Identification of Liver X Receptor-Retinoid X Receptor as an Activator of the Sterol Regulatory Element-Binding Protein 1c Gene Promoter

doi:10.1128/MCB.21.9.2991-3000.2001

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Molecular and Cellular Biology, May 2001, p. 2991-3000, Vol. 21, No. 9
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.9.2991-3000.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Identification of Liver X Receptor-Retinoid X Receptor as an Activator of the Sterol Regulatory Element-Binding Protein 1c Gene Promoter

Tomohiro Yoshikawa,¹ Hitoshi Shimano,²^,^* Michiyo Amemiya-Kudo,¹ Naoya Yahagi,¹ Alyssa H. Hasty,¹ Takashi Matsuzaka,² Hiroaki Okazaki,¹ Yoshiaki Tamura,¹ Yoko Iizuka,¹ Ken Ohashi,¹ Jun-Ichi Osuga,¹ Kenji Harada,¹ Takanari Gotoda,¹ Satoshi Kimura,¹ Shun Ishibashi,¹ and Nobuhiro Yamada²

Department of Metabolic Diseases, University of Tokyo, Bunkyo-ku, Tokyo 113-8655,¹ and Department of Internal Medicine, Institute of Clinical Medicine, University of Tsukuba, Ibaraki 305-8575,² Japan

Received 23 October 2000/Returned for modification 19 December 2000/Accepted 9 February 2001

In an attempt to identify transcription factors which activate sterol-regulatory element-binding protein 1c (SREBP-1c) transcription,we screened an expression cDNA library from adipose tissue ofSREBP-1 knockout mice using a reporter gene containing the 2.6-kbmouse SREBP-1 gene promoter. We cloned and identified the oxysterolreceptors liver X receptor (LXR $alpha$ ) and LXR $beta$ as strong activatorsof the mouse SREBP-1c promoter. In the transfection studies, expressionof either LXR $alpha$ or - $beta$ activated the SREBP-1c promoter-luciferasegene in a dose-dependent manner. Deletion and mutation studies,as well as gel mobility shift assays, located an LXR responseelement complex consisting of two new LXR-binding motifs whichshowed high similarity to an LXR response element recently foundin the ABC1 gene promoter, a reverse cholesterol transporter.Addition of an LXR ligand, 22(R)-hydroxycholesterol, increasedthe promoter activity. Coexpression of retinoid X receptor (RXR),a heterodimeric partner, and its ligand 9-cis-retinoic acid alsosynergistically activated the SREBP-1c promoter. In HepG2 cells,SREBP-1c mRNA and precursor protein levels were induced by treatmentwith 22(R)-hydroxycholesterol and 9-cis-retinoic acid, confirmingthat endogenous LXR-RXR activation can induce endogenous SREBP-1cexpression. The activation of SREBP-1c by LXR is associated witha slight increase in nuclear SREBP-1c, resulting in activationof the gene for fatty acid synthase, one of its downstream genes,as measured by the luciferase assay. These data demonstrate thatLXR-RXR can modify the expression of genes for lipogenic enzymesby regulating SREBP-1c expression, providing a novel link betweenfatty acid and cholesterolmetabolism.

^* Corresponding author. Mailing address: Department of Internal Medicine, Institute of Clinical Medicine, University of Tsukuba,1-1-1 Tennodai, Tsukuba, Ibaraki 305-8575, Japan. Phone and fax:81-298-63-2170. E-mail: shimano-tky{at}umin.ac.jp.

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Kocarek, T. A., Dahn, M. S., Cai, H., Strom, S. C., Mercer-Haines, N. A. (2002). Regulation of CYP2B6 and CYP3A Expression by Hydroxymethylglutaryl Coenzyme A Inhibitors in Primary Cultured Human Hepatocytes. Drug Metab. Dispos. 30: 1400-1405 [Abstract] [Full Text]
Muscat, G. E. O., Wagner, B. L., Hou, J., Tangirala, R. K., Bischoff, E. D., Rohde, P., Petrowski, M., Li, J., Shao, G., Macondray, G., Schulman, I. G. (2002). Regulation of Cholesterol Homeostasis and Lipid Metabolism in Skeletal Muscle by Liver X Receptors. J. Biol. Chem. 277: 40722-40728 [Abstract] [Full Text]
Brown, B. G., Cheung, M. C., Lee, A. C., Zhao, X.-Q., Chait, A. (2002). Antioxidant Vitamins and Lipid Therapy: End of a Long Romance?. Arterioscler. Thromb. Vasc. Bio. 22: 1535-1546 [Abstract] [Full Text]
Grefhorst, A., Elzinga, B. M., Voshol, P. J., Plosch, T., Kok, T., Bloks, V. W., van der Sluijs, F. H., Havekes, L. M., Romijn, J. A., Verkade, H. J., Kuipers, F. (2002). Stimulation of Lipogenesis by Pharmacological Activation of the Liver X Receptor Leads to Production of Large, Triglyceride-rich Very Low Density Lipoprotein Particles. J. Biol. Chem. 277: 34182-34190 [Abstract] [Full Text]
Duanmu, Z., Locke, D., Smigelski, J., Wu, W., Dahn, M. S., Falany, C. N., Kocarek, T. A., Runge-Morris, M. (2002). Effects of Dexamethasone on Aryl (SULT1A1)- and Hydroxysteroid (SULT2A1)-Sulfotransferase Gene Expression in Primary Cultured Human Hepatocytes. Drug Metab. Dispos. 30: 997-1004 [Abstract] [Full Text]
Brendel, C., Schoonjans, K., Botrugno, O. A., Treuter, E., Auwerx, J. (2002). The Small Heterodimer Partner Interacts with the Liver X Receptor {alpha} and Represses Its Transcriptional Activity. Mol. Endocrinol. 16: 2065-2076 [Abstract] [Full Text]
Amemiya-Kudo, M., Shimano, H., Hasty, A. H., Yahagi, N., Yoshikawa, T., Matsuzaka, T., Okazaki, H., Tamura, Y., Iizuka, Y., Ohashi, K., Osuga, J.-i., Harada, K., Gotoda, T., Sato, R., Kimura, S., Ishibashi, S., Yamada, N. (2002). Transcriptional activities of nuclear SREBP-1a, -1c, and -2 to different target promoters of lipogenic and cholesterogenic genes. J. Lipid Res. 43: 1220-1235 [Abstract] [Full Text]
Menke, J. G., Macnaul, K. L., Hayes, N. S., Baffic, J., Chao, Y.-S., Elbrecht, A., Kelly, L. J., Lam, M.-H., Schmidt, A., Sahoo, S., Wang, J., Wright, S. D., Xin, P., Zhou, G., Moller, D. E., Sparrow, C. P. (2002). A Novel Liver X Receptor Agonist Establishes Species Differences in the Regulation of Cholesterol 7{alpha}-Hydroxylase (CYP7a). Endocrinology 143: 2548-2558 [Abstract] [Full Text]
Matsuzaka, T., Shimano, H., Yahagi, N., Yoshikawa, T., Amemiya-Kudo, M., Hasty, A. H., Okazaki, H., Tamura, Y., Iizuka, Y., Ohashi, K., Osuga, J.-i., Takahashi, A., Yato, S., Sone, H., Ishibashi, S., Yamada, N. (2002). Cloning and characterization of a mammalian fatty acyl-CoA elongase as a lipogenic enzyme regulated by SREBPs. J. Lipid Res. 43: 911-920 [Abstract] [Full Text]
Joseph, S. B., McKilligin, E., Pei, L., Watson, M. A., Collins, A. R., Laffitte, B. A., Chen, M., Noh, G., Goodman, J., Hagger, G. N., Tran, J., Tippin, T. K., Wang, X., Lusis, A. J., Hsueh, W. A., Law, R. E., Collins, J. L., Willson, T. M., Tontonoz, P. (2002). Synthetic LXR ligand inhibits the development of atherosclerosis in mice. Proc. Natl. Acad. Sci. USA 99: 7604-7609 [Abstract] [Full Text]
Repa, J. J., Berge, K. E., Pomajzl, C., Richardson, J. A., Hobbs, H., Mangelsdorf, D. J. (2002). Regulation of ATP-binding Cassette Sterol Transporters ABCG5 and ABCG8 by the Liver X Receptors alpha and beta. J. Biol. Chem. 277: 18793-18800 [Abstract] [Full Text]
Zhang, Y., Mangelsdorf, D. J. (2002). LuXuRies of Lipid Homeostasis: The Unity of Nuclear Hormone Receptors, Transcription Regulation, and Cholesterol Sensing. Mol. Interv. 2: 78-87 [Abstract] [Full Text]
Joseph, S. B., Laffitte, B. A., Patel, P. H., Watson, M. A., Matsukuma, K. E., Walczak, R., Collins, J. L., Osborne, T. F., Tontonoz, P. (2002). Direct and Indirect Mechanisms for Regulation of Fatty Acid Synthase Gene Expression by Liver X Receptors. J. Biol. Chem. 277: 11019-11025 [Abstract] [Full Text]
Tobin, K. A. R., Ulven, S. M., Schuster, G. U., Steineger, H. H., Andresen, S. M., Gustafsson, J.-A., Nebb, H. I. (2002). Liver X Receptors as Insulin-mediating Factors in Fatty Acid and Cholesterol Biosynthesis. J. Biol. Chem. 277: 10691-10697 [Abstract] [Full Text]
del Castillo-Olivares, A., Gil, G. (2002). Differential Effects of Sterol Regulatory Binding Proteins 1 and 2 on Sterol 12alpha -Hydroxylase. SREBP-2 SUPPRESSES THE STEROL 12alpha -HYDROXYLASE PROMOTER. J. Biol. Chem. 277: 6750-6757 [Abstract] [Full Text]
Yang, X.-P., Freeman, L. A., Knapper, C. L., Amar, M. J. A., Remaley, A., Brewer, H. B. Jr., Santamarina-Fojo, S. (2002). The E-box motif in the proximal ABCA1 promoter mediates transcriptional repression of the ABCA1 gene. J. Lipid Res. 43: 297-306 [Abstract] [Full Text]
Edwards, P. A., Kast, H. R., Anisfeld, A. M. (2002). BAREing it all: the adoption of LXR and FXR and their roles in lipid homeostasis. J. Lipid Res. 43: 2-12 [Abstract] [Full Text]
Matsuzaka, T., Shimano, H., Yahagi, N., Amemiya-Kudo, M., Yoshikawa, T., Hasty, A. H., Tamura, Y., Osuga, J.-i., Okazaki, H., Iizuka, Y., Takahashi, A., Sone, H., Gotoda, T., Ishibashi, S., Yamada, N. (2002). Dual regulation of mouse {Delta}5- and {Delta}6-desaturase gene expression by SREBP-1 and PPAR{alpha}. J. Lipid Res. 43: 107-114 [Abstract] [Full Text]
Fu, X., Menke, J. G., Chen, Y., Zhou, G., MacNaul, K. L., Wright, S. D., Sparrow, C. P., Lund, E. G. (2001). 27-Hydroxycholesterol Is an Endogenous Ligand for Liver X Receptor in Cholesterol-loaded Cells. J. Biol. Chem. 276: 38378-38387 [Abstract] [Full Text]
Yoshikawa, T., Shimano, H., Yahagi, N., Ide, T., Amemiya-Kudo, M., Matsuzaka, T., Nakakuki, M., Tomita, S., Okazaki, H., Tamura, Y., Iizuka, Y., Ohashi, K., Takahashi, A., Sone, H., Osuga, J.-i., Gotoda, T., Ishibashi, S., Yamada, N. (2002). Polyunsaturated Fatty Acids Suppress Sterol Regulatory Element-binding Protein 1c Promoter Activity by Inhibition of Liver X Receptor (LXR) Binding to LXR Response Elements. J. Biol. Chem. 277: 1705-1711 [Abstract] [Full Text]

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