β-transducin repeat-containing protein 1 (β-TrCP1)-mediated silencing mediator of retinoic acid and thyroid hormone receptor (SMRT) protein degradation promotes tumor necrosis factor α (TNFα)-induced inflammatory gene expression

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25375-25386

  Hsu, Kuo Sheng ^a   Kao, Hung Ying ^a  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLAMMATORY GENE EXPRESSIONS; POLYUBIQUITINATION; PROINFLAMMATORY RESPONSE; PROTEIN DEGRADATION; RETINOIC ACIDS; TARGET GENES; THYROID HORMONE RECEPTOR; TUMOR NECROSIS FACTORS;

ENDOTHELIAL CELLS; PROTEOLYSIS;

GENE EXPRESSION;

BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; BETA TRANSDUCIN REPEAT CONTAINING PROTEIN 1; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; IMMUNE RESPONSE GENE; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; UBIQUITINATION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION;

E3 UBIQUITIN LIGASE; SIGNAL TRANSDUCTION; TRANSCRIPTION COREPRESSOR; TRANSCRIPTION REGULATION; TUMOR NECROSIS FACTOR (TNF); UBIQUITINATION;

BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MODELS, BIOLOGICAL; NUCLEAR RECEPTOR CO-REPRESSOR 2; PHOSPHORYLATION; PROTEOLYSIS; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN;

EID: 84883320839     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.473124     Document Type: Article

References (48)

1. Mehra, V. C., Ramgolam, V. S., and Bender, J. R. (2005) Cytokines and cardiovascular disease. J. Leukocyte Biol. 78, 805-818
2. Lawrence, T., Willoughby, D. A., and Gilroy, D. W. (2002) Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2, 787-795
3. Perissi, V., Jepsen, K., Glass, C. K., and Rosenfeld, M. G. (2010) Deconstructing repression. Evolving models of co-repressor action. Nat. Rev. Genet. 11, 109-123
4. Kleinbongard, P., Heusch, G., and Schulz, R. (2010) TNFα in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol. Ther. 127, 295-314
5. Zeuke, S., Ulmer, A. J., Kusumoto, S., Katus, H. A., and Heine, H. (2002) TLR4-mediated inflammatory activation of human coronary artery endothelial cells by LPS. Cardiovasc. Res. 56, 126-134
6. Sadik, C. D., and Luster, A. D. (2012) Lipid-cytokine-chemokine cascades orchestrate leukocyte recruitment in inflammation. J. Leukocyte Biol. 91, 207-215
7. Ghisletti, S., Huang, W., Jepsen, K., Benner, C., Hardiman, G., Rosenfeld, M. G., and Glass, C. K. (2009) Cooperative NCoR-SMRT interactions establish a corepressor-based strategy for integration of inflammatory and anti-inflammatory signaling pathways. Genes Dev. 23, 681-693
8. Barish, G. D., Yu, R. T., Karunasiri, M. S., Becerra, D., Kim, J., Tseng, T. W., Tai, L. J., Leblanc, M., Diehl, C., Cerchietti, L., Miller, Y. I., Witztum, J. L., Melnick, A. M., Dent, A. L., Tangirala, R. K., and Evans, R. M. (2012) The Bcl6-SMRT/NCoR cistrome represses inflammation to attenuate atherosclerosis. Cell Metab. 15, 554-562
9. Barish, G. D., Yu, R. T., Karunasiri, M., Ocampo, C. B., Dixon, J., Benner, C., Dent, A. L., Tangirala, R. K., and Evans, R. M. (2010) Bcl-6 and NF-κB cistromes mediate opposing regulation of the innate immune response. Genes Dev. 24, 2760-2765
10. Toney, L. M., Cattoretti, G., Graf, J. A., Merghoub, T., Pandolfi, P. P., Dalla-Favera, R., Ye, B. H., and Dent, A. L. (2000) BCL-6 regulates chemokine gene transcription in macrophages. Nat. Immunol. 1, 214-220
11. Hoffmann, A., Levchenko, A., Scott, M. L., and Baltimore, D. (2002) The IκB-NF-κB signaling module. Temporal control and selective gene activation. Science 298, 1241-1245
12. Hoffmann, A., Leung, T. H., and Baltimore, D. (2003) Genetic analysis of NF-κB/Rel transcription factors defines functional specificities. EMBO J. 22, 5530-5539
13. Nelson, D. E., Ihekwaba, A. E., Elliott, M., Johnson, J. R., Gibney, C. A., Foreman, B. E., Nelson, G., See, V., Horton, C. A., Spiller, D. G., Edwards, S. W., McDowell, H. P., Unitt, J. F., Sullivan, E., Grimley, R., Benson, N., Broomhead, D., Kell, D. B., and White, M. R. (2004) Oscillations in NF-κB signaling control the dynamics of gene expression. Science 306, 704-708
14. Sung, M. H., Salvatore, L., De Lorenzi, R., Indrawan, A., Pasparakis, M., Hager, G. L., Bianchi, M. E., and Agresti, A. (2009) Sustained oscillations of NF-κB produce distinct genome scanning and gene expression profiles. PLoS ONE 4, e71633
15. Smale, S. T. (2011) Hierarchies of NF-κB target-gene regulation. Nat. Immunol. 12, 689-694
16. Jang, M. K., Goo, Y. H., Sohn, Y. C., Kim, Y. S., Lee, S. K., Kang, H., Cheong, J., and Lee, J. W. (2001) Ca2+/calmodulin-dependent protein kinase IV stimulates nuclear factor-κB transactivation via phosphorylation of the p65 subunit. J. Biol. Chem. 276, 20005-20010
17. Hoberg, J. E., Yeung, F., and Mayo, M. W. (2004) SMRT derepression by the IκB kinase α. A prerequisite to NF-κB transcription and survival. Mol. Cell 16, 245-255
18. Toubal, A., Clément, K., Fan, R., Ancel, P., Pelloux, V., Rouault, C., Veyrie, N., Hartemann, A., Treuter, E., and Venteclef, N. (2013) SMRT-GPS2 corepressor pathway dysregulation coincides with obesity-linked adipocyte inflammation. J. Clin. Invest. 123, 362-379
19. Ann, E. J., Kim, H. Y., Seo, M. S., Mo, J. S., Kim, M. Y., Yoon, J. H., Ahn, J. S., and Park, H. S. (2012) Wnt5a controls Notch1 signaling through CaMKIImediated degradation of the SMRT corepressor protein. J. Biol. Chem. 287, 36814-36829
20. Stanya, K. J., Liu, Y., Means, A. R., and Kao, H. Y. (2008) Cdk2 and Pin1 negatively regulate the transcriptional corepressor SMRT. J. Cell Biol. 183, 49-61
21. Su, Y. T., Gao, C., Liu, Y., Guo, S., Wang, A., Wang, B., Erdjument-Bromage, H., Miyagi, M., Tempst, P., and Kao, H. Y. (2013) Monoubiquitination of filamin B regulates vascular endothelial growth factor-mediated trafficking of histone deacetylase 7. Mol. Cell Biol. 33, 1546-1560
22. Reineke, E. L., Lam, M., Liu, Q., Liu, Y., Stanya, K. J., Chang, K. S., Means, A. R., and Kao, H. Y. (2008) Degradation of the tumor suppressor PML by Pin1 contributes to the cancer phenotype of breast cancer MDA-MB-231 cells. Mol. Cell Biol. 28, 997-1006
23. Cheng, X., and Kao, H. Y. (2009) G protein pathway suppressor 2 (GPS2) is a transcriptional corepressor important for estrogen receptor α-mediated transcriptional regulation. J. Biol. Chem. 284, 36395-36404
24. Cheng, X., and Kao, H. Y. (2012) Microarray analysis revealing common and distinct functions of promyelocytic leukemia protein (PML) and tumor necrosis factor α (TNFα) signaling in endothelial cells. BMC Genomics 13, 453
25. Stanya, K. J., and Kao, H. Y. (2009) New insights into the functions and regulation of the transcriptional corepressors SMRT and N-CoR. Cell Div. 4, 7
26. Spiegelman, V. S., Stavropoulos, P., Latres, E., Pagano, M., Ronai, Z., Slaga, T. J., and Fuchs, S. Y. (2001) Induction of β-transducin repeat-containing protein by JNK signaling and its role in the activation of NF-κB. J. Biol. Chem. 276, 27152-27158
27. Margottin, F., Bour, S. P., Durand, H., Selig, L., Benichou, S., Richard, V., Thomas, D., Strebel, K., and Benarous, R. (1998) A novel human WD protein, h-β TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1, 565-574
28. Frescas, D., and Pagano, M. (2008) Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP. Tipping the scales of cancer. Nat. Rev. Cancer 8, 438-449
29. Wu, G., Xu, G., Schulman, B. A., Jeffrey, P. D., Harper, J. W., and Pavletich, N. P. (2003) Structure of a β-TrCP1-Skp1-β-catenin complex. Destruction motif binding and lysine specificity of the SCF(β-TrCP1) ubiquitin ligase. Mol. Cell 11, 1445-1456
30. Hart, M., Concordet, J. P., Lassot, I., Albert, I., del los Santos, R., Durand, H., Perret, C., Rubinfeld, B., Margottin, F., Benarous, R., and Polakis, P. (1999) The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr. Biol. 9, 207-210
31. Fuchs, S. Y., Spiegelman, V. S., and Kumar, K. G. (2004) The many faces of β-TrCP E3 ubiquitin ligases. Reflections in the magic mirror of cancer. Oncogene 23, 2028-2036
32. Spiegelman, V. S., Tang, W., Chan, A. M., Igarashi, M., Aaronson, S. A., Sassoon, D. A., Katoh, M., Slaga, T. J., and Fuchs, S. Y. (2002) Induction of homologue of Slimb ubiquitin ligase receptor by mitogen signaling. J. Biol. Chem. 277, 36624-36630
33. Jin, J., Shirogane, T., Xu, L., Nalepa, G., Qin, J., Elledge, S. J., and Harper, J. W. (2003) SCFβ-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 17, 3062-3074
34. Rice, N. R., and Ernst, M. K. (1993) In vivo control of NF-κ B activation by IκBα. EMBO J. 12, 4685-4695
35. Yaron, A., Hatzubai, A., Davis, M., Lavon, I., Amit, S., Manning, A. M., Andersen, J. S., Mann, M., Mercurio, F., and Ben-Neriah, Y. (1998) Identification of the receptor component of the IκBα-ubiquitin ligase. Nature 396, 590-594
36. Spencer, E., Jiang, J., and Chen, Z. J. (1999) Signal-induced ubiquitination of IκBα by the F-box protein Slimb/β-TrCP. Genes Dev. 13, 284-294
37. Guardavaccaro, D., Kudo, Y., Boulaire, J., Barchi, M., Busino, L., Donzelli, M., Margottin-Goguet, F., Jackson, P. K., Yamasaki, L., and Pagano, M. (2003) Control of meiotic and mitotic progression by the F box protein β-Trcp1 in vivo. Dev. Cell 4, 799-812
38. Aggarwal, B. B., Gupta, S. C., and Kim, J. H. (2012) Historical perspectives on tumor necrosis factor and its superfamily. 25 years later, a golden journey. Blood 119, 651-665
39. Perissi, V., Aggarwal, A., Glass, C. K., Rose, D. W., and Rosenfeld, M. G. (2004) A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 116, 511-526
40. Shi, Y., Hon, M., and Evans, R. M. (2002) The peroxisome proliferatoractivated receptor δ, an integrator of transcriptional repression and nuclear receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 99, 2613-2618
41. Hu, X., Li, S., Wu, J., Xia, C., and Lala, D. S. (2003) Liver X receptors interact with corepressors to regulate gene expression. Mol. Endocrinol. 17, 1019-1026
42. Greenberg, A. S., and Obin, M. S. (2006) Obesity and the role of adipose tissue in inflammation and metabolism. Am. J. Clin. Nutr. 83, 461S-465S
43. Lumeng, C. N., Bodzin, J. L., and Saltiel, A. R. (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117, 175-184
44. Fernández-Real, J. M., and Pickup, J. C. (2012) Innate immunity, insulin resistance and type 2 diabetes. Diabetologia 55, 273-278
45. Perissi, V., Scafoglio, C., Zhang, J., Ohgi, K. A., Rose, D. W., Glass, C. K., and Rosenfeld, M. G. (2008) TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR-SMRT transcriptional repression checkpoints. Mol. Cell 29, 755-766
46. Hoberg, J. E., Popko, A. E., Ramsey, C. S., and Mayo, M. W. (2006) IκB kinaseα-mediated derepression of SMRT potentiates acetylation of RelA/ p65 by p300. Mol. Cell Biol. 26, 457-471
47. Hong, S. H., and Privalsky, M. L. (2000) The SMRT corepressor is regulated by a MEK-1 kinase pathway. Inhibition of corepressor function is associated withSMRTphosphorylation and nuclear export. Mol. Cell Biol. 20, 6612-6625
48. Winston, J. T., Strack, P., Beer-Romero, P., Chu, C. Y., Elledge, S. J., and Harper, J. W. (1999) The SCFβ-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα andβ-catenin and stimulates IκBα ubiquitination in vitro. Genes Dev. 13, 270-283