The Fanconi anemia pathway in replication stress and DNA crosslink repair

Cellular and Molecular Life Sciences

Volumn 69, Issue 23, 2012, Pages 3963-3974

  Jones, Mathew J K ^a,b   Huang, Tony T ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Fanconi anemia; Genome stability; Homologous recombination repair; Interstrand crosslink repair; Translesion synthesis

Indexed keywords

BRCA2 PROTEIN; FANCONI ANEMIA D2 ASSOCIATED NUCLEASE; FANCONI ANEMIA GROUP A PROTEIN; FANCONI ANEMIA GROUP C PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA GROUP E PROTEIN; FANCONI ANEMIA GROUP F PROTEIN; FANCONI ANEMIA GROUP G PROTEIN; FANCONI ANEMIA GROUP I PROTEIN; FANCONI ANEMIA GROUP J PROTEIN; FANCONI ANEMIA GROUP L PROTEIN; FANCONI ANEMIA GROUP M PROTEIN; FANCONI ANEMIA GROUP N PROTEIN; FANCONI ANEMIA GROUP P PROTEIN; FANCONI ANEMIA P20 PROTEIN; FANCONI ANEMIA PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN SPECIFIC PROTEASE 1; UNCLASSIFIED DRUG; CROSS LINKING REAGENT; DNA;

BINDING AFFINITY; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; EXCISION REPAIR; FANC GENE; FANCONI ANEMIA; GENE; GENE FUNCTION; GENE MUTATION; HUMAN; NONHUMAN; PROTEIN DNA BINDING; REPLICATION STRESS; REVIEW; TRANSLESION SYNTHESIS; UBIQUITINATION; BIOLOGICAL MODEL; CHEMISTRY; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

CROSS-LINKING REAGENTS; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; HUMANS; MODELS, GENETIC; SIGNAL TRANSDUCTION;

EID: 84869086464     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1051-0     Document Type: Review

References (121)

1. Akkari YM, Bateman RL, Reifsteck CA, Olson SB, Grompe M (2000) DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 20(21):8283-8289
2. Ali AM, Pradhan A, Singh TR, Du C, Li J, Wahengbam K, Grassman E, Auerbach AD, Pang Q, Meetei AR (2012) FAAP20: a novel ubiquitin-binding FA nuclear core-complex protein required for functional integrity of the FA-BRCA DNA repair pathway. Blood 119(14):3285-3294
3. Alpi AF, Pace PE, Babu MM, Patel KJ (2008) Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol Cell 32(6):767-777
4. Alter BP, Greene MH, Velazquez I, Rosenberg PS (2003) Cancer in Fanconi anemia. Blood 101(5):2072
5. Andreassen PR, D'Andrea AD, Taniguchi T (2004) ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev 18(16):1958-1963
6. Auerbach AD (1993) Fanconi anemia diagnosis and the diepoxybutane (DEB) test. Exp Hematol 21(6):731-733
7. Bavoux C, Hoffmann JS, Cazaux C (2005) Adaptation to DNA damage and stimulation of genetic instability: the double-edged sword mammalian DNA polymerase kappa. Biochimie 87(7): 637-646
8. Ben-Yehoyada M, Wang LC, Kozekov ID, Rizzo CJ, Gottesman ME, Gautier J (2009) Checkpoint signaling from a single DNA interstrand crosslink. Mol Cell 35(5):704-715
9. Bienko M, Green CM, Crosetto N, Rudolf F, Zapart G, Coull B, Kannouche P, Wider G, Peter M, Lehmann AR et al (2005) Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310(5755):1821-1824
10. Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 19(9):1040-1052
11. Chan KL, Palmai-Pallag T, Ying S, Hickson ID (2009) Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat Cell Biol 11(6):753-760
12. Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, el Laghmani H, Joenje H, McDonald N, de Winter JP et al (2007) Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 25(3):331-343
13. Ciccia A, McDonald N, West SC (2008) Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 77:259-287
14. Cohn MA, Kowal P, Yang K, Haas W, Huang TT, Gygi SP, D'Andrea AD (2007) A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell 28(5):786-797
15. Colnaghi L, Jones MJ, Cotto-Rios XM, Schindler D, Hanenberg H, Huang TT (2011) Patient-derived C-terminal mutation of FANCI causes protein mislocalization and reveals putative EDGE motif function in DNA repair. Blood 117(7):2247-2256
16. Cotto-Rios XM, Jones MJ, Busino L, Pagano M, Huang TT (2011) APC/CCdh1-dependent proteolysis of USP1 regulates the response to UV-mediated DNA damage. J Cell Biol 194(2): 177-186
17. Cotto-Rios XM, Jones MJ, Huang TT (2011) Insights into phosphorylation-dependent mechanisms regulating USP1 protein stability during the cell cycle. Cell Cycle 10(23):4009-4016
18. D'Andrea AD, Grompe M (2003) The Fanconi anaemia/BRCA pathway. Nat Rev Cancer 3(1):23-34
19. de Winter JP, Joenje H (2009) The genetic and molecular basis of Fanconi anemia. Mutat Res 668(1-2):11-19
20. Deans AJ, West SC (2011) DNA interstrand crosslink repair and cancer. Nat Rev Cancer 11(7):467-480
21. Dorsman JC, Levitus M, Rockx D, Rooimans MA, Oostra AB, Haitjema A, Bakker ST, Steltenpool J, Schuler D, Mohan S et al (2007) Identification of the Fanconi anemia complementation group I gene, FANCI. Cell Oncol 29(3):211-218
22. Durkin SG, Glover TW (2007) Chromosome fragile sites. Annu Rev Genet 41:169-192
23. Friedberg EC (2005) Suffering in silence: the tolerance of DNA damage. Nat Rev Mol Cell Biol 6(12):943-953
24. Fu YV, Yardimci H, Long DT, Ho TV, Guainazzi A, Bermudez VP, Hurwitz J, van Oijen A, Scharer OD, Walter JC (2011) Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146(6):931-941
25. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, Grompe M, D'Andrea AD (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7(2):249-262
26. Gari K, Decaillet C, Delannoy M, Wu L, Constantinou A (2008) Remodeling of DNA replication structures by the branch point translocase FANCM. Proc Natl Acad Sci USA 105(42): 16107-16112
27. Gari K, Decaillet C, Stasiak AZ, Stasiak A, Constantinou A (2008) The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol Cell 29(1):141-148
28. Ge XQ, Jackson DA, Blow JJ (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev 21(24):3331-3341
29. Geng L, Huntoon CJ, Karnitz LM (2010) RAD18-mediated ubiquitination of PCNA activates the Fanconi anemia DNA repair network. J Cell Biol 191(2):249-257
30. Gerlich D, Hirota T, Koch B, Peters JM, Ellenberg J (2006) Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr Biol 16(4):333-344
31. Grompe M, D'Andrea A (2001) Fanconi anemia and DNA repair. Hum Mol Genet 10(20):2253-2259
32. Haracska L, Johnson RE, Unk I, Phillips B, Hurwitz J, Prakash L, Prakash S (2001) Physical and functional interactions of human DNA polymerase eta with PCNA. Mol Cell Biol 21(21):7199-7206
33. Haracska L, Johnson RE, Unk I, Phillips BB, Hurwitz J, Prakash L, Prakash S (2001) Targeting of human DNA polymerase iota to the replication machinery via interaction with PCNA. Proc Natl Acad Sci USA 98(25):14256-14261
34. Hewett DR, Handt O, Hobson L, Mangelsdorf M, Eyre HJ, Baker E, Sutherland GR, Schuffenhauer S, Mao JI, Richards RI (1998) FRA10B structure reveals common elements in repeat expansion and chromosomal fragile site genesis. Mol Cell 1(6):773-781
35. Hishiki A, Hashimoto H, Hanafusa T, Kamei K, Ohashi E, Shimizu T, Ohmori H, Sato M (2009) Structural basis for novel interactions between human translesion synthesis polymerases and proliferating cell nuclear antigen. J Biol Chem 284(16): 10552-10560
36. Hlavin EM, Smeaton MB, Miller PS (2010) Initiation of DNA interstrand cross-link repair in mammalian cells. Environ Mol Mutagen 51(6):604-624
37. Ho TV, Scharer OD (2010) Translesion DNA synthesis polymerases in DNA interstrand crosslink repair. Environ Mol Mutagen 51(6):552-566
38. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419(6903):135-141
39. Howlett NG, Harney JA, Rego MA, Kolling FW 4th, Glover TW (2009) Functional interaction between the Fanconi Anemia D2 protein and proliferating cell nuclear antigen (PCNA) via a conserved putative PCNA interaction motif. J Biol Chem 284(42):28935-28942
40. Howlett NG, Taniguchi T, Durkin SG, D'Andrea AD, Glover TW (2005) The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum Mol Genet 14(5):693-701
41. Huang TT, Nijman SM, Mirchandani KD, Galardy PJ, Cohn MA, Haas W, Gygi SP, Ploegh HL, Bernards R, D'Andrea AD (2006) Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat Cell Biol 8(4):339-347
42. Jones MJ, Colnaghi L, Huang TT (2012) Dysregulation of DNA polymerase kappa recruitment to replication forks results in genomic instability. EMBO J 31(4):908-918
43. Joo W, Xu G, Persky NS, Smogorzewska A, Rudge DG, Buzovetsky O, Elledge SJ, Pavletich NP (2011) Structure of the FANCI-FANCD2 complex: insights into the Fanconi anemia DNA repair pathway. Science 333(6040):312-316
44. Kannouche PL, Wing J, Lehmann AR (2004) Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol Cell 14(4):491-500
45. Kawabata T, Luebben SW, Yamaguchi S, Ilves I, Matise I, Buske T, Botchan MR, Shima N (2011) Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol Cell 41(5):543-553
46. Kee Y, D'Andrea AD (2010) Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 24(16):1680-1694
47. Kim H, Yang K, Dejsuphong D, D'Andrea AD (2012) Regulation of Rev1 by the Fanconi anemia core complex. Nat Struct Mol Biol 19(2):164-170
48. Kim JM, Kee Y, Gurtan A, D'Andrea AD (2008) Cell cycledependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood 111(10):5215-5222
49. Kim JM, Parmar K, Huang M, Weinstock DM, Ruit CA, Kutok JL, D'Andrea AD (2009) Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype. Dev Cell 16(2):314-320
50. Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho TV, Scharer OD, Elledge SJ, Walter JC (2009) The Fanconi anemia pathway promotes replication-dependent DNA interstrand crosslink repair. Science 326(5960):1698-1701
51. Kratz K, Schopf B, Kaden S, Sendoel A, Eberhard R, Lademann C, Cannavo E, Sartori AA, Hengartner MO, Jiricny J (2010) Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142(1): 77-88
52. Labib K, Tercero JA, Diffley JF (2000) Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 288(5471):1643-1647
53. Lage C, de Padula M, de Alencar TA, da Fonseca Goncalves SR, da Silva Vidal L, Cabral-Neto J, Leitao AC (2003) New insights on how nucleotide excision repair could remove DNA adducts induced by chemotherapeutic agents and psoralens plus UV-A (PUVA) in Escherichia coli cells. Mutat Res 544(2-3): 143-157
54. Lange SS, Takata K, Wood RD (2011) DNA polymerases and cancer. Nat Rev Cancer 11(2):96-110
55. Le Breton C, Hennion M, Arimondo PB, Hyrien O (2011) Replication-fork stalling and processing at a single psoralen interstrand crosslink in Xenopus egg extracts. PLoS One 6(4):e18554
56. Lehmann AR, Niimi A, Ogi T, Brown S, Sabbioneda S, Wing JF, Kannouche PL, Green CM (2007) Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst) 6(7):891-899
57. Lehoczky P, McHugh PJ, Chovanec M (2007) DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol Rev 31(2):109-133
58. Lei M, Tye BK (2001) Initiating DNA synthesis: from recruiting to activating the MCM complex. J Cell Sci 114(Pt 8):1447-1454
59. Letessier A, Millot GA, Koundrioukoff S, Lachages AM, Vogt N, Hansen RS, Malfoy B, Brison O, Debatisse M (2011) Celltype-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 470(7332):120-123
60. Leung JW, Wang Y, Fong KW, Huen MS, Li L, Chen J (2012) Fanconi anemia (FA) binding protein FAAP20 stabilizes FA complementation group A (FANCA) and participates in interstrand cross-link repair. Proc Natl Acad Sci USA 109(12): 4491-4496
61. Liu T, Ghosal G, Yuan J, Chen J, Huang J (2010) FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329(5992):693-696
62. Long DT, Raschle M, Joukov V, Walter JC (2011) Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333(6038):84-87
63. Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS, Grofte M, Chan KL, Hickson ID, Bartek J et al (2011) 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 13(3):243-253
64. Machida YJ, Machida Y, Chen Y, Gurtan AM, Kupfer GM, D'Andrea AD, Dutta A (2006) UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation. Mol Cell 23(4):589-596
65. MacKay C, Declais AC, Lundin C, Agostinho A, Deans AJ, MacArtney TJ, Hofmann K, Gartner A, West SC, Helleday T et al (2010) Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142(1):65-76
66. Maga G, Hubscher U (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 116(Pt 15): 3051-3060
67. Mechali M (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11(10):728-738
68. Meetei AR, de Winter JP, Medhurst AL, Wallisch M, Waisfisz Q, van de Vrugt HJ, Oostra AB, Yan Z, Ling C, Bishop CE et al (2003) A novel ubiquitin ligase is deficient in Fanconi anemia. Nat Genet 35(2):165-170
69. Meetei AR, Medhurst AL, Ling C, Xue Y, Singh TR, Bier P, Steltenpool J, Stone S, Dokal I, Mathew CG et al (2005) A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat Genet 37(9):958-963
70. Minko IG, Harbut MB, Kozekov ID, Kozekova A, Jakobs PM, Olson SB, Moses RE, Harris TM, Rizzo CJ, Lloyd RS (2008) Role for DNA polymerase kappa in the processing of N2-N2-guanine interstrand cross-links. J Biol Chem 283(25):17075-17082
71. Mirchandani KD, McCaffrey RM, D'Andrea AD (2008) The Fanconi anemia core complex is required for efficient point mutagenesis and Rev1 foci assembly. DNA Repair (Amst) 7(6):902-911
72. Mogi S, Butcher CE, Oh DH (2008) DNA polymerase eta reduces the gamma-H2AX response to psoralen interstrand crosslinks in human cells. Exp Cell Res 314(4):887-895
73. Moldovan GL, D'Andrea AD (2009) How the Fanconi anemia pathway guards the genome. Annu Rev Genet 43:223-249
74. Moldovan GL, Madhavan MV, Mirchandani KD, McCaffrey RM, Vinciguerra P, D'Andrea AD (2010) DNA polymerase POLN participates in cross-link repair and homologous recombination. Mol Cell Biol 30(4):1088-1096
75. Montes de Oca R, Andreassen PR, Margossian SP, Gregory RC, Taniguchi T, Wang X, Houghtaling S, Grompe M, D'Andrea AD (2005) Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 105(3):1003-1009
76. Mosedale G, Niedzwiedz W, Alpi A, Perrina F, Pereira-Leal JB, Johnson M, Langevin F, Pace P, Patel KJ (2005) The vertebrate Hef ortholog is a component of the Fanconi anemia tumorsuppressor pathway. Nat Struct Mol Biol 12(9):763-771
77. Moynahan ME, Jasin M (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 11(3):196-207
78. Muniandy PA, Thapa D, Thazhathveetil AK, Liu ST, Seidman MM (2009) Repair of laser-localized DNA interstrand crosslinks in G1 phase mammalian cells. J Biol Chem 284(41): 27908-27917
79. Murai J, Yang K, Dejsuphong D, Hirota K, Takeda S, D'Andrea AD (2011) The USP1/UAF1 complex promotes double-strand break repair through homologous recombination. Mol Cell Biol 31(12):2462-2469
80. Naim V, Rosselli F (2009) The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat Cell Biol 11(6):761-768
81. Nakanishi K, Cavallo F, Perrouault L, Giovannangeli C, Moynahan ME, Barchi M, Brunet E, Jasin M (2011) Homologydirected Fanconi anemia pathway cross-link repair is dependent on DNA replication. Nat Struct Mol Biol 18(4):500-503
82. Nakanishi K, Yang YG, Pierce AJ, Taniguchi T, Digweed M, D'Andrea AD, Wang ZQ, Jasin M (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc Natl Acad Sci USA 102(4):1110-1115
83. Niedernhofer LJ, Lalai AS, Hoeijmakers JH (2005) Fanconi anemia (cross) linked to DNA repair. Cell 123(7):1191-1198
84. Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, D'Andrea AD, Bernards R (2005) The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 17(3):331-339
85. Nojima K, Hochegger H, Saberi A, Fukushima T, Kikuchi K, Yoshimura M, Orelli BJ, Bishop DK, Hirano S, Ohzeki M et al (2005) Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res 65(24):11704-11711
86. Noll DM, Mason TM, Miller PS (2006) Formation and repair of interstrand cross-links in DNA. Chem Rev 106(2):277-301
87. Oestergaard VH, Langevin F, Kuiken HJ, Pace P, Niedzwiedz W, Simpson LJ, Ohzeki M, Takata M, Sale JE, Patel KJ (2007) Deubiquitination of FANCD2 is required for DNA crosslink repair. Mol Cell 28(5):798-809
88. Pace P, Johnson M, Tan WM, Mosedale G, Sng C, Hoatlin M, de Winter J, Joenje H, Gergely F, Patel KJ (2002) FANCE: the link between Fanconi anaemia complex assembly and activity. EMBO J 21(13):3414-3423
89. Papadopoulo D, Guillouf C, Mohrenweiser H, Moustacchi E (1990) Hypomutability in Fanconi anemia cells is associated with increased deletion frequency at the HPRT locus. Proc Natl Acad Sci USA 87(21):8383-8387
90. Patel KJ, Joenje H (2007) Fanconi anemia and DNA replication repair. DNA Repair (Amst) 6(7):885-890
91. Prakash S, Johnson RE, Prakash L (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu Rev Biochem 74:317-353
92. Raschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Scharer OD, Walter JC (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134(6):969-980
93. Rego MA, Harney JA, Mauro M, Shen M, Howlett NG (2012) Regulation of the activation of the Fanconi anemia pathway by the p21 cyclin-dependent kinase inhibitor. Oncogene 31(3): 366-375
94. Sarkar S, Davies AA, Ulrich HD, McHugh PJ (2006) DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase zeta. EMBO J 25(6):1285-1294
95. Sato K, Toda K, Ishiai M, Takata M, Kurumizaka H (2012) DNA robustly stimulates FANCD2 monoubiquitylation in the complex with FANCI. Nucleic Acids Res 40(10):4553-4561
96. Sclafani RA, Holzen TM (2007) Cell cycle regulation of DNA replication. Annu Rev Genet 41:237-280
97. Sengerova B, Wang AT, McHugh PJ (2011) Orchestrating the nucleases involved in DNA interstrand cross-link (ICL) repair. Cell Cycle 10(23):3999-4008
98. Shen X, Do H, Li Y, Chung WH, Tomasz M, de Winter JP, Xia B, Elledge SJ, Wang W, Li L (2009) Recruitment of Fanconi anemia and breast cancer proteins to DNA damage sites is differentially governed by replication. Mol Cell 35(5):716-723
99. Shen X, Jun S, O'Neal LE, Sonoda E, Bemark M, Sale JE, Li L (2006) REV3 and REV1 play major roles in recombinationindependent repair of DNA interstrand cross-links mediated by monoubiquitinated proliferating cell nuclear antigen (PCNA). J Biol Chem 281(20):13869-13872
100. Shereda RD, Machida Y, Machida YJ (2010) Human KIAA1018/FAN1 localizes to stalled replication forks via its ubiquitin-binding domain. Cell Cycle 9(19):3977-3983
101. Sims AE, Spiteri E, Sims RJ 3rd, Arita AG, Lach FP, Landers T, Wurm M, Freund M, Neveling K, Hanenberg H et al (2007) FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat Struct Mol Biol 14(6):564-567
102. Singh TR, Bakker ST, Agarwal S, Jansen M, Grassman E, Godthelp BC, Ali AM, Du CH, Rooimans MA, Fan Q et al (2009) Impaired FANCD2 monoubiquitination and hypersensitivity to camptothecin uniquely characterize Fanconi anemia complementation group M. Blood 114(1):174-180
103. Smeaton MB, Hlavin EM, McGregor Mason T, Noronha AM, Wilds CJ, Miller PS (2008) Distortion-dependent unhooking of interstrand cross-links in mammalian cell extracts. Biochemistry 47(37):9920-9930
104. Smogorzewska A, Desetty R, Saito TT, Schlabach M, Lach FP, Sowa ME, Clark AB, Kunkel TA, Harper JW, Colaiacovo MP et al (2010) A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39(1):36-47
105. Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald ER 3rd, Hurov KE, Luo J, Ballif BA, Gygi SP, Hofmann K, D'Andrea AD et al (2007) Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129(2):289-301
106. Spardy N, Duensing A, Charles D, Haines N, Nakahara T, Lambert PF, Duensing S (2007) The human papillomavirus type 16 E7 oncoprotein activates the Fanconi anemia (FA) pathway and causes accelerated chromosomal instability in FA cells. J Virol 81(23):13265-13270
107. Takahashi TS, Wigley DB, Walter JC (2005) Pumps, paradoxes and ploughshares: mechanism of the MCM2-7 DNA helicase. Trends Biochem Sci 30(8):437-444
108. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M, D'Andrea AD (2002) S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100(7):2414-2420
109. Timmers C, Taniguchi T, Hejna J, Reifsteck C, Lucas L, Bruun D, Thayer M, Cox B, Olson S, D'Andrea AD et al (2001) Positional cloning of a novel Fanconi anemia gene, FANCD2. Mol Cell 7(2):241-248
110. Tumini E, Plevani P, Muzi-Falconi M, Marini F (2011) Physical and functional crosstalk between Fanconi anemia core components and the GINS replication complex. DNA Repair (Amst) 10(2):149-158
111. Vagnarelli P, Hudson DF, Ribeiro SA, Trinkle-Mulcahy L, Spence JM, Lai F, Farr CJ, Lamond AI, Earnshaw WC (2006) Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat Cell Biol 8(10):1133-1142
112. 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(5):406-409
113. Wang LC, Gautier J (2010) The Fanconi anemia pathway and ICL repair: implications for cancer therapy. Crit Rev Biochem Mol Biol 45(5):424-439
114. Wang X, Peterson CA, Zheng H, Nairn RS, Legerski RJ, Li L (2001) Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand cross-link repair. Mol Cell Biol 21(3):713-720
115. Warbrick E (1998) PCNA binding through a conserved motif. BioEssays 20(3):195-199
116. Williams SA, Longerich S, Sung P, Vaziri C, Kupfer GM (2011) The E3 ubiquitin ligase RAD18 regulates ubiquitylation and chromatin loading of FANCD2 and FANCI. Blood 117(19): 5078-5087
117. Woodward AM, Gohler T, Luciani MG, Oehlmann M, Ge X, Gartner A, Jackson DA, Blow JJ (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol 173(5):673-683
118. Zheng H, Wang X, Warren AJ, Legerski RJ, Nairn RS, Hamilton JW, Li L (2003) Nucleotide excision repair-and polymerase eta-mediated error-prone removal of mitomycin C interstrand cross-links. Mol Cell Biol 23(2):754-761
119. Zhu W, Abbas T, Dutta A (2005) DNA replication and genomic instability. Adv Exp Med Biol 570:249-279
120. Zhu W, Dutta A (2006) An ATR-and BRCA1-mediated Fanconi anemia pathway is required for activating the G2/M checkpoint and DNA damage repair upon rereplication. Mol Cell Biol 26(12):4601-4611
121. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300(5625): 1542-1548