FANCP/SLX4: A Swiss army knife of DNA interstrand crosslink repair

Cell Cycle

Volumn 10, Issue 11, 2011, Pages 1757-1763

  Cybulski, Kelly E ^a   Howlett, Niall G ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

DNA interstrand crosslink repair; DNA repair; Fanconi anemia; FANCP SLX4; Ubiquitin

Indexed keywords

FANCONI ANEMIA PROTEIN; RAD51 PROTEIN; RAD51C PROTEIN; UNCLASSIFIED DRUG;

DNA CROSS LINKING; DNA DAMAGE; DNA DAMAGE RESPONSE; DNA REPAIR; FANCONI ANEMIA; GENE MUTATION; GENE REGULATORY NETWORK; HUMAN; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

EID: 79957904161     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.11.15818     Document Type: Review

References (78)

1. Lobitz S, Velleuer E. Guido Fanconi (1892-1979): a jack of all trades. Nat Rev Cancer 2006; 6:893-8.
2. Strathdee CA, Gavish H, Shannon WR, Buchwald M. Cloning of cDNAs for Fanconi's anaemia by functional complementation. Nature 1992; 356:763-7.
3. de Winter JP, Leveille F, van Berkel CGM, Rooimans MA, van der Weel L, Steltenpool J, et al. Isolation of a cDNA representing the Fanconi Anemia Complementation Group E gene. Am J Hum Genet 2000; 67:1306-8.
4. de Winter JP, Rooimans MA, van der Weel L, Van Berkel CM, Alon N, Bosnoyan-Collins L, et al. The Fanconi Anemia Complementation Gene FANCF encodes a novel protein with homology to ROM. Nat Genet 2000; 24:15-6.
5. de Winter JP, Waisfisz Q, Rooimans MA, van Berkel CGM, Bosnoyan-Collins L, Alon N, et al. The Fanconi anaemia group G gene is identical with human XRCC9. Nat Genet 1998; 20:281-3. (Pubitemid 28507674)
6. Lo Ten Foe JR, Rooimans MA, Bosnoyan-Collins L, et al. Expression cloning of a cDNA for the major Fanconi anemia gene, FAA. Nat Genet 1996; 14:320-3.
7. Moldovan GL, D'Andrea AD. How the fanconi anemia pathway guards the genome. Annu Rev Genet 2009; 43:223-49.
8. Rego MA, Kolling FW, Howlett NG. The Fanconi anemia protein interaction network: Casting a wide net. Mutat Res 2009; 668:27-41.
9. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 2001; 7:249-62. (Pubitemid 32206493)
10. Auerbach AD. Fanconi anemia diagnosis and the diepoxybutane (DEB) test. Exp Hematol 1993; 21:731-3. (Pubitemid 24215323)
11. Alpi A, Langevin F, Mosedale G, Machida YJ, Dutta A, Patel KJ. UBE2T, the Fanconi anemia core complex, and FANCD2 are recruited independently to chromatin: A basis for the regulation of FANCD2 monoubiquitination. Mol Cell Biol 2007; 27:8421-30.
12. Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 2007; 25:331-43. (Pubitemid 46206138)
13. Ling C, Ishiai M, Ali AM, Medhurst AL, Neveling K, Kalb R, et al. FAAP100 is essential for activation of the Fanconi anemia-associated DNA damage response pathway. EMBO J 2007; 26:2104-14. (Pubitemid 46625801)
14. Meetei AR, Sechi S, Wallisch M, Yang D, Young MK, Joenje H, et al. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol Cell Biol 2003; 23:3417-26. (Pubitemid 36539175)
15. Meetei AR, de Winter JP, Medhurst AL, Wallisch M, Waisfisz Q, van de Vrugt HJ, et al. A novel ubiquitin ligase is deficient in Fanconi anemia. Nat Genet 2003; 35:165-70. (Pubitemid 37187635)
16. Meetei AR, Levitus M, Xue Y, Medhurst AL, Zwaan M, Ling C, et al. X-linked inheritance of Fanconi anemia complementation group B. Nat Genet 2004; 36:1219-24.
17. Meetei AR, Medhurst AL, Ling C, Xue Y, Singh TR, Bier P, et al. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat Genet 2005; 37:958-63. (Pubitemid 43086152)
18. Joenje H, Patel KJ. The emerging genetic and molecular basis of fanconi anaemia. Nat Rev Genet 2001; 2:446-59.
19. Sims AE, Spiteri E, Sims RJ, 3rd, Arita AG, Lach FP, Landers T, et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat Struct Mol Biol 2007; 14:564-7. (Pubitemid 46871814)
20. Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald ER, 3rd, Hurov KE, Luo J, et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007; 129:289-301. (Pubitemid 46584733)
21. Bogliolo M, Lyakhovich A, Callen E, Castella M, Cappelli E, Ramirez MJ, et al. Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability. EMBO J 2007; 26:1340-51. (Pubitemid 46398698)
22. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M, D'Andrea AD. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 2002; 100:2414-20.
23. Cohn MA, Kowal P, Yang K, Haas W, Huang TT, Gygi SP, et al. A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell 2007; 28:786-97. (Pubitemid 350217060)
24. Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, D'Andrea AD, et al. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 2005; 17:331-9. (Pubitemid 40193305)
25. Reid S, Schindler D, Hanenberg H, Barker K, Hanks S, Kalb R, et al. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat Genet 2007; 39:162-4.
26. Xia B, Dorsman JC, Ameziane N, de Vries Y, Rooimans MA, Sheng Q, et al. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat Genet 2007; 39:159-61. (Pubitemid 46184344)
27. Xia B, Sheng Q, Nakanishi K, Ohashi A, Wu J, Christ N, et al. Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol Cell 2006; 22:719-29.
28. Boulton SJ. Cellular functions of the BRCA tumour-suppressor proteins. Biochem Soc Trans 2006; 34:633-45. (Pubitemid 44796392)
29. Davies AA, Masson JY, McIlwraith MJ, Stasiak AZ, Stasiak A, Venkitaraman AR, et al. Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol Cell 2001; 7:273-82. (Pubitemid 32206495)
30. Godthelp BC, Wiegant WW, Waisfisz Q, Medhurst AL, Arwert F, Joenje H, et al. Inducibility of nuclear Rad51 foci after DNA damage distinguishes all Fanconi anemia complementation groups from D1/ BRCA2. Mutat Res 2005; 594:39-48. (Pubitemid 43170985)
31. Holliday R. A mechanism for gene conversion in fungi. Genetical Research 1964; 5:282-304.
32. Ciccia A, McDonald N, West SC. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 2008; 77:259-87.
33. Cantor SB, Bell DW, Ganesan S, Kass EM, Drapkin R, Grossman S, et al. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 2001; 105:149-60. (Pubitemid 32323924)
34. Gupta R, Sharma S, Sommers JA, Jin Z, Cantor SB, Brosh RM Jr. Analysis of the DNA substrate specificity of the human BACH1 helicase associated with breast cancer. J Biol Chem 2005; 280:25450-60. (Pubitemid 40962249)
35. Litman R, Peng M, Jin Z, Zhang F, Zhang J, Powell S, et al. BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 2005; 8:255-65. (Pubitemid 41317595)
36. Moynahan ME, Pierce AJ, Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 2001; 7:263-72. (Pubitemid 32206494)
37. Lee W, St. Onge RP, Proctor M, Flaherty P, Jordan MI, Arkin AP, et al. Genome-wide requirements for resistance to functionally distinct DNA-damaging agents. PLoS Genet 2005; 1:24.
38. Wu HI, Brown JA, Dorie MJ, Lazzeroni L, Brown JM. Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin and mitomycin C. Cancer Res 2004; 64:3940-8. (Pubitemid 38697308)
39. Yildiz O, Majumder S, Kramer B, Sekelsky JJ. Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol Cell 2002; 10:1503-9. (Pubitemid 36050890)
40. Fekairi S, Scaglione S, Chahwan C, Taylor ER, Tissier A, Coulon S, et al. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 2009; 138:78-89.
41. Munoz IM, Hain K, Declais AC, Gardiner M, Toh GW, Sanchez-Pulido L, et al. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 2009; 35:116-27.
42. Svendsen JM, Smogorzewska A, Sowa ME, O'Connell BC, Gygi SP, Elledge SJ, et al. Mammalian BTBD12/ SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 2009; 138:63-77.
43. Kim Y, Lach FP, Desetty R, Hanenberg H, Auerbach AD, Smogorzewska A. Mutations of the SLX4 gene in Fanconi anemia. Nat Genet 2011; 43:142-6.
44. Stoepker C, Hain K, Schuster B, Hilhorst-Hofstee Y, Rooimans MA, Steltenpool J, et al. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet 2011; 43:138-41.
45. FARF I. Fanconi Anemia: Standards for Clinical Care. Eugene, Oregon: Fanconi Anemia Research Fund, Inc., 2003.
46. Singh TR, Bakker ST, Agarwal S, Jansen M, Grassman E, Godthelp BC, et al. Impaired FANCD2 monoubiquitination and hypersensitivity to camptothecin uniquely characterize Fanconi anemia complementation group M. Blood 2009; 114:174-80.
47. Vaz F, Hanenberg H, Schuster B, Barker K, Wiek C, Erven V, et al. Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat Genet 2010; 42:406-9.
48. Crossan GP, van der Weyden L, Rosado IV, Langevin F, Gaillard PH, McIntyre RE, et al. Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat Genet 2011; 43:147-52.
49. Hofmann K. Ubiquitin-binding domains and their role in the DNA damage response. DNA Repair (Amst) 2009; 8:544-56.
50. Fricke WM, Brill SJ. Slx1-Slx4 is a second structure-specific endonuclease functionally redundant with Sgs1-Top3. Genes Dev 2003; 17:1768-78. (Pubitemid 36870339)
51. Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 2001; 157:103-18.
52. Akkari YM, Bateman RL, Reifsteck CA, Olson SB, Grompe M. DNA replication is required To elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 2000; 20:8283-9.
53. Osman F, Whitby MC. Exploring the roles of Mus81-Eme1/Mms4 at perturbed replication forks. DNA Repair (Amst) 2007; 6:1004-17. (Pubitemid 46880480)
54. Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, Beverloo HB, et al. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 2007; 14:1096-104. (Pubitemid 350060335)
55. Hanada K, Budzowska M, Modesti M, Maas A, Wyman C, Essers J, et al. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J 2006; 25:4921-32. (Pubitemid 44607036)
56. Gari K, Decaillet C, Delannoy M, Wu L, Constantinou A. Remodeling of DNA replication structures by the branch point translocase FANCM. Proc Natl Acad Sci USA 2008; 105:16107-12.
57. Huang M, Kim JM, Shiotani B, Yang K, Zou L, D'Andrea AD. The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response. Mol Cell 2010; 39:259-68.
58. Andreassen PR, D'Andrea AD, Taniguchi T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev 2004; 18:1958-63. (Pubitemid 39071576)
59. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, Luo J, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007; 316:1160-6. (Pubitemid 46877472)
60. Kim JM, Kee Y, Gurtan A, D'Andrea AD. Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood 2008; 111:5215-22.
61. Mosedale G, Niedzwiedz W, Alpi A, Perrina F, Pereira-Leal JB, Johnson M, et al. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat Struct Mol Biol 2005; 12:763-71. (Pubitemid 43086250)
62. Bakker ST, van de Vrugt HJ, Rooimans MA, Oostra AB, Steltenpool J, Delzenne-Goette E, et al. Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M. Hum Mol Genet 2009; 18:3484-95.
63. Wood RD. Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ Mol Mutagen 2010; 51:520-6.
64. De Silva IU, McHugh PJ, Clingen PH, Hartley JA. Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol Cell Biol 2000; 20:7980-90.
65. Suhasini AN, Rawtani NA, Wu Y, Sommers JA, Sharma S, Mosedale G, et al. Interaction between the helicases genetically linked to Fanconi anemia group J and Bloom's syndrome. EMBO J 2011; 30:692-705.
66. Bergstralh DT, Sekelsky J. Interstrand crosslink repair: can XPF-ERCC1 be let off the hook? Trends Genet 2008; 24:70-6.
67. Kratz K, Schopf B, Kaden S, Sendoel A, Eberhard R, Lademann C, et al. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 2010; 142:77-88.
68. MacKay C, Declais AC, Lundin C, Agostinho A, Deans AJ, MacArtney TJ, et al. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 2010; 142:65-76.
69. Smogorzewska A, Desetty R, Saito TT, Schlabach M, Lach FP, Sowa ME, et al. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 2010; 39:36-47.
70. Niedernhofer LJ, Odijk H, Budzowska M, van Drunen E, Maas A, Theil AF, et al. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 2004; 24:5776-87. (Pubitemid 38787963)
71. Cannavo E, Gerrits B, Marra G, Schlapbach R, Jiricny J. Characterization of the interactome of the human MutL homologues MLH1, PMS1 and PMS2. J Biol Chem 2007; 282:2976-86. (Pubitemid 47084306)
72. Peng M, Litman R, Xie J, Sharma S, Brosh RM Jr, Cantor SB. The FANCJ/MutLalpha interaction is required for correction of the cross-link response in FA-J cells. EMBO J 2007; 26:3238-49. (Pubitemid 47057494)
73. Kadyrov FA, Dzantiev L, Constantin N, Modrich P. Endonucleolytic function of MutLalpha in human mismatch repair. Cell 2006; 126:297-308. (Pubitemid 44092957)
74. Wu Q, Christensen LA, Legerski RJ, Vasquez KM. Mismatch repair participates in error-free processing of DNA interstrand crosslinks in human cells. EMBO Rep 2005; 6:551-7.
75. Nojima K, Hochegger H, Saberi A, Fukushima T, Kikuchi K, Yoshimura M, et al. Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res 2005; 65:11704-11. (Pubitemid 41821731)
76. Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho TV, Scharer OD, et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009; 326:1698-701.
77. French CA, Masson JY, Griffin CS, O'Regan P, West SC, Thacker J. Role of mammalian RAD51L2 (RAD51C) in recombination and genetic stability. J Biol Chem 2002; 277:19322-30. (Pubitemid 34967437)
78. Godthelp BC, Wiegant WW, van Duijn-Goedhart A, Scharer OD, van Buul PP, Kanaar R, et al. Mammalian Rad51C contributes to DNA cross-link resistance, sister chromatid cohesion and genomic stability. Nucleic Acids Res 2002; 30:2172-82. (Pubitemid 34567938)