Rad18-dependent SUMOylation of human specialized DNA polymerase eta is required to prevent under-replicated DNA

Nature Communications

Volumn 7, Issue , 2016, Pages

  Despras, Emmanuelle ^a,b,c   Sittewelle, Méghane ^a,b,c   Pouvelle, Caroline ^a,b,c   Delrieu, Noémie ^a,b,c   Cordonnier, Agnès M ^d   Kannouche, Patricia L ^a,b,c  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b CNRS   (France)

^c INSTITUT GUSTAVE ROUSSY   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; DNA; DNA DIRECTED DNA POLYMERASE ETA; LYSINE; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN INHIBITOR OF ACTIVATED STAT 1; RAD18 PROTEIN; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE; PIAS1 PROTEIN, HUMAN; RAD18 PROTEIN, HUMAN;

CELLS AND CELL COMPONENTS; CHROMOSOME; DNA; ENZYME; PROTEIN;

ARTICLE; CELL CYCLE S PHASE; CHROMOSOME; CONTROLLED STUDY; DAUGHTER CELL; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA REPLICATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOSIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROCESSING; PROTEIN TARGETING; SUMOYLATION; UBIQUITINATION; CELL LINE; GENETICS; METABOLISM;

CELL LINE; DNA REPLICATION; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; HUMANS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN INHIBITORS OF ACTIVATED STAT; S PHASE; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; UBIQUITIN-PROTEIN LIGASES;

EID: 84994592291     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13326     Document Type: Article

References (71)

1. Sale, J. E., Lehmann, A. R., Woodgate, R. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell Biol. 13, 141-152 (2012).
2. Masutani, C., Kusumoto, R., Iwai, S., Hanaoka, F. Mechanisms of accurate translesion synthesis by human DNA polymerase eta. EMBO J. 19, 3100-3109 (2000).
3. Yoon, J. H., Prakash, L., Prakash, S. Highly error-free role of DNA polymerase eta in the replicative bypass of UV-induced pyrimidine dimers in mouse and human cells. Proc. Natl Acad. Sci. USA 106, 18219-18224 (2009).
4. Kannouche, P. L., Wing, J., 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, 491-500 (2004).
5. Bienko, M. et al. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310, 1821-1824 (2005).
6. Despras, E., Delrieu, N., Garandeau, C., Ahmed-Seghir, S., Kannouche, P. L. Regulation of the specialized DNA polymerase eta: revisiting the biological relevance of its PCNA-and ubiquitin-binding motifs. Environ. Mol. Mutagen. 53, 752-765 (2012).
7. Day, T. A. et al. Phosphorylated Rad18 directs DNA polymerase eta to sites of stalled replication. J. Cell Biol. 191, 953-966 (2010).
8. Watanabe, K. et al. Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 23, 3886-3896 (2004).
9. Chen, Y. W. et al. Human DNA polymerase eta activity and translocation is regulated by phosphorylation. Proc. Natl Acad. Sci. USA 105, 16578-16583 (2008).
10. Gohler, T., Sabbioneda, S., Green, C. M., Lehmann, A. R. ATR-mediated phosphorylation of DNA polymerase eta is needed for efficient recovery from UV damage. J. Cell Biol. 192, 219-227 (2011).
11. Davis, E. J. et al. DVC1 (C1orf124) recruits the p97 protein segregase to sites of DNA damage. Nat. Struct. Mol. Biol. 19, 1093-1100 (2012).
12. Jung, Y. S., Liu, G., Chen, X. Pirh2 E3 ubiquitin ligase targets DNA polymerase eta for 20S proteasomal degradation. Mol. Cell. Biol. 30, 1041-1048 (2010).
13. Mosbech, A. et al. DVC1 (C1orf124) is a DNA damage-targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks. Nat. Struct. Mol. Biol. 19, 1084-1092 (2012).
14. Bergoglio, V. et al. DNA synthesis by Pol eta promotes fragile site stability by preventing under-replicated DNA in mitosis. J. Cell Biol. 201, 395-408 (2013).
15. Rey, L. et al. Human DNA polymerase eta is required for common fragile site stability during unperturbed DNA replication. Mol. Cell. Biol. 29, 3344-3354 (2009).
16. Naim, V., Wilhelm, T., Debatisse, M., Rosselli, F. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat. Cell Biol. 15, 1008-1015 (2013).
17. Ying, S. et al. MUS81 promotes common fragile site expression. Nat. Cell Biol. 15, 1001-1007 (2013).
18. Chan, K. L., Palmai-Pallag, T., Ying, S., Hickson, I. D. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 11, 753-760 (2009).
19. Naim, V., Rosselli, F. The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat. Cell Biol. 11, 761-768 (2009).
20. Harrigan, J. A. et al. Replication stress induces 53BP1-containing OPT domains in G1 cells. J. Cell Biol. 193, 97-108 (2011).
21. Lukas, C. et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13, 243-253 (2011).
22. Kannouche, P. et al. Domain structure, localization, function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev. 15, 158-172 (2001).
23. Sirbu, B. M. et al. Analysis of protein dynamics at active, stalled, collapsed replication forks. Genes Dev. 25, 1320-1327 (2011).
24. Lopez-Contreras, A. J. et al. A proteomic characterization of factors enriched at nascent DNA molecules. Cell Rep. 3, 1105-1116 (2013).
25. Kim, S. H., Michael, W. M. Regulated proteolysis of DNA polymerase eta during the DNA-damage response in C. elegans. Mol. Cell 32, 757-766 (2008).
26. Tatham, M. H. et al. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J Biol Chem 276, 35368-35374 (2001).
27. Teng, S., Luo, H., Wang, L. Predicting protein sumoylation sites from sequence features. Amino acids 43, 447-455 (2012).
28. Xue, Y., Zhou, F., Fu, C., Xu, Y., Yao, X. SUMOsp: a web server for sumoylation site prediction. Nucleic acids research 34, W254-W257 (2006).
29. Bienko, M. et al. Regulation of translesion synthesis DNA polymerase eta by monoubiquitination. Mol Cell 37, 396-407 (2010).
30. Biertumpfel, C. et al. Structure and mechanism of human DNA polymerase eta. Nature 465, 1044-1048 (2010).
31. Arlett, C. F., Harcourt, S. A., Broughton, B. C. The influence of caffeine on cell survival in excision-proficient and excision-deficient xeroderma pigmentosum and normal human cell strains following ultraviolet-light irradiation. Mutat. Res. 33, 341-346 (1975).
32. Despras, E., Daboussi, F., Hyrien, O., Marheineke, K., Kannouche, P. L. 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 (2010).
33. Galanty, Y. et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939 (2009).
34. Gibbs-Seymour, I. et al. Ubiquitin-SUMO circuitry controls activated fanconi anemia ID complex dosage in response to DNA damage. Mol. Cell 57, 150-164 (2015).
35. Morris, J. R. et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890 (2009).
36. Nakajima, S. et al. Replication-dependent and-independent responses of RAD18 to DNA damage in human cells. J. Biol. Chem. 281, 34687-34695 (2006).
37. Miyauchi, Y., Yogosawa, S., Honda, R., Nishida, T., Yasuda, H. Sumoylation of Mdm2 by protein inhibitor of activated STAT (PIAS) and RanBP2 enzymes. J. Biol. Chem. 277, 50131-50136 (2002).
38. Huang, J. et al. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat. Cell Biol. 11, 592-603 (2009).
39. Tateishi, S., Sakuraba, Y., Masuyama, S., Inoue, H., Yamaizumi, M. Dysfunction of human Rad18 results in defective postreplication repair and hypersensitivity to multiple mutagens. Proc. Natl Acad. Sci. USA 97, 7927-7932 (2000).
40. Kannouche, P. L., Lehmann, A. R. Ubiquitination of PCNA and the polymerase switch in human cells. Cell Cycle 3, 1011-1013 (2004).
41. Terai, K., Abbas, T., Jazaeri, A. A., Dutta, A. CRL4(Cdt2) E3 ubiquitin ligase monoubiquitinates PCNA to promote translesion DNA synthesis. Mol. Cell 37, 143-149 (2010).
42. Zhang, S. et al. PCNA is ubiquitinated by RNF8. Cell Cycle 7, 3399-3404 (2008).
43. Bacquin, A. et al. The helicase FBH1 is tightly regulated by PCNA via CRL4(Cdt2)-mediated proteolysis in human cells. Nucleic Acids Res. 41, 6501-6513 (2013).
44. Tsanov, N. et al. PIP degron proteins, substrates of CRL4Cdt2, not PIP boxes, interfere with DNA polymerase eta and kappa focus formation on UV damage. Nucl. Acids Res. 42, 3692-3706 (2014).
45. Edmunds, C. E., Simpson, L. J., Sale, J. E. PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol. Cell 30, 519-529 (2008).
46. Hendel, A. et al. PCNA ubiquitination is important, but not essential for translesion DNA synthesis in mammalian cells. PLoS Genet. 7, e1002262 (2011).
47. Krijger, P. H. et al. PCNA ubiquitination-independent activation of polymerase eta during somatic hypermutation and DNA damage tolerance. DNA Repair 10, 1051-1059 (2011).
48. Dungrawala, H. et al. The replication checkpoint prevents two types of fork collapse without regulating replisome stability. Mol. Cell 59, 998-1010 (2015).
49. Kile, A. C. et al. HLTF's ancient HIRAN domain binds 3' DNA ends to drive replication fork reversal. Mol. Cell 58, 1090-1100 (2015).
50. Boyer, A. S., Grgurevic, S., Cazaux, C., Hoffmann, J. S. The human specialized DNA polymerases and non-B DNA: vital relationships to preserve genome integrity. J. Mol. Biol. 425, 4767-4781 (2013).
51. Lossaint, G. et al. FANCD2 binds MCM proteins and controls replisome function upon activation of s phase checkpoint signaling. Mol. Cell 51, 678-690 (2014).
52. Tsuji, Y. et al. Recognition of forked and single-stranded DNA structures by human RAD18 complexed with RAD6B protein triggers its recruitment to stalled replication forks. Genes Cells 13, 343-354 (2008).
53. Inagaki, A. et al. Dynamic localization of human RAD18 during the cell cycle and a functional connection with DNA double-strand break repair. DNA Repair 8, 190-201 (2009).
54. Miyase, S. et al. Differential regulation of Rad18 through Rad6-dependent mono-and polyubiquitination. J. Biol. Chem. 280, 515-524 (2005).
55. Watanabe, K. et al. RAD18 promotes DNA double-strand break repair during G1 phase through chromatin retention of 53BP1. Nucl. Acids Res. 37, 2176-2193 (2009).
56. Inagaki, A. et al. Human RAD18 interacts with ubiquitylated chromatin components and facilitates RAD9 recruitment to DNA double strand breaks. PloS ONE 6, e23155 (2011).
57. Hay, R. T. SUMO: a history of modification. Mol. Cell 18, 1-12 (2005).
58. Johnson, E. S. Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382 (2004).
59. Hendriks, I. A. et al. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat. Struct. Mol. Biol. 21, 927-936 (2014).
60. Bergink, S. et al. Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51-Rad52 interaction. Nat. Cell Biol. 15, 526-532 (2013).
61. Nie, M. et al. Dual recruitment of Cdc48 (p97)-Ufd1-Npl4 ubiquitin-selective segregase by small ubiquitin-like modifier protein (SUMO) and ubiquitin in SUMO-targeted ubiquitin ligase-mediated genome stability functions. J. Biol. Chem. 287, 29610-29619 (2012).
62. Stingele, J., Habermann, B., Jentsch, S. DNA-protein crosslink repair: proteases as DNA repair enzymes. Trends Biochem. Sci. 40, 67-71 (2015).
63. Balakirev, M. Y. et al. Wss1 metalloprotease partners with Cdc48/Doa1 in processing genotoxic SUMO conjugates. Elife 4, e06763 (2015).
64. Niimi, A. et al. Regulation of proliferating cell nuclear antigen ubiquitination in mammalian cells. Proc. Natl Acad. Sci. USA 105, 16125-16130 (2008).
65. Shiomi, N. et al. Human RAD18 is involved in S phase-specific singlestrand break repair without PCNA monoubiquitination. Nucl. Acids Res. 35, e9 (2007).
66. Stary, A., Kannouche, P., Lehmann, A. R., Sarasin, A. Role of DNA polymerase eta in the UV mutation spectrum in human cells. J. Biol. Chem. 278, 18767-18775 (2003).
67. Zlatanou, A. et al. 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 (2011).
68. Ahmed-Seghir, S. et al. Aberrant C-terminal domain of polymerase eta targets the functional enzyme to the proteosomal degradation pathway. DNA Repair 29, 154-165 (2015).
69. Petruk, S. et al. TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150, 922-933 (2012).
70. Napolitano, R. L., Fuchs, R. P. New strategy for the construction of singlestranded plasmids with single mutagenic lesions. Chem. Res. Toxicol. 10, 667-671 (1997).
71. Cordonnier, A. M., Lehmann, A. R., Fuchs, R. P. Impaired translesion synthesis in xeroderma pigmentosum variant extracts. Mol. Cell. Biol. 19, 2206-2211 (1999).