A Critical Role for the Ubiquitin-Conjugating Enzyme Ubc13 in Initiating Homologous Recombination

Molecular Cell

Volumn 25, Issue 5, 2007, Pages 663-675

  Zhao, Guang Yu ^a   Sonoda, Eiichiro ^a   Barber, Louise J ^b   Oka, Hayato ^a   Murakawa, Yasuhiro ^a   Yamada, Kouichi ^c   Ikura, Tsuyoshi ^d   Wang, Xin ^a   Kobayashi, Masahiko ^e   Yamamoto, Kenichi ^e   Boulton, Simon J ^b   Takeda, Shunichi ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c NATIONAL INSTITUTE OF HEALTH AND NUTRITION   (Japan)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e KANAZAWA UNIVERSITY   (Japan)

Author keywords

DNA; PROTEINS

Indexed keywords

BRCA1 PROTEIN; DNA BINDING PROTEIN; NUCLEIC ACID BINDING PROTEIN; NUCLEOPROTEIN; PROTEIN RAD18; PROTEIN RAD6; RAD51 PROTEIN; SINGLE STRANDED DNA; SMALL INTERFERING RNA; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME UBC13; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CHICKEN; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME ACTIVITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; NONHUMAN; POSTREPLICATION REPAIR; PROTEIN SYNTHESIS INHIBITION; RADIOSENSITIVITY; ULTRAVIOLET RADIATION; VERTEBRATE; YEAST;

ANIMALS; BRCA1 PROTEIN; CELL NUCLEUS; CHICKENS; CHROMOSOMES; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; ENZYME ACTIVATION; EXONS; GENE TARGETING; HELA CELLS; HISTONES; HUMANS; INFRARED RAYS; MODELS, GENETIC; MUTAGENS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; REPLICATION PROTEIN A; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES; ULTRAVIOLET RAYS;

SACCHAROMYCETALES; VERTEBRATA;

EID: 33847413700     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.01.029     Document Type: Article

References (50)

1. Adachi N., So S., and Koyama H. Loss of nonhomologous end joining confers camptothecin resistance in DT40 cells. Implications for the repair of topoisomerase I-mediated DNA damage. J. Biol. Chem. 279 (2004) 37343-37348
2. Andersen P.L., Zhou H., Pastushok L., Moraes T., McKenna S., Ziola B., Ellison M.J., Dixit V.M., and Xiao W. Distinct regulation of Ubc13 functions by the two ubiquitin-conjugating enzyme variants Mms2 and Uev1A. J. Cell Biol. 170 (2005) 745-755
3. 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
4. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003) 499-506
5. Bergink S., Salomons F.A., Hoogstraten D., Groothuis T.A., de Waard H., Wu J., Yuan L., Citterio E., Houtsmuller A.B., Neefjes J., et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 20 (2006) 1343-1352
6. 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 310 (2005) 1821-1824
7. Elliott B., Richardson C., and Jasin M. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol. Cell 17 (2005) 885-894
8. Garcia-Muse T., and Boulton S.J. Distinct modes of ATR activation after replication stress and DNA double-strand breaks in Caenorhabditis elegans. EMBO J. 24 (2005) 4345-4355
9. Greenberg R.A., Sobhian B., Pathania S., Cantor S.B., Nakatani Y., and Livingston D.M. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev. 20 (2006) 34-46
10. Guo C., Sonoda E., Tang T.S., Parker J.L., Bielen A.B., Takeda S., Ulrich H.D., and Friedberg E.C. REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol. Cell 23 (2006) 265-271
11. Hashizume R., Fukuda M., Maeda I., Nishikawa H., Oyake D., Yabuki Y., Ogata H., and Ohta T. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276 (2001) 14537-14540
12. Hatanaka A., Yamazoe M., Sale J.E., Takata M., Yamamoto K., Kitao H., Sonoda E., Kikuchi K., Yonetani Y., and Takeda S. Similar effects of Brca2 truncation and Rad51 paralog deficiency on immunoglobulin V gene diversification in DT40 cells support an early role for Rad51 paralogs in homologous recombination. Mol. Cell. Biol. 25 (2005) 1124-1134
13. 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
14. 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., and D'Andrea A.D. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat. Cell Biol. 8 (2006) 339-347
15. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., and Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102 (2000) 463-473
16. Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., and Jackson S.P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8 (2006) 37-45
17. Kannouche P.L., Wing J., and 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 14 (2004) 491-500
18. Kimura H., Takizawa N., Allemand E., Hori T., Iborra F.J., Nozaki N., Muraki M., Hagiwara M., Krainer A.R., Fukagawa T., and Okawa K. A novel histone exchange factor, protein phosphatase 2Cgamma, mediates the exchange and dephosphorylation of H2A-H2B. J. Cell Biol. 175 (2006) 389-400
19. Mallery D.L., Vandenberg C.J., and Hiom K. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J. 21 (2002) 6755-6762
20. Motegi A., Sood R., Moinova H., Markowitz S.D., Liu P.P., and Myung K. Human SHPRH suppresses genomic instability through proliferating cell nuclear antigen polyubiquitination. J. Cell Biol. 175 (2006) 703-708
21. O'Driscoll M., and Jeggo P.A. The role of double-strand break repair-insights from human genetics. Nat. Rev. Genet. 7 (2006) 45-54
22. 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
23. Polanowska J., Martin J.S., Garcia-Muse T., Petalcorin M.I., and Boulton S.J. A conserved pathway to activate BRCA1-dependent ubiquitylation at DNA damage sites. EMBO J. 25 (2006) 2178-2188
24. Prakash L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet. 184 (1981) 471-478
25. Prakash S., Johnson R.E., and Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74 (2005) 317-353
26. Saberi A., Hochegger H., Szuts D., Lan L., Yasui A., Sale J.E., Taniguchi Y., Murakawa Y., Zheng W., Yokomori K., et al. RAD18 and poly[ADP ribose]polymerase independently suppress the access of nonhomologous end joining to double strand breaks and facilitate homologous recombination mediated repair. Mol. Cell. Biol. (2007) 10.1128/MCB.01243-06 in press. Published online January 22, 2007
27. Saleh-Gohari N., Bryant H.E., Schultz N., Parker K.M., Cassel T.N., and Helleday T. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol. Cell. Biol. 25 (2005) 7158-7169
28. Shivji M.K., and Venkitaraman A.R. DNA recombination, chromosomal stability and carcinogenesis: insights into the role of BRCA2. DNA Repair (Amst.) 3 (2004) 835-843
29. Simon J.A., Szankasi P., Nguyen D.K., Ludlow C., Dunstan H.M., Roberts C.J., Jensen E.L., Hartwell L.H., and Friend S.H. Differential toxicities of anticancer agents among DNA repair and checkpoint mutants of Saccharomyces cerevisiae. Cancer Res. 60 (2000) 328-333
30. 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
31. Sonoda E., Sasaki M.S., Buerstedde J.M., Bezzubova O., Shinohara A., Ogawa H., Takata M., Yamaguchi-Iwai Y., and Takeda S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17 (1998) 598-608
32. Sonoda E., Sasaki M.S., Morrison C., Yamaguchi-Iwai Y., Takata M., and Takeda S. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 19 (1999) 5166-5169
33. Sonoda E., Okada T., Zhao G.Y., Tateishi S., Araki K., Yamaizumi M., Yagi T., Verkaik N.S., van Gent D.C., Takata M., and Takeda S. Multiple roles of Rev3, the catalytic subunit of polzeta in maintaining genome stability in vertebrates. EMBO J. 22 (2003) 3188-3197
34. Sonoda E., Hochegger H., Saberi A., Taniguchi Y., and Takeda S. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 5 (2006) 1021-1029
35. Sonoda E., Zhao G.Y., Kohzaki M., Dhar P.K., Kikuchi K., Redon C., Pilchc D.R., Bonner W.B., Nakano A., Watanabe M., et al. Collaborative roles of gamma-H2AX and the Rad51 paralog Xrcc3 in homologous recombinational repair. DNA Repair (Amst.) 6 (2007) 280-292
36. Stelter P., and Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425 (2003) 188-191
37. Sugawara N., Wang X., and Haber J.E. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12 (2003) 209-219
38. Szuts D., Simpson L.J., Kabani S., Yamazoe M., and Sale J.E. Role for RAD18 in homologous recombination in DT40 cells. Mol. Cell. Biol. 26 (2006) 8032-8041
39. Takata M., Sasaki M.S., Tachiiri S., Fukushima T., Sonoda E., Schild D., Thompson L.H., and Takeda S. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 21 (2001) 2858-2866
40. Thacker J. The RAD51 gene family, genetic instability and cancer. Cancer Lett. 219 (2005) 125-135
41. Tsubouchi H., and Ogawa H. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11 (2000) 2221-2233
42. Ulrich H.D., and Jentsch S. Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19 (2000) 3388-3397
43. Vandenberg C.J., Gergely F., Ong C.Y., Pace P., Mallery D.L., Hiom K., and Patel K.J. BRCA1-independent ubiquitination of FANCD2. Mol. Cell 12 (2003) 247-254
44. Wang H., Zhai L., Xu J., Joo H.Y., Jackson S., Erdjument-Bromage H., Tempst P., Xiong Y., and Zhang Y. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 22 (2006) 383-394
45. Watanabe K., Tateishi S., Kawasuji M., Tsurimoto T., Inoue H., and Yamaizumi M. Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 23 (2004) 3886-3896
46. Xiao W., Chow B.L., Broomfield S., and Hanna M. The Saccharomyces cerevisiae RAD6 group is composed of an error-prone and two error-free postreplication repair pathways. Genetics 155 (2000) 1633-1641
47. Xie A., Puget N., Shim I., Odate S., Jarzyna I., Bassing C.H., Alt F.W., and Scully R. Control of sister chromatid recombination by histone H2AX. Mol. Cell 16 (2004) 1017-1025
48. Yamaguchi-Iwai Y., Sonoda E., Sasaki M.S., Morrison C., Haraguchi T., Hiraoka Y., Yamashita Y.M., Yagi T., Takata M., Price C., et al. Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 18 (1999) 6619-6629
49. Yamazoe M., Sonoda E., Hochegger H., and Takeda S. Reverse genetic studies of the DNA damage response in the chicken B lymphocyte line DT40. DNA Repair (Amst.) 3 (2004) 1175-1185
50. Yoshimura A., Nishino K., Takezawa J., Tada S., Kobayashi T., Sonoda E., Kawamoto T., Takeda S., Ishii Y., Yamada K., et al. A novel Rad18 function involved in protection of the vertebrate genome after exposure to camptothecin. DNA Repair (Amst.) 5 (2006) 1307-1316