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Science 289 (5484): 1524-1529

Copyright © 2000 by the American Association for the Advancement of Science

Regulation of Absorption and ABC1-Mediated Efflux of Cholesterol by RXR Heterodimers

J. J. Repa,1 S. D. Turley,2 J.-M. A. Lobaccaro,1* J. Medina,3 L. Li,3 K. Lustig,3 B. Shan,3 R. A. Heyman,4 † J. M. Dietschy,2 D. J. Mangelsdorf1ddagger

Several nuclear hormone receptors involved in lipid metabolism form obligate heterodimers with retinoid X receptors (RXRs) and are activated by RXR agonists such as rexinoids. Animals treated with rexinoids exhibited marked changes in cholesterol balance, including inhibition of cholesterol absorption and repressed bile acid synthesis. Studies with receptor-selective agonists revealed that oxysterol receptors (LXRs) and the bile acid receptor (FXR) are the RXR heterodimeric partners that mediate these effects by regulating expression of the reverse cholesterol transporter, ABC1, and the rate-limiting enzyme of bile acid synthesis, CYP7A1, respectively. Thus, these RXR heterodimers serve as key regulators of cholesterol homeostasis by governing reverse cholesterol transport from peripheral tissues, bile acid synthesis in liver, and cholesterol absorption in intestine.

1 Howard Hughes Medical Institute and Department of Pharmacology,
2 Department of Internal Medicine, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9050, USA.
3 Tularik, Two Corporate Drive, South San Francisco, CA 94080, USA.
4 Ligand Pharmaceuticals, 10255 Science Center Drive, San Diego, CA 92121, USA.
*   Present address: Physiologie Comparée-Endocrinologie Moléculaire, UMR CNRS 6547-GEEM, Université Blaise Pascal, 63177 Aubière Cedex, France.

ddagger    To whom correspondence should be addressed. E-mail: davo.mango{at}utsouthwestern.edu

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Differential expression, distribution, and function of PPAR-{gamma} in the proximal and distal colon.
W. Su, C. R. Bush, B. M. Necela, S. R. Calcagno, N. R. Murray, A. P. Fields, and E. A. Thompson (2007)
Physiol Genomics 30, 342-353
   Abstract »    Full Text »    PDF »
Estrogen Deprivation and Inhibition of Breast Cancer Growth in Vivo through Activation of the Orphan Nuclear Receptor Liver X Receptor.
H. Gong, P. Guo, Y. Zhai, J. Zhou, H. Uppal, M. J. Jarzynka, W.-C. Song, S.-Y. Cheng, and W. Xie (2007)
Mol. Endocrinol. 21, 1781-1790
   Abstract »    Full Text »    PDF »
Modification of HDL3 by mild oxidative stress increases ATP-binding cassette transporter 1-mediated cholesterol efflux.
A. Pirillo, P. Uboldi, G. Pappalardo, H. Kuhn, and A. L. Catapano (2007)
Cardiovasc Res 75, 566-574
   Abstract »    Full Text »    PDF »
Sterol Regulatory Element-binding Protein-2- and Liver X Receptor-driven Dual Promoter Regulation of Hepatic ABC Transporter A1 Gene Expression: MECHANISM UNDERLYING THE UNIQUE RESPONSE TO CELLULAR CHOLESTEROL STATUS.
N. Tamehiro, Y. Shigemoto-Mogami, T. Kakeya, K.-i. Okuhira, K. Suzuki, R. Sato, T. Nagao, and T. Nishimaki-Mogami (2007)
J. Biol. Chem. 282, 21090-21099
   Abstract »    Full Text »    PDF »
A Key Role for Orphan Nuclear Receptor Liver Receptor Homologue-1 in Activation of Fatty Acid Synthase Promoter by Liver X Receptor.
K. E. Matsukuma, L. Wang, M. K. Bennett, and T. F. Osborne (2007)
J. Biol. Chem. 282, 20164-20171
   Abstract »    Full Text »    PDF »
SREBP-1-independent regulation of lipogenic gene expression in adipocytes.
M. Sekiya, N. Yahagi, T. Matsuzaka, Y. Takeuchi, Y. Nakagawa, H. Takahashi, H. Okazaki, Y. Iizuka, K. Ohashi, T. Gotoda, et al. (2007)
J. Lipid Res. 48, 1581-1591
   Abstract »    Full Text »    PDF »
Attenuation of neuroinflammation and Alzheimer's disease pathology by liver x receptors.
N. Zelcer, N. Khanlou, R. Clare, Q. Jiang, E. G. Reed-Geaghan, G. E. Landreth, H. V. Vinters, and P. Tontonoz (2007)
PNAS 104, 10601-10606
   Abstract »    Full Text »    PDF »
Selective Activation of Liver X Receptors by Acanthoic Acid-Related Diterpenes.
P. G. Traves, S. Hortelano, M. Zeini, T.-H. Chao, T. Lam, S. T. Neuteboom, E. A. Theodorakis, M. A. Palladino, A. Castrillo, and L. Bosca (2007)
Mol. Pharmacol. 71, 1545-1553
   Abstract »    Full Text »    PDF »
Mammalian Target of Rapamycin Activation Impairs Hepatocytic Differentiation and Targets Genes Moderating Lipid Homeostasis and Hepatocellular Growth.
R. Parent, D. Kolippakkam, G. Booth, and L. Beretta (2007)
Cancer Res. 67, 4337-4345
   Abstract »    Full Text »    PDF »
Multiple Roles of the Nuclear Receptors for Oxysterols Liver X Receptor to Maintain Male Fertility.
D. H. Volle, K. Mouzat, R. Duggavathi, B. Siddeek, P. Dechelotte, B. Sion, G. Veyssiere, M. Benahmed, and J.-M. A. Lobaccaro (2007)
Mol. Endocrinol. 21, 1014-1027
   Abstract »    Full Text »    PDF »
Liver X Receptor Alpha Associates With Human Life Span.
S. P. Mooijaart, M. Kuningas, R. G. J. Westendorp, J. J. Houwing-Duistermaat, P. E. Slagboom, P. C. N. Rensen, and D. van Heemst (2007)
J Gerontol A Biol Sci Med Sci 62, 343-349
   Abstract »    Full Text »    PDF »
A Mutant Thyroid Hormone Receptor {alpha} Antagonizes Peroxisome Proliferator-Activated Receptor {alpha} Signaling in Vivo and Impairs Fatty Acid Oxidation.
Y.-Y. Liu, R. S. Heymann, F. Moatamed, J. J. Schultz, D. Sobel, and G. A. Brent (2007)
Endocrinology 148, 1206-1217
   Abstract »    Full Text »    PDF »
Oxysterol Nuclear Receptor LXRbeta Regulates Cholesterol Homeostasis and Contractile Function in Mouse Uterus.
K. Mouzat, M. Prod'Homme, D. H. Volle, B. Sion, P. Dechelotte, K. Gauthier, J.-M. Vanacker, and J.-M. A. Lobaccaro (2007)
J. Biol. Chem. 282, 4693-4701
   Abstract »    Full Text »    PDF »
PXR induces CYP27A1 and regulates cholesterol metabolism in the intestine.
T. Li, W. Chen, and J. Y. L. Chiang (2007)
J. Lipid Res. 48, 373-384
   Abstract »    Full Text »    PDF »
The Liver X Receptor (LXR) and Hepatic Lipogenesis: THE CARBOHYDRATE-RESPONSE ELEMENT-BINDING PROTEIN IS A TARGET GENE OF LXR.
J.-Y. Cha and J. J. Repa (2007)
J. Biol. Chem. 282, 743-751
   Abstract »    Full Text »    PDF »
Liver X Receptors Regulate Adrenal Steroidogenesis and Hypothalamic-Pituitary-Adrenal Feedback.
M. Nilsson, T. M. Stulnig, C.-Y. Lin, A. L. Yeo, P. Nowotny, E. T. Liu, and K. R. Steffensen (2007)
Mol. Endocrinol. 21, 126-137
   Abstract »    Full Text »    PDF »
International Union of Pharmacology. LXII. The NR1H and NR1I Receptors: Constitutive Androstane Receptor, Pregnene X Receptor, Farnesoid X Receptor {alpha}, Farnesoid X Receptor beta, Liver X Receptor {alpha}, Liver X Receptor beta, and Vitamin D Receptor.
D. D. Moore, S. Kato, W. Xie, D. J. Mangelsdorf, D. R. Schmidt, R. Xiao, and S. A. Kliewer (2006)
Pharmacol. Rev. 58, 742-759
   Abstract »    Full Text »    PDF »
International Union of Pharmacology. LXIII. Retinoid X Receptors.
P. Germain, P. Chambon, G. Eichele, R. M. Evans, M. A. Lazar, M. Leid, A. R. De Lera, R. Lotan, D. J. Mangelsdorf, and H. Gronemeyer (2006)
Pharmacol. Rev. 58, 760-772
   Abstract »    Full Text »    PDF »
Coordinated control of bile acids and lipogenesis through FXR-dependent regulation of fatty acid synthase.
K. E. Matsukuma, M. K. Bennett, J. Huang, L. Wang, G. Gil, and T. F. Osborne (2006)
J. Lipid Res. 47, 2754-2761
   Abstract »    Full Text »    PDF »
Ceramide structural features required to stimulate ABCA1-mediated cholesterol efflux to apolipoprotein A-I.
A. B. Ghering and W. S. Davidson (2006)
J. Lipid Res. 47, 2781-2788
   Abstract »    Full Text »    PDF »
Correction of Apolipoprotein A-I-mediated Lipid Efflux and High Density Lipoprotein Particle Formation in Human Niemann-Pick Type C Disease Fibroblasts.
E. Boadu, H. Y. Choi, D. W. K. Lee, E. I. Waddington, T. Chan, B. Asztalos, J. E. Vance, A. Chan, G. Castro, and G. A. Francis (2006)
J. Biol. Chem. 281, 37081-37090
   Abstract »    Full Text »    PDF »
The RXR Agonist Bexarotene Improves Cholesterol Homeostasis and Inhibits Atherosclerosis Progression in a Mouse Model of Mixed Dyslipidemia.
F. Lalloyer, C. Fievet, S. Lestavel, G. Torpier, J. van der Veen, V. Touche, S. Bultel, S. Yous, F. Kuipers, R. Paumelle, et al. (2006)
Arterioscler Thromb Vasc Biol 26, 2731-2737
   Abstract »    Full Text »    PDF »
Oxidative stress influences cholesterol efflux in THP-1 macrophages: Role of ATP-binding cassette A1 and nuclear factors.
V. Marcil, E. Delvin, A. T. Sane, A. Tremblay, and E. Levy (2006)
Cardiovasc Res 72, 473-482
   Abstract »    Full Text »    PDF »
Human immunodeficiency virus infection and macrophage cholesterol metabolism..
M. Bukrinsky and D. Sviridov (2006)
J. Leukoc. Biol. 80, 1044-1051
   Abstract »    Full Text »    PDF »

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