An LXR-NCOA5 gene regulatory complex directs inflammatory crosstalk-dependent repression of macrophage cholesterol efflux

EMBO Journal

Volumn 34, Issue 9, 2015, Pages 1244-1258

  Gillespie, Mark A ^a   Gold, Elizabeth S ^b   Ramsey, Stephen A ^c   Podolsky, Irina ^b   Aderem, Alan ^b   Ranish, Jeffrey A ^a  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

atherosclerosis; inflammation; LXR; NCOA5; quantitative mass spectrometry

Indexed keywords

ABC TRANSPORTER A1; CELL NUCLEUS RECEPTOR; LIVER X RECEPTOR; NUCLEAR RECEPTOR COFACTOR NCOA5; RNA POLYMERASE II; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; ABCA1 PROTEIN, MOUSE; CHOLESTEROL; NCOA5 PROTEIN, MOUSE; NUCLEAR RECEPTOR COACTIVATOR; ORPHAN NUCLEAR RECEPTOR; TLR3 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE REPRESSION; IN VIVO STUDY; MACROPHAGE; MACROPHAGE CHOLESTEROL EFFLUX; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE STUDY; REGULATOR GENE; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; CHOLESTEROL; FEMALE; GENE EXPRESSION REGULATION; INFLAMMATION; MACROPHAGES; MASS SPECTROMETRY; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR RECEPTOR COACTIVATORS; ORPHAN NUCLEAR RECEPTORS; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 84929028624     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201489819     Document Type: Article

References (84)

1. Ahmad U, Ali R, Lebastchi AH, Qin L, Lo SF, Yakimov AO, Khan SF, Choy JC, Geirsson A, Pober JS, Tellides G, (2010) IFN-gamma primes intact human coronary arteries and cultured coronary smooth muscle cells to double-stranded RNA- and self-RNA-induced inflammatory responses by upregulating TLR3 and melanoma differentiation-associated gene 5. J Immunol 185: 1283-1294
2. Aiello RJ, Brees D, Bourassa PA, Royer L, Lindsey S, Coskran T, Haghpassand M, Francone OL, (2002) Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler Thromb Vasc Biol 22: 630-637
3. Alabert C, Bukowski-Wills JC, Lee SB, Kustatscher G, Nakamura K, de Lima AF, Menard P, Mejlvang J, Rappsilber J, Groth A, (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat Cell Biol 16: 281-293
4. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G, (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29
5. Baiersdorfer M, Schwarz M, Seehafer K, Lehmann C, Heit A, Wagner H, Kirschning CJ, Koch-Brandt C, (2010) Toll-like receptor 3 mediates expression of clusterin/apolipoprotein J in vascular smooth muscle cells stimulated with RNA released from necrotic cells. Exp Cell Res 316: 3489-3500
6. Bento JL, Palmer ND, Zhong M, Roh B, Lewis JP, Wing MR, Pandya H, Freedman BI, Langefeld CD, Rich SS, Bowden DW, Mychaleckyj JC, (2008) Heterogeneity in gene loci associated with type 2 diabetes on human chromosome 20q13.1. Genomics 92: 226-234
7. Bodzioch M, Orso E, Klucken J, Langmann T, Bottcher A, Diederich W, Drobnik W, Barlage S, Buchler C, Porsch-Ozcurumez M, Kaminski WE, Hahmann HW, Oette K, Rothe G, Aslanidis C, Lackner KJ, Schmitz G, (1999) The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 22: 347-351
8. Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, Yu L, Brewer C, Collins JA, Molhuizen HO, Loubser O, Ouelette BF, Fichter K, Ashbourne-Excoffon KJ, Sensen CW, Scherer S, Mott S, Denis M, Martindale D, Frohlich J, et al, (1999) Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 22: 336-345
9. Calkin AC, Tontonoz P, (2012) Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat Rev Mol Cell Biol 13: 213-224
10. Castrillo A, Joseph SB, Vaidya SA, Haberland M, Fogelman AM, Cheng G, Tontonoz P, (2003) Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol Cell 12: 805-816
11. Cavassani KA, Ishii M, Wen H, Schaller MA, Lincoln PM, Lukacs NW, Hogaboam CM, Kunkel SL, (2008) TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med 205: 2609-2621
12. Cole JE, Navin TJ, Cross AJ, Goddard ME, Alexopoulou L, Mitra AT, Davies AH, Flavell RA, Feldmann M, Monaco C, (2011) Unexpected protective role for Toll-like receptor 3 in the arterial wall. Proc Natl Acad Sci USA 108: 2372-2377
13. Costet P, Luo Y, Wang N, Tall AR, (2000) Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J Biol Chem 275: 28240-28245
14. Dejardin J, Kingston RE, (2009) Purification of proteins associated with specific genomic Loci. Cell 136: 175-186
15. Dickins RA, Hemann MT, Zilfou JT, Simpson DR, Ibarra I, Hannon GJ, Lowe SW, (2005) Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat Genet 37: 1289-1295
16. Dignam JD, Lebovitz RM, Roeder RG, (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11: 1475-1489
17. van Eck M, Bos IS, Kaminski WE, Orso E, Rothe G, Twisk J, Bottcher A, Van Amersfoort ES, Christiansen-Weber TA, Fung-Leung WP, Van Berkel TJ, Schmitz G, (2002) Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues. Proc Natl Acad Sci USA 99: 6298-6303
18. Egertson JD, Kuehn A, Merrihew GE, Bateman NW, MacLean BX, Ting YS, Canterbury JD, Marsh DM, Kellmann M, Zabrouskov V, Wu CC, MacCoss MJ, (2013) Multiplexed MS/MS for improved data-independent acquisition. Nat Methods 10: 744-746
19. Foulds CE, Feng Q, Ding C, Bailey S, Hunsaker TL, Malovannaya A, Hamilton RA, Gates LA, Zhang Z, Li C, Chan D, Bajaj A, Callaway CG, Edwards DP, Lonard DM, Tsai SY, Tsai MJ, Qin J, O'Malley BW, (2013) Proteomic analysis of coregulators bound to ERalpha on DNA and nucleosomes reveals coregulator dynamics. Mol Cell 51: 185-199
20. Gao S, Li A, Liu F, Chen F, Williams M, Zhang C, Kelley Z, Wu CL, Luo R, Xiao H, (2013) NCOA5 haploinsufficiency results in glucose intolerance and subsequent hepatocellular carcinoma. Cancer Cell 24: 725-737
21. Ghisletti S, Huang W, Ogawa S, Pascual G, Lin ME, Willson TM, Rosenfeld MG, Glass CK, (2007) Parallel SUMOylation-dependent pathways mediate gene- and signal-specific transrepression by LXRs and PPARgamma. Mol Cell 25: 57-70
22. Gilchrist M, Thorsson V, Li B, Rust AG, Korb M, Roach JC, Kennedy K, Hai T, Bolouri H, Aderem A, (2006) Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441: 173-178
23. Gillet LC, Navarro P, Tate S, Rost H, Selevsek N, Reiter L, Bonner R, Aebersold R, (2012) Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis. Mol Cell Proteomics 11: O111.016717
24. Gold ES, Ramsey SA, Sartain MJ, Selinummi J, Podolsky I, Rodriguez DJ, Moritz RL, Aderem A, (2012) ATF3 protects against atherosclerosis by suppressing 25-hydroxycholesterol-induced lipid body formation. J Exp Med 209: 807-817
25. Huang W, Ghisletti S, Saijo K, Gandhi M, Aouadi M, Tesz GJ, Zhang DX, Yao J, Czech MP, Goode BL, Rosenfeld MG, Glass CK, (2011) Coronin 2A mediates actin-dependent de-repression of inflammatory response genes. Nature 470: 414-418
26. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
27. Huuskonen J, Fielding PE, Fielding CJ, (2004) Role of p160 coactivator complex in the activation of liver X receptor. Arterioscler Thromb Vasc Biol 24: 703-708
28. Huuskonen J, Vishnu M, Fielding PE, Fielding CJ, (2005) Activation of ATP-binding cassette transporter A1 transcription by chromatin remodeling complex. Arterioscler Thromb Vasc Biol 25: 1180-1185
29. Jakobsson T, Venteclef N, Toresson G, Damdimopoulos AE, Ehrlund A, Lou X, Sanyal S, Steffensen KR, Gustafsson JA, Treuter E, (2009) GPS2 is required for cholesterol efflux by triggering histone demethylation, LXR recruitment, and coregulator assembly at the ABCG1 locus. Mol Cell 34: 510-518
30. Jiang C, Ito M, Piening V, Bruck K, Roeder RG, Xiao H, (2004) TIP30 interacts with an estrogen receptor alpha-interacting coactivator CIA and regulates c-myc transcription. J Biol Chem 279: 27781-27789
31. Joseph SB, McKilligin E, Pei L, Watson MA, Collins AR, Laffitte BA, Chen M, Noh G, Goodman J, Hagger GN, Tran J, Tippin TK, Wang X, Lusis AJ, Hsueh WA, Law RE, Collins JL, Willson TM, Tontonoz P, (2002) Synthetic LXR ligand inhibits the development of atherosclerosis in mice. Proc Natl Acad Sci USA 99: 7604-7609
32. Joseph SB, Castrillo A, Laffitte BA, Mangelsdorf DJ, Tontonoz P, (2003) Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat Med 9: 213-219
33. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D, (2004) mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 279: 12542-12550
34. Khera AV, Cuchel M, de la Llera-Moya M, Rodrigues A, Burke MF, Jafri K, French BC, Phillips JA, Mucksavage ML, Wilensky RL, Mohler ER, Rothblat GH, Rader DJ, (2011) Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N Engl J Med 364: 127-135
35. Kim B, Nesvizhskii AI, Rani PG, Hahn S, Aebersold R, Ranish JA, (2007) The transcription elongation factor TFIIS is a component of RNA polymerase II preinitiation complexes. Proc Natl Acad Sci USA 104: 16068-16073
36. Kinsella TM, Nolan GP, (1996) Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 7: 1405-1413
37. Lambert JP, Ivosev G, Couzens AL, Larsen B, Taipale M, Lin ZY, Zhong Q, Lindquist S, Vidal M, Aebersold R, Pawson T, Bonner R, Tate S, Gingras AC, (2013) Mapping differential interactomes by affinity purification coupled with data-independent mass spectrometry acquisition. Nat Methods 10: 1239-1245
38. Lee S, Lee J, Lee SK, Lee JW, (2008) Activating signal cointegrator-2 is an essential adaptor to recruit histone H3 lysine 4 methyltransferases MLL3 and MLL4 to the liver X receptors. Mol Endocrinol 22: 1312-1319
39. Lewis JP, Palmer ND, Ellington JB, Divers J, Ng MC, Lu L, Langefeld CD, Freedman BI, Bowden DW, (2010) Analysis of candidate genes on chromosome 20q12-13.1 reveals evidence for BMI mediated association of PREX1 with type 2 diabetes in European Americans. Genomics 96: 211-219
40. Lundberg AM, Ketelhuth DF, Johansson ME, Gerdes N, Liu S, Yamamoto M, Akira S, Hansson GK, (2013) Toll-like receptor 3 and 4 signalling through the TRIF and TRAM adaptors in haematopoietic cells promotes atherosclerosis. Cardiovasc Res 99: 364-373
41. Michelsen KS, Wong MH, Shah PK, Zhang W, Yano J, Doherty TM, Akira S, Rajavashisth TB, Arditi M, (2004) Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc Natl Acad Sci USA 101: 10679-10684
42. Mirzaei H, Knijnenburg TA, Kim B, Robinson M, Picotti P, Carter GW, Li S, Dilworth DJ, Eng JK, Aitchison JD, Shmulevich I, Galitski T, Aebersold R, Ranish J, (2013) Systematic measurement of transcription factor-DNA interactions by targeted mass spectrometry identifies candidate gene regulatory proteins. Proc Natl Acad Sci USA 110: 3645-3650
43. Mittler G, Butter F, Mann M, (2009) A SILAC-based DNA protein interaction screen that identifies candidate binding proteins to functional DNA elements. Genome Res 19: 284-293
44. Monaco C, Gregan SM, Navin TJ, Foxwell BM, Davies AH, Feldmann M, (2009) Toll-like receptor-2 mediates inflammation and matrix degradation in human atherosclerosis. Circulation 120: 2462-2469
45. Moore KJ, Sheedy FJ, Fisher EA, (2013) Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol 13: 709-721
46. Mostafavi S, Ray D, Warde-Farley D, Grouios C, Morris Q, (2008) GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function. Genome Biol 9 (Suppl 1): S4
47. Mullick AE, Tobias PS, Curtiss LK, (2005) Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest 115: 3149-3156
48. Mullick AE, Soldau K, Kiosses WB, Bell TA 3rd, Tobias PS, Curtiss LK, (2008) Increased endothelial expression of Toll-like receptor 2 at sites of disturbed blood flow exacerbates early atherogenic events. J Exp Med 205: 373-383
49. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B, Thurman RE, John S, Sandstrom R, Johnson AK, Maurano MT, Humbert R, Rynes E, Wang H, Vong S, Lee K, Bates D, Diegel M, Roach V, Dunn D, et al, (2012) An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489: 83-90
50. Ogawa S, Lozach J, Benner C, Pascual G, Tangirala RK, Westin S, Hoffmann A, Subramaniam S, David M, Rosenfeld MG, Glass CK, (2005) Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell 122: 707-721
51. Oram JF, Lawn RM, Garvin MR, Wade DP, (2000) ABCA1 is the cAMP-inducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J Biol Chem 275: 34508-34511
52. Orso E, Broccardo C, Kaminski WE, Bottcher A, Liebisch G, Drobnik W, Gotz A, Chambenoit O, Diederich W, Langmann T, Spruss T, Luciani MF, Rothe G, Lackner KJ, Chimini G, Schmitz G, (2000) Transport of lipids from golgi to plasma membrane is defective in tangier disease patients and Abc1-deficient mice. Nat Genet 24: 192-196
53. Paddison PJ, Cleary M, Silva JM, Chang K, Sheth N, Sachidanandam R, Hannon GJ, (2004) Cloning of short hairpin RNAs for gene knockdown in mammalian cells. Nat Methods 1: 163-167
54. Pourfarzad F, Aghajanirefah A, de Boer E, Ten Have S, Bryn van Dijk T, Kheradmandkia S, Stadhouders R, Thongjuea S, Soler E, Gillemans N, von Lindern M, Demmers J, Philipsen S, Grosveld F, (2013) Locus-specific proteomics by TChP: targeted chromatin purification. Cell Rep 4: 589-600
55. Rader DJ, Tall AR, (2012) The not-so-simple HDL story: is it time to revise the HDL cholesterol hypothesis? Nat Med 18: 1344-1346
56. Ramsey SA, Klemm SL, Zak DE, Kennedy KA, Thorsson V, Li B, Gilchrist M, Gold ES, Johnson CD, Litvak V, Navarro G, Roach JC, Rosenberger CM, Rust AG, Yudkovsky N, Aderem A, Shmulevich I, (2008) Uncovering a macrophage transcriptional program by integrating evidence from motif scanning and expression dynamics. PLoS Comput Biol 4: e1000021
57. Ramsey SA, Knijnenburg TA, Kennedy KA, Zak DE, Gilchrist M, Gold ES, Johnson CD, Lampano AE, Litvak V, Navarro G, Stolyar T, Aderem A, Shmulevich I, (2010) Genome-wide histone acetylation data improve prediction of mammalian transcription factor binding sites. Bioinformatics 26: 2071-2075
58. Ranish JA, Yi EC, Leslie DM, Purvine SO, Goodlett DR, Eng J, Aebersold R, (2003) The study of macromolecular complexes by quantitative proteomics. Nat Genet 33: 349-355
59. Ranish JA, Hahn S, Lu Y, Yi EC, Li XJ, Eng J, Aebersold R, (2004) Identification of TFB5, a new component of general transcription and DNA repair factor IIH. Nat Genet 36: 707-713
60. Repa JJ, Turley SD, Lobaccaro JA, Medina J, Li L, Lustig K, Shan B, Heyman RA, Dietschy JM, Mangelsdorf DJ, (2000) Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science 289: 1524-1529
61. Richards MR, Black AS, Bonnet DJ, Barish GD, Woo CW, Tabas I, Curtiss LK, Tobias PS, (2013) The LPS2 mutation in TRIF is atheroprotective in hyperlipidemic low density lipoprotein receptor knockout mice. Innate Immun 19: 20-29
62. Roach JC, Smith KD, Strobe KL, Nissen SM, Haudenschild CD, Zhou D, Vasicek TJ, Held GA, Stolovitzky GA, Hood LE, Aderem A, (2007) Transcription factor expression in lipopolysaccharide-activated peripheral-blood-derived mononuclear cells. Proc Natl Acad Sci USA 104: 16245-16250
63. Rust S, Rosier M, Funke H, Real J, Amoura Z, Piette JC, Deleuze JF, Brewer HB, Duverger N, Denefle P, Assmann G, (1999) Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat Genet 22: 352-355
64. Sarachana T, Hu VW, (2013) Differential recruitment of coregulators to the RORA promoter adds another layer of complexity to gene (dys) regulation by sex hormones in autism. Mol Autism 4: 39
65. Sauve F, McBroom LD, Gallant J, Moraitis AN, Labrie F, Giguere V, (2001) CIA, a novel estrogen receptor coactivator with a bifunctional nuclear receptor interacting determinant. Mol Cell Biol 21: 343-353
66. Schultz JR, Tu H, Luk A, Repa JJ, Medina JC, Li L, Schwendner S, Wang S, Thoolen M, Mangelsdorf DJ, Lustig KD, Shan B, (2000) Role of LXRs in control of lipogenesis. Genes Dev 14: 2831-2838
67. Sherwood RI, Hashimoto T, O'Donnell CW, Lewis S, Barkal AA, van Hoff JP, Karun V, Jaakkola T, Gifford DK, (2014) Discovery of directional and nondirectional pioneer transcription factors by modeling DNase profile magnitude and shape. Nat Biotechnol 32: 171-178
68. Spann NJ, Garmire LX, McDonald JG, Myers DS, Milne SB, Shibata N, Reichart D, Fox JN, Shaked I, Heudobler D, Raetz CR, Wang EW, Kelly SL, Sullards MC, Murphy RC, Merrill AH Jr, Brown HA, Dennis EA, Li AC, Ley K, et al, (2012) Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 151: 138-152
69. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, Moore KJ, (2010) CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 11: 155-161
70. Sun Z, Feng D, Fang B, Mullican SE, You SH, Lim HW, Everett LJ, Nabel CS, Li Y, Selvakumaran V, Won KJ, Lazar MA, (2013) Deacetylase-independent function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol Cell 52: 769-782
71. Tangirala RK, Bischoff ED, Joseph SB, Wagner BL, Walczak R, Laffitte BA, Daige CL, Thomas D, Heyman RA, Mangelsdorf DJ, Wang X, Lusis AJ, Tontonoz P, Schulman IG, (2002) Identification of macrophage liver X receptors as inhibitors of atherosclerosis. Proc Natl Acad Sci USA 99: 11896-11901
72. Vaisman BL, Lambert G, Amar M, Joyce C, Ito T, Shamburek RD, Cain WJ, Fruchart-Najib J, Neufeld ED, Remaley AT, Brewer HB Jr, Santamarina-Fojo S, (2001) ABCA1 overexpression leads to hyperalphalipoproteinemia and increased biliary cholesterol excretion in transgenic mice. J Clin Invest 108: 303-309
73. Venkateswaran A, Laffitte BA, Joseph SB, Mak PA, Wilpitz DC, Edwards PA, Tontonoz P, (2000a) Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXR alpha. Proc Natl Acad Sci USA 97: 12097-12102
74. Venkateswaran A, Repa JJ, Lobaccaro JM, Bronson A, Mangelsdorf DJ, Edwards PA, (2000b) Human white/murine ABC8 mRNA levels are highly induced in lipid-loaded macrophages. A transcriptional role for specific oxysterols. J Biol Chem 275: 14700-14707
75. Viturawong T, Meissner F, Butter F, Mann M, (2013) A DNA-centric protein interaction map of ultraconserved elements reveals contribution of transcription factor binding hubs to conservation. Cell Rep 5: 531-545
76. Wagner BL, Valledor AF, Shao G, Daige CL, Bischoff ED, Petrowski M, Jepsen K, Baek SH, Heyman RA, Rosenfeld MG, Schulman IG, Glass CK, (2003) Promoter-specific roles for liver X receptor/corepressor complexes in the regulation of ABCA1 and SREBP1 gene expression. Mol Cell Biol 23: 5780-5789
77. Wang X, Collins HL, Ranalletta M, Fuki IV, Billheimer JT, Rothblat GH, Tall AR, Rader DJ, (2007) Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo. J Clin Invest 117: 2216-2224
78. Weintz G, Olsen JV, Fruhauf K, Niedzielska M, Amit I, Jantsch J, Mages J, Frech C, Dolken L, Mann M, Lang R, (2010) The phosphoproteome of toll-like receptor-activated macrophages. Mol Syst Biol 6: 371
79. Xu XH, Shah PK, Faure E, Equils O, Thomas L, Fishbein MC, Luthringer D, Xu XP, Rajavashisth TB, Yano J, Kaul S, Arditi M, (2001) Toll-like receptor-4 is expressed by macrophages in murine and human lipid-rich atherosclerotic plaques and upregulated by oxidized LDL. Circulation 104: 3103-3108
80. Yvan-Charvet L, Ranalletta M, Wang N, Han S, Terasaka N, Li R, Welch C, Tall AR, (2007) Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J Clin Invest 117: 3900-3908
81. Yvan-Charvet L, Welch C, Pagler TA, Ranalletta M, Lamkanfi M, Han S, Ishibashi M, Li R, Wang N, Tall AR, (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
82. Zervou MI, Goulielmos GN, Castro-Giner F, Boumpas DT, Tosca AD, Krueger-Krasagakis S, (2011) A CD40 and an NCOA5 gene polymorphism confer susceptibility to psoriasis in a Southern European population: a case-control study. Hum Immunol 72: 761-765
83. Zhu X, Lee JY, Timmins JM, Brown JM, Boudyguina E, Mulya A, Gebre AK, Willingham MC, Hiltbold EM, Mishra N, Maeda N, Parks JS, (2008) Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J Biol Chem 283: 22930-22941
84. Zimmer S, Steinmetz M, Asdonk T, Motz I, Coch C, Hartmann E, Barchet W, Wassmann S, Hartmann G, Nickenig G, (2011) Activation of endothelial toll-like receptor 3 impairs endothelial function. Circ Res 108: 1358-1366