Structure of monoubiquitinated PCNA: Implications for DNA polymerase switching and Okazaki fragment maturation

Cell Cycle

Volumn 11, Issue 11, 2012, Pages 2128-2136

  Zhang, Zhongtao ^a   Zhang, Sufang ^a   Lin, Szu Hua Sharon ^a   Wang, Xiaoxiao ^a   Wu, Licheng ^a   Lee, Ernest Y C ^a   Lee, Marietta Y W T ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Fen1; Okazaki fragment maturation; PCNA; Polymerase delta; Polymerase switching; Translesion synthesis; Ubiquitination

Indexed keywords

ALKYLATING AGENT; CYCLINE; DNA POLYMERASE; OKAZAKI FRAGMENT;

ARTICLE; CELL STRUCTURE; CRYSTALLIZATION; DNA REPLICATION; PROTEIN CONFORMATION; SKIN CANCER; SKIN SENSITIVITY; SUNLIGHT; SYNTHESIS; UBIQUITINATION; ULTRAVIOLET RADIATION; XERODERMA PIGMENTOSUM;

EID: 84861858876     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20595     Document Type: Article

References (64)

1. Branzei D, Foiani M. Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 2010; 11:208-19; PMID:20177396; http://dx.doi.org/ 10.1038/nrm2852.
2. Moldovan GL, Pfander B, Jentsch S. PCNA, the maestro of the replication fork. Cell 2007; 129:665-79; PMID:17512402; http://dx.doi.org/10.1016/j.cell. 2007.05.003.
3. Kunkel TA, Burgers PM. Dividing the workload at a eukaryotic replication fork. Trends Cell Biol 2008; 18:521-7; PMID:18824354; http://dx.doi.org/10.1016/ j.tcb.2008.08.005.
4. Balakrishnan L, Bambara RA. The changing view of Dna2. Cell Cycle 2011; 10:2620-1; PMID:21829100; http://dx.doi.org/10.4161/cc.10.16.16545.
5. Kai M, Wang TS. Checkpoint responses to replication stalling: inducing tolerance and preventing mutagenesis. Mutat Res 2003; 532:59-73; PMID:14643429; http://dx.doi.org/10.1016/j.mrfmmm.2003.08.010.
6. Biertümpfel C, Zhao Y, Kondo Y, Ramón-Maiques S, Gregory M, Lee JY, et al. Structure and mechanism of human DNA polymerase eta. Nature 2010; 465:1044-8; PMID:20577208; http://dx.doi.org/10.1038/nature09196.
7. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002; 419:135-41; PMID:12226657; http://dx.doi.org/10.1038/nature00991.
8. Chen J, Bozza W, Zhuang Z. Ubiquitination of PCNA and its essential role in eukaryotic translesion synthesis. Cell Biochem Biophys 2011; 60:47-60; PMID:21461937; http://dx.doi.org/10.1007/s12013-011-9187-3.
9. Lehmann AR. Ubiquitin-family modifications in the replication of DNA damage. FEBS Lett 2011; 585:2772-9; PMID:21704031; http://dx.doi.org/10.1016/j. febslet.2011.06.005.
10. Lehmann AR, Niimi A, Ogi T, Brown S, Sabbioneda S, Wing JF, et al. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair 2007; 6:891-9; PMID:17363342; http://dx.doi.org/10.1016/j.dnarep.2007.02. 003.
11. Batters C, Zhu H, Sale JE. Visualisation of PCNA monoubiquitination in vivo by single pass spectral imaging FRET microscopy. PLoS ONE 2010; 5:9008; PMID:20126408; http://dx.doi.org/10.1371/journal.pone.0009008.
12. Daigaku Y, Davies AA, Ulrich HD. Ubiquitin-dependent DNA damage bypass is separable from genome replication. Nature 2010; 465:951-5; PMID:20453836; http://dx.doi.org/10.1038/nature09097.
13. Niimi A, Brown S, Sabbioneda S, Kannouche PL, Scott A, Yasui A, et al. Regulation of proliferating cell nuclear antigen ubiquitination in mammalian cells. Proc Natl Acad Sci USA 2008; 105:16125-30; PMID:18845679; http://dx.doi.org/10.1073/pnas.0802727105.
14. Ulrich HD. Timing and spacing of ubiquitin-dependent DNA damage bypass. FEBS Lett 2011; 585:2861-7; PMID:21605556; http://dx.doi.org/10.1016/j.febslet. 2011.05.028.
15. Lehmann AR. Translesion synthesis in mammalian cells. Exp Cell Res 2006; 312:2673-6; PMID:16854411; http://dx.doi.org/10.1016/j.yexcr.2006.06.010.
16. Waters LS, Minesinger BK, Wiltrout ME, D'Souza S, Woodruff RV, Walker GC. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Mol Biol Rev 2009; 73:134-54; PMID:19258535; http://dx.doi.org/10.1128/MMBR.00034-08.
17. Yang W, Woodgate R. What a difference a decade makes: insights into translesion DNA synthesis. Proc Natl Acad Sci USA 2007; 104:15591-8; PMID:17898175; http://dx.doi.org/10.1073/pnas.0704219104.
18. Zahn KE, Wallace SS, Doublié S. DNA polymerases provide a canon of strategies for translesion synthesis past oxidatively generated lesions. Curr Opin Struct Biol 2011; 21:358-69; PMID:21482102; http://dx.doi.org/10.1016/j. sbi.2011.03.008.
19. Shaheen M, Shanmugam I, Hromas R. The Role of PCNA Posttranslational Modifications in Translesion Synthesis. J Nucleic Acids 2010; 2010; PMID:20847899; http://dx.doi.org/10.4061/2010/761217.
20. Garg P, Burgers PM. Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases eta and REV1. Proc Natl Acad Sci USA 2005; 102:18361-6; PMID:16344468; http://dx.doi.org/10.1073/pnas.0505949102.
21. Kannouche PL, Wing J, Lehmann AR. 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; PMID:15149598; http://dx.doi.org/10.1016/S1097-2765(04)00259-X.
22. Zhang S, Chea J, Meng X, Zhou Y, Lee EY, Lee MY. PCNA is ubiquitinated by RNF8. Cell Cycle 2008; 7:3399-404; PMID:18948756; http://dx.doi.org/10.4161/cc. 7.21.6949.
23. Kontopidis G, Wu SY, Zheleva DI, Taylor P, McInnes C, Lane DP, et al. Structural and biochemical studies of human proliferating cell nuclear antigen complexes provide a rationale for cyclin association and inhibitor design. Proc Natl Acad Sci USA 2005; 102:1871-6; PMID:15681588; http://dx.doi.org/10.1073/ pnas.0406540102.
24. Krishna TS, Kong XP, Gary S, Burgers PM, Kuriyan J. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 1994; 79:1233-43; PMID:8001157; http://dx.doi.org/10.1016/0092-8674(94)90014-0.
25. Tsutakawa SE, Van Wynsberghe AW, Freudenthal BD, Weinacht CP, Gakhar L, Washington MT, et al. Solution X-ray scattering combined with computational modeling reveals multiple conformations of covalently bound ubiquitin on PCNA. Proc Natl Acad Sci USA 2011; 108:17672-7; PMID:22006297; http://dx.doi.org/10. 1073/pnas.1110480108.
26. Bruning JB, Shamoo Y. Structural and thermodynamic analysis of human PCNA with peptides derived from DNA polymerase-delta p66 subunit and flap endonuclease-1. Structure 2004; 12:2209-19; PMID:15576034; http://dx.doi.org/10. 1016/j.str.2004.09.018.
27. Bowman GD, O'Donnell M, Kuriyan J. Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature 2004; 429:724-30; PMID:15201901; http://dx.doi.org/10.1038/nature02585.
28. Ayyagari R, Gomes XV, Gordenin DA, Burgers PM. Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 AND DNA2. J Biol Chem 2003; 278:1618-25; PMID:12424238; http://dx.doi.org/10.1074/jbc.M209801200.
29. Balakrishnan L, Bambara RA. Eukaryotic lagging strand DNA replication employs a multi-pathway mechanism that protects genome integrity. J Biol Chem 2011; 286:6865-70; PMID:21177245; http://dx.doi.org/10.1074/jbc.R110.209502.
30. Sakurai S, Kitano K, Yamaguchi H, Hamada K, Okada K, Fukuda K, et al. Structural basis for recruitment of human flap endonuclease 1 to PCNA. EMBO J 2005; 24:683-93; PMID:15616578; http://dx.doi.org/10.1038/sj.emboj.7600519.
31. Orans J, McSweeney EA, Iyer RR, Hast MA, Hellinga HW, Modrich P, et al. Structures of human exonuclease 1 DNA complexes suggest a unified mechanism for nuclease family. Cell 2011; 145:212-23; PMID:21496642; http://dx.doi.org/10. 1016/j.cell.2011.03.005.
32. Tsutakawa SE, Classen S, Chapados BR, Arvai AS, Finger LD, Guenther G, et al. Human flap endonuclease structures, DNA double-base flipping and a unified understanding of the FEN1 superfamily. Cell 2011; 145:198-211; PMID:21496641; http://dx.doi.org/10.1016/j.cell.2011.03.004.
33. Garg P, Stith CM, Sabouri N, Johansson E, Burgers PM. Idling by DNA polymerase delta maintains a ligatable nick during lagging-strand DNA replication. Genes Dev 2004; 18:2764-73; PMID:15520275; http://dx.doi.org/10. 1101/gad.1252304.
34. Freudenthal BD, Gakhar L, Ramaswamy S, Washington MT. Structure of monoubiquitinated PCNA and implications for translesion synthesis and DNA polymerase exchange. Nat Struct Mol Biol 2010; 17:479-84; PMID:20305653; http://dx.doi.org/10.1038/nsmb.1776.
35. Pastushok L, Hanna M, Xiao W. Constitutive fusion of ubiquitin to PCNA provides DNA damage tolerance independent of translesion polymerase activities. Nucleic Acids Res 2010; 38:5047-58; PMID:20385585; http://dx.doi.org/10.1093/ nar/gkq239.
36. Bienko M, Green CM, Sabbioneda S, Crosetto N, Matic I, Hibbert RG, et al. Regulation of translesion synthesis DNA polymerase eta by monoubiquitination. Mol Cell 2010; 37:396-407; PMID:20159558; http://dx.doi.org/10.1016/j.molcel. 2009.12.039.
37. Ohmori H, Hanafusa T, Ohashi E, Vaziri C. Separate roles of structured and unstructured regions of Y-family DNA polymerases. Adv Protein Chem Struct Biol 2009; 78:99-146; PMID:20663485; http://dx.doi.org/10.1016/S1876-1623(08) 78004-0.
38. Zhang P, Mo JY, Perez A, Leon A, Liu L, Mazloum N, et al. Direct interaction of proliferating cell nuclear antigen with the p125 catalytic subunit of mammalian DNA polymerase delta. J Biol Chem 1999; 274:26647-53; PMID:10480866; http://dx.doi.org/10.1074/jbc.274.38.26647.
39. Mo J, Liu L, Leon A, Mazloum N, Lee MY. Evidence that DNA polymerase delta isolated by immunoaffinity chromatography exhibits high-molecular weight characteristics and is associated with the KIAA0039 protein and RPA. Biochemistry 2000; 39:7245-54; PMID:10852724; http://dx.doi.org/10.1021/ bi0000871.
40. Li H, Xie B, Zhou Y, Rahmeh A, Trusa S, Zhang S, et al. Functional roles of p12, the fourth subunit of human DNA polymerase delta. J Biol Chem 2006; 281:14748-55; PMID:16510448; http://dx.doi.org/10.1074/jbc.M600322200.
41. Barry ER, Bell SD. DNA replication in the archaea. Microbiol Mol Biol Rev 2006; 70:876-87; PMID:17158702; http://dx.doi.org/10.1128/MMBR.00029-06.
42. Dionne I, Nookala RK, Jackson SP, Doherty AJ, Bell SD. A heterotrimeric PCNA in the hyperthermophilic archaeon Sulfolobus solfataricus. Mol Cell 2003; 11:275-82; PMID:12535540; http://dx.doi.org/10.1016/S1097-2765(02)00824-9.
43. Beattie TR, Bell SD. Molecular machines in archaeal DNA replication. Curr Opin Chem Biol 2011; 15:614-9; PMID:21852183; http://dx.doi.org/10.1016/j.cbpa. 2011.07.017.
44. Beattie TR, Bell SD. The role of the DNA sliding clamp in Okazaki fragment maturation in archaea and eukaryotes. Biochem Soc Trans 2011; 39:70-6; PMID:21265749; http://dx.doi.org/10.1042/BST0390070.
45. Beattie TR, Bell SD. Coordination of multiple enzyme activities by a single PCNA in archaeal Okazaki fragment maturation. EMBO J 2012; 31:1556-67; PMID:22307085; http://dx.doi.org/10.1038/emboj.2012.12.
46. Doré AS, Kilkenny ML, Jones SA, Oliver AW, Roe SM, Bell SD, et al. Structure of an archaeal PCNA1-PCNA2-FEN1 complex: elucidating PCNA subunit and client enzyme specificity. Nucleic Acids Res 2006; 34:4515-26; PMID:16945955; http://dx.doi.org/10.1093/nar/gkl623.
47. Zheng L, Shen B. Okazaki fragment maturation: nucleases take centre stage. J Mol Cell Biol 2011; 3:23-30; PMID:21278448; http://dx.doi.org/10.1093/ jmcb/mjq048.
48. Pascal JM, Tsodikov OV, Hura GL, Song W, Cotner EA, Classen S, et al. A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA. Mol Cell 2006; 24:279-91; PMID:17052461; http://dx.doi.org/10.1016/j.molcel.2006.08.015.
49. Kaufmann WK. The human intra-S checkpoint response to UVC-induced DNA damage. Carcinogenesis 2010; 31:751-65; PMID:19793801; http://dx.doi.org/10. 1093/carcin/bgp230.
50. Seiler JA, Conti C, Syed A, Aladjem MI, Pommier Y. The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol Cell Biol 2007; 27:5806-18; PMID:17515603; http://dx.doi.org/10.1128/MCB.02278-06.
51. Meng X, Zhou Y, Lee EY, Lee MY, Frick DN. The p12 subunit of human polymerase delta modulates the rate and fidelity of DNA synthesis. Biochemistry 2010; 49:3545-54; PMID:20334433; http://dx.doi.org/10.1021/bi100042b.
52. Meng X, Zhou Y, Zhang S, Lee EY, Frick DN, Lee MY. DNA damage alters DNA polymerase delta to a form that exhibits increased discrimination against modified template bases and mismatched primers. Nucleic Acids Res 2009; 37:647-57; PMID:19074196; http://dx.doi.org/10.1093/nar/gkn1000.
53. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M. HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 2006; 62:859-66; PMID:16855301; http://dx.doi.org/10.1107/S0907444906019949.
54. Zwart PH, Afonine PV, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. Automated structure solution with the PHENIX suite. Methods Mol Biol 2008; 426:419-35; PMID:18542881; http://dx.doi.org/10.1007/978-1-60327-058-8-28.
55. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004; 60:2126-32; PMID:15572765; http://dx.doi.org/10.1107/S0907444904019158.
56. Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, Bricogne G. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 2004; 60:2210-21; PMID:15572774; http://dx.doi.org/10.1107/S0907444904016427.
57. McNally R, Bowman GD, Goedken ER, O'Donnell M, Kuriyan J. Analysis of the role of PCNA-DNA contacts during clamp loading. BMC Struct Biol 2010; 10:3; PMID:20113510; http://dx.doi.org/10.1186/1472-6807-10-3.
58. Swan MK, Johnson RE, Prakash L, Prakash S, Aggarwal AK. Structural basis of high-fidelity DNA synthesis by yeast DNA polymerase delta. Nat Struct Mol Biol 2009; 16:979-86; PMID:19718023; http://dx.doi.org/10.1038/nsmb.1663.
59. Silverstein TD, Johnson RE, Jain R, Prakash L, Prakash S, Aggarwal AK. Structural basis for the suppression of skin cancers by DNA polymerase eta. Nature 2010; 465:1039-43; PMID:20577207; http://dx.doi.org/10.1038/nature09104.
60. Hishiki A, Hashimoto H, Hanafusa T, Kamei K, Ohashi E, Shimizu T, et al. Structural basis for novel interactions between human translesion synthesis polymerases and proliferating cell nuclear antigen. J Biol Chem 2009; 284:10552-60; PMID:19208623; http://dx.doi.org/10.1074/jbc.M809745200.
61. Bomar MG, D'Souza S, Bienko M, Dikic I, Walker GC, Zhou P. Unconventional ubiquitin recognition by the ubiquitin-binding motif within the Y family DNA polymerases iota and Rev1. Mol Cell 2010; 37:408-17; PMID:20159559; http://dx.doi.org/10.1016/j.molcel.2009.12.038.
62. Bomar MG, Pai MT, Tzeng SR, Li SS, Zhou P. Structure of the ubiquitin-binding zinc finger domain of human DNA Y-polymerase eta. EMBO Rep 2007; 8:247-51; PMID:17304240; http://dx.doi.org/10.1038/sj.embor.7400901.
63. Burschowsky D, Rudolf F, Rabut G, Herrmann T, Peter M, Wider G. Structural analysis of the conserved ubiquitin-binding motifs (UBMs) of the translesion polymerase iota in complex with ubiquitin. J Biol Chem 2011; 286:1364-73; PMID:20929865; http://dx.doi.org/10.1074/jbc.M110.135038.
64. Gulbis JM, Kelman Z, Hurwitz J, O'Donnell M, Kuriyan J. Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA. Cell 1996; 87:297-306; PMID:8861913; http://dx.doi.org/10.1016/S0092-8674(00)81347-1.