol. Chem. 285, 2375-2385
35. Zhang, Y., Ma, K., Song, S., Elam, M. B., Cook, G. A., and Park, E. A. (2004) Peroxisomal proliferator-activated receptor-γ coactivator-1α (PGC-1α) enhances the thyroid hormone induction of carnitine palmitoyltransferase I (CPT-Iα). J. Biol. Chem. 279, 53963-53971 (Pubitemid 40053127)
36. Cook, G. A., Edwards, T. L., Jansen, M. S., Bahouth, S. W., Wilcox, H. G., and Park, E. A. (2001) Differential regulation of carnitine palmitoyltrans-ferase-I gene isoforms (CPT-Iα and CPT-Iβ) in the rat heart. J. Mol. Cell Cardiol. 33, 317-329 (Pubitemid 32537930)
37. Attia, R. R., Sharma, P., Janssen, R. C., Friedman, J. E., Deng, X., Lee, J. S., Elam, M. B., Cook, G. A., and Park, E. A. (2011) Regulation of pyruvate dehydrogenase kinase 4 (PDK4) by CCAAT/enhancer-binding protein β (C/EBP β). J. Biol. Chem. 286, 23799-23807
38. Shibusawa, N., Hollenberg, A. N., and Wondisford, F. E. (2003) Thyroid hormone receptor DNA binding is required for both positive and negative gene regulation. J. Biol. Chem. 278, 732-738 (Pubitemid 36790743)
39. Furumoto, H., Ying, H., Chandramouli, G. V., Zhao, L., Walker, R. L., Meltzer, P. S., Willingham, M. C., and Cheng, S. Y. (2005) An unliganded thyroid hormone β receptor activates the cyclin D1/cyclin-dependent kinase/retinoblastoma/E2F pathway and induces pituitary tumorigenesis. Mol. Cell Biol. 25, 124-135 (Pubitemid 40039805)
40. Liu, Y. Y., Nakatani, T., Kogai, T., Mody, K., and Brent, G. A. (2011) Thyroid hormone and COUP-TF1 regulate kallikrein-binding protein (KBP) gene expression. Endocrinology 152, 1143-1153
41. Marimuthu, A., Feng, W., Tagami, T., Nguyen, H., Jameson, J. L., Fletterick, R. J., Baxter, J. D., and West, B. L. (2002) TR surfaces and conformations required to bind nuclear receptor corepressor. Mol. Endocrinol. 16, 271-286 (Pubitemid 34131225)
42. Collingwood, T. N., Wagner, R., Matthews, C. H., Clifton-Bligh, R. J., Gurnell, M., Rajanayagam, O., Agostini, M., Fletterick, R. J., Beck-Peccoz, P., Reinhardt, W., Binder, G., Ranke, M. B., Hermus, A., Hesch, R. D., Lazarus, J., Newrick, P., Parfitt, V., Raggatt, P., de Zegher, F., and Chatterjee, V. K. (1998) A role for helix 3 of the TRβ ligand-binding domain in coactivator recruitment identified by characterization of a third cluster of mutations in resistance to thyroid hormone. EMBO J. 17, 4760-4770 (Pubitemid 28377176)
43. Watson, P. J., Fairall, L., and Schwabe, J. W. (2012) Nuclear hormone receptor co-repressors. Structure and function. Mol. Cell. Endocrinol. 348, 440-449
44. Sadana, P., Hwang, J. Y., Attia, R. R., Arnold, L. A., Neale, G., and Guy, R. K. (2011) Similarities and differences between two modes of antagonism of the thyroid hormone receptor. ACS Chem. Biol. 6, 1096-1106
45. Baxter, J. D., and Webb, P. (2009) Thyroid hormone mimetics. Potential applications in atherosclerosis, obesity and type 2 diabetes. Nat. Rev. Drug Discov. 8, 308-320
46. 2 activity, inflammation markers, and LDL alterations in obesity with or without type 2 diabetes. Obesity 18, 2023-2029
47. 2 revisited. J. Biochem. 150, 233-255
48. 2 in transgenic mice results in epidermal hyperplasia in the absence of inflammatory infiltrate. J. Clin. Invest. 97, 2233-2241
49. 2 activation in cultured mouse hepatocytes exposed to tumor necrosis factor-α. J. Biochem. Toxicol. 9, 181-190
50. Nevalainen, T. J., Kallajoki, M., Pesonen, E., Andersson, S., Kärkkäinen, P., and Höckerstedt, K. (1996) Origin of circulating group II phospholipase A2 in hepatocytes in a patient with epitheloid hemangioendothelioma of the liver. Lab. Invest. 74, 585-591 (Pubitemid 26105719)
51. 2 group IIA modulates adipocyte signaling and protects against diet-induced metabolic syndrome in rats. Diabetes 61, 2320-2329
52. Huggins, K. W., Boileau, A. C., and Hui, D. Y. (2002) Protection against diet-induced obesity and obesity-related insulin resistance in Group 1B PLA2-deficient mice. Am. J. Physiol. Endocrinol. Metab. 283, E994-E1001 (Pubitemid 35216958)
53. 2 inhibitor methyl indoxam suppresses diet-induced obesity and glucose intolerance in mice. Br. J. Pharmacol. 157, 1263-1269
54. Angelin, B., and Rudling, M. (2010) Lipid lowering with thyroid hormone and thyromimetics. Curr. Opin. Lipidol. 21, 499-506
55. Cable, E. E., Finn, P. D., Stebbins, J. W., Hou, J., Ito, B. R., van Poelje, P. D., Linemeyer, D. L., and Erion, M. D. (2009) Reduction of hepatic steatosis in rats and mice after treatment with a liver-targeted thyroid hormone receptor agonist. Hepatology 49, 407-417
56. Fugier, C., Tousaint, J. J., Prieur, X., Plateroti, M., Samarut, J., and Delerive, P. (2006) The lipoprotein lipase inhibitor ANGPTL3 is negatively regulated by thyroid hormone. J. Biol. Chem. 281, 11553-11559 (Pubitemid 43855411)
57. Rhen, T., and Cidlowski, J. A. (2005) Antiinflammatory action of glucocorticoids. New mechanisms for old drugs. N. Engl. J. Med. 353, 1711-1723
58. Santos, G. M., Afonso, V., Barra, G. B., Togashi, M., Webb, P., Neves, F. A., Lomri, N., and Lomri, A. (2006) Negative regulation of superoxide dismu-tase- 1 promoter by thyroid hormone. Mol. Pharmacol. 70, 793-800 (Pubitemid 44268436)
59. Lin, K. H., Shieh, H. Y., and Hsu, H. C. (2000) Negative regulation of the antimetastatic gene Nm23-H1 by thyroid hormone receptors. Endocrinology 141, 2540-2547
60. Kim, S. W., Ho, S. C., Hong, S. J., Kim, K. M., So, E. C., Christoffolete, M., and Harney, J. W. (2005) A novel mechanism of thyroid hormone-dependent negative regulation by thyroid hormone receptor, nuclear receptor corepressor (NCoR), and GAGA-binding factor on the rat cD44 promoter. J. Biol. Chem. 280, 14545-14555 (Pubitemid 40562797)
61. Hashimoto, K., Yamada, M., Matsumoto, S., Monden, T., Satoh, T., and Mori, M. (2006) Mouse sterol response element binding protein-1c gene expression is negatively regulated by thyroid hormone. Endocrinology 147, 4292-4302 (Pubitemid 44268380)
62. Nygård, M., Wahlström, G. M., Gustafsson, M. V., Tokumoto, Y. M., and Bondesson, M. (2003) Hormone-dependent repression of the E2F-1 gene by thyroid hormone receptors. Mol. Endocrinol. 17, 79-92 (Pubitemid 36132660)
63. Nygård, M., Becker, N., Demeneix, B., Pettersson, K., and Bondesson, M. (2006) Thyroid hormone-mediated negative transcriptional regulation of Necdin expression. J. Mol. Endocrinol. 36, 517-530
64. Sasaki, S., Lesoon-Wood, L. A., Dey, A., Kuwata, T., Weintraub, B. D., Humphrey, G., Yang, W. M., Seto, E., Yen, P. M., Howard, B. H., and Ozato, K. (1999) Ligand-induced recruitment of a histone deacetylase in the negative-feedback regulation of the thyrotropin β gene. EMBO J. 18, 5389-5398 (Pubitemid 29465588)
65. Villa, A., Santiago, J., Belandia, B., and Pascual, A. (2004)Aresponse unit in the first exon of the β-amyloid precursor protein gene containing thyroid hormone receptor and Sp1 binding sites mediates negative regulation by 3,5,3′-triiodothyronine. Mol. Endocrinol. 18, 863-873 (Pubitemid 38429478)
66. Berghagen, H., Ragnhildstveit, E., Krogsrud, K., Thuestad, G., Apriletti, J., and Saatcioglu, F. (2002) Corepressor SMRT functions as a coactivator for thyroid hormone receptor T3Rα from a negative hormone response element. J. Biol. Chem. 277, 49517-49522 (Pubitemid 36014389)
67. Ortiga-Carvalho, T. M., Shibusawa, N., Nikrodhanond, A., Oliveira, K. J., Machado, D. S., Liao, X. H., Cohen, R. N., Refetoff, S., and Wondisford, F. E. (2005) Negative regulation by thyroid hormone receptor requires an intact coactivator-binding surface. J. Clin. Invest. 115, 2517-2523 (Pubitemid 41266214)
68. Zhang, J., and Lazar, M. A. (2000) The mechanism of action of thyroid hormones. Annu. Rev. Physiol. 62, 439-466 (Pubitemid 30618270)
69. You, S. H., Liao, X., Weiss, R. E., and Lazar, M. A. (2010) The interaction between nuclear receptor corepressor and histone deacetylase 3 regulates both positive and negative thyroid hormone action in vivo. Mol. Endocrinol. 24, 1359-1367
70. Putcha, B. D., and Fernandez, E. J. (2009) Direct interdomain interactions can mediate allosterism in the thyroid receptor. J. Biol. Chem. 284, 22517-22524
71. Meijsing, S. H., Pufall, M. A., So, A. Y., Bates, D. L., Chen, L., and Yamamoto, K. R. (2009)DNAbinding site sequence directs glucocorticoid receptor structure and activity. Science 324, 407-410