The structure and duplex context of DNA interstrand crosslinks affects the activity of DNA polymerase η

Nucleic Acids Research

Volumn 44, Issue 15, 2016, Pages 7281-7291

  Roy, Upasana ^a   Mukherjee, Shivam ^a   Sharma, Anjali ^a   Frank, Ekaterina G ^b   Schärer, Orlando D ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORMETHINE; DNA DIRECTED DNA POLYMERASE ETA; DOUBLE STRANDED DNA; NUCLEASE; NUCLEOTIDE; SYNTHETIC DNA; CROSS LINKING REAGENT; DNA; DNA DIRECTED DNA POLYMERASE;

ARTICLE; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; DNA SYNTHESIS; ENZYME ACTIVITY; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; BIOSYNTHESIS; CHEMISTRY; CONFORMATION; DNA REPLICATION; GENETICS; METABOLISM;

CROSS-LINKING REAGENTS; DNA; DNA DAMAGE; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; NUCLEIC ACID CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84988363525     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw485     Document Type: Article

References (58)

1. Scharer, O.D. (2005) DNA interstrand crosslinks: natural and drug-induced DNA adducts that induce unique cellular responses. Chembiochem, 6, 27-32.
2. Noll, D.M., Mason, T.M. and Miller, P.S. (2006) Formation and repair of interstrand cross-links in DNA. Chem. Rev., 106, 277-301.
3. Deans, A.J. and West, S.C. (2011) DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer, 11, 467-480.
4. Clauson, C., Scharer, O.D. and Niedernhofer, L. (2013) Advances in understanding the complex mechanisms of DNA interstrand cross-link repair. Cold Spring Harbor Perspect. Biol., 5, a012732.
5. Kottemann, M.C. and Smogorzewska, A. (2013) Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature, 493, 356-363.
6. Raschle, M., Knipscheer, P., Enoiu, M., Angelov, T., Sun, J., Griffith, J.D., Ellenberger, T.E., Scharer, O.D. and Walter, J.C. (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell, 134, 969-980.
7. Zhang, J., Dewar, J.M., Budzowska, M., Motnenko, A., Cohn, M.A. and Walter, J.C. (2015) DNA interstrand cross-link repair requires replication-fork convergence. Nat. Struct. Mol. Biol., 22, 242-247.
8. Knipscheer, P., Raschle, M., Smogorzewska, A., Enoiu, M., Ho, T.V., Scharer, O.D., Elledge, S.J. andWalter, J.C. (2009) The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science, 326, 1698-1701.
9. Klein Douwel, D., Boonen, R.A., Long, D.T., Szypowska, A.A., Raschle, M., Walter, J.C. and Knipscheer, P. (2014) XPF-ERCC1 acts in Unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol. Cell, 54, 460-471.
10. Wang, A.T., Sengerova, B., Cattell, E., Inagawa, T., Hartley, J.M., Kiakos, K., Burgess-Brown, N.A., Swift, L.P., Enzlin, J.H., Schofield, C.J. et al. (2011) Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev., 25, 1859-1870.
11. Castor, D., Nair, N., Declais, A.C., Lachaud, C., Toth, R., Macartney, T.J., Lilley, D.M., Arthur, J.S. and Rouse, J. (2013) Cooperative control of holliday junction resolution and DNA repair by the SLX1 and MUS81-EME1 nucleases. Mol. Cell, 52, 221-233.
12. Zhang, J. and Walter, J.C. (2014) Mechanism and regulation of incisions during DNA interstrand cross-link repair. DNA Repair, 19, 135-142.
13. Xie, K., Doles, J., Hemann, M.T. and Walker, G.C. (2010) Error-prone translesion synthesis mediates acquired chemoresistance. Proc. Natl. Acad. Sci. U.S.A., 107, 20792-20797.
14. Doles, J., Oliver, T.G., Cameron, E.R., Hsu, G., Jacks, T., Walker, G.C. and Hemann, M.T. (2010) Suppression of Rev3, the catalytic subunit of Pol{zeta}, sensitizes drug-resistant lung tumors to chemotherapy. Proc. Natl. Acad. Sci. U.S.A., 107, 20786-20791.
15. Srivastava, A.K., Han, C., Zhao, R., Cui, T., Dai, Y., Mao, C., Zhao, W., Zhang, X., Yu, J. and Wang, Q.E. (2015) Enhanced expression of DNA polymerase eta contributes to cisplatin resistance of ovarian cancer stem cells. Proc. Natl. Acad. Sci. U.S.A., 112, 4411-4416.
16. Ho, T.V. and Scharer, O.D. (2010) Translesion DNA synthesis polymerases in DNA interstrand crosslink repair. Env. Mol. Mutagen., 51, 552-566.
17. Sonoda, E., Okada, T., Zhao, G.Y., Tateishi, S., Araki, K., Yamaizumi, M., Yagi, T., Verkaik, N.S., van Gent, D.C., Takata, M. et al. (2003) Multiple roles of Rev3, the catalytic subunit of pol[zeta] in maintaining genome stability in vertebrates. EMBO J., 22, 3188-3197.
18. Nojima, K., Hochegger, H., Saberi, A., Fukushima, T., Kikuchi, K., Yoshimura, M., Orelli, B.J., Bishop, D.K., Hirano, S., Ohzeki, M. et al. (2005) Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res., 65, 11704-11711.
19. Shen, X., Jun, S., ONeal, L.E., Sonoda, E., Bemark, M., Sale, J.E. and Li, L. (2006) REV3 and REV1 play major roles in recombination-independent repair of DNA interstrand cross-links mediated by monoubiquitinated proliferating cell nuclear antigen (PCNA). J. Biol. Chem., 281, 13869-13872.
20. Sarkar, S., Davies, A.A., Ulrich, H.D. and McHugh, P.J. (2006) DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J., 25, 1285-1294.
21. Budzowska, M., Graham, T.G., Sobeck, A., Waga, S. and Walter, J.C. (2015) Regulation of the Rev1-pol zeta complex during bypass of a DNA interstrand cross-link. EMBO J., 34, 1971-1985.
22. Misra, R.R. and Vos, J.M. (1993) Defective replication of psoralen adducts detected at the gene-specific level in xeroderma pigmentosum variant cells. Mol. Cell. Biol., 13, 1002-1012.
23. Albertella, M.R., Green, C.M., Lehmann, A.R. and OConnor, M.J. (2005) A role for polymerase in the cellular tolerance to cisplatin-induced damage. Cancer Res., 65, 9799-9806.
24. Chen, Y.-W., Cleaver, J.E., Hanaoka, F., Chang, C.-F. and Chou, K.-M. (2006) A novel role of DNA polymerase in modulating cellular sensitivity to chemotherapeutic agents. Mol. Cancer Res., 4, 257-265.
25. Minko, I.G., Harbut, M.B., Kozekov, I.D., Kozekova, A., Jakobs, P.M., Olson, S.B., Moses, R.E., Harris, T.M., Rizzo, C.J. and Lloyd, R.S. (2008) Role for DNA polymerase in the processing of N2-N2-guanine interstrand cross-links. J. Biol. Chem., 283, 17075-17082.
26. Williams, H.L., Gottesman, M.E. and Gautier, J. (2012) Replication-independent repair of DNA interstrand crosslinks. Mol. Cell, 47, 140-147.
27. Zietlow, L., Smith, L.A., Bessho, M. and Bessho, T. (2009) Evidence for the involvement of human DNA polymerase N in the repair of DNA interstrand cross-links. Biochemistry, 48, 11817-11824.
28. Moldovan, G.-L., Madhavan, M.V., Mirchandani, K.D., McCaffrey, R.M., Vinciguerra, P. and DAndrea, A.D. (2010) DNA polymerase POLN participates in cross-link repair and homologous recombination. Mol. Cell. Biol., 30, 1088-1096.
29. Ho, T.V., Guainazzi, A., Derkunt, S.B., Enoiu, M. and Scharer, O.D. (2011) Structure-dependent bypass of DNA interstrand crosslinks by translesion synthesis polymerases. Nucleic Acids Res., 39, 7455-7464.
30. Yamanaka, K., Minko, I.G., Takata, K.-I., Kolbanovskiy, A., Kozekov, I.D., Wood, R.D., Rizzo, C.J. and Lloyd, R.S. (2010) Novel enzymatic function of DNA polymerase in translesion DNA synthesis past major groove DNA-peptide and DNA-DNA cross-links. Chem. Res. Tox., 23, 689-695.
31. Klug, A.R., Harbut, M.B., Lloyd, R.S. and Minko, I.G. (2012) Replication bypass of N2-deoxyguanosine interstrand cross-links by human DNA polymerases. Chem. Res. Toxicol., 25, 755-762.
32. 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, 399, 700-704.
33. Johnson, R.E., Prakash, S. and Prakash, L. (1999) Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Pol eta. Science, 283, 1001-1004.
34. Tomicic, M.T., Aasland, D., Naumann, S.C., Meise, R., Barckhausen, C., Kaina, B. and Christmann, M. (2014) Translesion polymerase eta is upregulated by cancer therapeutics and confers anticancer drug resistance. Cancer Res., 74, 5585-5596.
35. Angelov, T., Guainazzi, A. and Scharer, O.D. (2009) Generation of DNA interstrand cross-links by post-synthetic reductive amination. Org. Lett., 11, 661-664.
36. Guainazzi, A., Campbell, A.J., Angelov, T., Simmerling, C. and Scharer, O.D. (2010) Synthesis and molecular modeling of a nitrogen mustard DNA interstrand crosslink. Chemistry, 16, 12100-12103.
37. Mukherjee, S., Guainazzi, A. and Scharer, O.D. (2014) Synthesis of structurally diverse major groove DNA interstrand crosslinks using three different aldehyde precursors. Nucleic Acids Res., 42, 7429-7435.
38. Frank, E.G. and Woodgate, R. (2007) Increased catalytic activity and altered fidelity of human DNA polymerase iota in the presence of manganese. J. Biol. Chem., 282, 24689-24696.
39. Millard, J.T., Raucher, S. and Hopkins, P.B. (1990) Mechlorethamine cross-links deoxyguanosine residues at 5-GNC sequences in duplex DNA fragments. J. Am. Chem. Soc., 112, 2459-2460.
40. Rink, S.M. and Hopkins, P.B. (1995) A mechlorethamine-induced DNA interstrand cross-link bends duplex DNA. Biochemistry, 34, 1439-1445.
41. Dong, Q., Barsky, D., Colvin, M.E., Melius, C.F., Ludeman, S.M., Moravek, J.F., Colvin, O.M., Bigner, D.D., Modrich, P. and Friedman, H.S. (1995) A structural basis for a phosphoramide mustard-induced DNA interstrand cross-link at 5-d(GAC). Proc. Natl. Acad. Sci. U.S.A., 92, 12170-12174.
42. Fan, Y.H. and Gold, B. (1999) Sequence-specificity for DNA interstrand cross-linking by alpha, omega-alkanediol dimethylsulfonate esters: Evidence for DNA distortion by the initial monofunctional lesion. J. Am. Chem. Soc., 121, 11942-11946.
43. Smeaton, M.B., Hlavin, E.M., Noronha, A.M., Murphy, S.P., Wilds, C.J. and Miller, P.S. (2009) Effect of cross-link structure on DNA interstrand cross-link repair synthesis. Chem. Res. Toxicol., 22, 1285-1297.
44. Prakash, S., Johnson, R.E. and Prakash, L. (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Ann. Rev. Biochem., 74, 317-353.
45. Shachar, S., Ziv, O., Avkin, S., Adar, S., Wittschieben, J., Reissner, T., Chaney, S., Friedberg, E.C., Wang, Z., Carell, T. et al. (2009) Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J., 28, 383-393.
46. 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, 6, 891-899.
47. Prober, J.M., Trainor, G.L., Dam, R.J., Hobbs, F.W., Robertson, C.W., Zagursky, R.J., Cocuzza, A.J., Jensen, M.A. and Baumeister, K. (1987) A system for rapid DNA sequencing with fluorescent chain-terminating dideoxynucleotides. Science, 238, 336-341.
48. 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.
49. 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.
50. Allerston, C.K., Lee, S.Y., Newman, J.A., Schofield, C.J., McHugh, P.J. and Gileadi, O. (2015) The structures of the SNM1A and SNM1B/Apollo nuclease domains reveal a potential basis for their distinct DNA processing activities. Nucleic Acids Res., 43, 11047-11060.
51. Wang, R., Persky, N.S., Yoo, B., Ouerfelli, O., Smogorzewska, A., Elledge, S.J. and Pavletich, N.P. (2014) DNA repair. Mechanism of DNA interstrand cross-link processing by repair nuclease FAN1. Science, 346, 1127-1130.
52. Pizzolato, J., Mukherjee, S., Scharer, O.D. and Jiricny, J. (2015) FANCD2-associated nuclease 1, but not exonuclease 1 or flap endonuclease 1, is able to unhook DNA interstrand cross-links in vitro. J. Biol. Chem., 290, 22602-22611.
53. Long, D.T., Raschle, M., Joukov, V. and Walter, J.C. (2011) Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science, 333, 84-87.
54. Nelson, J.R., Lawrence, C.W. and Hinkle, D.C. (1996) Deoxycytidyl transferase activity of yeast REV1 protein. Nature, 382, 729-731.
55. Haracska, L., Prakash, S. and Prakash, L. (2002) Yeast Rev1 protein is a G template-specific DNA polymerase. J. Biol. Chem., 277, 15546-15551.
56. Reissner, T., Schneider, S., Schorr, S. and Carell, T. (2010) Crystal structure of a cisplatin-(1, 3-GTG) cross-link within DNA polymerase eta. Angew. Chem. Int. Ed. Engl., 49, 3077-3080.
57. Zhao, Y., Biertumpfel, C., Gregory, M.T., Hua, Y.J., Hanaoka, F. and Yang, W. (2012) Structural basis of human DNA polymerase eta-mediated chemoresistance to cisplatin. Proc. Natl. Acad. Sci. U.S.A., 109, 7269-7274.
58. Silverstein, T.D., Johnson, R.E., Jain, R., Prakash, L., Prakash, S. and Aggarwal, A.K. (2010) Structural basis for the suppression of skin cancers by DNA polymerase eta. Nature, 465, 1039-1043.