Signaling regulates activity of DHCR24, the final enzyme in cholesterol synthesi[s]

Journal of Lipid Research

Volumn 55, Issue 3, 2014, Pages 410-420

  Luu, Winnie ^a   Zerenturk, Eser J ^a   Kristiana, Ika ^a   Bucknal, Martin P ^a   Sharpe, Laura J ^a   Brown, Andrew J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

3BETA HYDROXYSTEROL DELTA24 REDUCTASE; CHOLESTEROL; DESMOSTEROL; OXIDOREDUCTASE; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CHO CELL; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; MASS FRAGMENTOGRAPHY; MUTATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

3Β-HYDROXYSTEROL Δ24-REDUCTASE; BISINDOLYLMALEIMIDE I; DESMOSTEROL; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; PHOSPHORYLATION; PROTEIN KINASE C; REGULATION;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CHO CELLS; CHOLESTEROL; CRICETINAE; CRICETULUS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DESMOSTEROL; GENE EXPRESSION; HUMANS; INDOLES; ISOQUINOLINES; MUTATION; NERVE TISSUE PROTEINS; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SULFONAMIDES; TYROSINE;

EID: 84894720321     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M043257     Document Type: Article

References (64)

1. Waterham, H. R., J. Koster, G. J. Romeijn, R. C. Hennekam, P. Vreken, H. C. Andersson, D. R. FitzPatrick, R. I. Kelley, and R. J. Wanders. 2001. Mutations in the 3beta-hydroxysterol Delta24-reductase gene cause desmosterolosis, an autosomal recessive disorder of cholesterol biosynthesis. Am. J. Hum. Genet. 69: 685-694. (Pubitemid 32868514)
2. Finn, R. D., J. Mistry, J. Tate, P. Coggill, A. Heger, J. E. Pollington, O. L. Gavin, P. Gunasekaran, G. Ceric, K. Forslund, et al. 2010. The Pfam protein families database. Nucleic Acids Res. 38: D211-D222.
3. Mushegian, A. R., and E. V. Koonin. 1995. A putative FAD-binding domain in a distinct group of oxidases including a protein involved in plant development. Protein Sci. 4: 1243-1244.
4. Pedretti, A., E. Bocci, R. Maggi, and G. Vistoli. 2008. Homology modelling of human DHCR24 (seladin-1) and analysis of its binding properties through molecular docking and dynamics simulations. Steroids. 73: 708-719.
5. Crameri, A., E. Biondi, K. Kuehnle, D. Lutjohann, K. M. Thelen, S. Perga, C. G. Dotti, R. M. Nitsch, M. D. Ledesma, and M. H. Mohajeri. 2006. The role of seladin-1/DHCR24 in cholesterol biosynthesis, APP processing and Abeta generation in vivo. EMBO J. 25: 432-443. (Pubitemid 43152863)
6. Gilk, S. D., D. C. Cockrell, C. Luterbach, B. Hansen, L. A. Knodler, J. A. Ibarra, O. Steele-Mortimer, and R. A. Heinzen. 2013. Bacterial colonization of host cells in the absence of cholesterol. PLoS Pathog. 9: e1003107.
7. Jansen, M., V. M. Pietiaïnen, H. Pölönen, L. Rasilainen, M. Koivusalo, U. Ruotsalainen, E. Jokitalo, and E. Ikonen. 2008. Cholesterol substitution increases the structural heterogeneity of caveolae. J. Biol. Chem. 283: 14610-14618.
8. Kuehnle, K., A. Crameri, R. E. Kalin, P. Luciani, S. Benvenuti, A. Peri, F. Ratti, M. Rodolfo, L. Kulic, F. L. Heppner, et al. 2008. Prosurvival effect of DHCR24/Seladin-1 in acute and chronic responses to oxidative stress. Mol. Cell. Biol. 28: 539-550.
9. Wu, C., I. Miloslavskaya, S. Demontis, R. Maestro, and K. Galaktionov. 2004. Regulation of cellular response to oncogenic and oxidative stress by Seladin-1. Nature. 432: 640-645. (Pubitemid 39626272)
10. Greeve, I., I. Hermans-Borgmeyer, C. Brellinger, D. Kasper, T. Gomez-Isla, C. Behl, B. Levkau, and R. M. Nitsch. 2000. The human DIMINUTO/DWARF1 homolog seladin-1 confers resistance to Alzheimer's disease-associated neurodegeneration and oxidative stress. J. Neurosci. 20: 7345-7352.
11. Sarajärvi, T., A. Haapasalo, J. Viswanathan, P. Mäkinen, M. Laitinen, H. Soininen, and M. Hiltunen. 2009. Down-regulation of seladin-1 increases BACE1 levels and activity through enhanced GGA3 depletion during apoptosis. J. Biol. Chem. 284: 34433-34443.
12. Wu, B. J., K. Chen, S. Shrestha, K. L. Ong, P. J. Barter, and K. A. Rye. 2013. High-density lipoproteins inhibit vascular endothelial inflammation by increasing 3beta-hydroxysteroid-delta24 reductase expression and inducing heme oxygenase-1. Circ. Res. 112: 278-288.
13. McGrath, K. C., X. H. Li, R. Puranik, E. C. Liong, J. T. Tan, V. M. Dy, B. A. DiBartolo, P. J. Barter, K. A. Rye, and A. K. Heather. 2009. Role of 3beta-hydroxysteroid-delta 24 reductase in mediating antiinflammatory effects of high-density lipoproteins in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 29: 877-882.
14. Spann, N. J., L. X. Garmire, J. G. McDonald, D. S. Myers, S. B. Milne, N. Shibata, D. Reichart, J. N. Fox, I. Shaked, D. Heudobler, et al. 2012. Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell. 151: 138-152.
15. Battista, M. C., M. O. Guimond, C. Roberge, A. A. Doueik, L. Fazli, M. Gleave, R. Sabbagh, and N. Gallo-Payet. 2010. Inhibition of DHCR24/seladin-1 impairs cellular homeostasis in prostate cancer. Prostate. 70: 921-933.
16. Takano, T., K. Tsukiyama-Kohara, M. Hayashi, Y. Hirata, M. Satoh, Y. Tokunaga, C. Tateno, Y. Hayashi, T. Hishima, N. Funata, et al. 2011. Augmentation of DHCR24 expression by hepatitis C virus infection facilitates viral replication in hepatocytes. J. Hepatol. 55: 512-521.
17. Horvat, S., J. McWhir, and D. Rozman. 2011. Defects in cholesterol synthesis genes in mouse and in humans: lessons for drug development and safer treatments. Drug Metab. Rev. 43: 69-90.
18. FitzPatrick, D. R., J. W. Keeling, M. J. Evans, A. E. Kan, J. E. Bell, M. E. Porteous, K. Mills, R. M. Winter, and P. T. Clayton. 1998. Clinical phenotype of desmosterolosis. Am. J. Med. Genet. 75: 145-152. (Pubitemid 28034490)
19. Andersson, H. C., L. Kratz, and R. Kelley. 2002. Desmosterolosis presenting with multiple congenital anomalies and profound developmental delay. Am. J. Med. Genet. 113: 315-319. (Pubitemid 35416606)
20. Schaaf, C. P., J. Koster, P. Katsonis, L. Kratz, O. A. Shchelochkov, F. Scaglia, R. I. Kelley, O. Lichtarge, H. R. Waterham, and M. Shinawi. 2011. Desmosterolosis-phenotypic and molecular characterization of a third case and review of the literature. Am. J. Med. Genet. A. 155A: 1597-1604.
21. Zolotushko, J., H. Flusser, B. Markus, I. Shelef, Y. Langer, M. Heverin, I. Bjorkhem, S. Sivan, and O. S. Birk. 2011. The desmosterolosis phenotype: spasticity, microcephaly and micrognathia with agenesis of corpus callosum and loss of white matter. Eur. J. Hum. Genet. 19: 942-946.
22. Horton, J. D., N. A. Shah, J. A. Warrington, N. N. Anderson, S. W. Park, M. S. Brown, and J. L. Goldstein. 2003. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. USA. 100: 12027-12032. (Pubitemid 37271509)
23. Zerenturk, E. J., L. J. Sharpe, and A. J. Brown. 2012. Sterols regulate 3beta-hydroxysterol Delta24-reductase (DHCR24) via dual sterol regulatory elements: cooperative induction of key enzymes in lipid synthesis by Sterol Regulatory Element Binding Proteins. Biochim. Biophys. Acta. 1821: 1350-1360.
24. Bonaccorsi, L., P. Luciani, G. Nesi, E. Mannucci, C. Deledda, F. Dichiara, M. Paglierani, F. Rosati, L. Masieri, S. Serni, et al. 2008. Androgen receptor regulation of the seladin-1/DHCR24 gene: altered expression in prostate cancer. Lab. Invest. 88: 1049-1056.
25. Luciani, P., C. Deledda, F. Rosati, S. Benvenuti, I. Cellai, F. Dichiara, M. Morello, G. B. Vannelli, G. Danza, M. Serio, et al. 2008. Seladin-1 is a fundamental mediator of the neuroprotective effects of estrogen in human neuroblast long-term cell cultures. Endocrinology. 149: 4256-4266.
26. Battista, M. C., C. Roberge, A. Martinez, and N. Gallo-Payet. 2009. 24-dehydrocholesterol reductase/seladin-1: a key protein differentially involved in adrenocorticotropin effects observed in human and rat adrenal cortex. Endocrinology. 150: 4180-4190.
27. Ishida, E., K. Hashimoto, S. Okada, T. Satoh, M. Yamada, and M. Mori. 2013. Thyroid hormone receptor and liver X receptor competitively up-regulate human selective Alzheimer's disease indicator-1 gene expression at the transcriptional levels. Biochem. Biophys. Res. Commun. 432: 513-518.
28. Yoshinari, K., H. Ohno, S. Benoki, and Y. Yamazoe. 2012. Constitutive androstane receptor transactivates the hepatic expression of mouse Dhcr24 and human DHCR24 encoding a cholesterogenic enzyme 24-dehydrocholesterol reductase. Toxicol. Lett. 208: 185-191.
29. Drzewinska, J., A. Walczak-Drzewiecka, and M. Ratajewski. 2011. Identification and analysis of the promoter region of the human DHCR24 gene: involvement of DNA methylation and histone acetylation. Mol. Biol. Rep. 38: 1091-1101.
30. Zerenturk, E. J., I. Kristiana, S. Gill, and A. J. Brown. 2012. The endogenous regulator 24(S),25-epoxycholesterol inhibits cholesterol synthesis at DHCR24 (Seladin-1). Biochim. Biophys. Acta. 1821: 1269-1277.
31. Fernández, C., Y. Suárez, A. J. Ferruelo, D. Gómez-Coronado, and M. A. Lasunción. 2002. Inhibition of cholesterol biosynthesis by Delta22-unsaturated phytosterols via competitive inhibition of sterol Delta24-reductase in mammalian cells. Biochem. J. 366: 109-119. (Pubitemid 34971809)
32. Jansen, M., W. Wang, D. Greco, G. C. Bellenchi, U. di Porzio, A. J. Brown, and E. Ikonen. 2013. What dictates the accumulation of desmosterol in the developing brain? FASEB J. 27: 865-870.
33. Lindenthal, B., A. L. Holleran, T. A. Aldaghlas, B. Ruan, G. J. Schroepfer, Jr., W. K. Wilson, and J. K. Kelleher. 2001. Progestins block cholesterol synthesis to produce meiosis-activating sterols. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 15: 775-784.
34. Molina, H., D. M. Horn, N. Tang, S. Mathivanan, and A. Pandey. 2007. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. USA. 104: 2199-2204. (Pubitemid 46391375)
35. Rigbolt, K. T., T. A. Prokhorova, V. Akimov, J. Henningsen, P. T. Johansen, I. Kratchmarova, M. Kassem, M. Mann, J. V. Olsen, and B. Blagoev. 2011. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci. Signal. 4: rs3.
36. Hornbeck, P. V., J. M. Kornhauser, S. Tkachev, B. Zhang, E. Skrzypek, B. Murray, V. Latham, and M. Sullivan. 2012. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40: D261-D270.
37. Luu, W., L. J. Sharpe, I. C. Gelissen, and A. J. Brown. 2013. The role of signalling in cellular cholesterol homeostasis. IUBMB Life. 65: 675-684.
38. Metherall, J. E., J. L. Goldstein, K. L. Luskey, and M. S. Brown. 1989. Loss of transcriptional repression of three sterol-regulated genes in mutant hamster cells. J. Biol. Chem. 264: 15634-15641.
39. Goldstein, J. L., S. K. Basu, and M. S. Brown. 1983. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98: 241-260. (Pubitemid 14219888)
40. Brown, A. J., L. Sun, J. D. Feramisco, M. S. Brown, and J. L. Goldstein. 2002. Cholesterol addition to ER membranes alters conformation of SCAP, the SREBP escort protein that regulates cholesterol metabolism. Mol. Cell. 10: 237-245. (Pubitemid 35007339)
41. Tseng, W. C., J. W. Lin, T. Y. Wei, and T. Y. Fang. 2008. A novel megaprimed and ligase-free, PCR-based, site-directed mutagenesis method. Anal. Biochem. 375: 376-378.
42. Luu, W., L. J. Sharpe, J. Stevenson, and A. J. Brown. 2012. Akt acutely activates the cholesterogenic transcription factor SREBP-2. Biochim. Biophys. Acta. 1823: 458-464.
43. Sharpe, L. J., J. Wong, B. Garner, G. M. Halliday, and A. J. Brown. 2012. Is seladin-1 really a selective Alzheimer's disease indicator? J. Alzheimers Dis. 30: 35-39.
44. Du, X., I. Kristiana, J. Wong, and A. J. Brown. 2006. Involvement of Akt in ER-to-Golgi transport of SCAP/SREBP: a link between a key cell proliferative pathway and membrane synthesis. Mol. Biol. Cell. 17: 2735-2745. (Pubitemid 43825509)
45. Kielar, D., W. Dietmaier, T. Langmann, C. Aslanidis, M. Probst, M. Naruszewicz, and G. Schmitz. 2001. Rapid quantification of human ABCA1 mRNA in various cell types and tissues by real-time reverse transcription-PCR. Clin. Chem. 47: 2089-2097. (Pubitemid 33108872)
46. Kinoshita, E., and E. Kinoshita-Kikuta. 2011. Improved Phos-tag SDS-PAGE under neutral pH conditions for advanced protein phosphorylation profiling. Proteomics. 11: 319-323.
47. Bogoyevitch, M. A., Y. Y. Yeap, Z. Qu, K. R. Ngoei, Y. Y. Yip, T. T. Zhao, J. I. Heng, and D. C. Ng. 2012. WD40-repeat protein 62 is a JNK-phosphorylated spindle pole protein required for spindle maintenance and timely mitotic progression. J. Cell Sci. 125: 5096-5109.
48. Chijiwa, T., A. Mishima, M. Hagiwara, M. Sano, K. Hayashi, T. Inoue, K. Naito, T. Toshioka, and H. Hidaka. 1990. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino) ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 265: 5267-5272.
49. Barnett, S. F., D. Defeo-Jones, S. Fu, P. J. Hancock, K. M. Haskell, R. E. Jones, J. A. Kahana, A. M. Kral, K. Leander, L. L. Lee, et al. 2005. Identification and characterization of pleckstrin-homology-domain-dependent and isoenzyme-specific Akt inhibitors. Biochem. J. 385: 399-408. (Pubitemid 40165072)
50. Toullec, D., P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Boursier, F. Loriolle, et al. 1991. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266: 15771-15781. (Pubitemid 21907725)
51. Davis, P. D., C. H. Hill, E. Keech, G. Lawton, J. S. Nixon, A. D. Sedgwick, J. Wadsworth, D. Westmacott, and S. E. Wilkinson. 1989. Potent selective inhibitors of protein kinase C. FEBS Lett. 259: 61-63. (Pubitemid 20009946)
52. Wagner, S. A., P. Beli, B. T. Weinert, M. L. Nielsen, J. Cox, M. Mann, and C. Choudhary. 2011. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics. 10: 013284.
53. Wu-Zhang, A. X., and A. C. Newton. 2013. Protein kinase C pharmacology: refining the toolbox. Biochem. J. 452: 195-209.
54. Roberts, N. A., M. S. Marber, and M. Avkiran. 2004. Specificity of action of bisindolylmaleimide protein kinase C inhibitors: do they inhibit the 70 kDa ribosomal S6 kinase in cardiac myocytes? Biochem. Pharmacol. 68: 1923-1928. (Pubitemid 39346182)
55. Obenauer, J. C., L. C. Cantley, and M. B. Yaffe. 2003. Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31: 3635-3641. (Pubitemid 37442212)
56. Rodgers, M. A., V. A. Villareal, E. A. Schaefer, L. F. Peng, K. E. Corey, R. T. Chung, and P. L. Yang. 2012. Lipid metabolite profiling identifies desmosterol metabolism as a new antiviral target for hepatitis C virus. J. Am. Chem. Soc. 134: 6896-6899.
57. Sharpe, L. J., W. Luu, and A. J. Brown. 2011. Akt phosphorylates Sec24: new clues into the regulation of ER-to-Golgi trafficking. Traffic. 12: 19-27.
58. Danielsen, J. M., K. B. Sylvestersen, S. Bekker-Jensen, D. Szklarczyk, J. W. Poulsen, H. Horn, L. J. Jensen, N. Mailand, and M. L. Nielsen. 2011. Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol. Cell. Proteomics. 10: 003590.
59. Kim, W., E. J. Bennett, E. L. Huttlin, A. Guo, J. Li, A. Possemato, M. E. Sowa, R. Rad, J. Rush, M. J. Comb, et al. 2011. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell. 44: 325-340.
60. Wagner, S. A., P. Beli, B. T. Weinert, C. Scholz, C. D. Kelstrup, C. Young, M. L. Nielsen, J. V. Olsen, C. Brakebusch, and C. Choudhary. 2012. Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol. Cell. Proteomics. 11: 1578-1585.
61. Sharpe, L. J., and A. J. Brown. 2013. Controlling cholesterol synthesis beyond 3-hydroxy-3-methylglutaryl-CoA reductase (HMGCR). J. Biol. Chem. 288: 18707-18715.
62. Gill, S., J. Stevenson, I. Kristiana, and A. J. Brown. 2011. Cholesterol-dependent degradation of squalene monooxygenase, a control point in cholesterol synthesis beyond HMG-CoA reductase. Cell Metab. 13: 260-273.
63. Yang, C., J. G. McDonald, A. Patel, Y. Zhang, M. Umetani, F. Xu, E. J. Westover, D. F. Covey, D. J. Mangelsdorf, J. C. Cohen, et al. 2006. Sterol intermediates from cholesterol biosynthetic pathway as liver X receptor ligands. J. Biol. Chem. 281: 27816-27826. (Pubitemid 44414494)
64. Flicek, P., I. Ahmed, M. R. Amode, D. Barrell, K. Beal, S. Brent, D. Carvalho-Silva, P. Clapham, G. Coates, S. Fairley, et al. 2013. Ensembl 2013. Nucleic Acids Res. 41: D48-D55.