Insig-mediated degradation of HMG CoA reductase stimulated by lanosterol, an intermediate in the synthesis of cholesterol

Cell Metabolism

Volumn 1, Issue 3, 2005, Pages 179-189

  Song, Bao Liang ^a   Javitt, Norman B ^b   DeBose Boyd, Russell A ^a  

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

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INSIG PROTEIN; LANOSTEROL; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG; INSIG1 PROTEIN, HUMAN; INSIG2 PROTEIN, HUMAN; MEMBRANE PROTEIN; SIGNAL PEPTIDE; SREBP CLEAVAGE ACTIVATING PROTEIN; SREBP CLEAVAGE-ACTIVATING PROTEIN; UBIQUITIN;

ARTICLE; CELL CULTURE; CELL FRACTIONATION; CELL MEMBRANE PERMEABILITY; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME BINDING; ENZYME DEGRADATION; ENZYME INHIBITION; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; UBIQUITINATION; BIOSYNTHESIS; CELL LINE; FIBROBLAST; METABOLISM; STRUCTURE ACTIVITY RELATION;

CELL LINE, TRANSFORMED; CHOLESTEROL; ENDOPLASMIC RETICULUM; FEEDBACK, BIOCHEMICAL; FIBROBLASTS; HUMANS; HYDROXYMETHYLGLUTARYL COA REDUCTASES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LANOSTEROL; MEMBRANE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; UBIQUITIN;

EID: 18544378347     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2005.01.001     Document Type: Article

References (44)

1. Adams C.M., Goldstein J.L., and Brown M.S. Cholesterol-induced conformational change in SCAP enhanced by Insig proteins and mimicked by cationic amphiphiles. Proc. Natl. Acad. Sci. USA 100 (2003) 10647-10652
2. Adams C.M., Reitz J., De Brabander J.K., Feramisco J.D., Li L., Brown M.S., and Goldstein J.L. Cholesterol and 25-hydroxycholesterol inhibit activation of SREBPs by different mechanisms, both involving SCAP and Insigs. J. Biol. Chem. 279 (2004) 52772-52780
3. Brown M.S., and Goldstein J.L. Multivalent feedback regulation of HMG CoA reductase, a control mechanism coordinating isoprenoid synthesis and cell growth. J. Lipid Res. 21 (1980) 505-517
4. Brown M.S., and Goldstein J.L. A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. USA 96 (1999) 11041-11048
5. Brown M.S., Faust J.R., and Goldstein J.L. Induction of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity in human fibroblasts incubated with compactin (ML-236B), a competitive inhibitor of the reductase. J. Biol. Chem. 253 (1978) 1121-1128
6. Brown A.J., Sun L., Feramisco J.D., Brown M.S., and Goldstein J.L. Cholesterol addition to ER membranes alters conformation of SCAP, the SREBP escort protein that regulates cholesterol metabolism. Mol. Cell 10 (2002) 237-245
7. Camps L., Coll J., and Parente A. Selenium dioxide oxidation of substrates with acid labile groups. Synthesis (Mass.) 3 (1978) 215-216
8. Chen H.W., Leonard D.A., Fischer R.T., and Trzaskos J.M. A mammalian mutant cell lacking detectable lanosterol 14 alpha-methyl demethylase activity. J. Biol. Chem. 263 (1988) 1248-1254
9. DeBose-Boyd R.A., Brown M.S., Li W.P., Nohturfft A., Goldstein J.L., and Espenshade P.J. Transport-dependent proteolysis of SREBP: relocation of site-1 protease from Golgi to ER obviates the need for SREBP transport to Golgi. Cell 99 (1999) 703-712
10. Frye L.L., Cusack K.P., Leonard D.A., and Anderson J.A. Oxolanosterol oximes: dual-action inhibitors of cholesterol biosynthesis. J. Lipid Res. 35 (1994) 1333-1344
11. Gaylor J.L. Membrane-bound enzymes of cholesterol synthesis from lanosterol. Biochem. Biophys. Res. Commun. 292 (2002) 1139-1146
12. Gil G., Faust J.R., Chin D.J., Goldstein J.L., and Brown M.S. Membrane-bound domain of HMG CoA reductase is required for sterol-enhanced degradation of the enzyme. Cell 41 (1985) 249-258
13. Goldstein J.L., and Brown M.S. Regulation of the mevalonate pathway. Nature 343 (1990) 425-430
14. Goldstein J.L., Basu S.K., and Brown M.S. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98 (1983) 241-260
15. Grundy S.M., Cleeman J.I., Bairey Merz C.N., Brewer J., Clark L.T., Hunninghake D.B., Pasternak R.C., and Smith J. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III Guidelines. J. Am. Coll. Cardiol. 44 (2004) 720-732
16. Heart Protection Study Collaborative Group. MRC/BHF Heart Protection Study of cholesterol lowering with simvastatin in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet 360 (2002) 7-22
17. Hershko A., and Rose I.A. Ubiquitin-aldehyde: a general inhibitor of ubiquitin-recycling processes. Proc. Natl. Acad. Sci. USA 84 (1987) 1829-1833
18. Johnston N.L., and Cohen R.E. Uncoupling ubiquitin-protein conjugation from ubiquitin-dependent proteolysis by use of beta, gamma-nonhydrolyzable ATP analogues 2. Biochemistry 30 (1991) 7514-7522
19. Kita T., Brown M.S., and Goldstein J.L. Feedback regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase in livers of mice treated with mevinolin, a competitive inhibitor of the reductase. J. Clin. Invest. 66 (1980) 1094-1100
20. Leonard D.A., Kotarski M.A., Tessiatore J.E., Favata M.F., and Trzaskos J.M. Post-transcriptional regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase by 3 beta-hydroxy-lanost-8-en-32-al, an intermediate in the conversion of lanosterol to cholesterol. Arch. Biochem. Biophys. 310 (1994) 152-157
21. Liscum L., Luskey K.L., Chin D.J., Ho Y.K., Goldstein J.L., and Brown M.S. 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 (1983) 8450-8455
22. Liscum L., Finer-Moore J., Stroud R.M., Luskey K.L., Brown M.S., and Goldstein J.L. Domain structure of 3-hydroxy-3-methylglutaryl coenzyme A reductase, a glycoprotein of the endoplasmic reticulum. J. Biol. Chem. 260 (1985) 522-530
23. Miao L., Nielsen M., Thewalt J., Ipsen J.H., Bloom M., Zuckermann M.J., and Mouritsen O.G. From lanosterol to cholesterol: structural evolution and differential effects on lipid bilayers. Biophys. J. 82 (2002) 1429-1444
24. Nohturfft A., Brown M.S., and Goldstein J.L. Topology of SREBP cleavage-activating protein, a polytopic membrane protein with a sterol-sensing domain. J. Biol. Chem. 273 (1998) 17243-17250
25. Nohturfft A., Yabe D., Goldstein J.L., Brown M.S., and Espenshade P.J. Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes. Cell 102 (2000) 315-323
26. Pickart C.M., Kasperek E.M., Beal R., and Kim A. Substrate properties of site-specific mutant ubiquitin protein (G76A) reveal unexpected mechanistic features of ubiquitin-activating enzyme (E1). J. Biol. Chem. 269 (1994) 7115-7123
27. Pikuleva I., and Javitt N.B. Novel sterols synthesized via the CYP27A1 metabolic pathway. Arch. Biochem. Biophys. 420 (2003) 35-39
28. Radhakrishnan A., Sun L.P., Kwon H.J., Brown M.S., and Goldstein J.L. Direct binding of cholesterol to the purified membrane region of SCAP: Mechanism for a sterol-sensing domain. Mol. Cell 15 (2004) 259-268
29. Ravid T., Doolman R., Avner R., Harats D., and Roitelman J. The ubiquitin-proteasome pathway mediates the regulated degradation of mammalian 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J. Biol. Chem. 275 (2000) 35840-35847
30. Roitelman J., Olender E.H., Bar-Nun S., Dunn Jr. W.A., and Simoni R.D. Immunological evidence for eight spans in the membrane domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for enzyme degradation in the endoplasmic reticulum. J. Cell Biol. 117 (1992) 959-973
31. Sato R., Goldstein J.L., and Brown M.S. Replacement of serine-871 of hamster 3-hydroxy-3-methylglutaryl-CoA reductase prevents phosphorylation by AMP-activated kinase and blocks inhibition of sterol synthesis induced by ATP depletion. Proc. Natl. Acad. Sci. USA 90 (1993) 9261-9265
32. Scandinavian Simvastatin Study Group. Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). Lancet 344 (1994) 1383-1389
33. Sever N., Song B.L., Yabe D., Goldstein J.L., Brown M.S., and DeBose-Boyd R.A. Insig-dependent ubiquitination and degradation of mammalian 3-hydroxy-3-methylglutaryl-CoA reductase stimulated by sterols and geranylgeraniol. J. Biol. Chem. 278 (2003) 52479-52490
34. Sever N., Yang T., Brown M.S., Goldstein J.L., and DeBose-Boyd R.A. Accelerated degradation of HMG CoA reductase mediated by binding of insig-1 to its sterol-sensing domain. Mol. Cell 11 (2003) 25-33
35. Sever N., Lee P.C.W., Song B.L., Rawson R.B., and DeBose-Boyd R.A. Isolation of mutant cells lacking Insig-1 through selection with SR-12813, an agent that stimulates degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J. Biol. Chem. 279 (2004) 43136-43147
36. Singer I.I., Kawka D.W., Kazazis D.M., Alberts A.W., Chen J.S., Huff J.W., and Ness G.C. Hydroxymethylglutaryl-coenzyme A reductase-containing hepatocytes are distributed periportally in normal and mevinolin-treated rat livers. Proc. Natl. Acad. Sci. USA 81 (1984) 5556-5560
37. Smondyrev A.M., and Berkowitz M.L. Molecular dynamics simulation of the structure of dimyristoylphosphatidylcholine bilayers with cholesterol, ergosterol, and lanosterol. Biophys. J. 80 (2001) 1649-1658
38. Song B.L., and DeBose-Boyd R.A. Ubiquitination of 3-hydroxy-3-methylglutaryl-CoA reductase in permeabilized cells mediated by cytosolic E1 and a putative membrane-bound ubiquitin ligase. J. Biol. Chem. 279 (2004) 28798-28806
39. Spence J.T., and Gaylor J.L. Investigation of regulation of microsomal hydroxymethylglutaryl coenzyme A reductase and methyl sterol oxidase of cholesterol biosynthesis. J. Biol. Chem. 252 (1977) 5852-5858
40. Trzaskos J.M. Oxylanosterols as modifiers of cholesterol biosynthesis. Prog. Lipid Res. 34 (1995) 99-116
41. Williams M.T., Gaylor J.L., and Morris H.P. Investigation of the rate-determining microsomal reaction of cholesterol biosynthesis from lanosterol in Morris hepatomas and liver. Cancer Res. 37 (1977) 1377-1383
42. Yabe D., Brown M.S., and Goldstein J.L. Insig-2, a second endoplasmic reticulum protein that binds SCAP and blocks export of sterol regulatory element-binding proteins. Proc. Natl. Acad. Sci. USA 99 (2002) 12753-12758
43. Yamamoto T., Davis C.G., Brown M.S., Schneider W.J., Casey M.L., Goldstein J.L., and Russell D.W. The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 39 (1984) 27-38
44. Yang T., Espenshade P.J., Wright M.E., Yabe D., Gong Y., Aebersold R., Goldstein J.L., and Brown M.S. 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 (2002) 489-500