Architecture and Assembly of Poly-SUMO Chains on PCNA in Saccharomyces cerevisiae

Journal of Molecular Biology

Volumn 376, Issue 1, 2008, Pages 221-231

  Windecker, Hanna ^a   Ulrich, Helle D ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

PCNA; posttranslational protein modifications; Siz1; SUMO; Ubc9

Indexed keywords

CYCLINE; LIGASE; SUMO PROTEIN; UBIQUITIN;

AMINO ACID SEQUENCE; ARTICLE; BUDDING; CELL CYCLE S PHASE; CONJUGATION; DNA DAMAGE; ENZYME SPECIFICITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SUMOYLATION; UBIQUITINATION; YEAST;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 38049079191     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.12.008     Document Type: Article

References (44)

1. Kerscher O., Felberbaum R., and Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22 (2006) 159-180
2. Pickart C.M., and Eddins M.J. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695 (2004) 55-72
3. Chau V., Tobias J.W., Bachmair A., Marriott D., Ecker D.J., Gonda D.K., and Varshavsky A. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243 (1989) 1576-1583
4. Hershko A., and Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67 (1998) 425-479
5. Hicke L., and Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19 (2003) 141-172
6. Pickart C.M., and Fushman D. Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8 (2004) 610-616
7. Sun L., and Chen Z.J. The novel functions of ubiquitination in signaling. Curr. Opin. Cell Biol. 16 (2004) 119-126
8. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 73 (2004) 355-382
9. Bernier-Villamor V., Sampson D.A., Matunis M.J., and Lima C.D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108 (2002) 345-356
10. Johnson E.S., and Blobel G. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 147 (1999) 981-994
11. Sampson D.A., Wang M., and Matunis M.J. The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276 (2001) 21664-21669
12. Bylebyl G.R., Belichenko I., and Johnson E.S. The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J. Biol. Chem. 278 (2003) 44113-44120
13. Gocke C.B., Yu H., and Kang J. Systematic identification and analysis of mammalian small ubiquitin-like modifier substrates. J. Biol. Chem. 280 (2005) 5004-5012
14. Takahashi Y., Toh E.A., and Kikuchi Y. Comparative analysis of yeast PIAS-type SUMO ligases in vivo and in vitro. J. Biochem. (Tokyo) 133 (2003) 415-422
15. Yang M., Hsu C.T., Ting C.Y., Liu L.F., and Hwang J. Assembly of a polymeric chain of SUMO1 on human topoisomerase I in vitro. J. Biol. Chem. 281 (2006) 8264-8274
16. Matic I., van Hagen M., Schimmel J., Macek B., Ogg S.C., Tatham M.H., et al. In vivo identification of human SUMO polymerization sites by high accuracy mass spectrometry and an in-vitro to in vivo strategy. Mol. Cell Proteomics (2007) (advance online publication, Oct. 15, 2007)
17. Tatham M.H., Jaffray E., Vaughan O.A., Desterro J.M., Botting C.H., Naismith J.H., and Hay R.T. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276 (2001) 35368-35374
18. Cheng C.H., Lo Y.H., Liang S.S., Ti S.C., Lin F.M., Yeh C.H., et al. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev. 20 (2006) 2067-2081
19. Li S.-J., and Hochstrasser M. The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 20 (2000) 2367-2377
20. Ulrich H.D. Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell Biol. 15 (2005) 525-532
21. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
22. Stelter P., and Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425 (2003) 188-191
23. Kannouche P.L., Wing J., and Lehmann A.R. Interaction of human DNA polymerase η with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14 (2004) 491-500
24. Watanabe K., Tateishi S., Kawasuji M., Tsurimoto T., Inoue H., and Yamaizumi M. Rad18 guides polη to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 23 (2004) 3886-3896
25. Leach C.A., and Michael W.M. Ubiquitin/SUMO modification of PCNA promotes replication fork progression in Xenopus laevis egg extracts. J. Cell Biol. 171 (2005) 947-954
26. Frampton J., Irmisch A., Green C.M., Neiss A., Trickey M., Ulrich H.D., et al. Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Mol. Biol. Cell 17 (2006) 2976-2985
27. Simpson L.J., Ross A.L., Szuts D., Alviani C.A., Oestergaard V.H., Patel K.J., and Sale J.E. RAD18-independent ubiquitination of proliferating-cell nuclear antigen in the avian cell line DT40. EMBO Rep. 7 (2006) 927-932
28. Arakawa H., Moldovan G.L., Saribasak H., Saribasak N.N., Jentsch S., and Buerstedde J.M. A role for PCNA ubiquitination in immunoglobulin hypermutation. PLoS Biol. 4 (2006) e366
29. SUMO and Srs2: a model SUMO substrate-effector pair. Biochem. Soc. Trans. 35, 1385-1388.
30. Papouli E., Chen S., Davies A.A., Huttner D., Krejci L., Sung P., and Ulrich H.D. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19 (2005) 123-133
31. Pfander B., Moldovan G.L., Sacher M., Hoege C., and Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436 (2005) 428-433
32. Robert T., Dervins D., Fabre F., and Gangloff S. Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover. EMBO J. 25 (2006) 2837-2846
33. Johnson E.S., and Blobel G. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 272 (1997) 26799-26802
34. Johnson E.S., and Gupta A.A. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106 (2001) 735-744
35. Johnson E.S., Schwienhorst I., Dohmen R.J., and Blobel G. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J. 16 (1997) 5509-5519
36. Pichler A., Knipscheer P., Saitoh H., Sixma T.K., and Melchior F. The RanBP2 SUMO E3 ligase is neither HECT- nor RING-type. Nat. Struct. Mol. Biol. 11 (2004) 984-991
37. Reindle A., Belichenko I., Bylebyl G.R., Chen X.L., Gandhi N., and Johnson E.S. Multiple domains in Siz SUMO ligases contribute to substrate selectivity. J. Cell Sci. 119 (2006) 4749-4757
38. Takahashi Y., Kahyo T., Toh E.A., Yasuda H., and Kikuchi Y. Yeast Ull1/Siz1 is a novel SUMO1/Smt3 ligase for septin components and functions as an adaptor between conjugating enzyme and substrates. J. Biol. Chem. 276 (2001) 48973-48977
39. Reverter D., and Lima C.D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 435 (2005) 687-692
40. Pichler A., Knipscheer P., Oberhofer E., van Dijk W.J., Korner R., and Olsen J.V. SUMO modification of the ubiquitin-conjugating enzyme E2-25K. Nat. Struct. Mol. Biol. 12 (2005) 264-269
41. Knipscheer P., van Dijk W.J., Olsen J.V., Mann M., and Sixma T.K. Noncovalent interaction between Ubc9 and SUMO promotes SUMO chain formation. EMBO J. 26 (2007) 2797-2807
42. Capili A.D., and Lima C.D. Structure and analysis of a complex between SUMO and Ubc9 illustrates features of a conserved E2-Ubl interaction. J. Mol. Biol. 369 (2007) 608-618
43. Gietz R.D., and Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74 (1988) 527-534
44. Finley D., Ozkaynak E., and Varshavsky A. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48 (1987) 1035-1046