The p21 and PCNA partnership: A new twist for an old plot

Cell Cycle

Volumn 7, Issue 24, 2008, Pages 3840-3846

  Prives, Carol ^a   Gottifredi, Vanesa ^b,c  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

DNA replication; Nucleotide excision repair; p21; PCNA; Translesion DNA synthesis

Indexed keywords

CYCLINE; DNA; DNA POLYMERASE; PROTEIN P21;

DNA REPLICATION; DNA SYNTHESIS; DOWN REGULATION; EXCISION REPAIR; HUMAN; NONHUMAN; REVIEW; UBIQUITINATION;

EUKARYOTA;

EID: 58049215354     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.7.24.7243     Document Type: Review

References (89)

1. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993; 362:709-15.
2. Dotto GP. p21(WAF1/Cip1): more than a break to the cell cycle? Biochim Biophys Acta 2000; 1471:43-56.
3. Cip1/WAF1 downregulation is required for efficient PCNA ubiquitination after UV irradiation. Oncogene 2006; 25:2829-38.
4. Lee H, Zeng SX, Lu H. UV Induces p21 rapid turnover independently of ubiquitin and Skp2. J Biol Chem 2006; 281:26876-83.
5. WAF1/CIP1 for proteasomal degradation after UV irradiation. Mol Cell Biol 2007; 27:3187-98.
6. Kaur M, Pop M, Shi D, Brignone C, Grossman SR. hHR23B is required for genotoxic-specific activation of p53 and apoptosis. Oncogene 2007; 26:1231-7.
7. WAF1 to promote DNA repair. Cell 2003; 114:599-610.
8. Warbrick E. The puzzle of PCNA's many partners. Bioessays 2000; 22:997-1006.
9. Maga G, Hubscher U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 2003; 116:3051-60.
10. Moldovan GL, Pfander B, Jentsch S. PCNA, the maestro of the replication fork. Cell 2007; 129:665-79.
11. Burgers PM. Saccharomyces cerevisiae replication factor C II. Formation and activity of complexes with the proliferating cell nuclear antigen and with DNA polymerases delta and epsilon. J Biol Chem 1991; 266:22698-706.
12. Warbrick E. PCNA binding through a conserved motif. Bioessays 1998; 20:195-9.
13. 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.
14. Oku T, Ikeda S, Sasaki H, Fukuda K, Morioka H, Ohtsuka E, et al. Functional sites of human PCNA which interact with p21 (Cip1/Waf1), DNA polymerase delta and replication factor C. Genes Cells 1998; 3:357-69.
15. Soria G, Speroni J, Podhajcer OL, Prives C, Gottifredi V. p21 differentially regulates DNA replication and DNA-repair-associated processes after UV irradiation. J Cell Sci 2008; 121:3271-82.
16. Gottifredi V, McKinney K, Poyurovsky MV, Prives C. Decreased p21 levels are required for efficient restart of DNA synthesis after S phase block. J Biol Chem 2004; 279:5802-10.
17. Cip1. Nature 1995; 375:159-61.
18. Podust VN, Podust LM, Goubin F, Ducommun B, Hubscher U. Mechanism of inhibition of proliferating cell nuclear antigen-dependent DNA synthesis by the cyclin-dependent kinase inhibitor p21. Biochemistry 1995; 34:8869-75.
19. Waga S, Hannon GJ, Beach D, Stillman B. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 1994; 369:574-8.
20. Flores-Rozas H, Kelman Z, Dean FB, Pan ZQ, Harper JW, Elledge SJ, et al. Cdk-interacting protein 1 directly binds with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by the DNA polymerase delta holoenzyme. Proc Natl Acad Sci USA 1994; 91:8655-9.
21. Pan ZQ, Reardon JT, Li L, Flores-Rozas H, Legerski R, Sancar A, et al. Inhibition of nucleotide excision repair by the cyclin-dependent kinase inhibitor p21. J Biol Chem 1995; 270:22008-16.
22. Cdn1. Oncogene 1998; 17:2827-38.
23. Cooper MP, Balajee AS, Bohr VA. The C-terminal domain of p21 inhibits nucleotide excision repair In vitro and In vivo. Mol Biol Cell 1999; 10:2119-29.
24. SDI1/WAF1/CIP1 is involved in proliferating cell nuclear antigen binding but does not appear to be required for growth inhibition. J Biol Chem 1995; 270:17060-3.
25. WAF-1 gene activities. Mol Cell Biol 1996; 16:1786-93.
26. waf1 can block cells at two points in the cell cycle, but does not interfere with processive DNA-replication or stress-activated kinases. Oncogene 1998; 16:431-41.
27. Ogryzko VV, Wong P, Howard BH. WAF1 retards S-phase progression primarily by inhibition of cyclin-dependent kinases. Mol Cell Biol 1997; 17:4877-82.
28. Chen J, Jackson PK, Kirschner MW, Dutta A. Separate domains of p21 involved in the inhibition of Cdk kinase and PCNA. Nature 1995; 374:386-8.
29. 2 cell cycle arrest in p53-deficient cells. Oncogene 1998; 16:311-20.
30. 1/S phase transition. Cell Cycle 2003; 2:596-603.
31. Li R, Waga S, Hannon GJ, Beach D, Stillman B. Differential effects by the p21 CDK inhibitor on PCNA-dependent DNA replication and repair. Nature 1994; 371:534-7.
32. CDKN1A protein recruitment to DNA-damage sites and interaction with proliferating cell nuclear antigen. J Cell Sci 2006; 119:1517-27.
33. Adimoolam S, Lin CX, Ford JM. The p53-regulated cyclin-dependent kinase inhibitor, p21 (cip1, waf1, sdi1), is not required for global genomic and transcription-coupled nucleotide excision repair of UV-induced DNA photoproducts. J Biol Chem 2001; 276:25813-22.
34. Smith ML, Ford JM, Hollander MC, Bortnick RA, Amundson SA, Seo YR, et al. p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21 and/or gadd45 genes. Mol Cell Biol 2000; 20:3705-14.
35. Wani MA, Wani G, Yao J, Zhu Q, Wani AA. Human cells deficient in p53 regulated p21(waf1/cip1) expression exhibit normal nucleotide excision repair of UV-induced DNA damage. Carcinogenesis 2002; 23:403-10.
36. Waf1/Cip1. Mol Cell Biol 2008; 28:177-87.
37. WAF1/Cip1 in Gadd45-deficient keratinocytes restores DNA repair capacity. Carcinogenesis 2005; 26:1804-10.
38. Bloom J, Amador V, Bartolini F, DeMartino G, Pagano M. Proteasome-Mediated Degradation of p21 via N-Terminal Ubiquitinylation. Cell 2003; 115:71-82.
39. Avkin S, Sevilya Z, Toube L, Geacintov N, Chaney SG, Oren M, et al. p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol Cell 2006; 22:407-13.
40. 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 (Amst) 2007; 6:891-9.
41. Masutani C, Kusumoto R, Iwai S, Hanaoka F. Mechanisms of accurate translesion synthesis by human DNA polymerase eta. Embo J 2000; 19:3100-9.
42. Washington MT, Johnson RE, Prakash L, Prakash S. Accuracy of lesion bypass by yeast and human DNA polymerase eta. Proc Natl Acad Sci USA 2001; 98:8355-60.
43. Ogi T, Shinkai Y, Tanaka K, Ohmori H. Polkappa protects mammalian cells against the lethal and mutagenic effects of benzo[a]pyrene. Proc Natl Acad Sci USA 2002; 99:15548-53.
44. Avkin S, Goldsmith M, Velasco-Miguel S, Geacintov N, Friedberg EC, Livneh Z. Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells: the role of DNA polymerase kappa. J Biol Chem 2004; 279:53298-305.
45. Bassett E, King NM, Bryant MF, Hector S, Pendyala L, Chaney SG, et al. The role of DNA polymerase eta in translesion synthesis past platinum-DNA adducts in human fibroblasts. Cancer Res 2004; 64:6469-75.
46. Lehmann AR. Replication of damaged DNA by translesion synthesis in human cells. FEBS Lett 2005; 579:873-6.
47. Pages V, Fuchs RP. How DNA lesions are turned into mutations within cells? Oncogene 2002; 21:8957-66.
48. 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.
49. Albertella MR, Green CM, Lehmann AR, O'Connor MJ. A role for polymerase eta in the cellular tolerance to cisplatin-induced damage. Cancer Res 2005; 65:9799-806.
50. Bi X, Barkley LR, Slater DM, Tateishi S, Yamaizumi M, Ohmori H, et al. Rad18 regulates DNA polymerase kappa and is required for recovery from S-phase checkpoint-mediated arrest. Mol Cell Biol 2006; 26:3527-40.
51. Solomon DA, Cardoso MC, Knudsen ES. Dynamic targeting of the replication machinery to sites of DNA damage. J Cell Biol 2004; 166:455-63.
52. 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.
53. Stelter P, Ulrich HD. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 2003; 425:188-91.
54. 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.
55. Bienko M, Green CM, Crosetto N, Rudolf F, Zapart G, Coull B, et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 2005; 310:1821-4.
56. Parker JL, Bielen AB, Dikic I, Ulrich HD. Contributions of ubiquitin- and PCNA-binding domains to the activity of Polymerase eta in Saccharomyces cerevisiae. Nucleic Acids Res 2007; 35:881-9.
57. Plosky BS, Vidal AE, Fernandez de Henestrosa AR, McLenigan MP, McDonald JP, Mead S, et al. Controlling the subcellular localization of DNA polymerases iota and eta via interactions with ubiquitin. Embo J 2006; 25:2847-55.
58. Huang TT, Nijman SM, Mirchandani KD, Galardy PJ, Cohn MA, Haas W, et al. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat Cell Biol 2006; 8:339-47.
59. Garg P, Burgers PM. DNA polymerases that propagate the eukaryotic DNA replication fork. Crit Rev Biochem Mol Biol 2005; 40:115-28.
60. Haracska L, Unk I, Prakash L, Prakash S. Ubiquitylation of yeast proliferating cell nuclear antigen and its implications for translesion DNA synthesis. Proc Natl Acad Sci USA 2006; 103:6477-82.
61. Zhuang Z, Johnson RE, Haracska L, Prakash L, Prakash S, Benkovic SJ. Regulation of polymerase exchange between Poleta and Poldelta by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme. Proc Natl Acad Sci USA 2008; 105:5361-6.
62. Frampton J, Irmisch A, Green CM, Neiss A, Trickey M, Ulrich HD, et al. Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Mol Biol Cell 2006; 17:2976-85.
63. Rupp WD, Howard-Flanders P. Discontinuities in the DNA synthesized in an excision-defective strain of Escherichia coli following ultraviolet irradiation. J Mol Biol 1968; 31:291-304.
64. Lopes M, Foiani M, Sogo JM. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell 2006; 21:15-27.
65. Edmunds CE, Simpson LJ, Sale JE. PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol Cell 2008; 30:519-29.
66. Avkin S, Adar S, Blander G, Livneh Z. Quantitative measurement of translesion replication in human cells: evidence for bypass of abasic sites by a replicative DNA polymerase. Proc Natl Acad Sci USA 2002; 99:3764-9.
67. Boiteux S, Guillet M. Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair (Amst) 2004; 3:1-12.
68. Zhao B, Xie Z, Shen H, Wang Z. Role of DNA polymerase eta in the bypass of abasic sites in yeast cells. Nucleic Acids Res 2004; 32:3984-94.
69. -/- human cancer cells. Cancer Res 1996; 56:2250-5.
70. Kannouche P, Broughton BC, Volker M, Hanaoka F, Mullenders LH, Lehmann AR. Domain structure, localization and function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev 2001; 15:158-72.
71. Haracska L, Johnson RE, Unk I, Phillips B, Hurwitz J, Prakash L, et al. Physical and functional interactions of human DNA polymerase eta with PCNA. Mol Cell Biol 2001; 21:7199-206.
72. Haracska L, Acharya N, Unk I, Johnson RE, Hurwitz J, Prakash L, et al. A single domain in human DNA polymerase iota mediates interaction with PCNA: implications for translesion DNA synthesis. Mol Cell Biol 2005; 25:1183-90.
73. Johansson E, Garg P, Burgers PM. The Pol32 subunit of DNA polymerase delta contains separable domains for processive replication and proliferating cell nuclear antigen (PCNA) binding. J Biol Chem 2004; 279:1907-15.
74. Xu H, Zhang P, Liu L, Lee MY. A novel PCNA-binding motif identified by the panning of a random peptide display library. Biochemistry 2001; 40:4512-20.
75. 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.
76. Maga G, Jonsson ZO, Stucki M, Spadari S, Hubscher U. Dual mode of interaction of DNA polymerase epsilon with proliferating cell nuclear antigen in primer binding and DNA synthesis. J Mol Biol 1999; 285:259-67.
77. Eissenberg JC, Ayyagari R, Gomes XV, Burgers PM. Mutations in yeast proliferating cell nuclear antigen define distinct sites for interaction with DNA polymerase delta and DNA polymerase epsilon. Mol Cell Biol 1997; 17:6367-78.
78. LaBaer J, Garrett MD, Stevenson LF, Slingerland JM, Sandhu C, Chou HS, et al. New functional activities for the p21 family of CDK inhibitors. Genes Dev 1997; 11:847-62.
79. Wang SC, Nakajima Y, Yu YL, Xia W, Chen CT, Yang CC, et al. Tyrosine phosphorylation controls PCNA function through protein stability. Nat Cell Biol 2006; 8:1359-68.
80. Koundrioukoff S, Jonsson ZO, Hasan S, de Jong RN, van der Vliet PC, Hottiger MO, et al. A direct interaction between proliferating cell nuclear antigen (PCNA) and Cdk2 targets PCNA-interacting proteins for phosphorylation. J Biol Chem 2000; 275:22882-7.
81. Prosperi E. The fellowship of the rings: distinct pools of proliferating cell nuclear antigen trimer at work. Faseb J 2006; 20:833-7.
82. Nishitani H, Shiomi Y, Iida H, Michishita M, Takami T, Tsurimoto T. CDK inhibitor p21 is degraded by a PCNA coupled Cul4-DDB1Cdt2 pathway during S phase and after UV irradiation. J Biol Chem 2008.
83. Cdt2 ubiquitin ligase complex. Genes Dev 2008; 22:2496-506.
84. Cip1 to control replication licensing. Genes Dev 2008; 22:2507-19.
85. Chuang LC, Yew PR. Proliferating cell nuclear antigen recruits cyclin-dependent kinase inhibitor Xic1 to DNA and couples its proteolysis to DNA polymerase switching. J Biol Chem 2005; 280:35299-309.
86. You Z, Harvey K, Kong L, Newport J. Xic1 degradation in Xenopus egg extracts is coupled to initiation of DNA replication. Genes Dev 2002; 16:1182-94.
87. Furstenthal L, Swanson C, Kaiser BK, Eldridge AG, Jackson PK. Triggering ubiquitination of a CDK inhibitor at origins of DNA replication. Nat Cell Biol 2001; 3:715-22.
88. Livneh Z. Keeping mammalian mutation load in check: regulation of the activity of error-prone DNA polymerases by p53 and p21. Cell Cycle 2006; 5:1918-22.
89. CDKN1A in cells surviving UV-irradiation. DNA Repair (Amst) 2005; 4:1457-62.