XNCoR repression of LXRs restricts macrophage biosynthesis of insulin-sensitizing omega 3 fatty acids

Cell

Volumn 155, Issue 1, 2013, Pages

  Li, Pingping ^a,f   Spann, Nathanael J ^b   Kaikkonen, Minna U ^b,e   Lu, Min ^a   Oh, Da Young ^a   Fox, Jesse N ^b   Bandyopadhyay, Gautam ^a   Talukdar, Saswata ^a   Xu, Jianfeng ^a   Lagakos, William S ^a   Patsouris, David ^a   Armando, Aaron ^b   Quehenberger, Oswald ^a,c   Dennis, Edward A ^c,d   Watkins, Steven M ^f   Auwerx, Johan ^g   Glass, Christopher K ^a,b   Olefsky, Jerrold M ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d San Diego   (United States)

^e UNIVERSITY OF EASTERN FINLAND   (Finland)

^f Lipomics Technologies   (United States)

^g EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B; INSULIN; LIVER X RECEPTOR BETA; NUCLEAR RECEPTOR COREPRESSOR; OMEGA 3 FATTY ACID; PALMITOLEIC ACID; LIVER X RECEPTOR; ORPHAN NUCLEAR RECEPTOR; RECEPTOR INTERACTING PROTEIN 140;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; FATTY ACID METABOLISM; GENE REPRESSION; HISTONE ACETYLATION; MACROPHAGE; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; GENETICS; INSULIN RESISTANCE; KNOCKOUT MOUSE; METABOLISM;

HARNESS; MUS;

ANIMALS; FATTY ACIDS, OMEGA-3; INSULIN RESISTANCE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR RECEPTOR CO-REPRESSOR 1; ORPHAN NUCLEAR RECEPTORS;

EID: 84884821893     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.08.054     Document Type: Article

References (56)

1. G.D. Barish, R.T. Yu, M.S. Karunasiri, D. Becerra, J. Kim, T.W. Tseng, L.J. Tai, M. Leblanc, C. Diehl, and L. Cerchietti The Bcl6-SMRT/NCoR cistrome represses inflammation to attenuate atherosclerosis Cell Metab. 15 2012 554 562
2. M.A. Bouhlel, B. Derudas, E. Rigamonti, R. Dièvart, J. Brozek, S. Haulon, C. Zawadzki, B. Jude, G. Torpier, and N. Marx PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties Cell Metab. 6 2007 137 143
3. H.A. Brown, L.G. Henage, A.M. Preininger, Y. Xiang, and J.H. Exton Biochemical analysis of phospholipase D Methods Enzymol. 434 2007 49 87
4. H. Cao, K. Gerhold, J.R. Mayers, M.M. Wiest, S.M. Watkins, and G.S. Hotamisligil Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism Cell 134 2008 933 944
5. J.D. Chen, and R.M. Evans A transcriptional co-repressor that interacts with nuclear hormone receptors Nature 377 1995 454 457
6. B.E. Clausen, C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster Conditional gene targeting in macrophages and granulocytes using LysMcre mice Transgenic Res. 8 1999 265 277
7. A. Codina, J.D. Love, Y. Li, M.A. Lazar, D. Neuhaus, and J.W. Schwabe Structural insights into the interaction and activation of histone deacetylase 3 by nuclear receptor corepressors Proc. Natl. Acad. Sci. USA 102 2005 6009 6014
8. L. Escoubet-Lozach, C. Benner, M.U. Kaikkonen, J. Lozach, S. Heinz, N.J. Spann, A. Crotti, J. Stender, S. Ghisletti, and D. Reichart Mechanisms establishing TLR4-responsive activation states of inflammatory response genes PLoS Genet. 7 2011 e1002401
9. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226 1957 497 509
10. S. Ghisletti, W. Huang, K. Jepsen, C. Benner, G. Hardiman, M.G. Rosenfeld, and C.K. Glass Cooperative NCoR/SMRT interactions establish a corepressor-based strategy for integration of inflammatory and anti-inflammatory signaling pathways Genes Dev. 23 2009 681 693
11. C.K. Glass, and S. Ogawa Combinatorial roles of nuclear receptors in inflammation and immunity Nat. Rev. Immunol. 6 2006 44 55
12. C.K. Glass, and K. Saijo Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells Nat. Rev. Immunol. 10 2010 365 376
13. S. Haffner, and H. Taegtmeyer Epidemic obesity and the metabolic syndrome Circulation 108 2003 1541 1545
14. D.C. Hargreaves, T. Horng, and R. Medzhitov Control of inducible gene expression by signal-dependent transcriptional elongation Cell 138 2009 129 145
15. H.H. He, C.A. Meyer, H. Shin, S.T. Bailey, G. Wei, Q. Wang, Y. Zhang, K. Xu, M. Ni, and M. Lupien Nucleosome dynamics define transcriptional enhancers Nat. Genet. 42 2010 343 347
16. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
17. A.L. Hevener, J.M. Olefsky, D. Reichart, M.T. Nguyen, G. Bandyopadyhay, H.Y. Leung, M.J. Watt, C. Benner, M.A. Febbraio, and A.K. Nguyen Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones J. Clin. Invest. 117 2007 1658 1669
18. A.J. Hörlein, A.M. Näär, T. Heinzel, J. Torchia, B. Gloss, R. Kurokawa, A. Ryan, Y. Kamei, M. Söderström, and C.K. Glass Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor Nature 377 1995 397 404
19. X. Hu, S. Li, J. Wu, C. Xia, and D.S. Lala Liver X receptors interact with corepressors to regulate gene expression Mol. Endocrinol. 17 2003 1019 1026
20. J. Jager, T. Grémeaux, M. Cormont, Y. Le Marchand-Brustel, and J.F. Tanti Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression Endocrinology 148 2007 241 251
21. U. Kintscher, M. Hartge, K. Hess, A. Foryst-Ludwig, M. Clemenz, M. Wabitsch, P. Fischer-Posovszky, T.F. Barth, D. Dragun, and T. Skurk T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance Arterioscler. Thromb. Vasc. Biol. 28 2008 1304 1310
22. F. Lai, U.A. Orom, M. Cesaroni, M. Beringer, D.J. Taatjes, G.A. Blobel, and R. Shiekhattar Activating RNAs associate with Mediator to enhance chromatin architecture and transcription Nature 494 2013 497 501
23. N. Lanthier, O. Molendi-Coste, Y. Horsmans, N. van Rooijen, P.D. Cani, and I.A. Leclercq Kupffer cell activation is a causal factor for hepatic insulin resistance Am. J. Physiol. Gastrointest. Liver Physiol. 298 2010 G107 G116
24. P. Li, W. Fan, J. Xu, M. Lu, H. Yamamoto, J. Auwerx, D.D. Sears, S. Talukdar, D. Oh, and A. Chen Adipocyte NCoR knockout decreases PPARγ phosphorylation and enhances PPARγ activity and insulin sensitivity Cell 147 2011 815 826
25. R. Medzhitov, and T. Horng Transcriptional control of the inflammatory response Nat. Rev. Immunol. 9 2009 692 703
26. T.A. Mori, and L.J. Beilin Omega-3 fatty acids and inflammation Curr. Atheroscler. Rep. 6 2004 461 467
27. A. Mottis, L. Mouchiroud, and J. Auwerx Emerging roles of the corepressors NCoR1 and SMRT in homeostasis Genes Dev. 27 2013 819 835
28. S.E. Mullican, C.A. Gaddis, T. Alenghat, M.G. Nair, P.R. Giacomin, L.J. Everett, D. Feng, D.J. Steger, J. Schug, D. Artis, and M.A. Lazar Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation Genes Dev. 25 2011 2480 2488
29. H.H. Ng, F. Robert, R.A. Young, and K. Struhl Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity Mol. Cell 11 2003 709 719
30. J.I. Odegaard, R.R. Ricardo-Gonzalez, M.H. Goforth, C.R. Morel, V. Subramanian, L. Mukundan, A. Red Eagle, D. Vats, F. Brombacher, A.W. Ferrante, and A. Chawla Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance Nature 447 2007 1116 1120
31. S. Ogawa, J. Lozach, K. Jepsen, D. Sawka-Verhelle, V. Perissi, R. Sasik, D.W. Rose, R.S. Johnson, M.G. Rosenfeld, and C.K. Glass A nuclear receptor corepressor transcriptional checkpoint controlling activator protein 1-dependent gene networks required for macrophage activation Proc. Natl. Acad. Sci. USA 101 2004 14461 14466
32. D.Y. Oh, S. Talukdar, E.J. Bae, T. Imamura, H. Morinaga, W. Fan, P. Li, W.J. Lu, S.M. Watkins, and J.M. Olefsky GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects Cell 142 2010 687 698
33. J.M. Olefsky, and C.K. Glass Macrophages, inflammation, and insulin resistance Annu. Rev. Physiol. 72 2010 219 246
34. R. Ostuni, V. Piccolo, I. Barozzi, S. Polletti, A. Termanini, S. Bonifacio, A. Curina, E. Prosperini, S. Ghisletti, and G. Natoli Latent enhancers activated by stimulation in differentiated cells Cell 152 2013 157 171
35. G. Pascual, A.L. Fong, S. Ogawa, A. Gamliel, A.C. Li, V. Perissi, D.W. Rose, T.M. Willson, M.G. Rosenfeld, and C.K. Glass A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma Nature 437 2005 759 763
36. G.M. Reaven The insulin resistance syndrome: definition and dietary approaches to treatment Annu. Rev. Nutr. 25 2005 391 406
37. M.G. Rosenfeld, V.V. Lunyak, and C.K. Glass Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response Genes Dev. 20 2006 1405 1428
38. V. Rotter, I. Nagaev, and U. Smith Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects J. Biol. Chem. 278 2003 45777 45784
39. S.E. Shoelson, L. Herrero, and A. Naaz Obesity, inflammation, and insulin resistance Gastroenterology 132 2007 2169 2180
40. N.J. Spann, L.X. Garmire, J.G. McDonald, D.S. Myers, S.B. Milne, N. Shibata, D. Reichart, J.N. Fox, I. Shaked, and D. Heudobler Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses Cell 151 2012 138 152
41. B.L. Wagner, A.F. Valledor, G. Shao, C.L. Daige, E.D. Bischoff, M. Petrowski, K. Jepsen, S.H. Baek, R.A. Heyman, and M.G. Rosenfeld Promoter-specific roles for liver X receptor/corepressor complexes in the regulation of ABCA1 and SREBP1 gene expression Mol. Cell Biol. 23 2003 5780 5789
42. D. Wu, A.B. Molofsky, H.E. Liang, R.R. Ricardo-Gonzalez, H.A. Jouihan, J.K. Bando, A. Chawla, and R.M. Locksley Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis Science 332 2011 243 247
43. H. Xu, G.T. Barnes, Q. Yang, G. Tan, D. Yang, C.J. Chou, J. Sole, A. Nichols, J.S. Ross, L.A. Tartaglia, and H. Chen Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance J. Clin. Invest. 112 2003 1821 1830
44. H. Yamamoto, E.G. Williams, L. Mouchiroud, C. Cantó, W. Fan, M. Downes, C. Héligon, G.D. Barish, B. Desvergne, and R.M. Evans NCoR1 is a conserved physiological modulator of muscle mass and oxidative function Cell 147 2011 827 839
45. Z. Yang, J.H. Yik, R. Chen, N. He, M.K. Jang, K. Ozato, and Q. Zhou Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4 Mol. Cell 19 2005 535 545
46. H. Yang, Y.H. Youm, B. Vandanmagsar, A. Ravussin, J.M. Gimble, F. Greenway, J.M. Stephens, R.L. Mynatt, and V.D. Dixit Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance J. Immunol. 185 2010 1836 1845
47. L.J. Core, J.J. Waterfall, and J.T. Lis Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters Science 322 2008 1845 1848
48. W.T. Garvey, J.M. Olefsky, and S. Marshall Insulin receptor down-regulation is linked to an insulin-induced postreceptor defect in the glucose transport system in rat adipocytes J. Clin. Invest. 76 1985 22 30
49. W. He, Y. Barak, A. Hevener, P. Olson, D. Liao, J. Le, M. Nelson, E. Ong, J.M. Olefsky, and R.M. Evans Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle Proc. Natl. Acad. Sci. USA 100 2003 15712 15717
50. N.T. Ingolia, S. Ghaemmaghami, J.R. Newman, and J.S. Weissman Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling Science 324 2009 218 223
51. P. Li, M. Lu, M.T. Nguyen, E.J. Bae, J. Chapman, D. Feng, M. Hawkins, J.E. Pessin, D.D. Sears, and A.K. Nguyen Functional heterogeneity of CD11c-positive adipose tissue macrophages in diet-induced obese mice J. Biol. Chem. 285 2010 15333 15345
52. M. Lu, P. Li, J. Pferdekamper, W. Fan, M. Saberi, S. Schenk, and J.M. Olefsky Inducible nitric oxide synthase deficiency in myeloid cells does not prevent diet-induced insulin resistance Mol. Endocrinol. 24 2010 1413 1422
53. M.T. Nguyen, H. Satoh, S. Favelyukis, J.L. Babendure, T. Imamura, J.I. Sbodio, J. Zalevsky, B.I. Dahiyat, N.W. Chi, and J.M. Olefsky JNK and tumor necrosis factor-alpha mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes J. Biol. Chem. 280 2005 35361 35371
54. A. Spandidos, X. Wang, H. Wang, and B. Seed PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification Nucleic Acids Res. 38 Database issue 2010 D792 D799
55. R. Steele Influences of glucose loading and of injected insulin on hepatic glucose output Ann. N Y Acad. Sci. 82 1959 420 430
56. D. Wang, I. Garcia-Bassets, C. Benner, W. Li, X. Su, Y. Zhou, J. Qiu, W. Liu, M.U. Kaikkonen, and K.A. Ohgi Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA Nature 474 2011 390 394