Phosphorylation of Liver X Receptor α Selectively Regulates Target Gene Expression in Macrophages

REFERENCES

• Abagyan, R., and M. Totrov. 1994. Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins. J. Mol. Biol. 235:983–1002.
   PubMed Web of Science ®Google Scholar
• Arai, S., J. M. Shelton, M. Chen, M. N. Bradley, A. Castrillo, A. L. Bookout, P. A. Mak, P. A. Edwards, D. J. Mangelsdorf, P. Tontonoz, and T. Miyazaki. 2005. A role for the apoptosis inhibitory factor AIM/Spα/Api6 in atherosclerosis development. Cell Metab. 1:201–213.
   PubMed Web of Science ®Google Scholar
• Assmann, G., H. Schulte, and A. von Eckardstein. 1996. Hypertriglyceridemia and elevated lipoprotein(a) are risk factors for major coronary events in middle-aged men. Am. J. Cardiol. 77:1179–1184.
   PubMed Web of Science ®Google Scholar
• Babaev, V. R., S. Fazio, L. A. Gleaves, K. J. Carter, C. F. Semenkovich, and M. F. Linton. 1999. Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in vivo. J. Clin. Investig. 103:1697–1705.
   PubMedGoogle Scholar
• Babaev, V. R., M. B. Patel, C. F. Semenkovich, S. Fazio, and M. F. Linton. 2000. Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in low density lipoprotein receptor-deficient mice. J. Biol. Chem. 275:26293–26299.
   PubMedGoogle Scholar
• Barish, G. D. 2006. Peroxisome proliferator-activated receptors and liver X receptors in atherosclerosis and immunity. J. Nutr. 136:690–694.
   PubMed Web of Science ®Google Scholar
• Blaschke, F., O. Leppanen, Y. Takata, E. Caglayan, J. Liu, M. C. Fishbein, K. Kappert, K. I. Nakayama, A. R. Collins, E. Fleck, W. A. Hsueh, R. E. Law, and D. Bruemmer. 2004. Liver X receptor agonists suppress vascular smooth muscle cell proliferation and inhibit neointima formation in balloon-injured rat carotid arteries. Circ. Res. 95:e110–e123.
   PubMed Web of Science ®Google Scholar
• Bruck, N., J. Bastien, G. Bour, A. Tarrade, J. L. Plassat, A. Bauer, S. Adam-Stitah, and C. Rochette-Egly. 2005. Phosphorylation of the retinoid X receptor at the omega loop, modulates the expression of retinoic-acid-target genes with a promoter context specificity. Cell Signal 17:1229–1239.
   PubMedGoogle Scholar
• Chen, M., M. N. Bradley, S. W. Beaven, and P. Tontonoz. 2006. Phosphorylation of the liver X receptors. FEBS Lett. 580:4835–4841.
   PubMedGoogle Scholar
• Costet, P., Y. Luo, N. Wang, and A. R. Tall. 2000. Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J. Biol. Chem. 275:28240–28245.
   PubMed Web of Science ®Google Scholar
• Davies, J. D., K. L. Carpenter, I. R. Challis, N. L. Figg, R. McNair, D. Proudfoot, P. L. Weissberg, and C. M. Shanahan. 2005. Adipocytic differentiation and liver X receptor pathways regulate the accumulation of triacylglycerols in human vascular smooth muscle cells. J. Biol. Chem. 280:3911–3919.
   PubMedGoogle Scholar
• Desclozeaux, M., I. N. Krylova, F. Horn, R. J. Fletterick, and H. A. Ingraham. 2002. Phosphorylation and intramolecular stabilization of the ligand binding domain in the nuclear receptor steroidogenic factor 1. Mol. Cell. Biol. 22:7193–7203.
   PubMed Web of Science ®Google Scholar
• Eeckhoute, J., J. S. Carroll, T. R. Geistlinger, M. I. Torres-Arzayus, and M. Brown. 2006. A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev. 20:2513–2526.
   PubMed Web of Science ®Google Scholar
• Faust, M., and M. Montenarh. 2000. Subcellular localization of protein kinase CK2. A key to its function? Cell Tissue Res. 301:329–340.
   PubMed Web of Science ®Google Scholar
• Ganz, T., L. Liu, E. V. Valore, and A. Oren. 1993. Posttranslational processing and targeting of transgenic human defensin in murine granulocyte, macrophage, fibroblast, and pituitary adenoma cell lines. Blood 82:641–650.
   PubMed Web of Science ®Google Scholar
• Ghisletti, S., W. Huang, S. Ogawa, G. Pascual, M. E. Lin, T. M. Willson, M. G. Rosenfeld, and C. K. Glass. 2007. Parallel SUMOylation-dependent pathways mediate gene- and signal-specific transrepression by LXRs and PPARγ. Mol. Cell 25:57–70.
   PubMed Web of Science ®Google Scholar
• Guan, H. P., T. Ishizuka, P. C. Chui, M. Lehrke, and M. A. Lazar. 2005. Corepressors selectively control the transcriptional activity of PPARgα in adipocytes. Genes Dev. 19:453–461.
   PubMed Web of Science ®Google Scholar
• Guerra, B., S. Siemer, B. Boldyreff, and O. G. Issinger. 1999. Protein kinase CK2: evidence for a protein kinase CK2β subunit fraction, devoid of the catalytic CK2α subunit, in mouse brain and testicles. FEBS Lett. 462:353–357.
   PubMedGoogle Scholar
• Haley, K. J., C. M. Lilly, J. H. Yang, Y. Feng, S. P. Kennedy, T. G. Turi, J. F. Thompson, G. H. Sukhova, P. Libby, and R. T. Lee. 2000. Overexpression of eotaxin and the CCR3 receptor in human atherosclerosis: using genomic technology to identify a potential novel pathway of vascular inflammation. Circulation 102:2185–2189.
   PubMed Web of Science ®Google Scholar
• Hammer, G. D., I. Krylova, Y. Zhang, B. D. Darimont, K. Simpson, N. L. Weigel, and H. A. Ingraham. 1999. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: integration of hormone signaling in reproduction and stress. Mol. Cell 3:521–526.
   PubMed Web of Science ®Google Scholar
• Hu, X., S. Li, J. Wu, C. Xia, and D. S. Lala. 2003. Liver X receptors interact with corepressors to regulate gene expression. Mol. Endocrinol. 17:1019–1026.
   PubMed Web of Science ®Google Scholar
• Huang, C. J., D. Feltkamp, S. Nilsson, and J. A. Gustafsson. 1998. Synergistic activation of RLD-1 by agents triggering PKA and PKC dependent signalling. Biochem. Biophys. Res. Commun. 243:657–663.
   PubMedGoogle Scholar
• Ichikawa, T., J. Liang, S. Kitajima, T. Koike, X. Wang, H. Sun, M. Morimoto, H. Shikama, T. Watanabe, N. Yamada, and J. Fan. 2005. Macrophage-derived lipoprotein lipase increases aortic atherosclerosis in cholesterol-fed Tg rabbits. Atherosclerosis 179:87–95.
   PubMed Web of Science ®Google Scholar
• Joseph, S., A. Castrillo, B. Laffitte, D. Mangelsdorf, and P. Tontonoz. 2003. Reciprocal regulation of inflamation and lipid metabolism by liver X receptors. Nat. Med. 9:213–219.
   PubMed Web of Science ®Google Scholar
• Joseph, S. B., M. N. Bradley, A. Castrillo, K. W. Bruhn, P. A. Mak, L. Pei, J. Hogenesch, M. O'Connell, R. G. Cheng, E. Saez, J. F. Miller, and P. Tontonoz. 2004. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 119:299–309.
   PubMed Web of Science ®Google Scholar
• Joseph, S. B., E. McKilligin, L. Pei, M. A. Watson, A. R. Collins, B. A. Laffitte, M. Chen, G. Noh, J. Goodman, G. N. Hagger, J. Tran, T. K. Tippin, X. Wang, A. J. Lusis, W. A. Hsueh, R. E. Law, J. L. Collins, T. M. Willson, and P. Tontonoz. 2002. Synthetic LXR ligand inhibits the development of atherosclerosis in mice. Proc. Natl. Acad. Sci. USA 99:7604–7609.
   PubMed Web of Science ®Google Scholar
• Laffitte, B. A., S. B. Joseph, M. Chen, A. Castrillo, J. Repa, D. Wilpitz, D. Mangelsdorf, and P. Tontonoz. 2003. The phospholipid transfer protein gene is a liver X receptor target expressed by macrophages in atherosclerotic lesions. Mol. Cell. Biol. 23:2182–2191.
   PubMed Web of Science ®Google Scholar
• Levin, N., E. D. Bischoff, C. L. Daige, D. Thomas, C. T. Vu, R. A. Heyman, R. K. Tangirala, and I. G. Schulman. 2005. Macrophage liver X receptor is required for antiatherogenic activity of LXR agonists. Arterioscler. Thromb. Vasc. Biol. 25:135–142.
   PubMed Web of Science ®Google Scholar
• Li, W., C. N. Cavasotto, T. Cardozo, S. Ha, T. Dang, S. S. Taneja, S. K. Logan, and M. J. Garabedian. 2005. Androgen receptor mutations identified in prostate cancer and androgen insensitivity syndrome display aberrant ART-27 coactivator function. Mol. Endocrinol. 19:2273–2282.
   PubMedGoogle Scholar
• Lund, E. G., L. B. Peterson, A. D. Adams, M. H. Lam, C. A. Burton, J. Chin, Q. Guo, S. Huang, M. Latham, J. C. Lopez, J. G. Menke, D. P. Milot, L. J. Mitnaul, S. E. Rex-Rabe, R. L. Rosa, J. Y. Tian, S. D. Wright, and C. P. Sparrow. 2006. Different roles of liver X receptor alpha and beta in lipid metabolism: effects of an alpha-selective and a dual agonist in mice deficient in each subtype. Biochem. Pharmacol. 71:453–463.
   PubMed Web of Science ®Google Scholar
• Ma, Y., Y. Lu, H. Zeng, D. Ron, W. Mo, and T. A. Neubert. 2001. Characterization of phosphopeptides from protein digests using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and nanoelectrospray quadrupole time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 15:1693–1700.
   PubMed Web of Science ®Google Scholar
• Mo, J., S. J. Fang, W. Chen, and G. C. Blobe. 2002. Regulation of ALK-1 signaling by the nuclear receptor LXRβ. J. Biol. Chem. 277:50788–50794.
   PubMedGoogle Scholar
• Ogata, K., K. Sato, and T. H. Tahirov. 2003. Eukaryotic transcriptional regulatory complexes: cooperativity from near and afar. Curr. Opin. Struct. Biol. 13:40–48.
   PubMedGoogle Scholar
• Oxelmark, E., J. M. Roth, P. C. Brooks, S. E. Braunstein, R. J. Schneider, and M. J. Garabedian. 2006. The cochaperone p23 differentially regulates estrogen receptor target genes and promotes tumor cell adhesion and invasion. Mol. Cell. Biol. 26:5205–5213.
   PubMedGoogle Scholar
• Pagano, M. A., M. Andrzejewska, M. Ruzzene, S. Sarno, L. Cesaro, J. Bain, M. Elliott, F. Meggio, Z. Kazimierczuk, and L. A. Pinna. 2004. Optimization of protein kinase CK2 inhibitors derived from 4,5,6,7-tetrabromobenzimidazole. J. Med. Chem. 47:6239–6247.
   PubMed Web of Science ®Google Scholar
• Pascual, G., 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. 2005. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 437:759–763.
   PubMed Web of Science ®Google Scholar
• Pease, J. E. 2006. Asthma, allergy and chemokines. Curr. Drug. Targets 7:3–12.
   PubMed Web of Science ®Google Scholar
• Pineda Torra, I., L. P. Freedman, and M. J. Garabedian. 2004. Identification of DRIP205 as a coactivator for the Farnesoid X receptor. J. Biol. Chem. 279:36184–36191.
   PubMed Web of Science ®Google Scholar
• Quinet, E. M., D. A. Savio, A. R. Halpern, L. Chen, G. U. Schuster, J. A. Gustafsson, M. D. Basso, and P. Nambi. 2006. Liver X receptor (LXR)-β regulation in LXRα-deficient mice: implications for therapeutic targeting. Mol. Pharmacol. 70:1340–1349.
   PubMedGoogle Scholar
• Reily, M. M., C. Pantoja, X. Hu, Y. Chinenov, and I. Rogatsky. 2006. The GRIP1:IRF3 interaction as a target for glucocorticoid receptor-mediated immunosuppression. EMBO J. 25:108–117.
   PubMed Web of Science ®Google Scholar
• Rochette-Egly, C. 2003. Nuclear receptors: integration of multiple signalling pathways through phosphorylation. Cell Signal 15:355–366.
   PubMed Web of Science ®Google Scholar
• Roh, T. Y., S. Cuddapah, and K. Zhao. 2005. Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev. 19:542–552.
   PubMed Web of Science ®Google Scholar
• Rong, J. X., M. Shapiro, E. Trogan, and E. A. Fisher. 2003. Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc. Natl. Acad. Sci. USA 100:13531–13536.
   PubMed Web of Science ®Google Scholar
• Sanchez-Martinez, R., A. I. Castillo, A. Steinmeyer, and A. Aranda. 2006. The retinoid X receptor ligand restores defective signalling by the vitamin D receptor. EMBO Rep. 7:1030–1034.
   PubMedGoogle Scholar
• Schmidt-Spaniol, I., B. Grimm, and O. G. Issinger. 1993. Subcellular localization of protein kinase CK-2 alpha- and beta-subunits in synchronized cells from primary human fibroblasts and established cell lines. Cell Mol. Biol. Res. 39:761–772.
   PubMedGoogle Scholar
• Schultz, J. R., H. Tu, A. Luk, J. J. Repa, J. C. Medina, L. Li, S. Schwendner, S. Wang, M. Thoolen, D. J. Mangelsdorf, K. D. Lustig, and B. Shan. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14:2831–2838.
   PubMed Web of Science ®Google Scholar
• Schuster, G. U., P. Parini, L. Wang, S. Alberti, K. R. Steffensen, G. K. Hansson, B. Angelin, and J. A. Gustafsson. 2002. Accumulation of foam cells in liver X receptor-deficient mice. Circulation 106:1147–1153.
   PubMed Web of Science ®Google Scholar
• Sparrow, C. P., J. Baffic, M. H. Lam, E. G. Lund, A. D. Adams, X. Fu, N. Hayes, A. B. Jones, K. L. Macnaul, J. Ondeyka, S. Singh, J. Wang, G. Zhou, D. E. Moller, S. D. Wright, and J. G. Menke. 2002. A potent synthetic LXR agonist is more effective than cholesterol loading at inducing ABCA1 mRNA and stimulating cholesterol efflux. J. Biol. Chem. 277:10021–10027.
   PubMed Web of Science ®Google Scholar
• Svensson, S., T. Ostberg, M. Jacobsson, C. Norstrom, K. Stefansson, D. Hallen, I. C. Johansson, K. Zachrisson, D. Ogg, and L. Jendeberg. 2003. Crystal structure of the heterodimeric complex of LXRα and RXRβ ligand-binding domains in a fully agonistic conformation. EMBO J. 22:4625–4633.
   PubMed Web of Science ®Google Scholar
• Tamura, K., Y. E. Chen, M. Horiuchi, Q. Chen, L. Daviet, Z. Yang, M. Lopez-Ilasaca, H. Mu, R. E. Pratt, and V. Dzau. 2000. LXRα functions as cAMP-responsive transcriptional regulator of gene expression. Proc. Natl. Acad. Sci. USA 97:8513–8518.
   PubMed Web of Science ®Google Scholar
• Taneja, S. S., S. Ha, N. K. Swenson, H. Y. Huang, P. Lee, J. Melamed, E. Shapiro, M. J. Garabedian, and S. K. Logan. 2005. Cell-specific regulation of androgen receptor phosphorylation in vivo. J. Biol. Chem. 280:40916–40924.
   PubMed Web of Science ®Google Scholar
• Tangirala, R. K., E. D. Bischoff, S. B. Joseph, B. L. Wagner, R. Walczak, B. A. Laffitte, C. L. Daige, D. Thomas, R. A. Heyman, D. J. Mangelsdorf, X. Wang, A. J. Lusis, P. Tontonoz, and I. G. Schulman. 2002. Identification of macrophage liver X receptors as inhibitors of atherosclerosis. Proc. Natl. Acad. Sci. USA 99:11896–11901.
   PubMed Web of Science ®Google Scholar
• Valledor, A. F., L. C. Hsu, S. Ogawa, D. Sawka-Verhelle, M. Karin, and C. K. Glass. 2004. Activation of liver X receptors and retinoid X receptors prevents bacterial-induced macrophage apoptosis. Proc. Natl. Acad. Sci. USA 101:17813–17818.
   PubMed Web of Science ®Google Scholar
• Van Eck, M., R. Zimmermann, P. H. Groot, R. Zechner, and T. J. Van Berkel. 2000. Role of macrophage-derived lipoprotein lipase in lipoprotein metabolism and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 20:E53–E62.
   PubMedGoogle Scholar
• Venkateswaran, A., B. A. Laffitte, S. B. Joseph, A. Mak, D. C. Wilpitz, P. A. Edwards, and P. Tontonoz. 2000. Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXRα. Proc. Natl. Acad. Sci. USA 97:12097–12102.
   PubMed Web of Science ®Google Scholar
• Wagner, B. L., A. F. Valledor, G. Shao, C. L. Daige, E. D. Bischoff, M. Petrowski, K. Jepsen, S. H. Baek, R. A. Heyman, M. G. Rosenfeld, I. G. Schulman, and C. K. Glass. 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.
   PubMed Web of Science ®Google Scholar
• Wang, G., K. A. Ahmad, G. Unger, J. W. Slaton, and K. Ahmed. 2006. CK2 signaling in androgen-dependent and -independent prostate cancer. J. Cell Biochem. 99:382–391.
   PubMed Web of Science ®Google Scholar
• Wang, Z., J. Frederick, and M. J. Garabedian. 2002. Deciphering the phosphorylation code of the glucocorticoid receptor in vivo. J. Biol. Chem. 277:26573–26580.
   PubMed Web of Science ®Google Scholar
• Warnmark, A., E. Treuter, A. P. Wright, and J. A. Gustafsson. 2003. Activation functions 1 and 2 of nuclear receptors: molecular strategies for transcriptional activation. Mol. Endocrinol. 17:1901–1909.
   PubMedGoogle Scholar
• Watanabe, K., P. J. Jose, and S. M. Rankin. 2002. Eotaxin-2 generation is differentially regulated by lipopolysaccharide and IL-4 in monocytes and macrophages. J. Immunol. 168:1911–1918.
   PubMed Web of Science ®Google Scholar
• Weigel, N. L., and Y. Zhang. 1998. Ligand-independent activation of steroid hormone receptors. J. Mol. Med. 76:469–479.
   PubMedGoogle Scholar
• Willy, P. J., K. Umesono, E. S. Ong, R. M. Evans, R. A. Heyman, and D. J. Mangelsdorf. 1995. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 9:1033–1045.
   PubMed Web of Science ®Google Scholar
• Xu, C. F., Y. Lu, J. Ma, M. Mohammadi, and T. A. Neubert. 2005. Identification of phosphopeptides by MALDI Q.-TOF MS in positive and negative ion modes after methyl esterification. Mol. Cell Proteomics 4:809–818.
   PubMedGoogle Scholar
• Yamamoto, T., H. Shimano, N. Inoue, Y. Nakagawa, T. Matsuzaka, A. Takahashi, N. Yahagi, H. Sone, H. Suzuki, H. Toyoshima, and N. Yamada. 2007. Protein kinase A suppresses sterol regulatory element-binding protein-1C expression via phosphorylation of liver X receptor in the liver. J. Biol. Chem. 282:11687–11695.
   PubMedGoogle Scholar
• Yang, W., C. Rachez, and L. P. Freedman. 2000. Discrete roles for peroxisome proliferator-activated receptor gamma and retinoid X receptor in recruiting nuclear receptor coactivators. Mol. Cell. Biol. 20:8008–8017.
   PubMedGoogle Scholar
• Yee, J. K., A. Miyanohara, P. LaPorte, K. Bouic, J. C. Burns, and T. Friedmann. 1994. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc. Natl. Acad. Sci. USA 91:9564–9568.
   PubMed Web of Science ®Google Scholar
• Zelcer, N., and P. Tontonoz. 2006. Liver X receptors as integrators of metabolic and inflammatory signaling. J. Clin. Investig. 116:607–614.
   PubMed Web of Science ®Google Scholar