Hypoxia-inducible factor 1α activates insulin-induced gene 2 (Insig-2) transcription for degradation of 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase in the liver

Journal of Biological Chemistry

Volumn 292, Issue 22, 2017, Pages 9382-9393

  Hwang, Seonghwan ^a   Nguyen, Andrew D ^a   Jo, Youngah ^a   Engelking, Luke J ^a   Brugarolas, James ^b   DeBose Boyd, Russell A ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; BIOSYNTHESIS; CELL CULTURE; CELL MEMBRANES; CHOLESTEROL; GENES; OXYGEN; PROTEINS;

CHOLESTEROL SYNTHESIS; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATIONS; ENDOPLASMIC RETICULUM MEMBRANES; HMG-COA REDUCTASE; HYPOXIA INDUCIBLE FACTOR 1-ALPHA; OXYGEN CONSUMPTION; OXYGEN DEPRIVATION; RATE-LIMITING ENZYMES;

TRANSCRIPTION;

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INSIG 2 PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; STEROL; UNCLASSIFIED DRUG; HIF1A PROTEIN, HUMAN; HIF1A PROTEIN, MOUSE; HMGCR PROTEIN, HUMAN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INSIG2 PROTEIN, HUMAN; INSIG2 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL GROWTH; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME DEGRADATION; FEEDBACK SYSTEM; FIBROBLAST; GENE; HUMAN; HUMAN CELL; HYPOXIA; INSIG 2 GENE; LIVER; LIVER LEVEL; MALE; MOUSE; MOUSE MODEL; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE; UBIQUITINATION; ANIMAL; BIOSYNTHESIS; CELL HYPOXIA; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN DEGRADATION; TRANSFORMED CELL LINE;

ANIMALS; CELL HYPOXIA; CELL LINE, TRANSFORMED; FIBROBLASTS; HUMANS; HYDROXYMETHYLGLUTARYL COA REDUCTASES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER; MEMBRANE PROTEINS; MICE; PROTEOLYSIS; TRANSCRIPTION, GENETIC;

EID: 85020299178     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M117.788562     Document Type: Article

References (42)

1. Goldstein, J. L., DeBose-Boyd, R. A., and Brown, M. S. (2006) Protein sensors for membrane sterols. Cell 124, 35-46
2. Sever, N., Song, B. L., Yabe, D., Goldstein, J. L., Brown, M. S., and DeBose-Boyd, R. A. (2003) Insig-dependent ubiquitination and degradation of mammalian 3-hydroxy-3-methylglutaryl-CoA reductase stimulated by sterols and geranylgeraniol. J. Biol. Chem. 278, 52479-52490
3. Sever, N., Yang, T., Brown, M. S., Goldstein, J. L., and DeBose-Boyd, R. A. (2003) Accelerated degradation of HMG CoA reductase mediated by binding of insig-1 to its sterol-sensing domain. Mol. Cell 11, 25-33
4. Song, B. L., Javitt, N. B., and DeBose-Boyd, R. A. (2005) Insig-mediated degradation ofHMGCoA reductase stimulated by lanosterol, an intermediate in the synthesis of cholesterol. Cell Metab. 1, 179-189
5. Nguyen, A. D., Lee, S. H., and DeBose-Boyd, R. A. (2009) Insig-mediated, sterol-Accelerated degradation of the membrane domain of hamster 3-hydroxy-3-methylglutaryl-coenzyme A reductase in insect cells. J. Biol. Chem. 284, 26778-26788
6. Lange, Y., Ory, D. S., Ye, J., Lanier, M. H., Hsu, F. F., and Steck, T. L. (2008) Effectors of rapid homeostatic responses of endoplasmic reticulum cholesterol and 3-hydroxy-3-methylglutaryl-CoA reductase. J. Biol. Chem. 283, 1445-1455
7. Song, B. L., Sever, N., and DeBose-Boyd, R. A. (2005) Gp78, a membraneanchored ubiquitin ligase, associates with Insig-1 and couples sterol-regulated ubiquitination to degradation of HMG CoA reductase. Mol. Cell 19, 829-840
8. Jo, Y., Lee, P. C., Sguigna, P. V., and DeBose-Boyd, R. A. (2011) Sterolinduced degradation ofHMGCoA reductase depends on interplay of two Insigs and two ubiquitin ligases, gp78 and Trc8. Proc. Natl. Acad. Sci. U.S.A. 108, 20503-20508
9. Morris, L. L., Hartman, I. Z., Jun, D. J., Seemann, J., and DeBose-Boyd, R. A. (2014) Sequential actions of the AAA-ATPase valosin-containing protein (VCP)/p97 and the proteasome 19 S regulatory particle in sterol-Accelerated, endoplasmic reticulum (ER)-Associated degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J. Biol. Chem. 289, 19053-19066
10. Horton, J. D., Shah, N. A., Warrington, J. A., Anderson, N. N., Park, S. W., Brown, M. S., and Goldstein, J. L. (2003) Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. U.S.A. 100, 12027-12032
11. Yang, T., Espenshade, P. J., Wright, M. E., Yabe, D., Gong, Y., Aebersold, R., Goldstein, J. L., and Brown, M. S. (2002) Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 110, 489-500
12. Yabe, D., Brown, M. S., and Goldstein, J. L. (2002) Insig-2, a second endoplasmic reticulum protein that binds SCAP and blocks export of sterol regulatory element-binding proteins. Proc. Natl. Acad. Sci. U.S.A. 99, 12753-12758
13. Feramisco, J. D., Goldstein, J. L., and Brown, M. S. (2004) Membrane topology of human insig-1, a protein regulator of lipid synthesis. J. Biol. Chem. 279, 8487-8496
14. Yabe, D., Komuro, R., Liang, G., Goldstein, J. L., and Brown, M. S. (2003) Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis. Proc. Natl. Acad. Sci. U.S.A. 100, 3155-3160
15. Summons, R. E., Bradley, A. S., Jahnke, L. L., and Waldbauer, J. R. (2006) Steroids, triterpenoids and molecular oxygen. Philos. Trans. R. Soc. Lond B. Biol. Sci. 361, 951-968
16. Bloch, K. (1952) Biological synthesis of cholesterol. Harvey Lect. 48, 68-88
17. Nguyen, A. D., McDonald, J. G., Bruick, R. K., and DeBose-Boyd, R. A. (2007) Hypoxia stimulates degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase through accumulation of lanosterol and hypoxia-inducible factor-mediated induction of insigs. J. Biol. Chem. 282, 27436-27446
18. Semenza, G. L. (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148, 399-408
19. Kaelin, W. G., Jr., and Ratcliffe, P. J. (2008) Oxygen sensing by metazoans: The central role of the HIF hydroxylase pathway. Mol. Cell 30, 393-402
20. Wenger, R. H., Stiehl, D. P., and Camenisch, G. (2005) Integration of oxygen signaling at the consensus HRE. Sci. STKE 2005, re12
21. Jaakkola, P., Mole, D. R., Tian, Y. M., Wilson, M. I., Gielbert, J., Gaskell, S. J., von Kriegsheim, A., Hebestreit, H. F., Mukherji, M., Schofield, C. J., Maxwell, P. H., Pugh, C. W., and Ratcliffe, P. J. (2001) Targeting of HIF-To the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292, 468-472
22. Haase, V. H., Glickman, J. N., Socolovsky, M., and Jaenisch, R. (2001) Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 98, 1583-1588
23. Hwang, S., Hartman, I. Z., Calhoun, L. N., Garland, K., Young, G. A., Mitsche, M. A., McDonald, J., Xu, F., Engelking, L., and DeBose-Boyd, R. A. (2016) Contribution of accelerated degradation to feedback regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase and cholesterol metabolism in the liver. J. Biol. Chem. 291, 13479-13494
24. Firth, J. D., Ebert, B. L., Pugh, C. W., and Ratcliffe, P. J. (1994) Oxygenregulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3 enhancer 115. Proc. Natl. Acad. Sci. U.S.A. 91, 6496-6500
25. Wang, G. L., and Semenza, G. L. (1993) Characterization of hypoxiainducible factor 1 and regulation of DNA binding activity by hypoxia. J. Biol. Chem. 268, 21513-21518
26. Fernández-Alvarez, A., Soledad Alvarez, M., Cucarella, C., and Casado, M. (2010) Characterization of the human insulin-induced gene 2 (INSIG2) promoter: The role of Ets-binding motifs. J. Biol. Chem. 285, 11765-11774
27. Zhu, J., Jiang, X., and Chehab, F. F. (2014) FoxO4 interacts with the sterol regulatory factor SREBP2 and the hypoxia inducible factor HIF2-At the CYP51 promoter. J. Lipid Res. 55, 431-442
28. Dolt, K. S., Karar, J., Mishra, M. K., Salim, J., Kumar, R., Grover, S. K., and Qadar Pasha, M. A. (2007) Transcriptional downregulation of sterol metabolism genes in murine liver exposed to acute hypobaric hypoxia. Biochem. Biophys. Res. Comm. 354, 148-153
29. Drabkin, H. A., and Gemmill, R. M. (2012) Cholesterol and the development of clear-cell renal carcinoma. Curr. Opin. Pharmacol. 12, 742-750
30. Gebhard, R. L., Clayman, R. V., Prigge, W. F., Figenshau, R., Staley, N. A., Reesey, C., and Bear, A. (1987) Abnormal cholesterol metabolism in renal clear cell carcinoma. J. Lipid Res. 28, 1177-1184
31. Tugnoli, V., Trinchero, A., and Tosi, M. R. (2004) Evaluation of the lipid composition of human healthy and neoplastic renal tissues. Ital. J. Biochem. 53, 169-182
32. Yang, H., Minamishima, Y. A., Yan, Q., Schlisio, S., Ebert, B. L., Zhang, X., Zhang, L., Kim, W. Y., Olumi, A. F., and Kaelin, W. G., Jr. (2007)pVHLacts as an adaptor to promote the inhibitory phosphorylation of the NF-B agonist Card9 by CK2. Mol. Cell 28, 15-27
33. Gruenbacher, G., and Thurnher, M. (2015) Mevalonate metabolism in cancer. Cancer Lett. 356, 192-196
34. Russell, D. W., Schneider, W. J., Yamamoto, T., Luskey, K. L., Brown, M. S., and Goldstein, J. L. (1984) Domain map of the LDL receptor: sequence homology with the epidermal growth factor precursor. Cell 37, 577-585
35. Liang, G., Yang, J., Horton, J. D., Hammer, R. E., Goldstein, J. L., and Brown, M. S. (2002) Diminished hepatic response to fasting/refeeding and liver X receptor agonists in mice with selective deficiency of sterol regulatory element-binding protein-1c. J. Biol. Chem. 277, 9520-9528
36. Engelking, L. J., Liang, G., Hammer, R. E., Takaishi, K., Kuriyama, H., Evers, B. M., Li, W. P., Horton, J. D., Goldstein, J. L., and Brown, M. S. (2005) Schoenheimer effect explained: feedback regulation of cholesterol synthesis in mice mediated by Insig proteins. J. Clin. Invest. 115, 2489-2498
37. Jo, Y., Hartman, I. Z., and DeBose-Boyd, R. A. (2013) Ancient ubiquitous protein-1 mediates sterol-induced ubiquitination of 3-hydroxy-3-methylglutaryl CoA reductase in lipid droplet-Associated endoplasmic reticulum membranes. Mol. Biol. Cell 24, 169-183
38. Liscum, L., Luskey, K. L., Chin, D. J., Ho, Y. K., Goldstein, J. L., and Brown, M. S. (1983) Regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase and its mRNA in rat liver as studied with a monoclonal antibody and a cDNA probe. J. Biol. Chem. 258, 8450-8455
39. McFarlane, M. R., Liang, G., and Engelking, L. J. (2014) Insig proteins mediate feedback inhibition of cholesterol synthesis in the intestine. J. Biol. Chem. 289, 2148-2156
40. Schofield, C. J., and Ratcliffe, P. J. (2004) Oxygen sensing by HIF hydroxylase. Nat. Rev. Mol. Cell Biol. 5, 343-354
41. Semenza, G. L. (2004) Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19, 176-182
42. Mitsche, M. A., McDonald, J. G., Hobbs, H. H., and Cohen, J. C. (2015) Flux analysis of cholesterol biosynthesis in vivo reveals multiple tissue and cell-Type specific pathways. eLife 4, e07999