PIP degron proteins, substrates of CRL4Cdt2, and not PIP boxes, interfere with DNA polymerase g and i focus formation on UV damage

Nucleic Acids Research

Volumn 42, Issue 6, 2014, Pages 3692-3706

  Tsanov, Nikolay ^a,b   Kermi, Chames ^a   Coulombe, Philippe ^a   Van Der Laan, Siem ^a   Hodroj, Dana ^a   Maiorano, Domenico ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL CYCLE PROTEINS; CELL DEATH; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; MICE; NIH 3T3 CELLS; NUCLEAR PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEOLYSIS; UBIQUITIN-PROTEIN LIGASES; ULTRAVIOLET RAYS;

EID: 84898954695     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1400     Document Type: Article

References (80)

1. Moldovan, G. L., Pfander, B. and Jentsch, S. (2007) PCNA, the maestro of the replication fork. Cell, 129, 665-679.
2. McNally, R., Bowman, G. D., Goedken, E. R., O'Donnell, M. and Kuriyan, J. (2010) Analysis of the role of PCNA-DNA contacts during clamp loading. BMC Struct. Biol., 10, 3.
3. Krishna, T. S., Kong, X. P., Gary, S., Burgers, P. M. and Kuriyan, J. (1994) Crystal structure of the eukaryotic DNA polymerase processivity factor PCN A. Cell, 79, 1233-1243.
4. Warbrick, E., Lane, D. P., Glover, D. M. and Cox, L. S. (1997) Homologous regions of Fen1 and p21Cip1 compete for binding to the same site on PCNA: a potential mechanism to co-ordinate DNA replication and repair. Oncogene, 14, 2313-2321.
5. Bruning, J. B. and Shamoo, Y. (2004) Structural and thermodynamic analysis of human PCNA with peptides derived from DNA polymerase-delta p66 subunit and flap endonuclease-1. Structure, 12, 2209-2219.
6. Cazzalini, O., Perucca, P., Riva, F., Stivala, L. A., Bianchi, L., Vannini, V., Ducommun, B. and Prosperi, E. (2003) p21CDKN1A does not interfere with loading of PCNA at DNA replication sites, but inhibits subsequent binding of DNA polymerase delta at the G1/S phase transition. Cell Cycle, 2, 596-603.
7. Lehmann, A. R. (2006) Translesion synthesis in mammalian cells. Exp. Cell. Res., 312, 2673-2676.
8. Bienko, M., Green, C. M., Crosetto, N., Rudolf, F., Zapart, G., 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.
9. 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.
10. Watanabe, K., Tateishi, S., Kawasuji, M., Tsurimoto, T., Inoue, H. and Yamaizumi, M. (2004) Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J., 23, 3886-3896.
11. 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.
12. 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.
13. Biertumpfel, C., Zhao, Y., Kondo, Y., Ramon-Maiques, S., Gregory, M., Lee, J. Y., Masutani, C., Lehmann, A. R., Hanaoka, F. and Yang, W. (2010) Structure and mechanism of human DNA polymerase eta. Nature, 465, 1044-1048.
14. McCulloch, S. D., Kokoska, R. J., Masutani, C., Iwai, S., Hanaoka, F. and Kunkel, T. A. (2004) Preferential cis-syn thymine dimer bypass by DNA polymerase eta occurs with biased fidelity. Nature, 428, 97-100.
15. Kannouche, P., Broughton, B. C., Volker, M., Hanaoka, F., Mullenders, L. H. and Lehmann, A. R. (2001) Domain structure, localization, and function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev., 15, 158-172.
16. Sale, J. E., Lehmann, A. R. and Woodgate, R. (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell Biol., 13, 141-152.
17. Zlatanou, A., Despras, E., Braz-Petta, T., Boubakour-Azzouz, I., Pouvelle, C., Stewart, G. S., Nakajima, S., Yasui, A., Ishchenko, A. A. and Kannouche, P. L. (2011) The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol eta in response to oxidative DNA damage in human cells. Mol. Cell, 43, 649-662.
18. Ogi, T., Limsirichaikul, S., Overmeer, R. M., Volker, M., Takenaka, K., Cloney, R., Nakazawa, Y., Niimi, A., Miki, Y., Jaspers, N. G. et al. (2010) Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell, 37, 714-727.
19. 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.
20. Havens, C. G. and Walter, J. C. (2011) Mechanism of CRL4Cdt2, a PCNA-dependent E3 ubiquitin ligase. Genes Dev., 25, 1568-1582.
21. Arias, E. E. and Walter, J. C. (2006) PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell. Biol., 8, 84-90.
22. Havens, C. G. and Walter, J. C. (2009) Docking of a specialized PIP Box onto chromatin-bound PCNA creates a degron for the ubiquitin ligase CRL4Cdt2. Mol. Cell., 35, 93-104.
23. Michishita, M., Morimoto, A., Ishii, T., Komori, H., Shiomi, Y., Higuchi, Y. and Nishitani, H. (2011) Positively charged residues located downstream of PIP box, together with TD amino acids within PIP box, are important for CRL4(Cdt2) -mediated proteolysis. Genes Cell, 16, 12-22.
24. Zhong, W., Feng, H., Santiago, F. E. and Kipreos, E. T. (2003) CUL-4 ubiquitin ligase maintains genome stability by restraining DNA-replication licensing. Nature, 423, 885-889.
25. Higa, L. A., Mihaylov, I. S., Banks, D. P., Zheng, J. and Zhang, H. (2003) Radiation-mediated proteolysis of CDT1 by CUL4-ROC1 and CSN complexes constitutes a new checkpoint. Nat. Cell Biol., 5, 1008-1015.
26. Oda, H., Hubner, M. R., Beck, D. B., Vermeulen, M., Hurwitz, J., Spector, D. L. and Reinberg, D. (2010) Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNAdependent degradation during DNA damage. Mol. Cell, 40, 364-376.
27. Tardat, M., Brustel, J., Kirsh, O., Lefevbre, C., Callanan, M., Sardet, C. and Julien, E. (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol., 12, 1086-1093.
28. Abbas, T., Shibata, E., Park, J., Jha, S., Karnani, N. and Dutta, A. (2010) CRL4(Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol. Cell, 40, 9-21.
29. Centore, R. C., Havens, C. G., Manning, A. L., Li, J. M., Flynn, R. L., Tse, A., Jin, J., Dyson, N. J., Walter, J. C. and Zou, L. (2010) CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol. Cell, 40, 22-33.
30. Kim, Y., Starostina, N. G. and Kipreos, E. T. (2008) The CRL4Cdt2 ubiquitin ligase targets the degradation of p21Cip1 to control replication licensing. Genes Dev., 22, 2507-2519.
31. Abbas, T., Sivaprasad, U., Terai, K., Amador, V., Pagano, M. and Dutta, A. (2008) PCNA-dependent regulation of p21 ubiquitylation and degradation via the CRL4Cdt2 ubiquitin ligase complex. Genes Dev., 22, 2496-2506.
32. Nishitani, H., Shiomi, Y., Iida, H., Michishita, M., Takami, T. and Tsurimoto, T. (2008) CDK inhibitor p21 is degraded by a proliferating cell nuclear antigen-coupled Cul4-DDB1Cdt2 pathway during S phase and after UV irradiation. J. Biol. Chem., 283, 29045-29052.
33. Nishitani, H., Lygerou, Z., Nishimoto, T. and Nurse, P. (2000) The Cdt1 protein is required to license DNA for replication in fission yeast. Nature, 404, 625-628.
34. Maiorano, D., Moreau, J. and Mechali, M. (2000) XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis. Nature, 404, 622-625.
35. Ralph, E., Boye, E. and Kearsey, S. E. (2006) DNA damage induces Cdt1 proteolysis in fission yeast through a pathway dependent on Cdt2 and Ddb1. EMBO Rep., 7, 1134-1139.
36. Senga, T., Sivaprasad, U., Zhu, W., Park, J. H., Arias, E. E., Walter, J. C. and Dutta, A. (2006) PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated N-terminal ubiquitination. J. Biol. Chem., 281, 6246-6252.
37. Jin, J., Arias, E. E., Chen, J., Harper, J. W. and Walter, J. C. (2006) A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell, 23, 709-721.
38. Nishitani, H., Sugimoto, N., Roukos, V., Nakanishi, Y., Saijo, M., Obuse, C., Tsurimoto, T., Nakayama, K. I., Nakayama, K., Fujita, M. et al. (2006) Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J., 25, 1126-1136.
39. Maiorano, D., Krasinska, L., Lutzmann, M. and Mechali, M. (2005) Recombinant Cdt1 induces rereplication of G2 nuclei in Xenopus egg extracts. Curr. Biol., 15, 146-153.
40. Arias, E. E. and Walter, J. C. (2005) Replication-dependent destruction of Cdt1 limits DNA replication to a single round per cell cycle in Xenopus egg extracts. Genes Dev., 19, 114-126.
41. Stathopoulou, A., Roukos, V., Petropoulou, C., Kotsantis, P., Karantzelis, N., Nishitani, H., Lygerou, Z. and Taraviras, S. (2012) Cdt1 is differentially targeted for degradation by anticancer chemotherapeutic drugs. PLoS One, 7, e34621.
42. Shiomi, Y., Hayashi, A., Ishii, T., Shinmyozu, K., Nakayama, J., Sugasawa, K. and Nishitani, H. (2012) Two different replication factor C proteins, Ctf18 and RFC1, separately control PCNACRL4Cdt2-mediated Cdt1 proteolysis during S phase and following UV irradiation. Mol. Cell Biol., 32, 2279-2288.
43. Hu, J., McCall, C. M., Ohta, T. and Xiong, Y. (2004) Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat. Cell Biol., 6, 1003-1009.
44. Guarino, E., Shepherd, M. E., Salguero, I., Hua, H., Deegan, R. S. and Kearsey, S. E. (2011) Cdt1 proteolysis is promoted by dual PIP degrons and is modulated by PCNA ubiquitylation. Nucleic Acids Res., 39, 5978-5990.
45. Nishitani, H., Taraviras, S., Lygerou, Z. and Nishimoto, T. (2001) The human licensing factor for DNA replication Cdt1 accumulates in G1 and is destabilized after initiation of S-phase. J. Biol. Chem., 276, 44905-44911.
46. Rialland, M., Sola, F. and Santocanale, C. (2002) Essential role of human CDT1 in DNA replication and chromatin licensing. J. Cell Sci., 115, 1435-1440.
47. Kim, S. H. and Michael, W. M. (2008) Regulated proteolysis of DNA polymerase eta during the DNA-damage response in C. elegans. Mol. Cell, 32, 757-766.
48. Bergoglio, V., Bavoux, C., Verbiest, V., Hoffmann, J. S. and Cazaux, C. (2002) Localisation of human DNA polymerase kappa to replication foci. J. Cell Sci., 115, 4413-4418.
49. Coulombe, P., Rodier, G., Bonneil, E., Thibault, P. and Meloche, S. (2004) N-Terminal ubiquitination of extracellular signal-regulated kinase 3 and p21 directs their degradation by the proteasome. Mol. Cell. Biol., 24, 6140-6150.
50. Rodier, G., Coulombe, P., Tanguay, P. L., Boutonnet, C. and Meloche, S. (2008) Phosphorylation of Skp2 regulated by CDK2 and Cdc14B protects it from degradation by APC(Cdh1) in G1 phase. EMBO J., 27, 679-691.
51. Julien, C., Coulombe, P. and Meloche, S. (2003) Nuclear export of ERK3 by a CRM1-dependent mechanism regulates its inhibitory action on cell cycle progression. J. Biol. Chem., 278, 42615-42624.
52. Morgenstern, J. P. and Land, H. (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res., 18, 3587-3596.
53. Zalmas, L. P., Zhao, X., Graham, A. L., Fisher, R., Reilly, C., Coutts, A. S. and La Thangue, N. B. (2008) DNA-damage response control of E2F7 and E2F8. EMBO Rep., 9, 252-259.
54. Westbrook, T. F., Hu, G., Ang, X. L., Mulligan, P., Pavlova, N. N., Liang, A., Leng, Y., Maehr, R., Shi, Y., Harper, J. W. et al. (2008) SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature, 452, 370-374.
55. Soria, G., Belluscio, L., van Cappellen, W. A., Kanaar, R., Essers, J. and Gottifredi, V. (2009) DNA damage induced Pol eta recruitment takes place independently of the cell cycle phase. Cell Cycle, 8, 3340-3348.
56. Xouri, G., Squire, A., Dimaki, M., Geverts, B., Verveer, P. J., Taraviras, S., Nishitani, H., Houtsmuller, A. B., Bastiaens, P. I. and Lygerou, Z. (2007) Cdt1 associates dynamically with chromatin throughout G1 and recruits geminin onto chromatin. EMBO J., 26, 1303-1314.
57. Zhu, W., Chen, Y. and Dutta, A. (2004) Rereplication by depletion of geminin is seen regardless of p53 status and activates a G2/M checkpoint. Mol. Cell. Biol., 24, 7140-7150.
58. Vaziri, C., Saxena, S., Jeon, Y., Lee, C., Murata, K., Machida, Y., Wagle, N., Hwang, D. S. and Dutta, A. (2003) A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell, 11, 997-1008.
59. Hishiki, A., Hashimoto, H., Hanafusa, T., Kamei, K., Ohashi, E., Shimizu, T., Ohmori, H. and Sato, M. (2009) Structural basis for novel interactions between human translesion synthesis polymerases and proliferating cell nuclear antigen. J. Biol. Chem., 284, 10552-10560.
60. Soria, G., Speroni, J., Podhajcer, O. L., Prives, C. and Gottifredi, V. (2008) p21 differentially regulates DNA replication and DNArepair-associated processes after UV irradiation. J. Cell. Sci., 121, 3271-3282.
61. Soria, G. and Gottifredi, V. (2010) PCNA-coupled p21 degradation after DNA damage: the exception that confirms the rule? DNA Repair (Amst.), 9, 358-364.
62. Terai, K., Abbas, T., Jazaeri, A. A. and Dutta, A. (2010) CRL4(Cdt2) E3 ubiquitin ligase monoubiquitinates PCNA to promote translesion DNA synthesis. Mol. Cell, 37, 143-149.
63. 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.
64. Maiorano, D., Rul, W. and Mechali, M. (2004) Cell cycle regulation of the licensing activity of Cdt1 in Xenopus laevis. Exp. Cell Res., 295, 138-149.
65. Lutzmann, M., Maiorano, D. and Mechali, M. (2006) A Cdt1-geminin complex licenses chromatin for DNA replication and prevents rereplication during S phase in Xenopus. EMBO J., 25, 5764-5774.
66. Despras, E., Daboussi, F., Hyrien, O., Marheineke, K. and Kannouche, P. L. (2010) ATR/Chk1 pathway is essential for resumption of DNA synthesis and cell survival in UV-irradiated XP variant cells. Hum. Mol. Genet., 19, 1690-1701.
67. Bienko, M., Green, C. M., Sabbioneda, S., Crosetto, N., Matic, I., Hibbert, R. G., Begovic, T., Niimi, A., Mann, M., Lehmann, A. R. et al. (2010) Regulation of translesion synthesis DNA polymerase eta by monoubiquitination. Mol. Cell, 37, 396-407.
68. Jeong, Y. T., Rossi, M., Cermak, L., Saraf, A., Florens, L., Washburn, M. P., Sung, P., Schildkraut, C. and Pagano, M. (2013) FBH1 promotes DNA double-strand breakage and apoptosis in response to DNA replication stress. J. Cell Biol., 200, 141-149.
69. Fugger, K., Chu, W. K., Haahr, P., Nedergaard Kousholt, A., Beck, H., Payne, M. J., Hanada, K., Hickson, I. D. and Storgaard Sorensen, C. (2013) FBH1 co-operates with MUS81 in inducing DNA double-strand breaks and cell death following replication stress. Nat. Commun., 4, 1423.
70. Bacquin, A., Pouvelle, C., Siaud, N., Perderiset, M., Salome-Desnoulez, S., Tellier-Lebegue, C., Lopez, B., Charbonnier, J. B. and Kannouche, P. L. (2013) The helicase FBH1 is tightly regulated by PCNA via CRL4(Cdt2)-mediated proteolysis in human cells. Nucleic Acids Res., 41, 6501-6513.
71. Mansilla, S. F., Soria, G., Vallerga, M. B., Habif, M., Martinez-Lopez, W., Prives, C. and Gottifredi, V. (2013) UV-triggered p21 degradation facilitates damaged-DNA replication and preserves genomic stability. Nucleic Acids Res., 41, 6942-6951.
72. Terai, K., Shibata, E., Abbas, T. and Dutta, A. (2013) Degradation of p12 by CRL4Cdt2 E3 ligase inhibits fork progression after DNA damage. J. Biol. Chem., 288, 30509-30514.
73. Karras, G. I. and Jentsch, S. (2011) The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell, 141, 255-267.
74. Daigaku, Y., Davies, A. A. and Ulrich, H. D. (2010) Ubiquitindependent DNA damage bypass is separable from genome replication. Nature, 465, 951-955.
75. Diamant, N., Hendel, A., Vered, I., Carell, T., Reissner, T., de Wind, N., Geacinov, N. and Livneh, Z. (2012) DNA damage bypass operates in the S and G2 phases of the cell cycle and exhibits differential mutagenicity. Nucleic Acids Res., 40, 170-180.
76. Raman, M., Havens, C. G., Walter, J. C. and Harper, J. W. (2011) A genome-wide screen identifies p97 as an essential regulator of DNA damage-dependent CDT1 destruction. Mol. Cell, 44, 72-84.
77. Gulbis, J. M., Kelman, Z., Hurwitz, J., O'Donnell, M. and Kuriyan, J. (1996) Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCN A. Cell, 87, 297-306.
78. Arentson, E., Faloon, P., Seo, J., Moon, E., Studts, J. M., Fremont, D. H. and Choi, K. (2002) Oncogenic potential of the DNA replication licensing protein CDT1. Oncogene, 21, 1150-1158.
79. Karakaidos, P., Taraviras, S., Vassiliou, L. V., Zacharatos, P., Kastrinakis, N. G., Kougiou, D., Kouloukoussa, M., Nishitani, H., Papavassiliou, A. G., Lygerou, Z. et al. (2004) Overexpression of the replication licensing regulators hCdt1 and hCdc6 characterizes a subset of non-small-cell lung carcinomas: synergistic effect with mutant p53 on tumor growth and chromosomal instability -evidence of E2F-1 transcriptional control over hCdt1. Am. J. Pathol., 165, 1351-1365.
80. Xouri, G., Lygerou, Z., Nishitani, H., Pachnis, V., Nurse, P. and Taraviras, S. (2004) Cdt1 and geminin are down-regulated upon cell cycle exit and are over-expressed in cancer-derived cell lines. Eur. J. Biochem., 271, 3368-3378.