Wss1 metalloprotease partners with Cdc48/Doa1 in processing genotoxic SUMO conjugates

eLife

Volumn 4, Issue September2015, 2015, Pages

  Balakirev, Maxim Y ^a,b,c   Mullally, James E ^d,f   Favier, Adrien ^b   Assard, Nicole ^a,b,c   Sulpice, Eric ^a,b,c   Lindsey, David F ^e   Rulina, Anastasia V ^a,b,c   Gidrol, Xavier ^a,b,c   Wilkinson, Keith D ^d  

^a CEA GRENOBLE   (France)

^b UNIV GRENOBLE ALPES   (France)

^c INSERM   (France)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Walla Walla College   (United States)

^f CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDC48 PROTEIN; CYSTEINE; DNA TOPOISOMERASE; DOA1 PROTEIN; METALLOPROTEINASE; RECOMBINANT PROTEIN; SINGLE STRANDED DNA; SUMO PROTEIN; TERNARY COMPLEX FACTOR; UNCLASSIFIED DRUG; WSS 1 METALLOPROTEINASE; ZINC; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; DOA1 PROTEIN, S CEREVISIAE; MUTAGENIC AGENT; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; WSS1 PROTEIN, S CEREVISIAE;

ARTICLE; AUTOPHAGY; BIOINFORMATICS; CELL STRESS; CONTROLLED STUDY; CYTOFLUOROMETRY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; GENOTOXICITY; IN VITRO STUDY; MOLECULAR DOCKING; MUTAGENESIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SUMOYLATION; TEMPERATURE SENSITIVITY; WESTERN BLOTTING; ENZYMOLOGY; METABOLISM; SACCHAROMYCES CEREVISIAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATASES; CELL CYCLE PROTEINS; MUTAGENS; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION;

EID: 84942018040     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06763     Document Type: Article

References (78)

1. Balakirev MY, Zimmer G. 1998. Gradual changes in permeability of inner mitochondrial membrane precede the mitochondrial permeability transition. Archives of Biochemistry and Biophysics 356: 46-54. doi: 10. 1006/abbi. 1998. 0738.
2. Bergink S, Ammon T, Kern M, Schermelleh L, Leonhardt H, Jentsch S. 2013. Role of Cdc48/p97 as a SUMOtargeted segregase curbing Rad51-Rad52 interaction. Nature Cell Biology 15: 526-532. doi: 10. 1038/ncb2729.
3. Biggins S, Bhalla N, Chang A, Smith DL, Murray AW. 2001. Genes involved in sister chromatid separation and segregation in the budding yeast Saccharomyces cerevisiae. Genetics 159: 453-470.
4. Bruderer RM, Brasseur C, Meyer HH. 2004. The AAA ATPase p97/VCP interacts with its Alternative co-factors, Ufd1-Npl4 and p47, through a common bipartite binding mechanism. The Journal of Biological Chemistry 279: 49609-49616. doi: 10. 1074/jbc. M408695200.
5. Centore RichardC, Yazinski StephanieA, Tse A, Zou L. 2012. Spartan/C1orf124. a Reader of PCNA Ubiquitylation and a Regulator of UV-Induced DNA Damage Response. Mol. Cell 46: 625-635.
6. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T. 2003. Regulation of matrix metalloproteinases: an overview. Molecular and Cellular Biochemistry 253: 269-285. doi: 10. 1023/A: 1026028303196.
7. Ciccia A, Elledge SJ. 2010. The DNA damage response: Making it Safe to play with Knives. Molecular Cell 40: 179-204. doi: 10. 1016/j. molcel. 2010. 09. 019.
8. Cremona CatherineA, Sarangi P, Yang Y, Hang LisaE, Rahman S, Zhao X. 2012. Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the Mec1 checkpoint. Molecular Cell 45: 422-432. doi: 10. 1016/j. molcel. 2011. 11. 028.
9. Davis EJ, Lachaud C, Appleton P, Macartney TJ, Näthke I, Rouse J. 2012. DVC1 (C1orf124) recruits the p97 protein segregase to sites of DNA damage. Nature Structural & Molecular Biology 19: 1093-1100. doi: 10. 1038/nsmb. 2394.
10. Dixon SJ, Fedyshyn Y, Koh JLY, Prasad TSK, Chahwan C, Chua G, Toufighi K, Baryshnikova A, Hayles J, Hoe K-L, et al. 2008. Significant conservation of synthetic lethal genetic interaction networks between distantly related eukaryotes. Proceedings of the National Academy of Sciences of the United States of America 105: 16653-16658. doi: 10. 1073/pnas. 0806261105.
11. Dotiwala F, Eapen VV, Harrison JC, Arbel-Eden A, Ranade V, Yoshida S, Haber JE. 2013. DNA damage checkpoint triggers autophagy to regulate the initiation of anaphase. Proceedings of the National Academy of Sciences of the United States of America 110: E41-E49. doi: 10. 1073/pnas. 1218065109.
12. Eletr ZM, Wilkinson KD. 2014. Regulation of proteolysis by human deubiquitinating enzymes. Biochim. Biophys. Acta BBA 1843: 114-128. doi: 10. 1016/j. bbamcr. 2013. 06. 027.
13. Eng JK, McCormack AL, Yates JR. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. Journal of the American Society for Mass Spectrometry 5: 976-989. doi: 10. 1016/1044-0305(94)80016-2.
14. Fernandez-Miranda G, Perez de Castro I, Carmena M, Aguirre-Portoles C, Ruchaud S, Fant X, Montoya G, Earnshaw W, Malumbres M. 2010. SUMOylation modulates the function of Aurora-B kinase. Journal of Cell Science 123: 2823-2833. doi: 10. 1242/jcs. 065565.
15. Geurink PP, El Oualid F, Jonker A, Hameed DS, Ovaa H. 2012. A general chemical ligation approach towards isopeptide-linked ubiquitin and ubiquitin-like assay reagents. Chembiochem: a European journal of chemical biology 13: 293-297. doi: 10. 1002/cbic. 201100706.
16. Gomis-Ruth FX. 2003. Structural aspects of the metzincin clan of metalloendopeptidases. Molecular Biotechnology 24: 157-202.
17. Guntert P, Mumenthaler C, Wuthrich K. 1997. Torsion angle dynamics for NMR structure calculation with the new program DYANA. Journal of Molecular Biology 273: 283-298.
18. Guthrie C, Fink GR. 2002. Guide to yeast genetics and molecular and cell Biology: Part C (Gulf Professional publishing).
19. Hanzelmann P, Schindelin H. 2011. The Structural and Functional Basis of the p97/Valosin-containing Protein (VCP)-interacting Motif (VIM): MUTUALLY EXCLUSIVE BINDING OF COFACTORS TO THE N-TERMINAL DOMAIN OF p97. The Journal of Biological Chemistry 286: 38679-38690. doi: 10. 1074/jbc. M111. 274506.
20. Hardeland U, Steinacher R, Jiricny J, Schar P. 2002. Modification of the human thymine-DNA glycosylase by ubiquitinlike proteins facilitates enzymatic turnover. The EMBO Journal 21: 1456-1464. doi: 10. 1093/emboj/21. 6. 1456.
21. Heideker J, Prudden J, Perry JJP, Tainer JA, Boddy MN. 2011. SUMO-targeted ubiquitin ligase, Rad60, and Nse2 sumo ligase suppress spontaneous Top1-Mediated DNA damage and genome instability. Plos Genetics 7: e1001320. doi: 10. 1371/journal. pgen. 1001320.
22. Ii T, Mullen JR, Slagle CE, Brill SJ. 2007. Stimulation of in vitro sumoylation by Slx5-Slx8: evidence for a functional interaction with the SUMO pathway. DNA Repair 6: 1679-1691. doi: 10. 1016/j. dnarep. 2007. 06. 004.
23. Iyer LM, Koonin EV, Aravind L. 2004. Novel predicted peptidases with a potential role in the ubiquitin signaling pathway. Cell Cycle 3: 1440-1450. doi: 10. 4161/cc. 3. 11. 1206.
24. Jackson StephenP, Durocher D. 2013. Regulation of DNA damage responses by ubiquitin and sumo. Molecular Cell 49: 795-807. doi: 10. 1016/j. molcel. 2013. 01. 017.
25. Johnson ES, Gupta AA. 2001. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106: 735-744. doi: 10. 1016/S0092-8674(01)00491-3.
26. Johnson ES, Schwienhorst I, Dohmen RJ, Blobel G. 1997. The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. The EMBO Journal 16: 5509-5519. doi: 10. 1093/emboj/16. 18. 5509.
27. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4: 363-371. doi: 10. 1038/nprot. 2009. 2.
28. Kerscher O, Felberbaum R, Hochstrasser M. 2006. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annual Review of Cell and Developmental Biology 22: 159-180. doi: 10. 1146/annurev. cellbio. 22. 010605. 093503.
29. Kim MS, Machida Y, Vashisht AA, Wohlschlegel JA, Pang YP, Machida YJ. 2013. Regulation of error-prone translesion synthesis by Spartan/C1orf124. Nucleic Acids Research 41: 1661-1668. doi: 10. 1093/nar/gks1267.
30. Lee MT, Bakir AA, Nguyen KN, Bachant J. 2011. The SUMO isopeptidase Ulp2p is required to prevent recombination-induced chromosome segregation lethality following DNA replication stress. Plos Genetics 7: e1001355. doi: 10. 1371/journal. pgen. 1001355.
31. Lessel D, Vaz B, Halder S, Lockhart PJ, Marinovic-Terzic I, Lopez-Mosqueda J, Philipp M, Sim JC, Smith KR, Oehler J, et al. 2014. Mutations in SPRTN cause early onset hepatocellular carcinoma, genomic instability and progeroid features. Nature Genetics 46: 1239-1244. doi: 10. 1038/ng. 3103.
32. Liu C, Apodaca J, Davis LE, Rao H. 2007. Proteasome inhibition in wild-type yeast Saccharomyces cerevisiae cells. Biotechniques 42: 158, 160, 162.
33. Liu C, Pouliot JJ, Nash HA. 2002. Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proceedings of the National Academy of Sciences of the United States of America 99: 14970-14975. doi: 10. 1073/pnas. 182557199.
34. Lopez-Pelegrin M, Cerda-Costa N, Martinez-Jimenez F, Cintas-Pedrola A, Canals A, Peinado JR, Marti-Renom MA, Lopez-Otin C, Arolas JL, Gomis-Ruth FX. 2013. A novel family of soluble minimal scaffolds provides structural insight into the catalytic domains of integral membrane metallopeptidases. The Journal of Biological Chemistry 288: 21279-21294. doi: 10. 1074/jbc. M113. 476580.
35. Makhnevych T, Sydorskyy Y, Xin X, Srikumar T, Vizeacoumar FJ, Jeram SM, Li Z, Bahr S, Andrews BJ, Boone C, et al. 2009. Global map of sumo function revealed by protein-protein interaction and genetic networks. Molecular Cell 33: 124-135. doi: 10. 1016/j. molcel. 2008. 12. 025.
36. Maskey RS, Kim MS, Baker DJ, Childs B, Malureanu LA, Jeganathan KB, Machida Y, van Deursen JM, Machida YJ. 2014. Spartan deficiency causes genomic instability and progeroid phenotypes. Nature Communications 5: 5744. doi: 10. 1038/ncomms6744.
37. Merrill JC, Melhuish TA, Kagey MH, Yang S-H, Sharrocks AD, Wotton D. 2010. A role for non-covalent sumo interaction motifs in Pc2/CBX4 E3 activity. Plos One 5. doi: 10. 1371/journal. pone. 0008794.
38. Meyer H, Bug M, Bremer S. 2012. Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nature Cell Biology 14: 117-123. doi: 10. 1038/ncb2407.
39. Mosbech A, Gibbs-Seymour I, Kagias K, Thorslund T, Beli P, Povlsen L, Nielsen SV, Smedegaard S, Sedgwick G, Lukas C, et al. 2012. DVC1 (C1orf124) is a DNA damage-targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks. Nature Structural & Molecular Biology 19: 1084-1092. doi: 10. 1038/nsmb. 2395.
40. Mucha A, Drag M, Dalton JP, Kafarski P. 2010. Metallo-aminopeptidase inhibitors. Biochimie 92: 1509-1529. doi: 10. 1016/j. biochi. 2010. 04. 026.
41. Mullally JE, Chernova T, Wilkinson KD. 2006. Doa1 is a Cdc48 adapter that Possesses a novel ubiquitin binding domain. Molecular and Cellular Biology 26: 822-830. doi: 10. 1128/MCB. 26. 3. 822-830. 2006.
42. Mullen JR, Chen CF, Brill SJ. 2010. Wss1 is a sumo-dependent isopeptidase that interacts Genetically with the Slx5-Slx8 sumo-targeted ubiquitin ligase. Molecular and Cellular Biology 30: 3737-3748. doi: 10. 1128/MCB. 01649-09.
43. Mullen JR, Das M, Brill SJ. 2011. Genetic evidence that Polysumoylation Bypasses the need for a sumo-targeted ub ligase. Genetics 187: 73-87. doi: 10. 1534/genetics. 110. 124347.
44. Nakano T, Katafuchi A, Matsubara M, Terato H, Tsuboi T, Masuda T, Tatsumoto T, Pack SP, Makino K, Croteau DL. 2009. Homologous recombination but not nucleotide excision repair plays a pivotal role in tolerance of DNAprotein cross-links in mammalian cells. The Journal of Biological Chemistry 284: 27065-27076. doi: 10. 1074/jbc. M109. 019174.
45. Nakano T, Morishita S, Katafuchi A, Matsubara M, Horikawa Y, Terato H, Salem AM, Izumi S, Pack SP, Makino K. 2007. Nucleotide excision repair and homologous recombination systems commit differentially to the repair of DNA-protein crosslinks. Molecular Cell 28: 147-158. doi: 10. 1016/j. molcel. 2007. 07. 029.
46. Neims AH, Coffey DS, Hellerman L. 1966. Interaction between tetraethylthiuram disulfide and the sulfhydryl groups of D-amino acid oxidase and of hemoglobin. The Journal of Biological Chemistry 241: 5941-5948.
47. Nie M, Aslanian A, Prudden J, Heideker J, Vashisht AA, Wohlschlegel JA, Yates JR, Boddy MN. 2012. Dual Recruitment of Cdc48 (p97)-Ufd1-Npl4 ubiquitin-selective segregase by small ubiquitin-like modifier protein (SUMO) and ubiquitin in sumo-targeted ubiquitin ligase-mediated genome stability functions. The Journal of Biological Chemistry 287: 29610-29619. doi: 10. 1074/jbc. M112. 379768.
48. O'Neill BM. 2004. Coordinated functions of WSS1, PSY2 and TOF1 in the DNA damage response. Nucleic Acids Research 32: 6519-6530. doi: 10. 1093/nar/gkh994.
49. Ossareh-Nazari B, Bonizec M, Cohen M, Dokudovskaya S, Delalande F, Schaeffer C, Van Dorsselaer A, Dargemont C. 2010. Cdc48 and Ufd3, new partners of the ubiquitin protease Ubp3, are required for ribophagy. EMBO Rep 11: 548-554. doi: 10. 1038/embor. 2010. 74.
50. Parker JL, Ulrich HD. 2014. SIM-dependent enhancement of substrate-specific SUMOylation by a ubiquitin ligase in vitro. The Biochemical Journal 457: 435-440. doi: 10. 1042/BJ20131381.
51. 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. Journal of Proteome Research 2: 43-50. doi: 10. 1021/pr025556v.
52. Peng J, Gygi SP. 2001. Proteomics: the move to mixtures. Journal of Mass Spectrometry: JMS 36: 1083-1091. doi: 10. 1002/jms. 229.
53. Perry JJP, Tainer JA, Boddy MN. 2008. A SIM-ultaneous role for SUMO and ubiquitin. Trends in Biochemical Sciences 33: 201-208. doi: 10. 1016/j. tibs. 2008. 02. 001.
54. Polo SE, Jackson SP. 2011. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes & Development 25: 409-433. doi: 10. 1101/gad. 2021311.
55. Pommier Y, Barcelo JM, Rao VA, Sordet O, Jobson AG, Thibaut L, Miao ZH, Seiler JA, Zhang H, Marchand C, et al. 2006. Repair of topoisomerase I-Mediated DNA damage. Prog. Nucleic Acid Res. Mol. Biol: Elsevier. p. 179-229.
56. Psakhye I, Jentsch S. 2012. Protein group modification and Synergy in the sumo pathway as Exemplified in DNA repair. Cell 151: 807-820. doi: 10. 1016/j. cell. 2012. 10. 021.
57. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Seraphin B. 2001. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods: a Companion To Methods in enzymology. [methods (san Diego, Calif.)] 24: 218-229. doi: 10. 1006/meth. 2001. 1183.
58. Ren J, Pashkova N, Winistorfer S, Piper RC. 2008. DOA1/UFD3 plays a role in sorting ubiquitinated membrane proteins into Multivesicular bodies. The Journal of Biological Chemistry 283: 21599-21611. doi: 10. 1074/jbc. M802982200.
59. Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R, Botrugno OA, Parazzoli D, Oldani A, Minucci S, et al. 2011. HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 471: 74-79. doi: 10. 1038/nature09803.
60. Sarangi P, Bartosova Z, Altmannova V, Holland C, Chavdarova M, Lee SE, Krejci L, Zhao X. 2014. Sumoylation of the Rad1 nuclease promotes DNA repair and regulates its DNA association. Nucleic Acids Research 42: 6393-6404. doi: 10. 1093/nar/gku300.
61. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson H. 2005. Nucleic Acids Research 33: (Web Server issue). W363-W367.
62. Shen Y, Delaglio F, Cornilescu G, Bax A. 2009. TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. Journal of Biomolecular NMR 44: 213-223. doi: 10. 1007/s10858-009-9333-z.
63. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Analytical Chemistry 68: 850-858. doi: 10. 1021/ac950914h.
64. Sriramachandran AM, Dohmen RJ. 2014. SUMO-targeted ubiquitin ligases. Biochim. Biophys. Acta BBA 1843: 75-85. doi: 10. 1016/j. bbamcr. 2013. 08. 022.
65. Stapf C, Cartwright E, Bycroft M, Hofmann K, Buchberger A. 2011. The general Definition of the p97/Valosincontaining protein (VCP)-interacting motif (VIM) Delineates a new family of p97 cofactors. The Journal of Biological Chemistry 286: 38670-38678. doi: 10. 1074/jbc. M111. 274472.
66. Stingele J, Schwarz Michael S, Bloemeke N, Wolf Peter G, Jentsch S. 2014. A DNA-dependent protease involved in DNA-protein crosslink repair. Cell 158: 327-338. doi: 10. 1016/j. cell. 2014. 04. 053.
67. Takahashi Y, Toh EA, Kikuchi Y. 2003. Comparative analysis of yeast PIAS-type SUMO ligases in vivo and in vitro. Journal of Biochemistry 133: 415-422. doi: 10. 1093/jb/mvg054.
68. Vallari RC, Pietruszko R. 1982. Human aldehyde dehydrogenase: mechanism of inhibition of disulfiram. Science 216: 637-639. doi: 10. 1126/science. 7071604.
69. Van Heusden GPH, Steensma HY. 2008. The saccharomyces cerevisiae wss1 protein is only present in mother cells. FEMS Lett. 282: 100-104. doi: 10. 1111/j. 1574-6968. 2008. 01113. x.
70. Vance JR, Wilson TE. 2002. Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proceedings of the National Academy of Sciences of the United States of America 99: 13669-13674. doi: 10. 1073/pnas. 202242599.
71. Vaz B, Halder S, Ramadan K. 2013. Role of p97/VCP (Cdc48) in genome stability. Front. Genet 4. doi: 10. 3389/fgene. 2013. 00060.
72. Verma R, Oania R, Fang R, Smith GT, Deshaies RJ. 2011. Cdc48/p97 Mediates UV-Dependent Turnover of RNA Pol II. Mol. Cell 41: 82-92. doi: 10. 1016/j. molcel. 2010. 12. 017.
73. Vessoni AT, Filippi-Chiela EC, Menck CF, Lenz G. 2013. Autophagy and genomic integrity. Cell Death Different 20: 1444-1454. doi: 10. 1038/cdd. 2013. 103.
74. von der Haar T. 2007. Optimized protein extraction for quantitative proteomics of yeasts. Plos One 2: e1078. doi: 10. 1371/journal. pone. 0001078.
75. White HD, Rayment I. 1993. Kinetic characterization of reductively methylated myosin subfragment 1. Biochemistry 32: 9859-9865. doi: 10. 1021/bi00088a042.
76. Wilkinson KD, Gan-Erdene T, Kolli N. 2005. Derivitization of the C-terminus of ubiquitin and ubiquitin-like proteins using intein chemistry: methods and uses. Methods Enzymol 399: 37-51. doi: 10. 1016/S0076-6879(05)99003-4.
77. Wuthrich K. 1986. NMR of proteins and nucleic acids. The George Fisher Baker non-resident lectureship in chemistry at Cornell Unversity (USA).
78. Yeung Heidi O, Kloppsteck P, Niwa H, Isaacson Rivka L, Matthews S, Zhang X, Freemont Paul S. 2008. Insights into adaptor binding to the AAA protein p97. Biochemical Society Transactions 36. doi: 10. 1042/BST0360062.