FANCD2-associated nuclease 1, but not exonuclease 1 or flap endonuclease 1, is able to unhook DNA interstrand cross-links in vitro

Journal of Biological Chemistry

Volumn 290, Issue 37, 2015, Pages 22602-22611

  Pizzolato, Julia ^a   Mukherjee, Shivam ^b   Schärer, Orlando D ^b,c   Jiricny, Josef ^a,c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOTHERAPY; DNA; MACHINERY; NITROGEN; NITROGEN COMPOUNDS; NUCLEOTIDES; PLATINUM COMPOUNDS;

BIOLOGICAL FUNCTIONS; CANCER CHEMOTHERAPY; ENDONUCLEASES; FLAP ENDONUCLEASE-1; INTERSTRAND CROSS-LINKS; NITROGEN MUSTARDS; REPLICATION FORK; REPLICATION MACHINERY;

SUBSTRATES;

DNA; DOUBLE STRANDED DNA; EXONUCLEASE; EXONUCLEASE 1; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN ASSOCIATED NUCLEASE 1; FLAP ENDONUCLEASE; FLAP ENDONUCLEASE 1; NITROGEN; NUCLEASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; DNA LIGASE; EXO1 PROTEIN, HUMAN; EXODEOXYRIBONUCLEASE; FAN1 PROTEIN, HUMAN; FEN1 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; DNA CROSS LINKING; ENZYME ACTIVITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROCESSING; CELL LINE; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; METABOLISM;

CELL LINE; DNA; DNA REPAIR ENZYMES; EXODEOXYRIBONUCLEASES; FLAP ENDONUCLEASES; HUMANS; SUBSTRATE SPECIFICITY;

EID: 84941584645     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.663666     Document Type: Article

References (37)

1. Schärer, O. D. (2005) DNA interstrand crosslinks: natural and drug-induced DNA adducts that induce unique cellular responses. Chem-BioChem 6, 27-32
2. Hinz, J. M. (2010) Role of homologous recombination in DNA interstrand crosslink repair. Environ. Mol. Mutagen. 51, 582-603
3. Auerbach, A. D. (2009) Fanconi anemia and its diagnosis. Mutat. Res. 668, 4-10
4. Crossan, G. P., and Patel, K. J. (2012) The Fanconi anaemia pathway orchestrates incisions at sites of crosslinked DNA. J. Pathol. 226, 326-337
5. Zhang, J., and Walter, J. C. (2014) Mechanism and regulation of incisions during DNA interstrand cross-link repair. DNA Repair 19, 135-142
6. Clauson, C., Schärer, O. D., and Niedernhofer, L. (2013) Advances in understanding the complex mechanisms of DNA interstrand cross-link repair. Cold Spring Harb. Perspect. Biol. 5, a012732
7. Liu, T., Ghosal, G., Yuan, J., Chen, J., and Huang, J. (2010) FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329, 693-696
8. Smogorzewska, A., Desetty, R., Saito, T. T., Schlabach, M., Lach, F. P., Sowa, M. E., Clark, A. B., Kunkel, T. A., Harper, J. W., Colaiácovo, M. P., and Elledge, S. J. (2010) A genetic screen identifies FAN1, a Fanconi anemiaassociated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell 39, 36-47
9. Kratz, K., Schöpf, B., Kaden, S., Sendoel, A., Eberhard, R., Lademann, C., Cannavó, E., Sartori, A. A., Hengartner, M. O., and Jiricny, J. (2010) Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142, 77-88
10. MacKay, C., Déclais, A. C., Lundin, C., Agostinho, A., Deans, A. J., MacArtney, T. J., Hofmann, K., Gartner, A., West, S. C., Helleday, T., Lilley, D. M., and Rouse, J. (2010) Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142, 65-76
11. Pennell, S., Déclais, A. C., Li, J., Haire, L. F., Berg, W., Saldanha, J. W., Taylor, I. A., Rouse, J., Lilley, D. M., and Smerdon, S. J. (2014) FAN1 activity on asymmetric repair intermediates is mediated by an atypical monomeric virus-type replication-repair nuclease domain. Cell Rep. 8, 84-93
12. Munoz, I. M., Szyniarowski, P., Toth, R., Rouse, J., and Lachaud, C. (2014) Improved genome editing in human cell lines using the CRISPR method. PloS ONE 9, e109752
13. Yoshikiyo, K., Kratz, K., Hirota, K., Nishihara, K., Takata, M., Kurumizaka, H., Horimoto, S., Takeda, S., and Jiricny, J. (2010) KIAA1018/FAN1 nuclease protects cells against genomic instability induced by interstrand cross-linking agents. Proc. Natl. Acad. Sci. U. S. A. 107, 21553-21557
14. Zhou, W., Otto, E. A., Cluckey, A., Airik, R., Hurd, T. W., Chaki, M., Diaz, K., Lach, F. P., Bennett, G. R., Gee, H. Y., Ghosh, A. K., Natarajan, S., Thongthip, S., Veturi, U., Allen, S. J., Janssen, S., Ramaswami, G., Dixon, J., Burkhalter, F., Spoendlin, M., Moch, H., Mihatsch, M. J., Verine, J., Reade, R., Soliman, H., Godin, M., Kiss, D., Monga, G., Mazzucco, G., Amann, K., Artunc, F., Newland, R. C., Wiech, T., Zschiedrich, S., Huber, T. B., Friedl, A., Slaats, G. G., Joles, J. A., Goldschmeding, R., Washburn, J., Giles, R. H., Levy, S., Smogorzewska, A., and Hildebrandt, F. (2012) FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat. Genet. 44, 910-915
15. Orans, J., McSweeney, E. A., Iyer, R. R., Hast, M. A., Hellinga, H. W., Modrich, P., and Beese, L. S. (2011) Structures of human exonuclease 1 DNA complexes suggest a unified mechanism for nuclease family. Cell 145, 212-223
16. Tsutakawa, S. E., Classen, S., Chapados, B. R., Arvai, A. S., Finger, L. D., Guenther, G., Tomlinson, C. G., Thompson, P., Sarker, A. H., Shen, B., Cooper, P. K., Grasby, J. A., and Tainer, J. A. (2011) Human flap endonuclease structures, DNA double-base flipping, and a unified understanding of the FEN1 superfamily. Cell 145, 198-211
17. Tsutakawa, S. E., Lafrance-Vanasse, J., and Tainer, J. A. (2014) The cutting edges in DNA repair, licensing, and fidelity: DNA and RNA repair nucleases sculpt DNA to measure twice, cut once. DNA Repair 19, 95-107
18. Mukherjee, S., Guainazzi, A., and Schärer, O. D. (2014) Synthesis of structurally diverse major groove DNA interstrand crosslinks using three different aldehyde precursors. Nucleic Acids Res. 42, 7429-7435
19. Guainazzi, A., Campbell, A. J., Angelov, T., Simmerling, C., and Schärer, O. D. (2010) Synthesis and molecular modeling of a nitrogen mustard DNA interstrand crosslink. Chemistry 16, 12100-12103
20. Angelov, T., Guainazzi, A., and Schärer, O. D. (2009) Generation of DNA interstrand cross-links by post-synthetic reductive amination. Org. Lett. 11, 661-664
21. Bregenhorn, S., and Jiricny, J. (2014) Biochemical characterization of a cancer-associated E109K missense variant of human exonuclease 1. Nucleic Acids Res. 42, 7096-7103
22. Hanada, K., Budzowska, M., Davies, S. L., van Drunen, E., Onizawa, H., Beverloo, H. B., Maas, A., Essers, J., Hickson, I. D., and Kanaar, R. (2007) The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14, 1096-1104
23. Klein Douwel, D., Boonen, R. A., Long, D. T., Szypowska, A. A., Räschle, 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
24. Harrington, J. J., and Lieber, M. R. (1994) Functional domains within FEN-1 and RAD2 define a family of structure-specific endonucleases: implications for nucleotide excision repair. Genes Dev. 8, 1344-1355
25. Zhang, J., Dewar, J. M., Budzowska, M., Motnenko, A., Cohn, M. A., and Walter, J. C. (2015) DNA interstrand cross-link repair requires replicationfork convergence. Nat. Struct. Mol. Biol. 22, 242-247
26. Hanada, K., Budzowska, M., Modesti, M., Maas, A., Wyman, C., Essers, J., and Kanaar, R. (2006) The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J. 25, 4921-4932
27. Nair, N., Castor, D., Macartney, T., and Rouse, J. (2014) Identification and characterization of MUS81 point mutations that abolish interaction with the SLX4 scaffold protein. DNA Repair 24, 131-137
28. Ward, I. M., and Chen, J. (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276, 47759-47762
29. Vassin, V. M., Anantha, R. W., Sokolova, E., Kanner, S., and Borowiec, J. A. (2009) Human RPA phosphorylation by ATR stimulates DNA synthesis and prevents ssDNA accumulation during DNA-replication stress. J. Cell Sci. 122, 4070-4080
30. Petermann, E., Orta, M. L., Issaeva, N., Schultz, N., and Helleday, T. (2010) Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 37, 492-502
31. Chaudhury, I., Stroik, D. R., and Sobeck, A. (2014) FANCD2-controlled chromatin access of the Fanconi-associated nuclease FAN1 is crucial for the recovery of stalled replication forks. Mol. Cell. Biol. 34, 3939-3954
32. Gwon, G. H., Kim, Y., Liu, Y., Watson, A. T., Jo, A., Etheridge, T. J., Yuan, F., Zhang, Y., Kim, Y., Carr, A. M., and Cho, Y. (2014) Crystal structure of a Fanconi anemia-associated nuclease homolog bound to 5' flap DNA: basis of interstrand cross-link repair by FAN1. Genes Dev. 28, 2276-2290
33. 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
34. Zhao, Q., Xue, X., Longerich, S., Sung, P., and Xiong, Y. (2014) Structural insights into 5' flap DNA unwinding and incision by the human FAN1 dimer. Nat. Commun. 5, 5726
35. Fontebasso, Y., Etheridge, T. J., Oliver, A. W., Murray, J. M., and Carr, A. M. (2013) The conserved Fanconi anemia nuclease Fan1 and the SUMOE3 ligase Pli1 act in two novel Pso2-independent pathways of DNA interstrand crosslink repair in yeast. DNA Repair 12, 1011-1023
36. 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., Gileadi, O., Hartley, J. A., and McHugh, P. J. (2011) Human SNM1A and XPFERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev. 25, 1859-1870
37. Muniandy, P. A., Liu, J., Majumdar, A., Liu, S. T., and Seidman, M. M. (2010) DNA interstrand crosslink repair in mammalian cells: step by step. Crit. Rev. Biochem. Mol. Biol. 45, 23-49