Quality control of a transcriptional regulator by SUMO-targeted degradation

Molecular and Cellular Biology

Volumn 29, Issue 7, 2009, Pages 1694-1706

  Wang, Zheng ^a   Prelich, Gregory ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE DERIVATIVE; CANAVANINE; LYSINE; MUTANT PROTEIN; PROTEASOME; PROTEIN MOT1; PROTEIN MOT1 301; PROTEIN SLX5; PROTEIN SLX8; SUMO PROTEIN; SUMO TARGETED UBIQUITIN LIGASE; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME 4; UBIQUITIN CONJUGATING ENZYME 5; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; HELICASE; MOT1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TATA BINDING PROTEIN ASSOCIATED FACTOR; UBIQUITIN;

ARTICLE; CELL METABOLISM; CONTROLLED STUDY; DEGRADATION KINETICS; ENZYME ACTIVITY; ENZYME INHIBITION; FUNGAL STRAIN; FUNGUS GROWTH; GENE; GENE DELETION; GENE DISRUPTION; GENETIC STRAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; PROTEIN TARGETING; QUALITY CONTROL; SACCHAROMYCES CEREVISIAE; SLX5 GENE; SLX8 GENE; SUMOYLATION; TRANSCRIPTION REGULATION; WILD TYPE; AMINO ACID SEQUENCE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; ENZYME SPECIFICITY; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN PROCESSING;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CANAVANINE; DNA HELICASES; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUBSTRATE SPECIFICITY; TATA-BINDING PROTEIN ASSOCIATED FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN;

EID: 63049110916     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01470-08     Document Type: Article

References (62)

1. Adamkewicz, J. I., K. E. Hansen, W. A. Prud'homme, J. L. Davis, and J. Thorner. 2001. High affinity interaction of yeast transcriptional regulator, Motl, with TATA box-binding protein (TBP). J. Biol. Chem. 276:11883-11894.
2. Baba, D., N. Maita, J. G. Jee, Y. Uchimura, H. Saitoh, K. Sugasawa, F. Hanaoka, H. Tochio, H. Hiroaki, and M. Shirakawa. 2005. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435:979-982.
3. Cardone, L., J. Hirayama, F. Giordano, T. Tamaru, J. J. Palvimo, and P. Sassone-Corsi. 2005. Orcadian clock control by SUMOylation of BMAL1. Science 309:1390-1394.
4. Carlson, N., S. Rogers, and M. Rechsteiner. 1987. Microinjection of ubiq-uitin: changes in protein degradation in HeLa cells subjected to heat-shock. J. Cell Biol. 104:547-555.
5. Chen, X. L., A. Reindle, and E. S. Johnson. 2005. Misregulation of 2μm circle copy number in a SUMO pathway mutant. Mol. Cell. Biol. 25:4311-4320.
6. Cyr, D. M., J. Hohfeld, and C. Patterson. 2002. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem. Sci. 27:368-375.
7. Darst, R. P., A. Dasgupta, C. Zhu, J. Y. Hsu, A. Vroom, T. Muldrow, and D. T. Auble. 2003. Motl regulates the DNA binding activity of free TATA-binding protein in an ATP-dependent manner. J. Biol. Chem. 278:13216-13226.
8. Dasgupta, A., K. L. Ramsey, J. S. Smith, and D. T. Auble. 2004. Sir Antagonist 1 (Sanl) is a ubiquitin ligase. J. Biol. Chem. 279:26830-26838.
9. Denison, C., A. D. Rudner, S. A. Gerber, C. E. Bakalarski, D. Moazed, and S. P. Gygi. 2005. A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol. Cell. Proteomics 4:246-254.
10. Desterro, J. M, M. S. Rodriguez, and R. T. Hay. 1998. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 2:233-239.
11. Durr, H., C. Korner, M. Muller, V. Hickmann, and K. P. Hopfner. 2005. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121:363-373.
12. Gardner, R. G., Z. W. Nelson, and D. E. Gottschling. 2005. Degradation-mediated protein quality control in the nucleus. Cell 120:803-815.
13. Goldberg, A L. 1972. Degradation of abnormal proteins in Escherichia coli (protein breakdown-protein structure-mistranslation- amino acid analogs-pu-romycin). Proc. Natl. Acad. Sci. USA 69:422-426.
14. Goldberg, A. L. 2003. Protein degradation and protection against misfolded or damaged proteins. Nature 426:895-899.
15. Hampton, R. Y. 2002. ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell Biol. 14:476-482.
16. Hannich, J. T., A. Lewis, M. B. Kroetz, S. J. Li, H. Heide, A. Emili, and M. Hochstrasser. 2005. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280:4102-4110.
17. Hardeland, U., R. Steinacher, J. Jiricny, and P. Schar. 2002. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21:1456-1464.
18. Hirsch, C., E. Jarosch, T. Sommer, and D. H. Wolf. 2004. Endoplasmic reticulum-associated protein degradation - one model fits all? Biochim. Bio-phys. Acta 1695:215-223.
19. Ii, T., J. R. Mullen, C. E. Slagle, and S. J. Brill. 2007. Stimulation of in vitro sumoylation by Slx5-Slx8: evidence for a functional interaction with the SUMO pathway. DNA Repair 6:1679-1691.
20. Johnson, E. S. 2004. Protein modification by SUMO. Annu. Rev. Biochem. 73:355-382.
21. Johnson, E. S., and G. Blobel. 1999. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 147:981-994.
22. Johnson, E. S., and G. Blobel. 1997. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272:26799- 26802.
23. Johnson, E. S., and A. A. Gupta. 2001. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106:735-744.
24. Johnson, E. S., I. Schwienhorst, R. J. Dohmen, and G. Blobel. 1997. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aoslp/Uba2p heterodimer. EMBO J. 16:5509-5519.
25. Kerscher, O., R. Felberbaum, and M. Hochstrasser. 2006. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22:159-180.
26. Kurepa, J., J. M. Walker, J. Smalle, M. M. Gosink, S. J. Davis, T. L. Durham, D. Y. Sung, and R. D. Vierstra. 2003. The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J. Biol. Chem. 278:6862-6872.
27. Kushnirov, V. V. 2000. Rapid and reliable protein extraction from yeast. Yeast 16:857-860.
28. Lallemand-Breitenbach, V., M. Jeanne, S. Benhenda, R. Nasr, M. Lei, L. Peres, J. Zhou, J. Zhu, B. Raught, and H. de The. 2008. Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-me-diated pathway. Nat. Cell Biol. 10:547-555.
29. Lallemand-Breitenbach, V., J. Zhu, F. Puvion, M. Koken, N. Honore, A. Doubeikovsky, E. Duprez, P. P. Pandolfl, E. Puvion, P. Freemont, and H. de The. 2001. Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, IIS proteasome recruitment, and As2O3-in-duced PML or PML/retinoic acid receptor alpha degradation. J. Exp. Med. 193:1361-1371.
30. Li, S. J., and M. Hochstrasser. 1999. A new protease required for cell-cycle progression in yeast. Nature 398:246-251.
31. Li, S. J., and M. Hochstrasser. 2000. The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 20:2367-2377.
32. Liu, Y. C, J. Penninger, and M. Karin. 2005. Immunity by ubiquitylation: a reversible process of modification. Nat. Rev. Immunol. 5:941-952.
33. Mao, Y., S. D. Desai, and L. F. Liu. 2000. SUMO-1 conjugation to human DNA topoisomerase II isozymes. J. Biol. Chem. 275:26066-26073.
34. McClellan, A. J., S. Tam, D. Kaganovich, and J. Frydman. 2005. Protein quality control: chaperones culling corrupt conformations. Nat. Cell Biol. 7:736-741.
35. Minty, A., X. Dumont, M. Kaghad, and D. Caput. 2000. Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J. Biol. Chem. 275:36316-36323.
36. Mullen, J. R., and S. J. Brill. 2008. Activation of the Slx5-Slx8 ubiquitin ligase by poly-small ubiquitin-like modifier conjugates. J. Biol. Chem. 283: 19912-19921.
37. Panse, V. G., U. Hardeland, T. Werner, B. Kuster, and E. Hurt. 2004. A proteome-wide approach identifies sumoylated substrate proteins in yeast. J. Biol. Chem. 279:41346-41351.
38. Papouli, E., S. Chen, A. A. Davies, D. Huttner, L. Krejci, P. Sung, and H. D. Ulrich. 2005. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19:123-133.
39. Parag, H. A., B. Raboy, and R. G. Kulka. 1987. Effect of heat shock on protein degradation in mammalian cells: involvement of the ubiquitin system. EMBO J. 6:55-61.
40. Parker, J. L., A. Bucceri, A. A. Davies, K. Heidrich, H. Windecker, and H. D. Ulrich. 2008. SUMO modification of PCNA is controlled by DNA. EMBO J. 27:2422-2431.
41. Pfander, B., G. L. Moldovan, M. Sacher, C. Hoege, and S. Jentsch. 2005. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436:428-433.
42. Prudden, J., S. Pebernard, G. Raffa, D. A. Slavin, J. J. Perry, J. A. Tainer, C. H. McGowan, and M. N. Boddy. 2007. SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 26:4089-4101.
43. Reed, S. I. 2006. The ubiquitin-proteasome pathway in cell cycle control. Results Probl. Cell Differ. 42:147-181.
44. Reverter, D., and C. D. Lima. 2005. Insights into E3 ligase activity revealed by a SUMO-RanGAPl-Ubc9-Nup358 complex. Nature 435:687-692.
45. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Saitoh, H., and J. Hinchey. 2000. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275:6252-6258.
47. Seufert, W., and S. Jentsch. 1990. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 9:543-550.
48. Shang, F., X. Gong, and A. Taylor. 1997. Activity of ubiquitin-dependent pathway in response to oxidative stress. Ubiquitin-activating enzyme is transiently up-regulated. J. Biol. Chem. 272:23086-23093.
49. Sitia, R., and I. Braakman. 2003. Quality control in the endoplasmic retic-ulum protein factory. Nature 426:891-894.
50. Song, J., L. K. Durrin, T. A. Wilkinson, T. G. Krontiris, and Y. Chen. 2004. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. USA 101:14373-14378.
51. Sprouse, R. O., M. Brenowitz, and D. T. Auble. 2006. Snf2/Swi2-related ATPase Motl drives displacement of TATA-binding protein by gripping DNA. EMBO J. 25:1492-1504.
52. Steinacher, R., and P. Schar. 2005. Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 15:616-623.
53. Strunnikov, A. V., L. Aravind, and E. V. Koonin. 2001. Saccharomyces cerevisiae SMT4 encodes an evolutionarily conserved protease with a role in chromosome condensation regulation. Genetics 158:95-107.
54. Sun, H., J. D. Leverson, and T. Hunter. 2007. Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J. 26:4102-4112.
55. Tatham, M. H., M. C. Geoffroy, L. Shen, A. Plechanovova, N. Hattersley, E. G. Jaffray, J. J. Palvimo, and R. T. Hay. 2008. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10:538-546.
56. Ulrich, H. D. 2005. Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell Biol. 15:525-532.
57. Uzunova, K., K. Gottsche, M. Miteva, S. R. Weisshaar, C. Glanemann, M. Schnellhardt, M. Niessen, H. Scheel, K. Hofmann, E. S. Johnson, G. J. Praefcke, and R. J. Dohmen. 2007. Ubiquitin-dependent proteolytic control of SUMO conjugates. J. Biol. Chem. 282:34167-34175.
58. Wang, Z., G. M. Jones, and G. Prelich. 2006. Genetic analysis connects SLX5 and SLX8 to the SUMO pathway in Saccharomyces cerevisiae. Genetics 172:1499-1509.
59. Wohlschlegel, J. A., E. S. Johnson, S. I. Reed, and J. R. Yates III. 2004. Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279:45662-45668.
60. Xie, Y., O. Kerscher, M. B. Kroetz, H. F. McConchie, P. Sung, and M. Hochstrasser. 2007. The yeast Hex3 • Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J. Biol. Chem. 282:34176- 34184.
61. Zhao, X., and G. Blobel. 2005. A SUMO ligase is part of a nuclear multi-protein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. USA 102:4777-4782.
62. Zhu, J., V. Lallemand-Breitenbach, and H. de The. 2001. Pathways of reti-noic acid- or arsenic trioxide-induced PML/RARa catabolism, role of on-cogene degradation in disease remission. Oncogene 20:7257-7265.