SHPRH and HLTF Act in a Damage-Specific Manner to Coordinate Different Forms of Postreplication Repair and Prevent Mutagenesis

Molecular Cell

Volumn 42, Issue 2, 2011, Pages 237-249

  Lin, Jia Ren ^a   Zeman, Michelle K ^a   Chen, Jia Yun ^a   Yee, Muh Ching ^a   Cimprich, Karlene A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE LIKE TRANSCRIPTION FACTOR; PROTEIN; RAD18 PROTEIN; SNF2 HISTONE LINKER PHD FINGER RING FINGER HELICASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; MUTAGENESIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; ULTRAVIOLET RADIATION;

CELL NUCLEUS; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; HEK293 CELLS; HUMANS; METHYL METHANESULFONATE; MUTAGENESIS; MUTAGENS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; ULTRAVIOLET RAYS;

MAMMALIA;

EID: 79954505570     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.02.026     Document Type: Article

References (39)

1. Bi X., Barkley L.R., Slater D.M., Tateishi S., Yamaizumi M., Ohmori H., Vaziri C. Rad18 regulates DNA polymerase kappa and is required for recovery from S-phase checkpoint-mediated arrest. Mol. Cell. Biol. 2006, 26:3527-3540.
2. Bienko M., Green C.M., Crosetto N., Rudolf F., Zapart G., Coull B., Kannouche P., Wider G., Peter M., Lehmann A.R., et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 2005, 310:1821-1824.
3. Blastyak A., Pinter L., Unk I., Prakash L., Prakash S., Haracska L. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell 2007, 28:167-175.
4. Blastyak A., Hajdu I., Unk I., Haracska L. Role of double-stranded DNA translocase activity of human HLTF in replication of damaged DNA. Mol. Cell. Biol. 2010, 30:684-693.
5. Branzei D., Foiani M. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 2008, 9:297-308.
6. Branzei D., Foiani M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 2010, 11:208-219.
7. Broomfield S., Hryciw T., Xiao W. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. 2001, 486:167-184.
8. Chang D.J., Cimprich K.A. DNA damage tolerance: when it's OK to make mistakes. Nat. Chem. Biol. 2009, 5:82-90.
9. Choi J.H., Pfeifer G.P. The role of DNA polymerase eta in UV mutational spectra. DNA Repair (Amst.) 2005, 4:211-220.
10. Coulon S., Ramasubramanyan S., Alies C., Philippin G., Lehmann A., Fuchs R.P. Rad8Rad5/Mms2-Ubc13 ubiquitin ligase complex controls translesion synthesis in fission yeast. EMBO J. 2010, 29:2048-2058.
11. Creagh E.M., Murphy B.M., Duriez P.J., Duckett C.S., Martin S.J. Smac/Diablo antagonizes ubiquitin ligase activity of inhibitor of apoptosis proteins. J. Biol. Chem. 2004, 279:26906-26914.
12. Friedberg E.C. Suffering in silence: the tolerance of DNA damage. Nat. Rev. Mol. Cell Biol. 2005, 6:943-953.
13. Gangavarapu V., Haracska L., Unk I., Johnson R.E., Prakash S., Prakash L. Mms2-Ubc13-dependent and -independent roles of Rad5 ubiquitin ligase in postreplication repair and translesion DNA synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 2006, 26:7783-7790.
14. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002, 419:135-141.
15. Huang T.T., Nijman S.M., Mirchandani K.D., Galardy P.J., Cohn M.A., Haas W., Gygi S.P., Ploegh H.L., Bernards R., D'Andrea A.D. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat. Cell Biol. 2006, 8:339-347.
16. Johnson R.E., Henderson S.T., Petes T.D., Prakash S., Bankmann M., Prakash L. Saccharomyces cerevisiae RAD5-encoded DNA repair protein contains DNA helicase and zinc-binding sequence motifs and affects the stability of simple repetitive sequences in the genome. Mol. Cell. Biol. 1992, 12:3807-3818.
17. Johnson R.E., Prakash S., Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Pol eta. Science 1999, 283:1001-1004.
18. Johnson R.E., Yu S.L., Prakash S., Prakash L. A role for yeast and human translesion synthesis DNA polymerases in promoting replication through 3-methyl adenine. Mol. Cell. Biol. 2007, 27:7198-7205.
19. Kannouche P., Broughton B.C., Volker M., Hanaoka F., Mullenders L.H., Lehmann A.R. Domain structure, localization, and function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev. 2001, 15:158-172.
20. Kannouche P.L., Wing J., Lehmann A.R. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 2004, 14:491-500.
21. Lee K.Y., Myung K. PCNA modifications for regulation of post-replication repair pathways. Mol. Cells 2008, 26:5-11.
22. Masutani C., Araki M., Yamada A., Kusumoto R., Nogimori T., Maekawa T., Iwai S., Hanaoka F. Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J. 1999, 18:3491-3501.
23. Motegi A., Sood R., Moinova H., Markowitz S.D., Liu P.P., Myung K. Human SHPRH suppresses genomic instability through proliferating cell nuclear antigen polyubiquitination. J. Cell Biol. 2006, 175:703-708.
24. Motegi A., Liaw H.J., Lee K.Y., Roest H.P., Maas A., Wu X., Moinova H., Markowitz S.D., Ding H., Hoeijmakers J.H., et al. Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc. Natl. Acad. Sci. USA 2008, 105:12411-12416.
25. Myers J.W., Jones J.T., Meyer T., Ferrell J.E. Recombinant Dicer efficiently converts large dsRNAs into siRNAs suitable for gene silencing. Nat. Biotechnol. 2003, 21:324-328.
26. Ohashi E., Ogi T., Kusumoto R., Iwai S., Masutani C., Hanaoka F., Ohmori H. Error-prone bypass of certain DNA lesions by the human DNA polymerase kappa. Genes Dev. 2000, 14:1589-1594.
27. Pages V., Bresson A., Acharya N., Prakash S., Fuchs R.P., Prakash L. Requirement of Rad5 for DNA polymerase zeta-dependent translesion synthesis in Saccharomyces cerevisiae. Genetics 2008, 180:73-82.
28. Parris C.N., Seidman M.M. A signature element distinguishes sibling and independent mutations in a shuttle vector plasmid. Gene 1992, 117:1-5.
29. Plosky B.S., Frank E.G., Berry D.A., Vennall G.P., McDonald J.P., Woodgate R. Eukaryotic Y-family polymerases bypass a 3-methyl-2′-deoxyadenosine analog in vitro and methyl methanesulfonate-induced DNA damage in vivo. Nucleic Acids Res. 2008, 36:2152-2162.
30. Prakash S., Johnson R.E., Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 2005, 74:317-353.
31. Stelter P., Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 2003, 425:188-191.
32. Takenaka K., Ogi T., Okada T., Sonoda E., Guo C., Friedberg E.C., Takeda S. Involvement of vertebrate Pol kappa in translesion DNA synthesis across DNA monoalkylation damage. J. Biol. Chem. 2006, 281:2000-2004.
33. Ulrich H.D. Regulating post-translational modifications of the eukaryotic replication clamp PCNA. DNA Repair (Amst.) 2009, 8:461-469.
34. Ulrich H.D., Jentsch S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 2000, 19:3388-3397.
35. Unk I., Hajdu I., Fatyol K., Szakal B., Blastyak A., Bermudez V., Hurwitz J., Prakash L., Prakash S., Haracska L. Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. USA 2006, 103:18107-18112.
36. Unk I., Hajdu I., Fatyol K., Hurwitz J., Yoon J.H., Prakash L., Prakash S., Haracska L. Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc. Natl. Acad. Sci. USA 2008, 105:3768-3773.
37. Unk I., Hajdu I., Blastyak A., Haracska L. Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance. DNA Repair (Amst.) 2010, 9:257-267.
38. Watanabe K., Tateishi S., Kawasuji M., Tsurimoto T., Inoue H., Yamaizumi M. Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 2004, 23:3886-3896.
39. Waters L.S., Minesinger B.K., Wiltrout M.E., D'Souza S., Woodruff R.V., Walker G.C. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 2009, 73:134-154.