Damage-dependent regulation of MUS81-EME1 by Fanconi anemia complementation group A protein

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 1671-1683

  Benitez, Anaid ^a   Yuan, Fenghua ^a   Nakajima, Satoshi ^b   Wei, Leizhen ^b   Qian, Liangyue ^a   Myers, Richard ^a   Hu, Jennifer J ^a   Lan, Li ^b   Zhang, Yanbin ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS-LINKING REAGENTS; DNA DAMAGE; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; FANCONI ANEMIA COMPLEMENTATION GROUP A PROTEIN; HUMANS; METHOXSALEN;

EID: 84894243457     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt975     Document Type: Article

References (79)

1. Akkari, Y.M., Bateman, R.L., Reifsteck, C.A., Olson, S.B. and Grompe, M. (2000) DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol. Cell. Biol., 20, 8283-8289.
2. De Silva, I.U., McHugh, P.J., Clingen, P.H. and Hartley, J.A. (2000) Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol. Cell. Biol., 20, 7980-7990.
3. Raschle, M., Knipsheer, 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.
4. Knipscheer, P., Raschle, M., Smogorzewska, A., Enoiu, M., Ho, T.V., Scharer, O.D., Elledge, S.J. and Walter, J.C. (2009) The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science, 326, 1698-1701.
5. Wang, W. (2007) Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet., 8, 735-748.
6. 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.
7. Kee, Y. and D'Andrea, A.D. (2010) Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev., 24, 1680-1694.
8. 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.
9. Yuan, F., Song, L., Qian, L., Hu, J.J. and Zhang, Y. (2010) Assembling an orchestra: Fanconi anemia pathway of DNA repair. Front. Biosci., 15, 1131-1149.
10. Dronkert, M.L. and Kanaar, R. (2001) Repair of DNA interstrand cross-links. Mutat. Res., 486, 217-247.
11. Mathew, C.G. (2006) Fanconi anaemia genes and susceptibility to cancer. Oncogene, 25, 5875-5884.
12. Levitus, M., Joenje, H. and de Winter, J.P. (2006) The Fanconi anemia pathway of genomic maintenance. Cell. Oncol., 28, 3-29.
13. Thompson, L.H., Hinz, J.M., Yamada, N.A. and Jones, N.J. (2005) How Fanconi anemia proteins promote the four Rs: replication, recombination, repair, and recovery. Environ. Mol, Mutagen., 45, 128-142.
14. Niedernhofer, L.J., Lalai, A.S. and Hoeijmakers, J.H. (2005) Fanconi anemia (cross)linked to DNA repair. Cell, 123, 1191-1198.
15. Auerbach, A.D. (2009) Fanconi anemia and its diagnosis. Mutat. Res., 668, 4-10.
16. Patel, K.J. and Joenje, H. (2007) Fanconi anemia and DNA replication repair. DNA Repair (Amst), 6, 885-890.
17. Kottemann, M.C. and Smogorzewska, A. (2013) Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature, 493, 356-363.
18. Kee, Y. and D'Andrea, A.D. (2012) Molecular pathogenesis and clinical management of Fanconi anemia. J. Clin. Invest., 122, 3799-3806.
19. Sasaki, M.S. (1975) Is Fanconi's anaemia defective in a process essential to the repair of DNA cross links? Nature, 257, 501-503.
20. Hinz, J.M., Nham, P.B., Urbin, S.S., Jones, I.M. and Thompson, L.H. (2007) Disparate contributions of the Fanconi anemia pathway and homologous recombination in preventing spontaneous mutagenesis. Nucleic Acids Res., 35, 3733-3740.
21. Sobeck, A., Stone, S., Costanzo, V., de Graaf, B., Reuter, T., de Winter, J., Wallisch, M., Akkari, Y., Olson, S., Wang, W. et al. (2006) Fanconi anemia proteins are required to prevent accumulation of replication-Associated DNA double-strand breaks. Mol. Cell. Biol., 26, 425-437.
22. Thompson, L.H. and Hinz, J.M. (2009) Cellular and molecular consequences of defective Fanconi anemia proteins in replicationcoupled DNA repair: mechanistic insights. Mutat. Res., 668, 54-72.
23. Wang, L.C., Stone, S., Hoatlin, M.E. and Gautier, J. (2008) Fanconi anemia proteins stabilize replication forks. DNA Repair (Amst), 7, 1973-1981.
24. Yuan, F., El Hokayem, J., Zhou, W. and Zhang, Y. (2009) FANCI protein binds to DNA and interacts with FANCD2 to recognize branched structures. J. Biol. Chem., 284, 24443-24452.
25. Xue, Y., Li, Y., Guo, R., Ling, C. and Wang, W. (2008) FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair. Hum. Mol. Genet., 17, 1641-1652.
26. Otsuki, T., Furukawa, Y., Ikeda, K., Endo, H., Yamashita, T., Shinohara, A., Iwamatsu, A., Ozawa, K. and Liu, J.M. (2001) Fanconi anemia protein, FANCA, associates with BRG1, a component of the human SWI/SNF complex. Hum. Mol. Genet., 10, 2651-2660.
27. Qiao, F., Moss, A. and Kupfer, G.M. (2001) Fanconi anemia proteins localize to chromatin and the nuclear matrix in a DNA damage- and cell cycle-regulated manner. J. Biol. Chem., 276, 23391-23396.
28. Yuan, F., Qian, L., Zhao, X., Liu, J.Y., Song, L., D'Urso, G., Jain, C. and Zhang, Y. (2012) Fanconi anemia complementation group A (FANCA) protein has intrinsic affinity for nucleic acids with preference for single-stranded forms. J. Biol. Chem., 287, 4800-4807.
29. Papadopoulo, D., Averbeck, D. and Moustacchi, E. (1987) The fate of 8-methoxypsoralen-photoinduced DNA interstrand crosslinks in Fanconi's anemia cells of defined genetic complementation groups. Mutat. Res., 184, 271-280.
30. Kumaresan, K.R. and Lambert, M.W. (2000) Fanconi anemia, complementation group A, cells are defective in ability to produce incisions at sites of psoralen interstrand cross-links. Carcinogenesis, 21, 741-751.
31. Niedernhofer, L.J., Odijk, H., Budzowska, M., van Drunen, E., Maas, A., Theil, A.F., de Wit, J., Jaspers, N.G., Beverloo, H.B., Hoeijmakers, J.H. et al. (2004) The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-linkinduced double-strand breaks. Mol. Cell. Biol., 24, 5776-5787.
32. Rothfuss, A. and Grompe, M. (2004) Repair kinetics of genomic interstrand DNA cross-links: evidence for DNA double-strand break-dependent activation of the Fanconi anemia/BRCA pathway. Mol. Cell. Biol., 24, 123-134.
33. Ciccia, A., McDonald, N. and West, S.C. (2008) Structural and functional relationships of the XPF/MUS81 family of proteins. Annu. Rev. Biochem., 77, 259-287.
34. Sengerova, B., Wang, A.T. and McHugh, P.J. (2011) Orchestrating the nucleases involved in DNA interstrand cross-link (ICL) repair. Cell Cycle, 10, 3999-4008.
35. Bhagwat, N., Olsen, A.L., Wang, A.T., Hanada, K., Stuckert, P., Kanaar, R., D'Andrea, A., Niedernhofer, L.J. and McHugh, P.J. (2009) XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair. Mol. Cell. Biol., 29, 6427-6437.
36. Kim, Y., Spitz, G.S., Veturi, U., Lach, F.P., Auerbach, A.D. and Smogorzewska, A. (2013) Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood, 121, 54-63.
37. Bastin-Shanower, S.A., Fricke, W.M., Mullen, J.R. and Brill, S.J. (2003) The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol., 23, 3487-3496.
38. Ciccia, A., Constantinou, A. and West, S.C. (2003) Identification and characterization of the human mus81-eme1 endonuclease. J. Biol. Chem., 278, 25172-25178.
39. Gaillard, P.H., Noguchi, E., Shanahan, P. and Russell, P. (2003) The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism. Mol. Cell, 12, 747-759.
40. Osman, F., Dixon, J., Doe, C.L. and Whitby, M.C. (2003) Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell, 12, 761-774.
41. Gaskell, L.J., Osman, F., Gilbert, R.J. and Whitby, M.C. (2007) Mus81 cleavage of Holliday junctions: a failsafe for processing meiotic recombination intermediates? EMBO J., 26, 1891-1901.
42. Boddy, M.N., Gaillard, P.H., McDonald, W.H., Shanahan, P., Yates, J.R. 3rd and Russell, P. (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell, 107, 537-548.
43. Chen, X.B., Melchionna, R., Denis, C.M., Gaillard, P.H., Blasina, A., Van de Weyer, I., Boddy, M.N., Russell, P., Vialard, J. and McGowan, C.H. (2001) Human Mus81-Associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell, 8, 1117-1127.
44. Constantinou, A., Chen, X.B., McGowan, C.H. and West, S.C. (2002) Holliday junction resolution in human cells: two junction endonucleases with distinct substrate specificities. EMBO J., 21, 5577-5585.
45. Kaliraman, V., Mullen, J.R., Fricke, W.M., Bastin-Shanower, S.A. and Brill, S.J. (2001) Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev., 15, 2730-2740.
46. Ogrunc, M. and Sancar, A. (2003) Identification and characterization of human MUS81-MMS4 structure-specific endonuclease. J. Biol. Chem., 278, 21715-21720.
47. Doe, C.L., Ahn, J.S., Dixon, J. and Whitby, M.C. (2002) Mus81- Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem., 277, 32753-32759.
48. 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.
49. Rechkoblit, O., Zhang, Y., Guo, D., Wang, Z., Amin, S., Krzeminsky, J., Louneva, N. and Geacintov, N.E. (2002) trans- Lesion synthesis past bulky benzo[a]pyrene diol epoxide N2-dG and N6-dA lesions catalyzed by DNA bypass polymerases. J. Biol. Chem., 277, 30488-30494.
50. Gold, R.L., Anderson, R.R., Natoli, V.D. and Gange, R.W. (1988) An action spectrum for photoinduction of prolonged cutaneous photosensitivity by topical 8-MOP. J. Invest. Dermatol., 90, 818-822.
51. Cruz, L.A., Guecheva, T.N., Bonato, D. and Henriques, J.A. (2012) Relationships between chromatin remodeling and DNA damage repair induced by 8-methoxypsoralen and UVA in yeast Saccharomyces cerevisiae. Genet. Mol. Biol., 35, 1052-1059.
52. Whitby, M.C., Osman, F. and Dixon, J. (2003) Cleavage of model replication forks by fission yeast Mus81-Eme1 and budding yeast Mus81-Mms4. J. Biol. Chem., 278, 6928-6935.
53. 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.
54. Lee, J.H., Park, C.J., Arunkumar, A.I., Chazin, W.J. and Choi, B.S. (2003) NMR study on the interaction between RPA and DNA decamer containing cis-syn cyclobutane pyrimidine dimer in the presence of XPA: implication for damage verification and strandspecific dual incision in nucleotide excision repair. Nucleic Acids Res., 31, 4747-4754.
55. Hollingsworth, N.M. and Brill, S.J. (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev., 18, 117-125.
56. Gari, K., Decaillet, C., Delannoy, M., Wu, L. and Constantinou, A. (2008) Remodeling of DNA replication structures by the branch point translocase FANCM. Proc. Natl Acad. Sci. USA, 105, 16107-16112.
57. Gari, K., Decaillet, C., Stasiak, A.Z., Stasiak, A. and Constantinou, A. (2008) The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell, 29, 141-148.
58. 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.
59. Medhurst, A.L., Laghmani el, H., Steltenpool, J., Ferrer, M., Fontaine, C., de Groot, J., Rooimans, M.A., Scheper, R.J., Meetei, A.R., Wang, W. et al. (2006) Evidence for subcomplexes in the Fanconi anemia pathway. Blood, 108, 2072-2080.
60. Meetei, A.R., Medhurst, A.L., Ling, C., Xue, Y., Singh, T.R., Bier, P., Steltenpool, J., Stone, S., Dokal, I., Mathew, C.G. et al. (2005) A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet., 37, 958-963.
61. Ling, C., Ishiai, M., Ali, A.M., Medhurst, A.L., Neveling, K., Kalb, R., Yan, Z., Xue, Y., Oostra, A.B., Auerbach, A.D. et al. (2007) FAAP100 is essential for activation of the Fanconi anemia-Associated DNA damage response pathway. EMBO J., 26, 2104-2114.
62. 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.
63. 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.
64. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M. and D'Andrea, A.D. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell, 7, 249-262.
65. Montes de Oca, R., Andreassen, P.R., Margossian, S.P., Gregory, R.C., Taniguchi, T., Wang, X., Houghtaling, S., Grompe, M. and D'Andrea, A.D. (2005) Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood, 105, 1003-1009.
66. 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.
67. 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.
68. 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.
69. Meetei, A.R., Sechi, S., Wallisch, M., Yang, D., Young, M.K., Joenje, H., Hoatlin, M.E. and Wang, W. (2003) A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol. Cell. Biol., 23, 3417-3426.
70. Sridharan, D., Brown, M., Lambert, W.C., McMahon, L.W. and Lambert, M.W. (2003) Nonerythroid alphaII spectrin is required for recruitment of FANCA and XPF to nuclear foci induced by DNA interstrand cross-links. J. Cell. Sci., 116, 823-835.
71. Reuter, T.Y., Medhurst, A.L., Waisfisz, Q., Zhi, Y., Herterich, S., Hoehn, H., Gross, H.J., Joenje, H., Hoatlin, M.E., Mathew, C.G. et al. (2003) Yeast two-hybrid screens imply involvement of Fanconi anemia proteins in transcription regulation, cell signaling, oxidative metabolism, and cellular transport. Exp. Cell Res., 289, 211-221.
72. Fisher, L.A., Bessho, M. and Bessho, T. (2008) Processing of a psoralen DNA interstrand cross-link by XPF-ERCC1 complex in vitro. J. Biol. Chem., 283, 1275-1281.
73. Kuraoka, I., Kobertz, W.R., Ariza, R.R., Biggerstaff, M., Essigmann, J.M. and Wood, R.D. (2000) Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J. Biol. Chem., 275, 26632-26636.
74. Andersen, S.L., Bergstralh, D.T., Kohl, K.P., LaRocque, J.R., Moore, C.B. and Sekelsky, J. (2009) Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell, 35, 128-135.
75. 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.
76. Fekairi, S., Scaglione, S., Chahwan, C., Taylor, E.R., Tissier, A., Coulon, S., Dong, M.Q., Ruse, C., Yates, J.R. 3rd, Russell, P. et al. (2009) Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell, 138, 78-89.
77. Munoz, I.M., Hain, K., Declais, A.C., Gardiner, M., Toh, G.W., Sanchez-Pulido, L., Heuckmann, J.M., Toth, R., Macartney, T., Eppink, B. et al. (2009) Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell, 35, 116-127.
78. 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.
79. Svendsen, J.M., Smogorzewska, A., Sowa, M.E., O'Connell, B.C., Gygi, S.P., Elledge, S.J. and Harper, J.W. (2009) Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell, 138, 63-77.