A novel interplay between the Fanconi anemia core complex and ATR-ATRIP kinase during DNA cross-link repair

Nucleic Acids Research

Volumn 41, Issue 14, 2013, Pages 6930-6941

  Tomida, Junya ^a   Itaya, Akiko ^a,b   Shigechi, Tomoko ^a,c   Unno, Junya ^a   Uchida, Emi ^a   Ikura, Masae ^a   Masuda, Yuji ^d   Matsuda, Shun ^e   Adachi, Jun ^f   Kobayashi, Masahiko ^g   Meetei, Amom Ruhikanta ^h   Maehara, Yoshihiko ^c   Yamamoto, Ken Ichi ^g   Kamiya, Kenji ⁱ   Matsuura, Akira ^j   Matsuda, Tomonari ^e   Ikura, Tsuyoshi ^a   Ishiai, Masamichi ^a   Takata, Minoru ^a  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d NAGOYA UNIVERSITY   (Japan)

^e KYOTO UNIVERSITY   (Japan)

^f NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^g KANAZAWA UNIVERSITY   (Japan)

^h UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

ⁱ HIROSHIMA UNIVERSITY   (Japan)

^j CHIBA UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ATR INTERACTING PROTEIN; ATR PROTEIN; BINDING PROTEIN; CISPLATIN; DNA; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA GROUP L PROTEIN; FANCONI ANEMIA PROTEIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN RAD17; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHICKEN; CHROMATIN; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL CYCLE PROTEINS; CELL LINE; CHROMATIN; DNA REPAIR; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; HELA CELLS; HUMANS; PROTEIN-SERINE-THREONINE KINASES; REPLICATION PROTEIN A;

EID: 84881539569     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt467     Document Type: Article

References (63)

1. Kim H. and D'Andrea A.D. (2012) Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev., 26, 1393-1408
2. Wang W. (2007) Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet., 8, 735-748
3. Kim J.M., Kee Y., Gurtan A. and D'Andrea A.D. (2008) Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood, 111, 5215-5222
4. Ciccia A., Ling C., Coulthard R., Yan Z., Xue Y., Meetei A.R., Laghmani el H., Joenje H., McDonald N., de Winter J.P. et al. (2007) Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol. Cell, 25, 331-343
5. Kee Y. and D'Andrea A.D. (2010) Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev., 24, 1680-1694
6. Smogorzewska A., Matsuoka S., Vinciguerra P., McDonald E.R. 3rd, Hurov K.E., Luo J., Ballif B.A., Gygi S.P., Hofmann K., D'Andrea A.D. et al. (2007) Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell, 129, 289-301
7. Huang M. and D'Andrea A.D. (2010) A new nuclease member of the FAN club. Nat. Struct. Mol. Biol., 17, 926-928
8. Sato K., Ishiai M., Toda K., Furukoshi S., Osakabe A., Tachiwana H., Takizawa Y., Kagawa W., Kitao H., Dohmae N. et al. (2012) Histone chaperone activity of Fanconi anemia proteins, FANCD2 and FANCI, is required for DNA crosslink repair. EMBO J., 31, 3524-3536
9. Matsushita N., Kitao H., Ishiai M., Nagashima N., Hirano S., Okawa K., Ohta T., Yu D.S., McHugh P.J., Hickson I.D. et al. (2005) A FancD2-monoubiquitin fusion reveals hidden functions of Fanconi anemia core complex in DNA repair. Mol. Cell, 19, 841-847
10. Walsh T. and King M.C. (2007) Ten genes for inherited breast cancer. Cancer Cell, 11, 103-105
11. Levy-Lahad E. (2010) Fanconi anemia and breast cancer susceptibility meet again. Nat. Genet., 42, 368-369
12. Vaz F., Hanenberg H., Schuster B., Barker K., Wiek C., Erven V., Neveling K., Endt D., Kesterton I., Autore F. et al. (2010) Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat. Genet., 42, 406-409
13. Stoepker C., Hain K., Schuster B., Hilhorst-Hofstee Y., Rooimans M.A., Steltenpool J., Oostra A.B., Eirich K., Korthof E.T., Nieuwint A.W. et al. (2011) SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat. Genet., 43, 138-141
14. Kim Y., Lach F.P., Desetty R., Hanenberg H., Auerbach A.D. and Smogorzewska A. (2011) Mutations of the SLX4 gene in Fanconi anemia. Nat. Genet., 43, 142-146
15. Yamamoto K.N., Kobayashi S., Tsuda M., Kurumizaka H., Takata M., Kono K., Jiricny J., Takeda S. and Hirota K. (2011) Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc. Natl Acad. Sci. USA, 108, 6492-6496
16. Crossan G.P., van der Weyden L., Rosado I.V., Langevin F., Gaillard P.H., McIntyre R.E., Gallagher F., Kettunen M.I., Lewis D.Y., Brindle K. et al. (2011) Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat. Genet., 43, 147-152
17. Ishiai M., Kitao H., Smogorzewska A., Tomida J., Kinomura A., Uchida E., Saberi A., Kinoshita E., Kinoshita-Kikuta E., Koike T. et al. (2008) FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat. Struct. Mol. Biol., 15, 1138-1146
18. Andreassen P.R., D'Andrea A.D. and Taniguchi T. (2004) ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev., 18, 1958-1963
19. Wang L.C., Stone S., Hoatlin M.E. and Gautier J. (2008) Fanconi anemia proteins stabilize replication forks. DNA Repair (Amst.), 7, 1973-1981
20. Shigechi T., Tomida J., Sato K., Kobayashi M., Eykelenboom J.K., Pessina F., Zhang Y., Uchida E., Ishiai M., Lowndes N.F. et al. (2012) ATR-ATRIP kinase complex triggers activation of the Fanconi anemia DNA repair pathway. Cancer Res., 72, 1149-1156
21. Cimprich K.A. and Cortez D. (2008) ATR: An essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol., 9, 616-627
22. Burrows A.E. and Elledge S.J. (2008) How ATR turns on: TopBP1 goes on ATRIP with ATR. Genes Dev., 22, 1416-1421
23. Flynn R.L. and Zou L. (2010) ATR: A master conductor of cellular responses to DNA replication stress. Trends Biochem. Sci., 36, 133-140
24. Takao N., Kato H., Mori R., Morrison C., Sonada E., Sun X., Shimizu H., Yoshioka K., Takeda S. and Yamamoto K. (1999) Disruption of ATM in p53-null cells causes multiple functional abnormalities in cellular response to ionizing radiation. Oncogene, 18, 7002-7009
25. Kobayashi M., Hirano A., Kumano T., Xiang S.L., Mihara K., Haseda Y., Matsui O., Shimizu H. and Yamamoto K. (2004) Critical role for chicken Rad17 and Rad9 in the cellular response to DNA damage and stalled DNA replication. Genes Cells, 9, 291-303
26. Hirano S., Yamamoto K., Ishiai M., Yamazoe M., Seki M., Matsushita N., Ohzeki M., Yamashita Y.M., Arakawa H., Buerstedde J.M. et al. (2005) Functional relationships of FANCC to homologous recombination, translesion synthesis, and BLM. EMBO J., 24, 418-427
27. Seki S., Ohzeki M., Uchida A., Hirano S., Matsushita N., Kitao H., Oda T., Yamashita T., Kashihara N., Tsubahara A. et al. (2007) A requirement of FancL and FancD2 monoubiquitination in DNA repair. Genes Cell, 12, 299-310
28. Yamamoto K., Hirano S., Ishiai M., Morishima K., Kitao H., Namikoshi K., Kimura M., Matsushita N., Arakawa H., Buerstedde J.M. et al. (2005) Fanconi anemia protein FANCD2 promotes immunoglobulin gene conversion and DNA repair through a mechanism related to homologous recombination. Mol. Cell. Biol., 25, 34-43
29. Mosedale G., Niedzwiedz W., Alpi A., Perrina F., Pereira-Leal J.B., Johnson M., Langevin F., Pace P. and Patel K.J. (2005) The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat. Struct. Mol. Biol., 12, 763-771
30. Rosado I.V., Niedzwiedz W., Alpi A.F. and Patel K.J. (2009) The Walker B motif in avian FANCM is required to limit sister chromatid exchanges but is dispensable for DNA crosslink repair. Nucleic Acids Res., 37, 4360-4370
31. Oestergaard V.H., Langevin F., Kuiken H.J., Pace P., Niedzwiedz W., Simpson L.J., Ohzeki M., Takata M., Sale J.E. and Patel K.J. (2007) Deubiquitination of FANCD2 is required for DNA crosslink repair. Mol. Cell, 28, 798-809
32. Alpi A., Langevin F., Mosedale G., Machida Y.J., Dutta A. and Patel K.J. (2007) UBE2T, the Fanconi anemia core complex, and FANCD2 are recruited independently to chromatin: A basis for the regulation of FANCD2 monoubiquitination. Mol. Cell. Biol., 27, 8421-8430
33. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J. and Nakatani Y. (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell, 102, 463-473
34. Itakura E., Umeda K., Sekoguchi E., Takata H., Ohsumi M. and Matsuura A. (2004) ATR-dependent phosphorylation of ATRIP in response to genotoxic stress. Biochem. Biophys. Res. Commun., 323, 1197-1202
35. 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. USA, 107, 21553-21557
36. Liu P., Barkley L.R., Day T., Bi X., Slater D.M., Alexandrow M.G., Nasheuer H.P. and Vaziri C. (2006) The Chk1-mediated S-phase checkpoint targets initiation factor Cdc45 via a Cdc25A/Cdk2-independent mechanism. J. Biol. Chem., 281, 30631-30644
37. Namiki Y. and Zou L. (2006) ATRIP associates with replication protein A-coated ssDNA through multiple interactions. Proc. Natl Acad. Sci. USA, 103, 580-585
38. Henricksen L.A., Umbricht C.B. and Wold M.S. (1994) Recombinant replication protein A: Expression, complex formation, and functional characterization. J. Biol. Chem., 269, 11121-11132
39. Masuda Y., Suzuki M., Piao J., Gu Y., Tsurimoto T. and Kamiya K. (2007) Dynamics of human replication factors in the elongation phase of DNA replication. Nucleic Acids Res., 35, 6904-6916
40. Sato K., Toda K., Ishiai M., Takata M. and Kurumizaka H. (2012) DNA robustly stimulates FANCD2 monoubiquitylation in the complex with FANCI. Nucleic Acids Res., 40, 4553-4561
41. Zou L. and Elledge S.J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548
42. Sala-Trepat M., Rouillard D., Escarceller M., Laquerbe A., Moustacchi E. and Papadopoulo D. (2000) Arrest of S-phase progression is impaired in Fanconi anemia cells. Exp. Cell Res., 260, 208-215
43. Centurion S.A., Kuo H.R. and Lambert W.C. (2000) Damageresistant DNA synthesis in Fanconi anemia cells treated with a DNA cross-linking agent. Exp. Cell Res., 260, 216-221
44. Pichierri P. and Rosselli F. (2004) The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J., 23, 1178-1187
45. Ball H.L., Myers J.S. and Cortez D. (2005) ATRIP binding to replication protein A-single-stranded DNA promotes ATRATRIP localization but is dispensable for Chk1 phosphorylation. Mol. Biol. Cell, 16, 2372-2381
46. Itakura E., Takai K.K., Umeda K., Kimura M., Ohsumi M., Tamai K. and Matsuura A. (2004) Amino-Terminal domain of ATRIP contributes to intranuclear relocation of the ATR-ATRIP complex following DNA damage. FEBS Lett., 577, 289-293
47. Itakura E., Sawada I. and Matsuura A. (2005) Dimerization of the ATRIP protein through the coiled-coil motif and its implication to the maintenance of stalled replication forks. Mol. Biol. Cell, 16, 5551-5562
48. Ball H.L. and Cortez D. (2005) ATRIP oligomerization is required for ATR-dependent checkpoint signaling. J. Biol. Chem., 280, 31390-31396
49. Ball H.L., Ehrhardt M.R., Mordes D.A., Glick G.G., Chazin W.J. and Cortez D. (2007) Function of a conserved checkpoint recruitment domain in ATRIP proteins. Mol. Cell. Biol., 27, 3367-3377
50. Bakker S.T., van de Vrugt H.J., Rooimans M.A., Oostra A.B., Steltenpool J., Delzenne-Goette E., van der Wal A., van der Valk M., Joenje H., te Riele H. et al. (2009) Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M. Hum. Mol. Genet., 18, 3484-3495
51. Singh T.R., Bakker S.T., Agarwal S., Jansen M., Grassman E., Godthelp B.C., Ali A.M., Du C.H., Rooimans M.A., Fan Q. et al. (2009) Impaired FANCD2 monoubiquitination and hypersensitivity to camptothecin uniquely characterize Fanconi anemia complementation group M. Blood, 114, 174-180
52. Wang Y., Leung J.W., Jiang Y., Lowery M.G., Do H., Vasquez K.M., Chen J., Wang W. and Li L. (2013) FANCM and FAAP24 Maintain Genome Stability via Cooperative as Well as Unique Functions. Mol. Cell, 49, 997-1009
53. Collis S.J., Ciccia A., Deans A.J., Horejsi Z., Martin J.S., Maslen S.L., Skehel J.M., Elledge S.J., West S.C. and Boulton S.J. (2008) FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the fanconi anemia core complex. Mol. Cell, 32, 313-324
54. Schwab R.A., Blackford A.N. and Niedzwiedz W. (2010) ATR activation and replication fork restart are defective in FANCMdeficient cells. EMBO J., 29, 806-818
55. Huang M., Kim J.M., Shiotani B., Yang K., Zou L. and D'Andrea A.D. (2010) The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response. Mol. Cell, 39, 259-268
56. Duquette M.L., Zhu Q., Taylor E.R., Tsay A.J., Shi L.Z., Berns M.W. and McGowan C.H. (2012) CtIP is required to initiate replication-dependent interstrand crosslink repair. PLoS Genet., 8, e1003050
57. Ben-Yehoyada M., Wang L.C., Kozekov I.D., Rizzo C.J., Gottesman M.E. and Gautier J. (2009) Checkpoint signaling from a single DNA interstrand crosslink. Mol. Cell, 35, 704-715
58. Sareen A., Chaudhury I., Adams N. and Sobeck A. (2012) Fanconi anemia proteins FANCD2 and FANCI exhibit different DNA damage responses during S-phase. Nucleic Acids Res., 40, 8425-8439
59. Mordes D.A. and Cortez D. (2008) Activation of ATR and related PIKKs. Cell Cycle, 7, 2809-2812
60. Pace P., Johnson M., Tan W.M., Mosedale G., Sng C., Hoatlin M., de Winter J., Joenje H., Gergely F. and Patel K.J. (2002) FANCE: The link between Fanconi anaemia complex assembly and activity. EMBO J., 21, 3414-3423
61. Cole A.R., Lewis L.P. and Walden H. (2010) The structure of the catalytic subunit FANCL of the Fanconi anemia core complex. Nat. Struct. Mol. Biol., 17, 294-298
62. Liu S., Shiotani B., Lahiri M., Marechal A., Tse A., Leung C.C., Glover J.N., Yang X.H. and Zou L. (2011) ATR Autophosphorylation as a Molecular Switch for Checkpoint Activation. Mol. Cell, 43, 192-202
63. Pichierri P., Franchitto A. and Rosselli F. (2004) BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. EMBO J., 23, 3154-3163