Browse > Article

PCNA Modifications for Regulation of Post-Replication Repair Pathways  

Lee, Kyoo-young (Genome Instability Section, Genetics and Molecular Biology Branch, National Human Genome Research Institute, National Institutes of Health)
Myung, Kyungjae (Genome Instability Section, Genetics and Molecular Biology Branch, National Human Genome Research Institute, National Institutes of Health)
Abstract
Stalled DNA replication forks activate specific DNA repair mechanism called post-replication repair (PRR) pathways that simply bypass DNA damage. The bypassing of DNA damage by PRR prevents prolonged stalling of DNA replication that could result in double strand breaks (DSBs). Proliferating cell nuclear antigen (PCNA) functions to initiate and choose different bypassing pathways of PRR. In yeast, DNA replication forks stalled by DNA damage induces monoubiquitination of PCNA at K164, which is catalyzed by Rad6/Rad18 complex. PCNA monoubiquitination triggers the replacement of replicative polymerase with special translesion synthesis (TLS) polymerases that are able to replicate past DNA lesions. The PCNA interaction motif and/or the ubiquitin binding motif in most TLS polymerases seem to be important for the regulation of TLS. The TLS pathway is usually error-prone because TLS polymerases have low fidelity and no proofreading activity. PCNA can also be further polyubiquitinated by Ubc13/ Mms2/Rad5 complex, which adds an ubiquitin chain onto monoubiquitinated K164 of PCNA. PCNA polyubiquitination directs a different PRR pathway known as error-free damage avoidance, which uses the newly synthesized sister chromatid as a template to bypass DNA damage presumably through template switching mechanism. Mammalian homologues of all of the yeast PRR proteins have been identified, thus PRR is well conserved throughout evolution. Mutations of some PRR genes are associated with a higher risk for cancers in mice and human patients, strongly supporting the importance of PRR as a tumor suppressor pathway.
Keywords
damage bypass; PCNA ubiquitination; post-replication repair; RAD6/RAD18 complex; template switching; translesion synthesis; UBC13/MMS2/RAD5 complex;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 35  (Related Records In Web of Science)
연도 인용수 순위
1 Li, Z., Xiao, W., McCormick, J.J., and Maher, V.M. (2002). Identification of a protein essential for a major pathway used by human cells to avoid UV- induced DNA damage. Proc. Natl. Acad. Sci. USA99, 4459-4464
2 Murakumo, Y., Ogura, Y., Ishii, H., Numata, S., Ichihara, M.,and Croce, C.M., Fishel, R., and Takahashi, M. (2001). Interactions in the error-prone postreplication repair proteins hREV1, hREV3, and hREV7. J. Biol. Chem.276, 35644-35651   DOI   ScienceOn
3 Nelson, J.R., Lawrence, C.W., and Hinkle, D.C. (1996). Thyminethymine dimer bypass by yeast DNA polymerase zeta. Science 272, 1646-1649   DOI   ScienceOn
4 Nikolaishvili-Feinberg, N., Jenkins, G.S., Nevis, K.R., Staus, D.P., Scarlett, C.O., Unsal-Kacmaz, K., Kaufmann, W.K., and Cordeiro- Stone, M. (2008). Ubiquitylation of proliferating cell nuclear antigen and recruitment of human DNA polymerase eta. Biochemistry 47, 4141-4150   DOI   ScienceOn
5 Prakash, S., Johnson, R.E., and Prakash, L. (2005). Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem.74, 317-353   DOI   ScienceOn
6 Sood, R., Makalowska, I., Galdzicki, M., Hu, P., Eddings, E.I Robbins, C.M., Moses, T., Namkoong, J., Chen, S., and Trent, J.M. (2003). Cloning and characterization of a novel gene, SHPRH, encoding a conserved putative protein with SNF2/helicase and PHD-finger domains from the 6q24 region. Genomics 82, 153- 161   DOI   ScienceOn
7 Tercero, J.A., and Diffley, J.F. (2001). Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412, 553-557   DOI   ScienceOn
8 Ulrich, H.D., and Jentsch, S. (2000). Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19, 3388-3397   DOI   ScienceOn
9 Unk, I., Hajdu, I., Fatyol, K., Hurwitz, J., Yoon, J.H., Prakash, L., Prakash, S., and Haracska, L. (2008). Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc. Natl. Acad. Sci. USA 105, 3768-3773
10 Watanabe, K., Tateishi, S., Kawasuji, M., Tsurimoto, T., Inoue, H.I and Yamaizumi, M. (2004). Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 23, 3886-3896   DOI   ScienceOn
11 Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21   DOI   ScienceOn
12 Acharya, N., Brahma, A., Haracska, L., Prakash, L., and Prakash, S. (2007). Mutations in the ubiquitin binding UBZ motif of DNA polymerase eta do not impair its function in translesion synthesis during replication. Mol. Cell. Biol. 27, 7266-7272   DOI   ScienceOn
13 Bailly, V., Lauder, S., Prakash, S., and Prakash, L. (1997). Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J. Biol. Chem. 272, 23360-23365   DOI   ScienceOn
14 Barbour, L., and Xiao, W. (2003). Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat. Res.532, 137- 155   DOI
15 Byun, T.S., Pacek, M., Yee, M.C., Walter, J.C., and Cimprich, K.A. (2005). Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 19, 1040-1052   DOI   ScienceOn
16 Chang, D.J., Lupardus, P.J., and Cimprich, K.A. (2006). Monoubiquitination of proliferating cell nuclear antigen induced by stalled replication requires uncoupling of DNA polymerase and mini-chromosome maintenance helicase activities. J. Biol. Chem. 281, 32081-32088   DOI   ScienceOn
17 Dumstorf, C.A., Clark, A.B., Lin, Q., Kissling, G.E., Yuan, T., Kucherlapati, R., McGregor, W.G., and Kunkel, T.A.(2006). Participation of mouse DNA polymerase iota in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer. Proc. Natl. Acad. Sci. USA 103, 18083-18088
18 Haracska, L., Unk, I., Johnson, R.E., Johansson, E., Burgers, P.M., Prakash, S., and Prakash, L. (2001). Roles of yeast DNA polymerases delta and zeta and of Rev1 in the bypass of abasic sites. Genes Dev.15, 945-954   DOI   ScienceOn
19 Frampton, J., Irmisch, A., Green, C.M., Neiss, A., Trickey, M.I Ulrich, H.D., Furuya, K., Watts, F.Z., Carr, A.M., and Lehmann, A.R. (2006). Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Mol. Biol. Cell.17, 2976-2985   DOI   ScienceOn
20 Garg, P., and Burgers, P.M. (2005). Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases eta and REV1. Proc. Natl. Acad. Sci. USA 102, 18361-18366
21 Haracska, L., Unk, I., Prakash, L., and Prakash, S. (2006). Ubiquitylation of yeast proliferating cell nuclear antigen and its implications for translesion DNA synthesis. Proc. Natl. Acad. Sci. USA 103, 6477-6482
22 Hoege, C., Pfander, B., Moldovan, G.L., Pyrowolakis, G., and Jentsch, S. (2002). RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141   DOI   ScienceOn
23 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.,(2006). Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat. Cell Biol. 8, 339-347
24 Johnson, R.E., Henderson, S.T., Petes, T.D., Prakash, S., Bankmann, M.,and Prakash, L. (1992). 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. 12, 3807- 3818   DOI
25 Johnson, R.E., Kondratick, C.M., Prakash, S., and Prakash, L. (1999). hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285, 263-265   DOI   ScienceOn
26 Lawrence, C. (1994). The RAD6 DNA repair pathway in Saccharomyces cerevisiae: what does it do, and how does it do it? Bioessays NS, 253-258   DOI   ScienceOn
27 Parker, J.L., Bielen, A.B., Dikic, I., and Ulrich, H.D. (2007). Contributions of ubiquitin- and PCNA-binding domains to the activity of Polymerase eta in Saccharomyces cerevisiae. Nucleic Acids Res.35, 881-889   DOI   ScienceOn
28 Lawrence, C.W., Gibbs, P.E., Murante, R.S., Wang, X.D., Li, Z., McManus, T.P., McGregor, W.G., Nelson, J.R., Hinkle, D.C., and Maher, V.M. (2000). Roles of DNA polymerase zeta and Rev1 protein in eukaryotic mutagenesis and translesion replication. Cold Spring Harb. Symp. Quant. Biol. 65, 61-69
29 Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K., and Hanaoka, F.(1999). The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 339, 700-704
30 Ogi, T., Kannouche, P., and Lehmann, A.R. (2005). Localisation of human Y-family DNA polymerase kappa: relationship to PCNA foci. J. Cell Sci. 118, 129-136   DOI   ScienceOn
31 Hofmann, R.M., and Pickart, C.M. (1999). Noncanonical MMS2- encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96, 645-653   DOI   ScienceOn
32 Johnson, R.E., Washington, M.T., Haracska, L., Prakash, S., and Prakash, L. (2000). Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions. Nature 406, 1015-1019   DOI   ScienceOn
33 Guo, C., Fischhaber, P.L., Luk-Paszyc, M.J., Masuda, Y., Zhou, J.I. Kamiya, K., Kisker, C., and Friedberg, E.C.(2003). Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 22, 6621-6630   DOI   ScienceOn
34 Blastyak, A., Pinter, L., Unk, I., Prakash, L., Prakash, S.I and Haracska, L. (2007). Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell 28, 167-175   DOI   ScienceOn
35 Kannouche, P.L., Wing, J., and Lehmann, A.R. (2004). Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14, 491-500   DOI   ScienceOn
36 Lawrence, C.W., O'Brien, T., and Bond, J. (1984). UV-induced reversion of his4 frameshift mutations in rad6, rev1, and rev3 mutants of yeast. Mol. Gen. Genet. 195, 487-490   DOI
37 McCulloch, S.D., Kokoska, R.J., Masutani, C., Iwai, S., Hanaoka, F., and Kunkel, T.A. (2004b). Preferential cis-syn thymine dimer bypass by DNA polymerase eta occurs with biased fidelity. Nature 428, 97-100   DOI   ScienceOn
38 Spence, J., Sadis, S., Haas, A.L., and Finley, D. (1995). A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol. Cell. Biol. 15, 1265-1273   DOI
39 Stelter, P., and Ulrich, H.D. (2003). Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425, 188-191   DOI   ScienceOn
40 Ogi, T., and Lehmann, A.R. (2006). The Y-family DNA polymerase kappa (pol kappa). functions in mammalian nucleotide-excision repair. Nat. Cell Biol.8, 640-642   DOI   ScienceOn
41 Pfander, B., Moldovan, G.L., Sacher, M., Hoege, C., and Jentsch, S. (2005). SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436, 428-433   DOI
42 Otsuka, C., Kunitomi, N., Iwai, S., Loakes, D., and Negishi, K. (2005). Roles of the polymerase and BRCT domains of Rev1 protein in translesion DNA synthesis in yeast in vivo. Mutat Res. 578, 79-87   DOI
43 Zhuang, Z., Johnson, R.E., Haracska, L., Prakash, L., Prakash, S., and Benkovic, S.J. (2008). Regulation of polymerase exchange between Poleta and Poldelta by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme. Proc. Natl. Acad. Sci. USA 105, 5361-5366
44 Choi, J.H., Besaratinia, A., Lee, D.H., Lee, C.S., and Pfeifer, G.P. (2006). The role of DNA polymerase iota in UV mutational spectra. Mutat. Res.599, 58-65   DOI
45 Broomfield, S., Chow, B.L., and Xiao, W. (1998). MMS2, encoding a ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway. Proc. Natl. Acad. Sci. USA 95, 5678-5683
46 Brusky, J., Zhu, Y., and Xiao, W. (2000). UBC13, a DNA-damageinducible gene, is a member of the error-free postreplication repair pathway in Saccharomyces cerevisiae. Curr. Genet. 37, 168-174   DOI
47 Plosky, B.S., Vidal, A.E., Fernandez de Henestrosa, A.R., McLenigan, M.P., McDonald, J.P. Mead, S., and Woodgate, R. (2006). Controlling the subcellular localization of DNA polymerases iota and eta via interactions with ubiquitin. EMBO J. 25, 2847-2855   DOI   ScienceOn
48 Zhang, H., and Lawrence, C.W. (2005). The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. USA 102, 15954-15959
49 Chiu, R.K., Brun, J., Ramaekers, C., Theys, J., Weng, L.,Lambin, P., Gray, D.A., and Wouters, B.G. (2006). Lysine 63-polyubiquitination guards against translesion synthesis-induced mutations. PLoS Genet.2, e116   DOI   ScienceOn
50 Jansen, J.G., Langerak, P., Tsaalbi-Shtylik, A., van den Berk, P., Jacobs, H.,and de Wind, N.,(2006). Strand-biased defect in C/G transversions in hypermutating immunoglobulin genes in Rev1- deficient mice. J. Exp. Med. 203, 319-323   DOI   ScienceOn
51 McDonald, J.P., Levine, A.S., and Woodgate, R. (1997). The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics 147, 1557-1568
52 Avkin, S., Sevilya, Z., Toube, L., Geacintov, N., Chaney, S.G. Oren, M., and Livneh, Z. (2006). p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol. Cell 22, 407-413
53 Bemark, M., Khamlichi, A.A., Davies, S.L., and Neuberger, M.S. (2000). Disruption of mouse polymerase zeta (Rev3). leads to embryonic lethality and impairs blastocyst development in vitro. Curr. Biol. 10, 1213-1216   DOI   ScienceOn
54 Bienko, M., Green, C.M., Crosetto, N., Rudolf, F., Zapart, G.I Coull, B., Kannouche, P., Wider, G., Peter, M., Lehmann, A.R., et al. (2005). Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310, 1821-1824   DOI   ScienceOn
55 Davies, A.A., Huttner, D., Daigaku, Y., Chen, S., and Ulrich, H.D. (2008). Activation of ubiquitin-dependent DNA damage bypass is mediated by replication protein a. Mol. Cell 29, 625-636   DOI   ScienceOn
56 Masutani, C., Kusumoto, R., Iwai, S., and Hanaoka, F. (2000). Mechanisms of accurate translesion synthesis by human DNA polymerase eta. EMBO J. 19, 3100-3109   DOI   ScienceOn
57 Papouli, E., Chen, S., Davies, A.A., Huttner, D., Krejci, L.I Sung, P., and Ulrich, H.D. (2005). Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19, 123-133   DOI   ScienceOn
58 Parrilla-Castellar, E.R., Arlander, S.J., and Karnitz, L. (2004). Dial 9- 1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1). clamp complex. DNA Repair (Amst). 3, 1009-1014   DOI   ScienceOn
59 Sogo, J.M., Lopes, M., and Foiani, M. (2002). Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297, 599-602   DOI   ScienceOn
60 Wood, A., Garg, P., and Burgers, P.M. (2007). A ubiquitin-binding motif in the translesion DNA polymerase Rev1 mediates its essential functional interaction with ubiquitinated proliferating cell nuclear antigen in response to DNA damage. J. Biol. Chem. 282, 20256-20263   DOI   ScienceOn
61 Lehmann, A.R., Niimi, A., Ogi, T., Brown, S., Sabbioneda, S., Wing, J.F., Kannouche, P.L., and Green, C.M. (2007). Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst). 6, 891-899   DOI   ScienceOn
62 Ogi, T., Ohashi, E., and Ohmori, H. (2001). Mutagenesis by Escherichia coli DinB and its mammalian homolog Pol kappa. Tanpakushitsu Kakusan Koso 46, 1155-1161
63 Motegi, A., Liaw, H.J., Lee, K.Y., Roest, H.P., Mass, A.,et alK (2008). Lysine 63-linked polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc. Natl. Acad. Sci. USA(in press)
64 Soria, G., Podhajcer, O., Prives, C., and Gottifredi, V. (2006). P21Cip1/WAF1 downregulation is required for efficient PCNA ubiquitination after UV irradiation. Oncogene OR, 2829-2838   DOI   ScienceOn
65 Washington, M.T., Johnson, R.E., Prakash, S., and Prakash, L. (2001). Mismatch extension ability of yeast and human DNA polymerase eta. J. Biol. Chem. 276, 2263-2266   DOI
66 McCulloch, S.D., Kokoska, R.J., and Kunkel, T.A. (2004a). Efficiency, fidelity and enzymatic switching during translesion DNA synthesis. Cell Cycle 3, 580-583
67 Yang, X.H., Shiotani, B., Classon, M., and Zou, L. (2008). Chk1 and Claspin potentiate PCNA ubiquitination. Genes Dev. 22, 1147- 1152   DOI   ScienceOn
68 Motegi, A., Sood, R., Moinova, H., Markowitz, S.D., Liu, P.P., and Myung K.,(2006). Human SHPRH suppresses genomic instability through proliferating cell nuclear antigen polyubiquitination. J. Cell Biol.175, 703-708   DOI   ScienceOn
69 Esposito, G., Godindagger, I., Klein, U., Yaspo, M.L., Cumano, A., and Rajewsky, K. (2000). Disruption of the Rev3l-encoded catalytic subunit of polymerase zeta in mice results in early embryonic lethality. Curr. Biol. 10, 1221-1224   DOI   ScienceOn
70 Johnson, R.E., Torres-Ramos, C.A., Izumi, T., Mitra, S., Prakash, S., and Prakash, L. (1998). Identification of APN2, the Saccharomyces cerevisiae homolog of the major human AP endonuclease HAP1, and its role in the repair of abasic sites. Genes Dev. 12, 3137-3143   DOI
71 Unk, I., Hajdu, I., Fatyol, K., Szakal, B., Blastyak, A.,Bermudez, V., Hurwitz, J., Prakash, L., Prakash, S., and Haracska, L. (2006). Human SHPRH is a ubiquitin ligase for Mms2-Ubc13- dependent polyubiquitylation of proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. USA 103, 18107-18112
72 Tissier, A., Frank, E.G., McDonald, J.P., Iwai, S., Hanaoka, F., and Woodgate, R. (2000). Misinsertion and bypass of thyminethymine dimers by human DNA polymerase iota. EMBO J. 19, 5259-5266   DOI   ScienceOn
73 Ohashi, E., Murakumo, Y., Kanjo, N., Akagi, J., Masutani, C.I Hanaoka, F., and Ohmori, H. (2004). Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells 9, 523- 531   DOI   ScienceOn
74 Tissier, A., Kannouche, P., Reck, M.P., Lehmann, A.R., Fuchs, R.P.I and Cordonnier, A. (2004). Co-localization in replication foci and interaction of human Y-family members, DNA polymerase pol eta and REVl protein. DNA Repair (Amst) 3, 1503-1514   DOI   ScienceOn
75 Wittschieben, J., Shivji, M.K., Lalani, E., Jacobs, M.A., Marini, F.I Gearhart, P.J., Rosewell, I., Stamp, G., and Wood, R.D. (2000). Disruption of the developmentally regulated Rev3l gene causes embryonic lethality. Curr. Biol. 10, 1217-1220   DOI   ScienceOn
76 Iyer, L.M., Babu, M.M., and Aravind, L. (2006). The HIRAN domain and recruitment of chromatin remodeling and repair activities to-496 damaged DNA. Cell Cycle 5, 775-782   DOI   ScienceOn
77 Cordonnier, A.M., and Fuchs, R.P. (1999). Replication of damaged DNA: molecular defect in xeroderma pigmentosum variant cells. Mutat. Res.435, 111-119   DOI   ScienceOn
78 Gangavarapu, V., Prakash, S., and Prakash, L. (2007). Requirement of RAD52 group genes for postreplication repair of UVdamaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 27, 7758-7764   DOI   ScienceOn
79 Brun, J., Chiu, R., Lockhart, K., Xiao, W., Wouters, B.G.I and Gray, D.A. (2008). hMMS2 serves a redundant role in human PCNA polyubiquitination. BMC Mol. Biol. 9, 24   DOI   ScienceOn
80 Haracska, L., Torres-Ramos, C.A., Johnson, R.E., Prakash, S., and Prakash, L. (2004). Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae. Mol. Cell. Biol.24, 4267-4274   DOI
81 Kannouche, P., Fernandez de Henestrosa, A.R., Coull, B., Vidal, A.E., Gray, C., Zicha, D., Woodgate, R., and Lehmann, A.R. (2003). Localization of DNA polymerases eta and iota to the replication machinery is tightly co-ordinated in human cells. EMBO J. 22, 1223-1233   DOI
82 Choi, J.Y., and Guengerich, F.P. (2006). Kinetic evidence for inefficient and error-prone bypass across bulky N2-guanine DNA adducts by human DNA polymerase iota. J. Biol. Chem. 281, 12315-12324   DOI   ScienceOn
83 Guo, C., Tang, T.S., Bienko, M., Parker, J.L., Bielen, A.B.Sonoda, E., Takeda, S., Ulrich, H.D., Dikic, I., and Friedberg, E.C. (2006). Ubiquitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol. Cell Biol. 26, 8892-8900   DOI   ScienceOn