Structure of the WD40 domain of SCAP from fission yeast reveals the molecular basis for SREBP recognition

Cell Research

Volumn 25, Issue 4, 2015, Pages 401-411

  Gong, Xin ^a,b   Li, Jingxian ^a,b   Shao, Wei ^c   Wu, Jianping ^a,b   Qian, Hongwu ^a,b   Ren, Ruobing ^a,b   Espenshade, Peter ^c   Yan, Nieng ^a,b  

^a Peking University   (China)

^b TSINGHUA UNIVERSITY   (China)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Lipid homeostasis; SCAP; SREBP; Structure

Indexed keywords

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

ACTIN BINDING PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN BINDING; SCHIZOSACCHAROMYCES POMBE PROTEIN; SCP1 PROTEIN, S POMBE; SRE1 PROTEIN, S POMBE; STEROL; STEROL REGULATORY ELEMENT BINDING PROTEIN;

ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HAMSTER; METABOLISM; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SCHIZOSACCHAROMYCES; X RAY CRYSTALLOGRAPHY;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; CRYSTALLOGRAPHY, X-RAY; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; MICROFILAMENT PROTEINS; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; STEROL REGULATORY ELEMENT BINDING PROTEINS; STEROLS;

EID: 84926522124     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2015.32     Document Type: Article

References (41)

1. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 2002; 109:1125-1131.
2. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997; 89:331-340.
3. Shao W, Espenshade PJ. Expanding roles for SREBP in metabolism. Cell Metab 2012; 16:414-419.
4. Espenshade PJ, Hughes AL. Regulation of sterol synthesis in eukaryotes. Annu Rev Genet 2007; 41:401-427.
5. Goldstein JL, DeBose-Boyd RA, Brown MS. Protein sensors for membrane sterols. Cell 2006; 124:35-46.
6. Shao W, Espenshade PJ. Sterol regulatory element-binding protein (SREBP) cleavage regulates Golgi-to-endoplasmic reticulum recycling of SREBP cleavage-activating protein (SCAP). J Biol Chem 2014; 289:7547-7557.
7. Nohturfft A, DeBose-Boyd RA, Scheek S, Goldstein JL, Brown MS. Sterols regulate cycling of SREBP cleavage-activating protein (SCAP) between endoplasmic reticulum and Golgi. Proc Natl Acad Sci USA 1999; 96:11235-11240.
8. Bien CM, Espenshade PJ. Sterol regulatory element binding proteins in fungi: hypoxic transcription factors linked to pathogenesis. Eukaryot Cell 2010; 9:352-359.
9. Osborne TF, Espenshade PJ. Evolutionary conservation and adaptation in the mechanism that regulates SREBP action: what a long, strange tRIP it's been. Genes Dev 2009; 23:2578-2591.
10. Todd BL, Stewart EV, Burg JS, Hughes AL, Espenshade PJ. Sterol regulatory element binding protein is a principal regulator of anaerobic gene expression in fission yeast. Mol Cell Biol 2006; 26:2817-2831.
11. Hughes AL, Todd BL, Espenshade PJ. SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast. Cell 2005; 120:831-842.
12. Stewart EV, Nwosu CC, Tong Z, et al. Yeast SREBP cleavage activation requires the Golgi Dsc E3 ligase complex. Mol Cell 2011; 42:160-171.
13. Nohturfft A, Brown MS, Goldstein JL. Topology of SREBP cleavage-activating protein, a polytopic membrane protein with a sterol-sensing domain. J Biol Chem 1998; 273:17243-17250.
14. Kuwabara PE, Labouesse M. The sterol-sensing domain: multiple families, a unique role? Trends Genet 2002; 18:193-201.
15. Luskey KL, Stevens B. Human 3-Hydroxy-3-Methylglutaryl coenzyme-a reductase-conserved domains responsible for catalytic activity and sterol-regulated degradation. J Biol Chem 1985; 260:271-277.
16. Carstea ED, Morris JA, Coleman KG, et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997; 277:228-231.
17. Loftus SK, Morris JA, Carstea ED, et al. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 1997; 277:232-235.
18. Ingham PW, Taylor AM, Nakano Y. Role of the Drosophila patched gene in positional signalling. Nature 1991; 353:184-187.
19. Burke R, Nellen D, Bellotto M, et al. Dispatched, a novel sterol-sensing domain protein dedicated to the release of cholesterol-modified hedgehog from signaling cells. Cell 1999; 99:803-815.
20. Sakai J, Nohturfft A, Cheng D, Ho YK, Brown MS, Goldstein JL. Identification of complexes between the COOH-terminal domains of sterol regulatory element-binding proteins (SREBPs) and SREBP cleavage-activating protein. J Biol Chem 1997; 272:20213-20221.
21. Stirnimann CU, Petsalaki E, Russell RB, Muller CW. WD40 proteins propel cellular networks. Trends Biochem Sci 2010; 35:565-574.
22. Matsuda M, Korn BS, Hammer RE, et al. SREBP cleavage-activating protein (SCAP) is required for increased lipid synthesis in liver induced by cholesterol deprivation and insulin elevation. Genes Dev 2001; 15:1206-1216.
23. Moon YA, Liang G, Xie X, et al. The Scap/SREBP pathway is essential for developing diabetic fatty liver and carbohydrate-induced hypertriglyceridemia in animals. Cell Metab 2012; 15:240-246.
24. Hua X, Nohturfft A, Goldstein JL, Brown MS. Sterol resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein. Cell 1996; 87:415-426.
25. Cerna D, Wilson DK. The structure of Sif2p, a WD repeat protein functioning in the SET3 corepressor complex. J Mol Biol 2005; 351:923-935.
26. Hughes BT, Nwosu CC, Espenshade PJ. Degradation of sterol regulatory element-binding protein precursor requires the endoplasmic reticulum-associated degradation components Ubc7 and Hrd1 in fission yeast. J Biol Chem 2009; 284:20512-20521.
27. Yu L, Gaitatzes C, Neer E, Smith TF. Thirty-plus functional families from a single motif. Protein Sci 2000; 9:2470-2476.
28. Barlowe C. Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol 2003; 13:295-300.
29. Sun LP, Li L, Goldstein JL, Brown MS. Insig required for sterol-mediated inhibition of Scap/SREBP binding to COPII proteins in vitro. J Biol Chem 2005; 280:26483-26490.
30. Hughes AL, Stewart EV, Espenshade PJ. Identification of twenty-three mutations in fission yeast Scap that constitutively activate SREBP. J Lipid Res 2008; 49:2001-2012.
31. DeLano WL. The PyMOL Molecular Graphics System on World Wide Web http://www.pymol.org. 2002.
32. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol 1997; 276:307-326.
33. Collaborative Computational Project, Number 4. The Ccp4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994; 50(Pt 5):760-763.
34. Schneider TR, Sheldrick GM. Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 2002; 58(Pt 2):1772-1779.
35. Cowtan K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 2006; 62(Pt 9):1002-1011.
36. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004; 60(Pt 12 Pt 1):2126-2132.
37. Adams PD, Grosse-Kunstleve RW, Hung LW, et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 2002; 58(Pt 11):1948-1954.
38. Mccoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr 2007; 40:658-674.
39. Hentges P, Van Driessche B, Tafforeau L, Vandenhaute J, Carr AM. Three novel antibiotic marker cassettes for gene disruption and marker switching in Schizosaccharomyces pombe. Yeast 2005; 22:1013-1019.
40. Bahler J, Wu JQ, Longtine MS, et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 1998; 14:943-951.
41. Stewart EV, Lloyd SJ, Burg JS, et al. Yeast sterol regulatory element-binding protein (SREBP) cleavage requires Cdc48 and Dsc5, a ubiquitin regulatory X domain-containing subunit of the Golgi Dsc E3 ligase. J Biol Chem 2012; 287:672-681.