Rapid proteasomal elimination of 3-hydroxy-3-methylglutaryl-CoA reductase by interferon-γ in primary macrophages requires endogenous 25-hydroxycholesterol synthesis

Steroids

Volumn 99, Issue PB, 2015, Pages 219-229

  Lu, Hongjin ^a   Talbot, Simon ^a   Robertson, Kevin A ^a   Watterson, Steven ^b   Forster, Thorsten ^a   Roy, Douglas ^a   Ghazal, Peter ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

25 Hydroxycholesterol; CH25H; Cholesterol biosynthesis; Immunity; Infection; Macrophages

Indexed keywords

25 HYDROXYCHOLESTEROL; ACTIVATING TRANSCRIPTION FACTOR 3; GAMMA INTERFERON; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; PROTEASOME; 25-HYDROXYCHOLESTEROL; ATF3 PROTEIN, MOUSE; CHOLESTEROL 25-HYDROXYLASE; CHOLESTEROL DERIVATIVE; MESSENGER RNA; RNA; STEROID MONOOXYGENASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ANIMAL CELL; ARTICLE; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVATION; MACROPHAGE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETIC TRANSCRIPTION; GENETICS; KINETICS; METABOLISM; PROTEOMICS; TIME FACTOR;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; HYDROXYCHOLESTEROLS; HYDROXYMETHYLGLUTARYL COA REDUCTASES; INTERFERON-GAMMA; KINETICS; MACROPHAGES; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; PROTEOMICS; RNA; RNA, MESSENGER; STEROID HYDROXYLASES; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84937422325     PISSN: 0039128X     EISSN: 18785867     Source Type: Journal    
DOI: 10.1016/j.steroids.2015.02.022     Document Type: Article

References (56)

1. M.S. Brown, and J.L. Goldstein Multivalent feedback regulation of HMG CoA reductase, a control mechanism coordinating isoprenoid synthesis and cell growth J Lipid Res 21 5 1980 505 517
2. J.L. Goldstein, and M.S. Brown Regulation of the mevalonate pathway Nature 343 6257 1990 425 430
3. M.S. Brown, and J.L. Goldstein The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor Cell 89 3 1997 331 340
4. J.L. Goldstein, R.A. DeBose-Boyd, and M.S. Brown Protein sensors for membrane sterols Cell 124 1 2006 35 46
5. R.A. DeBose-Boyd Feedback regulation of cholesterol synthesis: sterol-accelerated ubiquitination and degradation of HMG CoA reductase Cell Res 18 6 2008 609 621
6. T. Yang, P.J. Espenshade, M.E. Wright, D. Yabe, and Y. Gong 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 4 2002 489 500
7. C.M. Adams, J.L. Goldstein, and M.S. Brown Cholesterol-induced conformational change in SCAP enhanced by Insig proteins and mimicked by cationic amphiphiles Proc Natl Acad Sci 100 19 2003 10647 10652
8. A. Radhakrishnan, L.-P. Sun, H.J. Kwon, M.S. Brown, and J.L. Goldstein Direct binding of cholesterol to the purified membrane region of SCAP mechanism for a sterol-sensing domain Mol Cell 15 2 2004 259 268
9. L.-P. Sun, L. Li, J.L. Goldstein, and M.S. Brown Insig required for sterol-mediated inhibition of Scap/SREBP binding to COPII proteins in vitro J Biol Chem 280 28 2005 26483 26490
10. X. Hua, A. Nohturfft, J.L. Goldstein, and M.S. Brown Sterol Resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein Cell 87 3 1996 415 426
11. P.J. Espenshade, D. Cheng, J.L. Goldstein, and M.S. Brown Autocatalytic processing of site-1 protease removes propeptide and permits cleavage of sterol regulatory element-binding proteins J Biol Chem 274 32 1999 22795 22804
12. N.G. Zelenski, R.B. Rawson, M.S. Brown, and J.L. Goldstein Membrane topology of S2P, a protein required for intramembranous cleavage of sterol regulatory element-binding proteins J Biol Chem 274 31 1999 21973 21980
13. A. Nohturfft, D. Yabe, J.L. Goldstein, M.S. Brown, and P.J. Espenshade Regulated step in cholesterol feedback localized to budding of SCAP from ER membranes Cell 102 3 2000 315 323
14. T. Yang, J.L. Goldstein, and M.S. Brown Overexpression of membrane domain of SCAP prevents sterols from inhibiting SCAP. SREBP exit from endoplasmic reticulum J Biol Chem 275 38 2000 29881 29886
15. P. Edwards Regulation of gene expression by SREBP and SCAP Biochim Biophys Acta 1529 1-3 2000 103 113
16. T. Ravid, R. Doolman, R. Avner, D. Harats, and J. Roitelman The ubiquitin-proteasome pathway mediates the regulated degradation of mammalian 3-hydroxy-3-methylglutaryl-coenzyme A reductase J Biol Chem 275 46 2000 35840 35847
17. B.-L. Song, and R.A. DeBose-Boyd 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 27 2004 28798 28806
18. Y.C. Tsai, G.S. Leichner, M.M.P. Pearce, G.L. Wilson, R.J.H. Wojcikiewicz, J. Roitelman, and A.M. Weissman Differential regulation of HMG-CoA reductase and Insig-1 by enzymes of the ubiquitin-proteasome system Mol Biol Cell 23 23 2012 4484 4494
19. G. Gil, J.R. Faust, D.J. Chin, J.L. Goldstein, and M.S. Brown Membrane-bound domain of HMG CoA reductase is required for sterol-enhanced degradation of the enzyme Cell 41 1 1985 249 258
20. J.R. Faust, K.L. Luskey, D.J. Chin, J.L. Goldstein, and M.S. Brown Regulation of synthesis and degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase by low density lipoprotein and 25-hydroxycholesterol in UT-1 cells Proc Natl Acad Sci 79 17 1982 5205 5209
21. N. Sever, T. Yang, M.S. Brown, J.L. Goldstein, and R.A. Debose-Boyd Accelerated degradation of HMG CoA reductase mediated by binding of Insig-1 to Its sterol-sensing domain Mol Cell 11 1 2003 25 33
22. M.S. Brown, and J.L. Goldstein Cholesterol feedback: from Schoenheimer's bottle to Scap's MELADL J Lipid Res 50 Supplement 2009 S15 S27
23. J.G. Cyster, E.V. Dang, A. Reboldi, and T. Yi 25-Hydroxycholesterols in innate and adaptive immunity Nat Rev Immunol 14 11 2014 731 743
24. M. Blanc, W.Y. Hsieh, K.A. Robertson, S. Watterson, G. Shui, P. Lacaze, and et al. Host defense against viral infection involves interferon mediated down-regulation of sterol biosynthesis PLoS Biol 9 3 2011 e1000598
25. J. Ecker, G. Liebisch, M. Englmaier, M. Grandl, H. Robenek, and G. Schmitz Induction of fatty acid synthesis is a key requirement for phagocytic differentiation of human monocytes. 107 17 2010 7817 7822
26. D.R. Bauman, A.D. Bitmansour, J.G. McDonald, B.M. Thompson, G. Liang, and D.W. Russell 25-Hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production Proc Natl Acad Sci 106 39 2009 16764 16769
27. A. Reboldi, E.V. Dang, J.G. McDonald, G. Liang, D.W. Russell, and J.G. Cyster Inflammation. 25-Hydroxycholesterol suppresses interleukin-1-driven inflammation downstream of type I interferon Science 345 6197 2014 679 684
28. E.S. Gold, A.H. Diercks, I. Podolsky, R.L. Podyminogin, P.S. Askovich, P.M. Treuting, and et al. 25-Hydroxycholesterol acts as an amplifier of inflammatory signaling Proc Natl Acad Sci USA 111 29 2014 10666 10671
29. K. Park, and A.L. Scott Cholesterol 25-hydroxylase production by dendritic cells and macrophages is regulated by type I interferons J Leukoc Biol 88 6 2010 1081 1087
30. M. Blanc, W.Y. Hsieh, K.A. Robertson, K.A. Kropp, T. Forster, G. Shui, and et al. The transcription factor STAT-1 couples macrophage synthesis of 25-Hydroxycholesterol to the interferon antiviral response Immunity 38 1 2013 106 118
31. S.-Y. Liu, R. Aliyari, K. Chikere, G. Li, M.D. Marsden, J.K. Smith, and et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol Immunity 38 1 2013 92 105
32. G. del Real Statins inhibit HIV-1 infection by down-regulating rho activity J Exp Med 200 4 2004 541 547
33. M. Ikeda, K.-I. Abe, M. Yamada, H. Dansako, K. Naka, and N. Kato Different anti-HCV profiles of statins and their potential for combination therapy with interferon Hepatology 44 1 2006 117 125
34. J. Peng, D. Zhang, Y. Ma, G. Wang, Z. Guo, and J. Lu Protective effect of fluvastatin on influenza virus infection Mol Med Rep 9 6 2014 2221 2226
35. B. Kwak, F. Mulhaupt, S. Myit, and F. Mach Statins as a newly recognized type of immunomodulator Nat Med 6 12 2000 1399 1402
36. L. Dolken, Z. Ruzsics, B. Radle, C.C. Friedel, R. Zimmer, J. Mages, and et al. High-resolution gene expression profiling for simultaneous kinetic - PubMed - NCBI RNA 14 9 2008 1959 1972
37. R.A. Irizarry, B.M. Bolstad, F. Collin, L.M. Cope, B. Hobbs, and T.P. Speed Summaries of Affymetrix GeneChip probe level data Nucleic Acids Res 31 4 2003 e15
38. A. Conesa, M.J. Nueda, A. Ferrer, and M. Talón maSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments Bioinformatics (Oxford, England) 22 9 2006 1096 1102
39. C.C. Friedel, L. Dölken, Z. Ruzsics, U.H. Koszinowski, and R. Zimmer Conserved principles of mammalian transcriptional regulation revealed by RNA half-life Nucleic Acids Res 37 17 2009 e115 e125
40. R Core Team R: a language and environment for statistical computing 2013 R Foundation for Statistical Computing Vienna, Austria http://www.R-project.org/
41. MATLAB, version 7.10.0, Natick, Massachusetts: The MathWorks Inc.; 2010.
42. N. Shibata, A.F. Carlin, N.J. Spann, K. Saijo, C.S. Morello, J.G. McDonald, and et al. 25-Hydroxycholesterol activates the integrated stress response to reprogram transcription and translation in macrophages J Biol Chem 288 50 2013 35812 35823
43. Lipopolysaccharide-induced expression of matrix metalloproteinases in human monocytes is suppressed by IFN-gamma via superinduction of ATF-3 and suppression of AP-1 J Imunol (Baltimore, MD: 1950) 181 7 2008 5089 5097
44. PIKfyve, a class III lipid kinase, is required for TLR-induced type I IFN production via modulation of ATF3 J Immunol (Baltimore, MD: 1950) 192 7 2014 3383 3389
45. E.S. Gold, S.A. Ramsey, M.J. Sartain, J. Selinummi, I. Podolsky, D.J. Rodriguez, and et al. ATF3 protects against atherosclerosis by suppressing 25-hydroxycholesterol-induced lipid body formation J Exp Med 209 4 2012 807 817
46. B.E. Drysdale, D.L. Howard, and R.J. Johnson Identification of a lipopolysaccharide inducible transcription factor in murine macrophages Mol Immunol 33 11-12 1996 989 998
47. M.W. Taylor, W.M. Grosse, J.E. Schaley, C. Sanda, X. Wu, S.-C. Chien, and et al. Global effect of PEG-IFN-alpha and ribavirin on gene expression in - PubMed - NCBI J Interferon Cytokine Res 24 2 2004 107 118
48. C.M. Rosenberger, A.E. Clark, P.M. Treuting, C.D. Johnson, and A. Aderem ATF3 regulates MCMV infection in mice by modulating IFN-gamma expre- PubMed - NCBI Proc Natl Acad Sci 105 7 2008 2544 2549
49. M. Gilchrist, V. Thorsson, B. Li, A.G. Rust, M. Korb, K. Kennedy, and et al. Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4 Nature 441 7090 2006 173 178
50. G.E. Stokker, W.F. Hoffman, A.W. Alberts, E.J. Cragoe, A.A. Deana, J.L. Gilfillan, and et al. 3-Hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors. I. Structural modification of 5-substituted 3,5-dihydroxypentanoic acids and their lactone derivatives J Med Chem 28 3 1985 347 358
51. B.D. Roth, C.J. Blankley, A.W. Chucholowski, E. Ferguson, M.L. Hoefle, D.F. Ortwine, and et al. Inhibitors of cholesterol biosynthesis. 3. Tetrahydro-4-hydroxy-6-[2-(1H-pyrrol-1-yl)ethyl]-2H-pyran 2-one inhibitors of HMG-CoA reductase. 2. Effects of introducing substituents at positions three and four of the pyrrole nucleus J Med Chem 34 1 1991 357 366
52. G.M. Coppola, R.E. Damon, H. Yu, R.G. Engstrom, and T.J. Scallen Design and biological evaluation of a series of thiophene-based 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibitors Bioorg Med Chem Lett 7 5 1997 549 554
53. S. Hosoda, D. Matsuda, H. Tomoda, M. Hashimoto, H. Aoyama, and Y. Hashimoto Application of a 3,3-diphenylpentane skeleton as a multi-template for creation of HMG-CoA reductase inhibitors Bioorg Med Chem Lett 19 15 2009 4228 4231
54. N. Le Novère, M. Hucka, H. Mi, S. Moodie, F. Schreiber, A. Sorokin, and et al. The systems biology graphical notation Nat Biotechnol 27 8 2009 735 741
55. P. Ghazal, J.C. González Armas, S. Kurz, and A. Angulo Viruses: hostages to the cell Virology 275 2 2000 233 237
56. A.A. Kandutsch, and H.W. Chen Inhibition of sterol synthesis in cultured mouse cells by cholesterol derivatives oxygenated in the side chain J Biol Chem 249 19 1974 6057 6061