Desumoylation of the endoplasmic reticulum membrane VAP family protein Scs2 by Ulp1 and SUMO regulation of the inositol synthesis pathway

Molecular and Cellular Biology

Volumn 32, Issue 1, 2012, Pages 64-75

  Felberbaum, Rachael ^a,c   Wilson, Nicole R ^a   Cheng, Dongmei ^b   Peng, Junmin ^b,d   Hochstrasser, Mark ^a  

^a YALE UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Protein Sciences Corp   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE; PHOSPHATIDYLINOSITOL; SACCHAROMYCES CEREVISIAE PROTEIN; SCS2 PROTEIN; SUMO PROTEIN; UBIQUITIN LIKE PROTEIN SPECIFIC PROTEASE 1; UNCLASSIFIED DRUG;

ARTICLE; AUXOTROPHY; CELL GROWTH; COILED BODY; CONJUGATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FUNGUS MUTATION; GROWTH INHIBITION; IN VIVO STUDY; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SUMOYLATION;

CYSTEINE ENDOPEPTIDASES; ENDOPEPTIDASES; GENE EXPRESSION REGULATION, FUNGAL; INOSITOL; MEMBRANE PROTEINS; MUTATION; MYO-INOSITOL-1-PHOSPHATE SYNTHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; TRANSCRIPTIONAL ACTIVATION;

EID: 84856808507     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05878-11     Document Type: Article

References (51)

1. Bankaitis VA, Mousley CJ, Schaaf G. 2010. The Sec14 superfamily and mechanisms for crosstalk between lipid metabolism and lipid signaling. Trends Biochem. Sci. 35:150-160.
2. Bischof O, et al. 2006. The E3 SUMO ligase PIASy is a regulator of cellular senescence and apoptosis. Mol. Cell 22:783-794.
3. Brickner JH, Walter P. 2004. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2:e342.
4. Bylebyl GR, Belichenko I, Johnson ES. 2003. The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J. Biol. Chem. 278:44113-44120.
5. Carman GM, Han GS. 2009. Regulation of phospholipid synthesis in yeast. J. Lipid Res. 50(Suppl):S69-S73.
6. Carman GM, Henry SA. 1999. Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes. Prog. Lipid Res. 38:361-399.
7. Chang HJ, Jones EW, Henry SA. 2002. Role of the unfolded protein response pathway in regulation of INO1 and in the sec14 bypass mechanism in Saccharomyces cerevisiae. Genetics 162:29-43.
8. Craven RJ, Petes TD. 2001. The Saccharomyces cerevisiae suppressor of choline sensitivity (SCS2) gene is a multicopy suppressor of mec1 telomeric silencing defects. Genetics 158:145-154.
9. Cuperus G, Shore D. 2002. Restoration of silencing in Saccharomyces cerevisiae by tethering of a novel Sir2-interacting protein, Esc8. Genetics 162:633-645.
10. Drag M, Salvesen GS. 2008. DeSUMOylating enzymes-SENPs. IUBMB Life 60:734-742.
11. Funakoshi M, Hochstrasser M. 2009. Small epitope-linker modules for PCR-based C-terminal tagging in Saccharomyces cerevisiae. Yeast 26:185-192.
12. Gietz RD, Sugino A. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527-534.
13. Guthrie C, Fink GR (ed). 1991. Methods in enzymology, vol 194. Guide to yeast genetics and molecular biology. Academic Press, Inc, San Diego, CA.
14. Hannich JT, et al. 2005. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280:4102-4110.
15. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141.
16. Hosaka K, Nikawa J, Kodaki T, Yamashita S. 1992. A dominant mutation that alters the regulation of INO1 expression in Saccharomyces cerevisiae. J. Biochem. 111:352-358.
17. Jesch SA, Zhao X, Wells MT, Henry SA. 2005. Genome-wide analysis reveals inositol, not choline, as the major effector of Ino2p-Ino4p and unfolded protein response target gene expression in yeast. J. Biol. Chem. 280:9106-9118.
18. Johnson ES. 2004. Protein modification by SUMO. Annu. Rev. Biochem. 73:355-382.
19. Johnson ES, Blobel G. 1999. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 147:981-994.
20. Johnson ES, Blobel G. 1997. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272:26799-26802.
21. Johnson ES, Gupta AA. 2001. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106:735-744.
22. Johnson ES, Schwienhorst I, Dohmen RJ, Blobel G. 1997. The ubiquitinlike protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 16:5509-5519.
23. Kagiwada S, Hosaka K, Murata M, Nikawa J-I, Takatsuki A. 1998. The Saccharomyces cerevisiae SCS2 gene product, a homolog of a synaptobrevin-associated protein, is an integral membrane protein of the endoplasmic reticulum and is required for inositol metabolism. J. Bacteriol. 180:1700-1708.
24. Kashyap AK, Schieltz D, Yates J III, Kellogg DR. 2005. Biochemical and genetic characterization of Yra1p in budding yeast. Yeast 22:43-56.
25. Kerscher O. 2007. SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 8:550-555.
26. Klig LS, Henry SA. 1984. Isolation of the yeast INO1 gene: located on an autonomously replicating plasmid, the gene is fully regulated. Proc. Natl. Acad. Sci. U. S. A. 81:3816-3820.
27. Lev S, Ben Halevy D, Peretti D, Dahan N. 2008. The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol. 18:282-290.
28. Lewis A, Felberbaum R, Hochstrasser M. 2007. A nuclear envelope protein linking nuclear pore basket assembly, SUMO protease regulation, and mRNA surveillance. J. Cell Biol. 178:813-827.
29. Li SJ, Hochstrasser M. 1999. A new protease required for cell-cycle progression in yeast. Nature 398:246-251.
30. Li SJ, Hochstrasser M. 2003. The Ulp1 SUMO isopeptidase: distinct domains required for viability, nuclear envelope localization, and substrate specificity. J. Cell Biol. 160:1069-1081.
31. Li SJ, Hochstrasser M. 2000. The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 20:2367-2377.
32. Loewen CJ, Young BP, Tavassoli S, Levine TP. 2007. Inheritance of cortical ER in yeast is required for normal septin organization. J. Cell Biol. 179:467-483.
33. Longtine MS, et al. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
34. Lyst MJ, Stancheva I. 2007. A role for SUMO modification in transcriptional repression and activation. Biochem. Soc. Trans. 35:1389-1392.
35. Nikawa J, Murakami A, Esumi E, Hosaka K. 1995. Cloning and sequence of the SCS2 gene, which can suppress the defect of INO1 expression in an inositol auxotrophic mutant of Saccharomyces cerevisiae. J. Biochem. 118:39-45.
36. Nishimura AL, Al-Chalabi A, Zatz M. 2005. A common founder for amyotrophic lateral sclerosis type 8 (ALS8) in the Brazilian population. Hum. Genet. 118:499-500.
37. Nishimura AL, et al. 2004. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet. 75:822-831.
38. Panse VG, Hardeland U, Werner T, Kuster B, Hurt E. 2004. A proteome-wide approach identifies sumoylated substrate proteins in yeast. J. Biol. Chem. 279:41346-41351.
39. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP. 2003. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2:43-50.
40. Peng J, et al. 2003. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21:921-926.
41. Sarge KD, Park-Sarge OK. 2009. Sumoylation and human disease pathogenesis. Trends Biochem. Sci. 34:200-205.
42. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
43. Tong AH, et al. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364-2368.
44. Vertegaal AC, et al. 2006. Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell. Proteomics 5:2298-2310.
45. Villa-Garcia MJ, et al. 2011. Genome-wide screen for inositol auxotrophy in Saccharomyces cerevisiae implicates lipid metabolism in stress response signaling. Mol. Genet. Genomics 285:125-149.
46. Wilson JD, Thompson SL, Barlowe C. 2011. Yet1p-Yet3p interacts with Scs2p-Opi1p to regulate ER localization of the Opi1p repressor. Mol. Biol. Cell 22:1430-1439.
47. Wohlschlegel JA, Johnson ES, Reed SI, Yates JR III. 2004. Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279:45662-45668.
48. Xu P, Duong DM, Peng J. 2009. Systematical optimization of reversephase chromatography for shotgun proteomics. J. Proteome Res. 8:3944-3950.
49. Yang XJ, Seto E. 2008. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell 31:449-461.
50. Zhao X, Blobel G. 2005. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. U. S. A. 102:4777-4782.
51. Zhou W, Ryan JJ, Zhou H. 2004. Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J. Biol. Chem. 279:32262-32268.