Cholesterol regulation of receptor-interacting protein 140 via microRNA-33 in inflammatory cytokine production

FASEB Journal

Volumn 25, Issue 5, 2011, Pages 1758-1766

  Ho, Ping Chih ^a   Chang, Kun Che ^a   Chuang, Ya Shan ^a   Wei, Li Na ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

3 UTR; High fat diet; NF B; Sepsis; Simvastatin

Indexed keywords

CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MEVALONIC ACID; MICRORNA; MICRORNA 33; RECEPTOR INTERACTING PROTEIN 140; SIMVASTATIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CYTOKINE PRODUCTION; INFLAMMATION; LIPID DIET; MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

3' UNTRANSLATED REGIONS; ANIMALS; ANTICHOLESTEREMIC AGENTS; CELL LINE; CHOLESTEROL; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; INTERLEUKIN-1BETA; MACROPHAGES; MALE; MICE; MICRORNAS; NF-KAPPA B; NUCLEAR RECEPTOR CO-REPRESSOR 1; POLYMERASE CHAIN REACTION; SHOCK, SEPTIC; SIMVASTATIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79955673018     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-179267     Document Type: Article

References (50)

1. Chawla, A. (2010) Control of macrophage activation and function by PPARs. Circ. Res. 106, 1559-1569
2. Maxfield, F. R., and Tabas, I. (2005) Role of cholesterol and lipid organization in disease. Nature 438, 612-621 (Pubitemid 41740565)
3. Chen, G. Y., and Nunez, G. (2010) Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10, 826-837
4. Russell, J. A. (2006) Management of sepsis. N. Engl. J. Med. 355, 1699-1713
5. Vachharajani, V., and Vital, S. (2006) Obesity and sepsis. J. Intens. Care Med. 21, 287-295
6. Rivera, C. A., Gaskin, L., Singer, G., Houghton, J., and Allman, M. (2010) Western diet enhances hepatic inflammation in mice exposed to cecal ligation and puncture. BMC Physiol. 10, 20
7. Hotamisligil, G. S., and Erbay, E. (2008) Nutrient sensing and inflammation in metabolic diseases. Nat. Rev. Immunol. 8, 923-934
8. Naura, A. S., Hans, C. P., Zerfaoui, M., Errami, Y., Ju, J., Kim, H., Matrougui, K., Kim, J. G., and Boulares, A. H. (2009) High-fat diet induces lung remodeling in ApoE-deficient mice: an association with an increase in circulatory and lung inflammatory factors. Lab. Invest. 89, 1243-1251
9. Yvan-Charvet, L., Wang, N., and Tall, A. R. (2010) Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 30, 139-143
10. Yvan-Charvet, L., Welch, C., Pagler, T. A., Ranalletta, M., Lamkanfi, M., Han, S., Ishibashi, M., Li, R., Wang, N., and Tall, A. R. (2008) Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation 118, 1837-1847
11. Schonbeck, U., and Libby, P. (2004) Inflammation, immunity, and HMG-CoA reductase inhibitors: statins as antiinflammatory agents? Circulation 109, II18-26
12. Gao, F., Linhartova, L., Johnston, A. M., and Thickett, D. R. (2008) Statins and sepsis. Br. J. Anaesth. 100, 288-298
13. Gilroy, D. W., Lawrence, T., Perretti, M., and Rossi, A. G. (2004) Inflammatory resolution: new opportunities for drug discovery. Nat. Rev. Drug Discov. 3, 401-416
14. Lefevre, L., Gales, A., Olagnier, D., Bernad, J., Perez, L., Burcelin, R., Valentin, A., Auwerx, J., Pipy, B., and Coste, A. (2010) PPARγ ligands switched high fat diet-induced macrophage M2b polarization toward M2a thereby improving intestinal Candida elimination. PLoS One 5, e12828
15. Strandberg, L., Verdrengh, M., Enge, M., Andersson, N., Amu, S., Onnheim, K., Benrick, A., Brisslert, M., Bylund, J., Bokarewa, M., Nilsson, S., and Jansson, J. O. (2009) Mice chronically fed high-fat diet have increased mortality and disturbed immune response in sepsis. PLoS One 4, e7605
16. White, R., Morganstein, D., Christian, M., Seth, A., Herzog, B., and Parker, M. G. (2008) Role of RIP140 in metabolic tissues: connections to disease. FEBS Lett. 582, 39-45
17. Fritah, A., Christian, M., and Parker, M. G. (2010) The metabolic coregulator RIP140: an update. Am. J. Physiol. Endocrinol. Metab. 299, E335-E340
18. Lee, C. H., Chinpaisal, C., and Wei, L. N. (1998) Cloning and characterization of mouse RIP140, a corepressor for nuclear orphan receptor TR2. Mol. Cell. Biol. 18, 6745-6755
19. Cavailles, V., Dauvois, S., L'Horset, F., Lopez, G., Hoare, S., Kushner, P. J., and Parker, M. G. (1995) Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J. 14, 3741-3751
20. Ho, P. C., Lin, Y. W., Tsui, Y. C., Gupta, P., and Wei, L. N. (2009) A negative regulatory pathway of GLUT4 trafficking in adipocyte: new function of RIP140 in the cytoplasm via AS160. Cell. Metab. 10, 516-523
21. White, R., Leonardsson, G., Rosewell, I., Ann Jacobs, M., Milligan, S., and Parker, M. (2000) The nuclear receptor corepressor nrip1 (RIP140) is essential for female fertility. Nat. Med. 6, 1368-1374
22. Leonardsson, G., Steel, J. H., Christian, M., Pocock, V., Milligan, S., Bell, J., So, P. W., Medina-Gomez, G., Vidal-Puig, A., White, R., and Parker, M. G. (2004) Nuclear receptor corepressor RIP140 regulates fat accumulation. Proc. Natl. Acad. Sci. U. S. A. 101, 8437-8442
23. Christian, M., Kiskinis, E., Debevec, D., Leonardsson, G., White, R., and Parker, M. G. (2005) RIP140-targeted repression of gene expression in adipocytes. Mol. Cell. Biol. 25, 9383-9391
24. Powelka, A. M., Seth, A., Virbasius, J. V., Kiskinis, E., Nicoloro, S. M., Guilherme, A., Tang, X., Straubhaar, J., Cherniack, A. D., Parker, M. G., and Czech, M. P. (2006) Suppression of oxidative metabolism and mitochondrial biogenesis by the transcriptional corepressor RIP140 in mouse adipocytes. J. Clin. Invest. 116, 125-136
25. Mostaqul Huq, M. D., Gupta, P., and Wei, L. N. (2008) Post-translational modifications of nuclear co-repressor RIP140: a therapeutic target for metabolic diseases. Curr. Med. Chem. 15, 386-392
26. Mostaqul Huq, M. D., Gupta, P., Tsai, N. P., White, R., Parker, M. G., and Wei, L. N. (2006) Suppression of receptor interacting protein 140 repressive activity by protein arginine methylation. EMBO J. 25, 5094-5104
27. Gupta, P., Huq, M. D., Khan, S. A., Tsai, N. P., and Wei, L. N. (2005) Regulation of co-repressive activity of and HDAC recruitment to RIP140 by site-specific phosphorylation. Mol. Cell. Proteomics 4, 1776-1784
28. Huq, M. D., Khan, S. A., Park, S. W., and Wei, L. N. (2005) Mapping of phosphorylation sites of nuclear corepressor receptor interacting protein 140 by liquid chromatography-tandem mass spectroscopy. Proteomics 5, 2157-2166
29. Huq, M. D., Ha, S. G., Barcelona, H., and Wei, L. N. (2009) Lysine methylation of nuclear co-repressor receptor interacting protein 140. J. Proteome Res. 8, 1156-1167
30. Huq, M. D., Tsai, N. P., Lin, Y. P., Higgins, L., and Wei, L. N. (2007) Vitamin B6 conjugation to nuclear corepressor RIP140 and its role in gene regulation. Nat. Chem. Biol. 3, 161-165
31. Gupta, P., Ho, P. C., Huq, M. D., Khan, A. A., Tsai, N. P., and Wei, L. N. (2008) PKCepsilon stimulated arginine methylation of RIP140 for its nuclear-cytoplasmic export in adipocyte differentiation. PLoS One 3, e2658
32. Zschiedrich, I., Hardeland, U., Krones-Herzig, A., Berriel Diaz, M., Vegiopoulos, A., Muggenburg, J., Sombroek, D., Hofmann, T. G., Zawatzky, R., Yu, X., Gretz, N., Christian, M., White, R., Parker, M. G., and Herzig, S. (2008) Coactivator function of RIP140 for NFκB/RelA-dependent cytokine gene expression. Blood 112, 264-276
33. O'Connell, R. M., Rao, D. S., Chaudhuri, A. A., and Baltimore, D. (2010) Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111-122
34. O'Connell, R. M., Taganov, K. D., Boldin, M. P., Cheng, G., and Baltimore, D. (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. U. S. A. 104, 1604-1609
35. Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., Fabbri, M., Alder, H., Liu, C. G., Calin, G. A., and Croce, C. M. (2007) Modulation of miR-155 and miR-125b levels following lipopolysaccharide/ TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 179, 5082-5089
36. El Gazzar, M., and McCall, C. E. (2010) MicroRNAs distinguish translational from transcriptional silencing during endotoxin tolerance. J. Biol. Chem. 285, 20940-20951
37. Najafi-Shoushtari, S. H., Kristo, F., Li, Y., Shioda, T., Cohen, D. E., Gerszten, R. E., and Naar, A. M. (2010) MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328, 1566-1569
38. Rayner, K. J., Suarez, Y., Davalos, A., Parathath, S., Fitzgerald, M. L., Tamehiro, N., Fisher, E. A., Moore, K. J., and Fernandez-Hernando, C. (2010) MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328, 1570-1573
39. Horie, T., Ono, K., Horiguchi, M., Nishi, H., Nakamura, T., Nagao, K., Kinoshita, M., Kuwabara, Y., Marusawa, H., Iwanaga, Y., Hasegawa, K., Yokode, M., Kimura, T., and Kita, T. (2010) MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo. Proc. Natl. Acad. Sci. U. S. A. 107, 17321-17326
40. Marquart, T. J., Allen, R. M., Ory, D. S., and Baldan, A. (2010) miR-33 links SREBP-2 induction to repression of sterol transporters. Proc. Natl. Acad. Sci. U. S. A. 107, 12228-12232
41. Gerin, I., Clerbaux, L. A., Haumont, O., Lanthier, N., Das, A. K., Burant, C. F., Leclercq, I. A., MacDougald, O. A., and Bommer, G. T. (2010) Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J. Biol. Chem. 285, 33652-33661
42. Ho, P. C., Gupta, P., Tsui, Y. C., Ha, S. G., Huq, M., and Wei, L. N. (2008) Modulation of lysine acetylation-stimulated repressive activity by Erk2-mediated phosphorylation of RIP140 in adipocyte differentiation. Cell. Signal. 20, 1911-1919
43. Park, S. W., Huq, M. D., Hu, X., and Wei, L. N. (2005) Tyrosine nitration on p65: a novel mechanism to rapidly inactivate nuclear factor-κB. Mol. Cell. Proteomics 4, 300-309
44. Chang, M., Jin, W., and Sun, S. C. (2009) Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nat. Immunol. 10, 1089-1095
45. Tabas, I. (2010) Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10, 36-46
46. Hernandez-Presa, M. A., Ortego, M., Tunon, J., Martin-Ventura, J. L., Mas, S., Blanco-Colio, L. M., Aparicio, C., Ortega, L., Gomez-Gerique, J., Vivanco, F., and Egido, J. (2003) Simvastatin reduces NF-κB activity in peripheral mononuclear and in plaque cells of rabbit atheroma more markedly than lipid lowering diet. Cardiovasc. Res. 57, 168-177
47. Redmond, H. P., Chavin, K. D., Bromberg, J. S., and Daly, J. M. (1991) Inhibition of macrophage-activating cytokines is beneficial in the acute septic response. Ann Surg 214, 502-508; discussion 508-509
48. Tsai, N. P., Lin, Y. L., and Wei, L. N. (2009) MicroRNA mir-346 targets the 5′-untranslated region of receptor-interacting protein 140 (RIP140) mRNA and up-regulates its protein expression. Biochem. J. 424, 411-418
49. Chen, Y., Kerimo, A., Khan, S., and Wei, L. N. (2002) Real-time analysis of molecular interaction of retinoid receptors and receptor-interacting protein 140 (RIP140). Mol. Endocrinol. 16, 2528-2537
50. Chen, Y., Hu, X., and Wei, L. N. (2004) Molecular interaction of retinoic acid receptors with coregulators PCAF and RIP140. Mol. Cell. Endocrinol. 226, 43-50