Fanconi anemia proteins, DNA interstrand crosslink repair pathways, and cancer therapy

Current Cancer Drug Targets

Volumn 9, Issue 1, 2009, Pages 101-117

  Andreassen, Paul R ^a,b   Ren, Keqin ^a  

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

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

Author keywords

Bifunctional alkylating agents; Chemotherapy; DNA damage responses; DNA interstrand crosslinks; DNA repair; Fanconi anemia; Homologous recombination; Platinum compounds

Indexed keywords

ALSTERPAULLONE; BRCA1 PROTEIN; BUTADIENE DIEPOXIDE; CARBOPLATIN; CISPLATIN; CISPLATIN DERIVATIVE; COMPLEMENTARY RNA; CURCUMIN; DNA; DOUBLE STRANDED DNA; ENZYME INHIBITOR; FANCONI ANEMIA PROTEIN; HYBRID PROTEIN; MELPHALAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOMYCIN C; MRE11 RAD50 NBS1 FUSION PROTEIN; MUS81 EME1 FUSION PROTEIN; N (2 AMINOETHYL) 5 ISOQUINOLINESULFONAMIDE; PSORALEN; RAD51C XRCC3 FUSION PROTEIN; SINGLE STRANDED DNA; SMALL INTERFERING RNA; TARGET OF RAPAMYCIN KINASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; WORTMANNIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; BREAST CANCER; BREAST TUMOR; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GENE THERAPY; CANCER SUSCEPTIBILITY; CANCER THERAPY; CELL ACTIVITY; CELL CYCLE ARREST; CHROMOSOME ABERRATION; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIZATION; DRUG TARGETING; EXCISION REPAIR; FANCONI ANEMIA; GENE EXPRESSION PROFILING; GENE MUTATION; GENE SILENCING; HEAD AND NECK CARCINOMA; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; HUMAN; IONIZING RADIATION; LUNG NON SMALL CELL CANCER; MISMATCH REPAIR; NONHUMAN; OVARY CANCER; OVARY TUMOR; POINT MUTATION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REVIEW; RNA INTERFERENCE; SOMATIC MUTATION; SQUAMOUS CELL CARCINOMA; TREATMENT OUTCOME; UBIQUITINATION; ULTRAVIOLET A RADIATION; UTERINE CERVIX CANCER; WERNER SYNDROME;

DNA DAMAGE; DNA REPAIR; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; GENE SILENCING; HUMANS; MUTATION; NEOPLASMS; PHENOTYPE;

EID: 62549114478     PISSN: 15680096     EISSN: None     Source Type: Journal    
DOI: 10.2174/156800909787314011     Document Type: Review

References (233)

1. Epstein, R. J. Drug-induced DNA damage and tumor chemosensitivity. J. Clin. Oncol. 1990, 8, 2062-2084.
2. La Porta, C. A. Cellular targets for anticancer strategies. Curr. Drug Targets 2004, 5, 347-355.
3. Ding, J.; Miao, Z. H.; Meng, L. H.; Geng, M. Y. Emerging cancer therapeutic opportunities target DNA-repair systems. Trends Pharmacol. Sci. 2006, 27, 338-344.
4. Madhusudan, S.; Middleton, M. R. The emerging role of DNA repair proteins as predictive, prognostic and therapeutic targets in cancer. Cancer Treat. Rev. 2005, 31, 603-617.
5. Sancar, A.; Lindsey-Boltz, L. A.; Unsal-Kacmaz, K.; Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 2004, 73, 39-85.
6. Kennedy, R. D.; D'Andrea, A. D. DNA repair pathways in clinical practice: lessons from pediatric cancer susceptibility syndromes. J. Clin. Oncol. 2006, 24, 3799-3808.
7. Eyfjord, J. E.; Bodvarsdottir, S. K. Genomic instability and cancer: networks involved in response to DNA damage. Mutat. Res. 2005, 592, 18-28.
8. Shiloh, Y. ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 2001, 11, 71-77.
9. McGowan, C. H.; Russell, P. The DNA damage response: sensing and signaling. Curr. Opin. Cell Biol. 2004, 16, 629-633.
10. Zhou, B. B.; Elledge, S. J. The DNA damage response: putting checkpoints in perspective. Nature 2000, 408, 433-439.
11. Drablos, F.; Feyzi, E.; Aas, P. A.; Vaagbo, C. B.; Kavli, B.; Bratlie, M. S.; Pena-Diaz, J.; Otterlei, M.; Slupphaug, G.; Krokan, H. E. Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair (Amst.) 2004, 3, 1389-1407.
12. McHugh, P. J.; Spanswick, V. J.; Hartley, J. A. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol. 2001, 2, 483-490.
13. Sanderson, B. J.; Shield, A. J. Mutagenic damage to mammalian cells by therapeutic alkylating agents. Mutat. Res. 1996, 355, 4157.
14. th ed.; DeVita Jr., V. T.; Hellman, S.; Rosenberg, S.A., Eds; Lippin-cott-Raven Publishers: Philadelphia, PA, 1997, pp. 405-418.
15. Povirk, L. F.; Shuker, D. E. DNA damage and mutagenesis induced by nitrogen mustards. Mutat. Res. 1994, 318, 205-226.
16. Palom, Y.; Suresh Kumar, G.; Tang, L. Q.; Paz, M. M.; Musser, S. M.; Rockwell, S.; Tomasz, M. Relative toxicities of DNA crosslinks and monoadducts: new insights from studies of decarbamoyl mitomycin C and mitomycin C. Chem. Res. Toxicol. 2002, 15, 1398-1406.
17. th ed.; DeVita Jr., V. T.; Hellman, S.; Rosenberg, S. A., Eds; Lippincott-Raven Publishers: Philadelphia, PA, 1997, pp. 405-418.
18. Thompson, L. H.; Hinz, J. M.; Yamada, N. A.; Jones, N. J. How Fanconi anemia proteins promote the four Rs: replication, recombination, repair, and recovery. Environ. Mol. Mutagen. 2005, 45, 128-142.
19. Niedernhofer, L. J.; Lalai, A. S.; Hoeijmakers, J. H. Fanconi anemia (cross)linked to DNA repair. Cell 2005, 123, 1191-1198.
20. Sanderson, B. J.; Ferguson, L. R.; Denny, W. A. Mutagenic and carcinogenic properties of platinum-based anticancer drugs. Mutat. Res. 1996, 355, 59-70.
21. Risinger, M. A.; Groden, J. Crosslinks and crosstalk: human cancer syndromes and DNA repair defects. Cancer Cell 2004, 6, 539-545.
22. Grompe, M.; D'Andrea, A. Fanconi anemia and DNA repair. Hum. Mol. Genet. 2001, 10, 2253-2259.
23. Joenje, H.; Patel, K. J. The emerging genetic and molecular basis of Fanconi anaemia. Nat. Rev. Genet. 2001, 2, 446-457.
24. Taniguchi, T.; D'Andrea, A. D. Molecular pathogenesis of Fanconi anemia: recent progress. Blood 2006, 107, 4223-4233.
25. Kennedy, R. D.; D'Andrea, A. D. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev. 2005, 19, 2925-2940.
26. Mirchandani, K. D.; D'Andrea, A. D. The Fanconi anemia/BRCA pathway: a coordinator of cross-link repair. Exp. Cell Res. 2006, 312, 2647-2653.
27. Osborn, A. J.; Elledge, S. J.; Zou, L. Checking on the fork: the DNA-replication stress-response pathway. Trends Cell Biol. 2002, 12, 509-516.
28. Wang, H.; Wang, H.; Powell, S. N.; Iliakis, G.; Wang, Y. ATR affecting cell radiosensitivity is dependent on homologous recombination repair but independent of nonhomologous end joining. Cancer Res. 2004, 64, 7139-7143.
29. Sorensen, C. S.; Hansen, L. T.; Dziegielewski, J.; Syljuasen, R. G.; Lundin, C.; Bartek, J.; Helleday, T. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol. 2005, 7, 195-201.
30. Kunkel, T. A.; Erie, D. A. DNA mismatch repair. Annu. Rev. Biochem. 2005, 74, 681-710.
31. Zhang, N.; Lu, X.; Zhang, X.; Peterson, C. A.; Legerski, R. J. hMutSbeta is required for the recognition and uncoupling of psoralen interstrand cross-links in vitro. Mol. Cell. Biol. 2002, 22, 2388-2397.
32. Wu, Q.; Christensen, L. A.; Legerski, R. J.; Vasquez, K. M. Mismatch repair participates in error-free processing of DNA inter-strand crosslinks in human cells. EMBO Rep. 2005, 6, 551-557.
33. Bignami, M.; Casorelli, I.; Karran, P. Mismatch repair and response to DNA-damaging antitumour therapies. Eur. J. Cancer 2003, 39, 2142-2149.
34. Rothfuss, A.; Grompe, M. 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. 2004, 24, 123-134.
35. Kuraoka, I.; Kobertz, W. R.; Ariza, R. R.; Biggerstaff, M.; Essigmann, J. M.; Wood, R. D. Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J. Biol. Chem. 2000, 275, 26632-26636.
36. Wang, X.; Peterson, C. A.; Zheng, H.; Nairn, R. S.; Legerski, R. J.; Li, L. Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand cross-link repair. Mol. Cell. Biol. 2001, 21, 713-720.
37. Tian, M.; Shinkura, R.; Shinkura, N.; Alt, F. W. Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF. Mol. Cell. Biol. 2004, 24, 1200-1205.
38. Melton, D. W.; Ketchen, A. M.; Nunez, F.; Bonatti-Abbondandolo, S.; Abbondandolo, A.; Squires, S.; Johnson, R. T. Cells from ERCC1-deficient mice show increased genome instability and a reduced frequency of S-phase-dependent illegitimate chromosome exchange but a normal frequency of homologous recombination. J. Cell Sci. 1998, 111(Pt 3), 395-404.
39. Prakash, S.; Johnson, R. E.; Prakash, L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 2005, 74, 317-353.
40. Cipak, L.; Watanabe, N.; Bessho, T. The role of BRCA2 in replication-coupled DNA interstrand cross-link repair in vitro. Nat. Struct. Mol. Biol. 2006, 13, 729-733.
41. Trujillo, K. M.; Yuan, S. S.; Lee, E. Y.; Sung, P. Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 1998, 273, 21447-21450.
42. Kraakman-van der Zwet, M.; Overkamp, W. J.; Friedl, A. A.; Klein, B.; Verhaegh, G. W.; Jaspers, N. G.; Midro, A. T.; Eckardt-Schupp, F.; Lohman, P. H.; Zdzienicka, M. Z. Immortalization and characterization of Nijmegen Breakage syndrome fibroblasts. Mutat. Res. 1999, 434, 17-27.
43. Williams, B. R.; Mirzoeva, O. K.; Morgan, W. F.; Lin, J.; Dunnick, W.; Petrini, J. H. A murine model of Nijmegen breakage syndrome. Curr. Biol. 2002, 12, 648-653.
44. Nakanishi, K.; Taniguchi, T.; Ranganathan, V.; New, H. V.; Moreau, L. A.; Stotsky, M.; Mathew, C. G.; Kastan, M. B.; Weaver, D. T.; D'Andrea, A. D. Interaction of FANCD2 and NBS1 in the DNA damage response. Nat. Cell Biol. 2002, 4, 913-920.
45. Bohr, V. A.; Souza Pinto, N.; Nyaga, S. G.; Dianov, G.; Kraemer, K.; Seidman, M. M.; Brosh, R. M., Jr. DNA repair and mutagenesis in Werner syndrome. Environ. Mol. Mutagen. 2001, 38, 227-234.
46. Saintigny, Y.; Makienko, K.; Swanson, C.; Emond, M. J.; Monnat, R. J., Jr. Homologous recombination resolution defect in werner syndrome. Mol. Cell. Biol. 2002, 22, 6971-6978.
47. Cheng, W. H.; von Kobbe, C.; Opresko, P. L.; Arthur, L. M.; Komatsu, K.; Seidman, M. M.; Carney, J. P.; Bohr, V. A. Linkage between Werner syndrome protein and the Mre11 complex via Nbs1. J. Biol. Chem. 2004, 279, 21169-21176.
48. Huang, S.; Li, B.; Gray, M. D.; Oshima, J.; Mian, I. S.; Campisi, J. The premature ageing syndrome protein, WRN, is a 3′->5′' exonuclease. Nat. Genet. 1998, 20, 114-116.
49. Pellegrini, L.; Venkitaraman, A. Emerging functions of BRCA2 in DNA recombination. Trends Biochem. Sci. 2004, 29, 310-316.
50. Daboussi, F.; Thacker, J.; Lopez, B. S. Genetic interactions between RAD51 and its paralogues for centrosome fragmentation and ploidy control, independently of the sensitivity to genotoxic stresses. Oncogene 2005, 24, 3691-3696.
51. Kraakman-van der Zwet, M.; Overkamp, W. J.; van Lange, R. E.; Essers, J.; van Duijn-Goedhart, A.; Wiggers, I.; Swaminathan, S.; van Buul, P. P.; Errami, A.; Tan, R. T.; Jaspers, N. G.; Sharan, S. K.; Kanaar, R.; Zdzienicka, M. Z. Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions. Mol. Cell. Biol. 2002, 22, 669-679.
52. Howlett, N. G.; Taniguchi, T.; Olson, S.; Cox, B.; Waisfisz, Q.; De Die-Smulders, C.; Persky, N.; Grompe, M.; Joenje, H.; Pals, G.; Ikeda, H.; Fox, E. A.; D'Andrea, A. D. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 2002, 297, 606-609.
53. Donoho, G.; Brenneman, M. A.; Cui, T. X.; Donoviel, D.; Vogel, H.; Goodwin, E. H.; Chen, D. J.; Hasty, P. Deletion of Brca2 exon 27 causes hypersensitivity to DNA crosslinks, chromosomal instability, and reduced life span in mice. Genes Chromosomes Cancer 2003, 36, 317-331.
54. Helleday, T. Pathways for mitotic homologous recombination in mammalian cellsMutat. Res. 2003, 532, 103-115.
55. Essers, J.; van Steeg, H.; de Wit, J.; Swagemakers, S. M.; Vermeij, M.; Hoeijmakers, J. H.; Kanaar, R. Homologous and non- homologous recombination differentially affect DNA damage repair in mice. EMBO J. 2000, 19, 1703-1710.
56. Moynahan, M. E.; Cui, T. Y.; Jasin, M. Homology-directed dna repair, mitomycin-c resistance, and chromosome stability is re-stored with correction of a Brca1 mutation. Cancer Res. 2001, 61, 4842-4850.
57. Tan, T. L.; Kanaar, R.; Wyman, C. Rad54, a Jack of all trades in homologous recombination. DNA Repair (Amst.) 2003, 2, 787-794.
58. Takata, M.; Sasaki, M. S.; Tachiiri, S.; Fukushima, T.; Sonoda, E.; Schild, D.; Thompson, L. H.; Takeda, S. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 2001, 21, 2858-2866.
59. Godthelp, B. C.; Wiegant, W. W.; van Duijn-Goedhart, A.; Scharer, O. D.; van Buul, P. P.; Kanaar, R.; Zdzienicka, M. Z. Mammalian Rad51C contributes to DNA cross-link resistance, sister chromatid cohesion and genomic stability. Nucleic Acids Res. 2002, 30, 2172-2182.
60. Cui, X.; Brenneman, M.; Meyne, J.; Oshimura, M.; Goodwin, E. H.; Chen, D. J. The XRCC2 and XRCC3 repair genes are required for chromosome stability in mammalian cells. Mutat. Res. 1999, 434, 75-88.
61. Thacker, J. The RAD51 gene family, genetic instability and cancer. Cancer Lett. 2005, 219, 125-135.
62. Liu, Y.; Masson, J. Y.; Shah, R.; O'Regan, P.; West, S. C. RAD51C is required for Holliday junction processing in mammalian cells. Science 2004, 303, 243-246.
63. McPherson, J. P.; Lemmers, B.; Chahwan, R.; Pamidi, A.; Migon, E.; Matysiak-Zablocki, E.; Moynahan, M. E.; Essers, J.; Hanada, K.; Poonepalli, A.; Sanchez-Sweatman, O.; Khokha, R.; Kanaar, R.; Jasin, M.; Hande, M. P.; Hakem, R. Involvement of mammalian Mus81 in genome integrity and tumor suppression. Science 2004, 304, 1822-1826.
64. Abraham, J.; Lemmers, B.; Hande, M. P.; Moynahan, M. E.; Chahwan, C.; Ciccia, A.; Essers, J.; Hanada, K.; Chahwan, R.; Khaw, A. K.; McPherson, P.; Shehabeldin, A.; Laister, R.; Ar- rowsmith, C.; Kanaar, R.; West, S. C.; Jasin, M.; Hakem, R. Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J. 2003, 22, 6137-6147.
65. Hanada, K.; Budzowska, M.; Modesti, M.; Maas, A.; Wyman, C.; Essers, J.; Kanaar, R. The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J. 2006, 25, 4921-4932.
66. Boddy, M. N.; Gaillard, P. H.; McDonald, W. H.; Shanahan, P.; Yates, J. R., 3rd; Russell, P. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 2001, 107, 537-548.
67. Alter, B. P. Cancer in Fanconi anemia, 1927-2001. Cancer 2003, 97, 425-440.
68. Tischkowitz, M. D.; Hodgson, S. V. Fanconi anaemia. J. Med. Genet. 2003, 40, 1-10.
69. Butturini, A.; Gale, R. P.; Verlander, P. C.; Adler-Brecher, B.; Gillio, A. P.; Auerbach, A. D. Hematologic abnormalities in Fanconi anemia: an International Fanconi Anemia Registry study. Blood 1994, 84, 1650-1655.
70. Dokal, I. The genetics of Fanconi's anaemia. Baillieres Best Pract. Res. Clin. Haematol. 2000, 13, 407-425.
71. Levitus, M.; Waisfisz, Q.; Godthelp, B. C.; Vries, Y.; Hussain, S.; Wiegant, W. W.; Elghalbzouri-Maghrani, E.; Steltenpool, J.; Rooimans, M. A.; Pals, G.; Arwert, F.; Mathew, C. G.; Zdzienicka, M. Z.; Hiom, K.; De Winter, J. P.; Joenje, H. The DNA helicase BRIP1 is defective in Fanconi anemia complementation group J. Nat. Genet. 2005, 37, 934-935.
72. Levran, O.; Attwooll, C.; Henry, R. T.; Milton, K. L.; Neveling, K.; Rio, P.; Batish, S. D.; Kalb, R.; Velleuer, E.; Barral, S.; Ott, J.; Petrini, J.; Schindler, D.; Hanenberg, H.; Auerbach, A. D. The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia. Nat. Genet. 2005, 37, 931-933.
73. Meetei, A. R.; de Winter, J. P.; Medhurst, A. L.; Wallisch, M.; Waisfisz, Q.; van de Vrugt, H. J.; Oostra, A. B.; Yan, Z.; Ling, C.; Bishop, C. E.; Hoatlin, M. E.; Joenje, H.; Wang, W. A novel ubiquitin ligase is deficient in Fanconi anemia. Nat. Genet. 2003, 35, 165-170.
74. Meetei, A. R.; Levitus, M.; Xue, Y.; Medhurst, A. L.; Zwaan, M.; Ling, C.; Rooimans, M. A.; Bier, P.; Hoatlin, M.; Pals, G.; de Winter, J. P.; Wang, W.; Joenje, H. X-linked inheritance of Fanconi anemia complementation group B. Nat. Genet. 2004, 36, 1219-1224.
75. Meetei, A. R.; Medhurst, A. L.; Ling, C.; Xue, Y.; Singh, T. R.; Bier, P.; Steltenpool, J.; Stone, S.; Dokal, I.; Mathew, C. G.; Hoatlin, M.; Joenje, H.; de Winter, J. P.; Wang, W. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 2005, 37, 958-963.
76. de Winter, J. P.; Leveille, F.; van Berkel, C. G.; Rooimans, M. A.; van Der Weel, L.; Steltenpool, J.; Demuth, I.; Morgan, N. V.; Alon, N.; Bosnoyan-Collins, L.; Lightfoot, J.; Leegwater, P. A.; Waisfisz, Q.; Komatsu, K.; Arwert, F.; Pronk, J. C.; Mathew, C. G.; Dig-weed, M.; Buchwald, M.; Joenje, H. Isolation of a cDNA representing the Fanconi anemia complementation group E gene. Am. J. Hum. Genet. 2000, 67, 1306-1308.
77. de Winter, J. P.; Waisfisz, Q.; Rooimans, M. A.; van Berkel, C. G.; Bosnoyan-Collins, L.; Alon, N.; Carreau, M.; Bender, O.; Demuth, I.; Schindler, D.; Pronk, J. C.; Arwert, F.; Hoehn, H.; Digweed, M.; Buchwald, M.; Joenje, H. The Fanconi anaemia group G gene FANCG is identical with XRCC9. Nat. Genet. 1998, 20, 281-283.
78. Lo Ten Foe, J. R.; Rooimans, M. A.; Bosnoyan-Collins, L.; Alon, N.; Wijker, M.; Parker, L.; Lightfoot, J.; Carreau, M.; Callen, D. F.; Savoia, A.; Cheng, N. C.; van Berkel, C. G.; Strunk, M. H.; Gille, J. J.; Pals, G.; Kruyt, F. A.; Pronk, J. C.; Arwert, F.; Buchwald, M.; Joenje, H. Expression cloning of a cDNA for the major Fanconi anaemia gene, FAA. Nat. Genet. 1996, 14, 320-323.
79. Strathdee, C. A.; Gavish, H.; Shannon, W. R.; Buchwald, M. Cloning of cDNAs for Fanconi's anaemia by functional complementation. Nature 1992, 356, 763-767.
80. Timmers, C.; Taniguchi, T.; Hejna, J.; Reifsteck, C.; Lucas, L.; Bruun, D.; Thayer, M.; Cox, B.; Olson, S.; D'Andrea, A. D.; Moses, R.; Grompe, M. Positional cloning of a novel Fanconi anemia gene, FANCD2. Mol. Cell 2001, 7, 241-248.
81. de Winter, J. P.; Rooimans, M. A.; van Der Weel, L.; van Berkel, C. G.; Alon, N.; Bosnoyan-Collins, L.; de Groot, J.; Zhi, Y.; Waisfisz, Q.; Pronk, J. C.; Arwert, F.; Mathew, C. G.; Scheper, R. J.; Hoatlin, M. E.; Buchwald, M.; Joenje, H. The Fanconi anaemia gene FANCF encodes a novel protein with homology to ROM. Nat. Genet. 2000, 24, 15-16.
82. 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.; Elledge, S. J. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007, 129, 289-301.
83. Sims, A. E.; Spiteri, E.; Sims, R. J., 3rd; Arita, A. G.; Lach, F. P.; Landers, T.; Wurm, M.; Freund, M.; Neveling, K.; Hanenberg, H.; Auerbach, A. D.; Huang, T. T. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 2007, 14, 564-567.
84. Xia, B.; Dorsman, J. C.; Ameziane, N.; de Vries, Y.; Rooimans, M. A.; Sheng, Q.; Pals, G.; Errami, A.; Gluckman, E.; Llera, J.; Wang, W.; Livingston, D. M.; Joenje, H.; de Winter, J. P. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat. Genet. 2007, 39, 159-161.
85. Reid, S.; Schindler, D.; Hanenberg, H.; Barker, K.; Hanks, S.; Kalb, R.; Neveling, K.; Kelly, P.; Seal, S.; Freund, M.; Wurm, M.; Batish, S. D.; Lach, F. P.; Yetgin, S.; Neitzel, H.; Ariffin, H.; Tischkowitz, M.; Mathew, C. G.; Auerbach, A. D.; Rahman, N. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat. Genet. 2007, 39, 162-164.
86. The Fanconi anaemia/breast cancer consortium. Positional cloning of the Fanconi anaemia group A gene. Nat. Genet. 1996, 14, 324-328.
87. Dorsman, J. C.; Levitus, M.; Rockx, D.; Rooimans, M. A.; Oostra, A. B.; Haitjema, A.; Bakker, S. T.; Steltenpool, J.; Schuler, D.; Mohan, S.; Schindler, D.; Arwert, F.; Pals, G.; Mathew, C. G.; Waisfisz, Q.; de Winter, J. P.; Joenje, H. Identification of the Fanconi anemia complementation group I gene, FANCI. Cell. Oncol. 2007, 29, 211-218.
88. Kupfer, G. M.; D'Andrea, A. D. The effect of the Fanconi anemia polypeptide, FAC, upon p53 induction and G2 checkpoint regulation. Blood 1996, 88, 1019-1025.
89. Zdzienicka, M. Z.; Arwert, F.; Neuteboom, I.; Rooimans, M.; Simons, J. W. The Chinese hamster V79 cell mutant V-H4 is phe- notypically like Fanconi anemia cells. Somat. Cell Mol. Genet. 1990, 16, 575-581.
90. Godthelp, B. C.; van Buul, P. P.; Jaspers, N. G.; Elghalbzouri-Maghrani, E.; van Duijn-Goedhart, A.; Arwert, F.; Joenje, H.; Zdzienicka, M. Z. Cellular characterization of cells from the Fanconi anemia complementation group, FA-D1/BRCA2. Mutat. Res. 2006, 601, 191-201.
91. Kalb, R.; Duerr, M.; Wagner, M.; Herterich, S.; Gross, M.; Dig-weed, M.; Joenje, H.; Hoehn, H.; Schindler, D. Lack of sensitivity of primary Fanconi's anemia fibroblasts to UV and ionizing radiation. Radiat. Res. 2004, 161, 318-325.
92. Carreau, M.; Alon, N.; Bosnoyan-Collins, L.; Joenje, H.; Buchwald, M. Drug sensitivity spectra in Fanconi anemia lymphoblastoid cell lines of defined complementation groups. Mutat. Res. 1999, 435, 103-109.
93. Auerbach, A. D. Fanconi anemia diagnosis and the diepoxybutane (DEB) test. Exp. Hematol. 1993, 21, 731-733.
94. Chandra, S.; Levran, O.; Jurickova, I.; Maas, C.; Kapur, R.; Schindler, D.; Henry, R.; Milton, K.; Batish, S. D.; Cancelas, J. A.; Hanenberg, H.; Auerbach, A. D.; Williams, D. A. A rapid method for retrovirus-mediated identification of complementation groups in Fanconi anemia patients. Mol. Ther. 2005, 12, 976-984.
95. Kaiser, T. N.; Lojewski, A.; Dougherty, C.; Juergens, L.; Sahar, E.; Latt, S. A. Flow cytometric characterization of the response of Fanconi's anemia cells to mitomycin C treatment. Cytometry 1982, 2, 291-297.
96. Heinrich, M. C.; Hoatlin, M. E.; Zigler, A. J.; Silvey, K. V.; Bakke, A. C.; Keeble, W. W.; Zhi, Y.; Reifsteck, C. A.; Grompe, M.; Brown, M. G.; Magenis, R. E.; Olson, S. B.; Bagby, G. C. DNA cross-linker-induced G2/M arrest in group C Fanconi anemia lymphoblasts reflects normal checkpoint function. Blood 1998, 91, 275-287.
97. Litman, R.; Peng, M.; Jin, Z.; Zhang, F.; Zhang, J.; Powell, S.; Andreassen, P. R.; Cantor, S. B. BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 2005, 8, 255-265.
98. Kupfer, G. M.; Yamashita, T.; Naf, D.; Suliman, A.; Asano, S.; D'Andrea, A. D. The Fanconi anemia polypeptide, FAC, binds to the cyclin-dependent kinase, cdc2. Blood 1997, 90, 1047-1054.
99. Garcia-Higuera, I.; Taniguchi, T.; Ganesan, S.; Meyn, M. S.; Timmers, C.; Hejna, J.; Grompe, M.; D'Andrea, A. D. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 2001, 7, 249-262.
100. Siddique, M. A.; Nakanishi, K.; Taniguchi, T.; Grompe, M.; D'Andrea, A. D. Function of the Fanconi anemia pathway in Fanconi anemia complementation group F and D1 cells. Exp. Hematol. 2001, 29, 1448-1455.
101. Pace, P.; Johnson, M.; Tan, W. M.; Mosedale, G.; Sng, C.; Hoatlin, M.; de Winter, J.; Joenje, H.; Gergely, F.; Patel, K. J. FANCE: the link between Fanconi anaemia complex assembly and activity. EMBO J. 2002, 21, 3414-3423.
102. Ciccia, A.; Ling, C.; Coulthard, R.; Yan, Z.; Xue, Y.; Meetei, A. R.; Laghmani el, H.; Joenje, H.; McDonald, N.; de Winter, J. P.; Wang, W.; West, S. C. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol. Cell 2007, 25, 331-343.
103. Ling, C.; Ishiai, M.; Ali, A. M.; Medhurst, A. L.; Neveling, K.; Kalb, R.; Yan, Z.; Xue, Y.; Oostra, A. B.; Auerbach, A. D.; Hoatlin, M. E.; Schindler, D.; Joenje, H.; de Winter, J. P.; Takata, M.; Meetei, A. R.; Wang, W. FAAP100 is essential for activation of the Fanconi anemia-associated DNA damage response pathway. EMBO J. 2007, 26, 2104-2114.
104. Seal, S.; Thompson, D.; Renwick, A.; Elliott, A.; Kelly, P.; Bar-foot, R.; Chagtai, T.; Jayatilake, H.; Ahmed, M.; Spanova, K.; North, B.; McGuffog, L.; Evans, D. G.; Eccles, D.; Easton, D. F.; Stratton, M. R.; Rahman, N. Truncating mutations in the Fanconi anemia J gene BRIP1 are low-penetrance breast cancer susceptibility alleles. Nat. Genet. 2006, 38, 1239-1241.
105. Wooster, R.; Bignell, G.; Lancaster, J.; Swift, S.; Seal, S.; Mangion, J.; Collins, N.; Gregory, S.; Gumbs, C.; Micklem, G. Identification of the breast cancer susceptibility gene BRCA2. Nature 1995, 378, 789-792.
106. Rahman, N.; Seal, S.; Thompson, D.; Kelly, P.; Renwick, A.; Elliott, A.; Reid, S.; Spanova, K.; Barfoot, R.; Chagtai, T.; Jayatilake, H.; McGuffog, L.; Hanks, S.; Evans, D. G.; Eccles, D.; Easton, D. F.; Stratton, M. R. PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat. Genet. 2007, 39, 165-167.
107. Levitus, M.; Rooimans, M. A.; Steltenpool, J.; Cool, N. F.; Oostra, A. B.; Mathew, C. G.; Hoatlin, M. E.; Waisfisz, Q.; Arwert, F.; de Winter, J. P.; Joenje, H. Heterogeneity in Fanconi anemia: evidence for 2 new genetic subtypes. Blood2004, 103, 2498-2503.
108. Taniguchi, T.; Garcia-Higuera, I.; Andreassen, P. R.; Gregory, R. C.; Grompe, M.; D'Andrea, A. D. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 2002, 100, 2414-2420.
109. Garcia-Higuera, I.; Kuang, Y.; Naf, D.; Wasik, J.; D'Andrea, A. D. Fanconi anemia proteins FANCA, FANCC, and FANCG/XRCC9 interact in a functional nuclear complex. Mol. Cell. Biol. 1999, 19, 4866-4873.
110. Taniguchi, T.; D'Andrea, A. D. The Fanconi anemia protein, FANCE, promotes the nuclear accumulation of FANCC. Blood 2002, 100, 2457-2462.
111. 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.; Joenje, H.; de Winter, J. P. Evidence for subcom- plexes in the Fanconi anemia pathway. Blood 2006, 108, 2072-2080.
112. Medhurst, A. L.; Huber, P. A.; Waisfisz, Q.; de Winter, J. P.; Mathew, C. G. Direct interactions of the five known Fanconi anaemia proteins suggest a common functional pathway. Hum. Mol. Genet. 2001, 10, 423-429.
113. Gordon, S. M.; Alon, N.; Buchwald, M. FANCC, FANCE, and FANCD2 form a ternary complex essential to the integrity of the Fanconi anemia DNA damage response pathway. J. Biol. Chem. 2005, 280, 36118-36125.
114. Gordon, S. M.; Buchwald, M. Fanconi anemia protein complex: mapping protein interactions in the yeast 2-and 3-hybrid systems. Blood 2003, 102, 136-141.
115. Gurtan, A. M.; D'Andrea, A. D. Dedicated to the core: understanding the Fanconi anemia complex. DNA Repair (Amst.) 2006, 5, 1119-1125.
116. Blom, E.; van de Vrugt, H. J.; de Vries, Y.; de Winter, J. P.; Arwert, F.; Joenje, H. Multiple TPR motifs characterize the Fanconi anemia FANCG protein. DNA Repair (Amst.) 2004, 3, 77-84.
117. Gurtan, A. M.; Stuckert, P.; D'Andrea, A. D. The WD40 repeats of FANCL are required for Fanconi anemia core complex assembly. J. Biol. Chem. 2006, 281, 10896-10905.
118. Leveille, F.; Blom, E.; Medhurst, A. L.; Bier, P.; Laghmani el, H.; Johnson, M.; Rooimans, M. A.; Sobeck, A.; Waisfisz, Q.; Arwert, F.; Patel, K. J.; Hoatlin, M. E.; Joenje, H.; de Winter, J. P. The Fanconi anemia gene product FANCF is a flexible adaptor protein. J. Biol. Chem. 2004, 279, 39421-39430.
119. Kowal, P.; Gurtan, A. M.; Stuckert, P.; D'Andrea, A. D.; Ellen-berger, T. Structural determinants of human FANCF protein that function in the assembly of a DNA damage signaling complex. J. Biol. Chem. 2007, 282, 2047-2055.
120. Gari, K.; Decaillet, C.; Stasiak, A. Z.; Stasiak, A.; Constantinou, A. The fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell 2008, 29, 141-148.
121. Xue, Y.; Li, Y.; Guo, R.; Ling, C.; Wang, W. FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair. Hum. Mol. Genet. 2008, 17, 1641-1652.
122. Mosedale, G.; Niedzwiedz, W.; Alpi, A.; Perrina, F.; Pereira-Leal, J. B.; Johnson, M.; Langevin, F.; Pace, P.; Patel, K. J. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat. Struct. Mol. Biol. 2005, 12, 763-771.
123. Kim, J. M.; Kee, Y.; Gurtan, A.; D'Andrea, A. D. Cell cycle dependent chromatin loading of the fanconi anemia core complex by FANCM/FAAP24. Blood 2008, 111, 5215-5222.
124. Hicke, L.; Dunn, R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell. Dev. Biol. 2003, 19, 141-172.
125. Sun, L.; Chen, Z. J. The novel functions of ubiquitination in signaling. Curr. Opin. Cell. Biol. 2004, 16, 119-126.
126. Solomon, D. A.; Cardoso, M. C.; Knudsen, E. S. Dynamic targeting of the replication machinery to sites of DNA damage. J. Cell. Biol. 2004, 166, 455-463.
127. Plosky, B. S.; Woodgate, R. Switching from high-fidelity replicases to low-fidelity lesion-bypass polymerases. Curr. Opin. Genet. Dev. 2004, 14, 113-119.
128. Pickart, C. M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70, 503-533.
129. Yang, Y.; Ludwig, R. L.; Jensen, J. P.; Pierre, S. A.; Medaglia, M. V.; Davydov, I. V.; Safiran, Y. J.; Oberoi, P.; Kenten, J. H.; Phillips, A. C.; Weissman, A. M.; Vousden, K. H. Small molecule inhibitors of HDM2 ubiquitin ligase activity stabilize and activate p53 in cells. Cancer Cell 2005, 7, 547-559.
130. Auger, K. R.; Copeland, R. A.; Lai, Z. Quantitative assays of mdm2 ubiquitin ligase activity and other ubiquitin-utilizing enzymes for inhibitor discovery. Methods Enzymol. 2005, 399, 701717.
131. Sun, Y. Targeting E3 ubiquitin ligases for cancer therapy. Cancer Biol. Ther. 2003, 2, 623-629.
132. Machida, Y. J.; Machida, Y.; Chen, Y.; Gurtan, A. M.; Kupfer, G. M.; D'Andrea, A. D.; Dutta, A. UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation. Mol. Cell 2006, 23, 589-596.
133. Nijman, S. M.; Huang, T. T.; Dirac, A. M.; Brummelkamp, T. R.; Kerkhoven, R. M.; D'Andrea, A. D.; Bernards, R. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol. Cell 2005, 17, 331-339.
134. Cohn, M. A.; Kowal, P.; Yang, K.; Haas, W.; Huang, T. T.; Gygi, S. P.; D'Andrea, A. D. A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol. Cell 2007, 28, 786-797.
135. Oestergaard, V. H.; Langevin, F.; Kuiken, H. J.; Pace, P.; Niedzwiedz, W.; Simpson, L. J.; Ohzeki, M.; Takata, M.; Sale, J. E.; Patel, K. J. Deubiquitination of FANCD2 is required for DNA crosslink repair. Mol. Cell 2007, 28, 798-809.
136. Kruyt, F. A.; Hoshino, T.; Liu, J. M.; Joseph, P.; Jaiswal, A. K.; Youssoufian, H. Abnormal microsomal detoxification implicated in Fanconi anemia group C by interaction of the FAC protein with NADPH cytochrome P450 reductase. Blood 1998, 92, 3050-3056.
137. Cumming, R. C.; Lightfoot, J.; Beard, K.; Youssoufian, H.; O'Brien, P. J.; Buchwald, M. Fanconi anemia group C protein prevents apoptosis in hematopoietic cells through redox regulation of GSTP1. Nat. Med. 2001, 7, 814-820.
138. Futaki, M.; Igarashi, T.; Watanabe, S.; Kajigaya, S.; Tatsuguchi, A.; Wang, J.; Liu, J. M. The FANCG Fanconi anemia protein interacts with CYP2E1: possible role in protection against oxidative DNA damage. Carcinogenesis 2002, 23, 67-72.
139. Mukhopadhyay, S. S.; Leung, K. S.; Hicks, M. J.; Hastings, P. J.; Youssoufian, H.; Plon, S. E. Defective mitochondrial peroxiredoxin-3 results in sensitivity to oxidative stress in Fanconi anemia. J. Cell Biol. 2006, 175, 225-235.
140. Hoatlin, M. E.; Zhi, Y.; Ball, H.; Silvey, K.; Melnick, A.; Stone, S.; Arai, S.; Hawe, N.; Owen, G.; Zelent, A.; Licht, J. D. A novel BTB/POZ transcriptional repressor protein interacts with the Fan- coni anemia group C protein and PLZF. Blood 1999, 94, 3737-3747.
141. Hussain, S.; Wilson, J. B.; Blom, E.; Thompson, L. H.; Sung, P.; Gordon, S. M.; Kupfer, G. M.; Joenje, H.; Mathew, C. G.; Jones, N. J. Tetratricopeptide-motif-mediated interaction of FANCG with recombination proteins XRCC3 and BRCA2. DNA Repair (Amst.) 2006, 5, 629-640.
142. Folias, A.; Matkovic, M.; Bruun, D.; Reid, S.; Hejna, J.; Grompe, M.; D'Andrea, A.; Moses, R. BRCA1 interacts directly with the Fanconi anemia protein FANCA. Hum. Mol. Genet. 2002, 11, 2591-2597.
143. Ting, N. S.; Lee, W. H. The DNA double-strand break response pathway: becoming more BRCAish than ever. DNA Repair (Amst.) 2004, 3, 935-944.
144. Otsuki, T.; Furukawa, Y.; Ikeda, K.; Endo, H.; Yamashita, T.; Shinohara, A.; Iwamatsu, A.; Ozawa, K.; Liu, J. M. Fanconi anemia protein, FANCA, associates with BRG1, a component of the human SWI/SNF complex. Hum. Mol. Genet. 2001, 10, 2651-2660.
145. Meetei, A. R.; Sechi, S.; Wallisch, M.; Yang, D.; Young, M. K.; Joenje, H.; Hoatlin, M. E.; Wang, W. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol. Cell. Biol. 2003, 23, 3417-3426.
146. 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.; Huber, P. A. Yeast two-hybrid screens imply involvement of Fanconi anemia proteins in transcription regulation, cell signaling, oxidative metabolism, and cellular transport. Exp. Cell. Res. 2003, 289, 211-221.
147. Andreassen, P. R.; D'Andrea, A. D.; Taniguchi, T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev. 2004, 78, 1958-1963.
148. Pichierri, P.; Franchitto, A.; Rosselli, F. BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. EMBO J. 2004, 23, 3154-3163.
149. Wang, X.; Andreassen, P. R.; D'Andrea, A. D. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell. Biol. 2004, 24, 5850-5862.
150. Hirano, S.; Yamamoto, K.; Ishiai, M.; Yamazoe, M.; Seki, M.; Matsushita, N.; Ohzeki, M.; Yamashita, Y. M.; Arakawa, H.; Buerstedde, J. M.; Enomoto, T.; Takeda, S.; Thompson, L. H.; Takata, M. Functional relationships of FANCC to homologous recombination, translesion synthesis, and BLM. EMBO J. 2005, 24, 418-427.
151. Moynahan, M. E.; Chiu, J. W.; Koller, B. H.; Jasin, M. Brca1 controls homology-directed DNA repair. Mol. Cell 1999, 4, 511-518.
152. Morrison, C.; Shinohara, A.; Sonoda, E.; Yamaguchi-Iwai, Y.; Takata, M.; Weichselbaum, R. R.; Takeda, S. The essential functions of human Rad51 are independent of ATP hydrolysis. Mol. Cell. Biol. 1999, 79, 6891-6897.
153. Hussain, S.; Wilson, J. B.; Medhurst, A. L.; Hejna, J.; Witt, E.; Ananth, S.; Davies, A.; Masson, J. Y.; Moses, R.; West, S. C.; de Winter, J. P.; Ashworth, A.; Jones, N. J.; Mathew, C. G. Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum. Mol. Genet. 2004, 73, 1241-1248.
154. Montes de Oca, R.; Andreassen, P. R.; Margossian, S. P.; Gregory, R. C.; Taniguchi, T.; Wang, X.; Houghtaling, S.; Grompe, M.; D'Andrea, A. D. Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 2005, 705, 1003-1009.
155. Matsushita, N.; Kitao, H.; Ishiai, M.; Nagashima, N.; Hirano, S.; Okawa, K.; Ohta, T.; Yu, D. S.; McHugh, P. J.; Hickson, I. D.; Venkitaraman, A. R.; Kurumizaka, H.; Takata, M. A FancD2-Monoubiquitin Fusion Reveals Hidden
156. Kalb, R.; Neveling, K.; Hoehn, H.; Schneider, H.; Linka, Y.; Batish, S. D.; Hunt, C.; Berwick, M.; Callen, E.; Surralles, J.; Casado, J. A.; Bueren, J.; Dasi, A.; Soulier, J.; Gluckman, E.; Zwaan, C. M.; van Spaendonk, R.; Pals, G.; de Winter, J. P.; Joenje, H.; Grompe, M.; Auerbach, A. D.; Hanenberg, H.; Schindler, D. Hypomorphic mutations in the gene encoding a key Fanconi anemia protein, FANCD2, sustain a significant group of FA-D2 patients with severe phenotype. Am. J. Hum. Genet. 2007, 80, 895-910.
157. Stiff, T.; Reis, C.; Alderton, G. K.; Woodbine, L.; O'Driscoll, M.; Jeggo, P. A. Nbs1 is required for ATR-dependent phosphorylation events. EMBO J. 2005, 24, 199-208.
158. Zou, L.; Elledge, S. J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003, 300, 1542-1548.
159. Pichierri, P.; Rosselli, F. The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J. 2004, 23, 1178-1187.
160. Ho, G. P.; Margossian, S.; Taniguchi, T.; D'Andrea, A. D. Phosphorylation of FANCD2 on two novel sites is required for mitomycin C resistance. Mol. Cell. Biol. 2006, 26, 7005-7015.
161. Bogliolo, M.; Lyakhovich, A.; Callen, E.; Castella, M.; Cappelli, E.; Ramirez, M. J.; Creus, A.; Marcos, R.; Kalb, R.; Neveling, K.; Schindler, D.; Surralles, J. Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability. EMBO J. 2007, 26, 1340-1351.
162. Taniguchi, T.; Garcia-Higuera, I.; Xu, B.; Andreassen, P. R.; Gregory, R. C.; Kim, S. T.; Lane, W. S.; Kastan, M. B.; D'Andrea, A. D. Convergence of the fanconi anemia and ataxia telangiectasia signaling pathways. Cell 2002, 709, 459-472
163. D'Andrea, A. D.; Grompe, M. The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer 2003, 3, 23-34.
164. Hussain, S.; Witt, E.; Huber, P. A.; Medhurst, A. L.; Ashworth, A.; Mathew, C. G. Direct interaction of the Fanconi anaemia protein FANCG with BRCA2/FANCD1. Hum. Mol. Genet. 2003, 12, 2503-2510.
165. Ohashi, A.; Zdzienicka, M. Z.; Chen, J.; Couch, F. J. Fanconi anemia complementation group D2 (FANCD2) functions independently of BRCA2-and RAD51-associated homologous recombination in response to DNA damage. J. Biol. Chem. 2005, 280, 14877-14883.
166. Kitao, H.; Yamamoto, K.; Matsushita, N.; Ohzeki, M.; Ishiai, M.; Takata, M. Functional interplay between BRCA2/FancD1 and FancC in DNA repair. J. Biol. Chem. 2006, 287, 21312-21320.
167. Wagner, J. E.; Tolar, J.; Levran, O.; Scholl, T.; Deffenbaugh, A.; Satagopan, J.; Ben-Porat, L.; Mah, K.; Batish, S. D.; Kutler, D. I.; MacMillan, M. L.; Hanenberg, H.; Auerbach, A. D. Germline mutations in BRCA2: shared genetic susceptibility to breast cancer, early onset leukemia, and Fanconi anemia. Blood 2004, 703, 3226-3229.
168. Hirsch, B.; Shimamura, A.; Moreau, L.; Baldinger, S.; Hagalshiekh, M.; Bostrom, B.; Sencer, S.; D'Andrea, A. D. Association of biallelic BRCA2/FANCD1 mutations with spontaneous chromosomal instability and solid tumors of childhood. Blood 2004, 703, 2554-2559.
169. Nakanishi, K.; Yang, Y. G.; Pierce, A. J.; Taniguchi, T.; Digweed, M.; D'Andrea, A. D.; Wang, Z. Q.; Jasin, M. Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc. Natl. Acad. Sci. USA 2005, 702, 1110-1115.
170. Dong, Y.; Hakimi, M. A.; Chen, X.; Kumaraswamy, E.; Cooch, N. S.; Godwin, A. K.; Shiekhattar, R. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol. Cell 2003, 72, 1087-1099.
171. Wong, J. M.; Ionescu, D.; Ingles, C. J. Interaction between BRCA2 and replication protein A is compromised by a cancer-predisposing mutation in BRCA2. Oncogene 2003, 22, 28-33.
172. Marston, N. J.; Richards, W. J.; Hughes, D.; Bertwistle, D.; Marshall, C. J.; Ashworth, A. Interaction between the product of the breast cancer susceptibility gene BRCA2 and DSS1, a protein functionally conserved from yeast to mammals. Mol. Cell. Biol. 1999, 79, 4633-4642.
173. Chen, J.; Silver, D. P.; Walpita, D.; Cantor, S. B.; Gazdar, A. F.; Tomlinson, G.; Couch, F. J.; Weber, B. L.; Ashley, T.; Livingston, D. M.; Scully, R. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell 1998, 2, 317-328.
174. Chen, P. L.; Chen, C. F.; Chen, Y.; Xiao, J.; Sharp, Z. D.; Lee, W. H. The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment. Proc. Natl. Acad. Sci. USA 1998, 95, 5287-5292.
175. Xia, B.; Sheng, Q.; Nakanishi, K.; Ohashi, A.; Wu, J.; Christ, N.; Liu, X.; Jasin, M.; Couch, F. J.; Livingston, D. M. Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol. Cell 2006, 22, 719-729.
176. Digweed, M.; Rothe, S.; Demuth, I.; Scholz, R.; Schindler, D.; Stumm, M.; Grompe, M.; Jordan, A.; Sperling, K. Attenuation of the formation of DNA-repair foci containing RAD51 in Fanconi anaemia. Carcinogenesis 2002, 23, 1121-1126.
177. Godthelp, B. C.; Wiegant, W. W.; Waisfisz, Q.; Medhurst, A. L.; Arwert, F.; Joenje, H.; Zdzienicka, M. Z. Inducibility of nuclear Rad51 foci after DNA damage distinguishes all Fanconi anemia complementation groups from D1/BRCA2. Mutat. Res. 2006, 594, 39-48.
178. Yang, Y. G.; Herceg, Z.; Nakanishi, K.; Demuth, I.; Piccoli, C.; Michelon, J.; Hildebrand, G.; Jasin, M.; Digweed, M.; Wang, Z. Q. The Fanconi anemia group A protein modulates homologous repair of DNA double-strand breaks in mammalian cells. Carcinogenesis 2005, 26, 1731-1740.
179. Cantor, S. B.; Bell, D. W.; Ganesan, S.; Kass, E. M.; Drapkin, R.; Grossman, S.; Wahrer, D. C.; Sgroi, D. C.; Lane, W. S.; Haber, D. A.; Livingston, D. M. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 2001, 705, 149-160.
180. Cantor, S. B.; Andreassen, P. R. Assessing the link between BACH1 and BRCA1 in the FA pathway. Cell Cycle 2006, 5, 164-167.
181. Kumaraswamy, E.; Shiekhattar, R. Activation of BRCA1/BRCA2-associated helicase BACH1 is required for timely progression through S phase. Mol. Cell. Biol. 2007, 27, 6733-6741.
182. Yu, X.; Chini, C. C.; He, M.; Mer, G.; Chen, J. The BRCT domain is a phospho-protein binding domain. Science 2003, 302, 639-642.
183. Cantor, S.; Drapkin, R.; Zhang, F.; Lin, Y.; Han, J.; Pamidi, S.; Livingston, D. M. The BRCA1-associated protein BACH1 is a DNA helicase targeted by clinically relevant inactivating mutations. Proc. Natl. Acad. Sci. USA 2004, 707, 2357-2362.
184. Sharma, S.; Doherty, K. M.; Brosh, R. M., Jr. DNA helicases as targets for anti-cancer drugs. Curr. Med. Chem. Anticancer Agents 2005, 5, 183-199.
185. Peng, M.; Litman, R.; Xie, J.; Sharma, S.; Brosh, R. M., Jr.; Cantor, S. B. The FANCJ/MutLalpha interaction is required for correction of the cross-link response in FA-J cells. EMBO J. 2007, 26, 3238-3249.
186. Houghtaling, S.; Timmers, C.; Noll, M.; Finegold, M. J.; Jones, S. N.; Meyn, M. S.; Grompe, M. Epithelial cancer in Fanconi anemia complementation group D2 (Fancd2) knockout mice. Genes Dev. 2003, 17, 2021-2035.
187. Niedzwiedz, W.; Mosedale, G.; Johnson, M.; Ong, C. Y.; Pace, P.; Patel, K. J. The Fanconi Anaemia Gene FANCC Promotes Homologous Recombination and Error-Prone DNA Repair. Mol. Cell 2004, 15, 607-620.
188. Yamamoto, K.; Hirano, S.; Ishiai, M.; Morishima, K.; Kitao, H.; Namikoshi, K.; Kimura, M.; Matsushita, N.; Arakawa, H.; Buerstedde, J. M.; Komatsu, K.; Thompson, L. H.; Takata, M. Fanconi anemia protein FANCD2 promotes immunoglobulin gene conversion and DNA repair through a mechanism related to homologous recombination. Mol. Cell. Biol. 2005, 25, 34-43.
189. Yamamoto, K.; Ishiai, M.; Matsushita, N.; Arakawa, H.; Lamerdin, J. E.; Buerstedde, J. M.; Tanimoto, M.; Harada, M.; Thompson, L. H.; Takata, M. Fanconi anemia FANCG protein in mitigating radiation-and enzyme-induced DNA double-strand breaks by homologous recombination in vertebrate cells. Mol. Cell. Biol. 2003, 23, 5421-5430.
190. Hinz, J. M.; Nham, P. B.; Salazar, E. P.; Thompson, L. H. The Fanconi anemia pathway limits the severity of mutagenesis. DNA Repair (Amst.) 2006, 5, 875-884.
191. Zhang, N.; Liu, X.; Li, L.; Legerski, R. Double-strand breaks induce homologous recombinational repair of interstrand cross-links via cooperation of MSH2, ERCC1-XPF, REV3, and the Fanconi anemia pathway. DNA Repair (Amst.) 2007, 6, 1670-1678.
192. Sobeck, A.; Stone, S.; Costanzo, V.; de Graaf, B.; Reuter, T.; de Winter, J.; Wallisch, M.; Akkari, Y.; Olson, S.; Wang, W.; Joenje, H.; Christian, J. L.; Lupardus, P. J.; Cimprich, K. A.; Gautier, J.; Hoatlin, M. E. Fanconi anemia proteins are required to prevent accumulation of replication-associated DNA double-strand breaks. Mol. Cell. Biol. 2006, 26, 425-437.
193. Moynahan, M. E.; Pierce, A. J.; Jasin, M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 2001, 7, 263-272.
194. Lomonosov, M.; Anand, S.; Sangrithi, M.; Davies, R.; Venkitaraman, A. R. Stabilization of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev. 2003, 17, 3017-3022.
195. Howlett, N. G.; Taniguchi, T.; Durkin, S. G.; D'Andrea, A. D.; Glover, T. W. The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum. Mol. Genet. 2005, 14, 693-701.
196. Mi, J.; Kupfer, G. M. The Fanconi anemia core complex associates with chromatin during S phase. Blood 2005, 105, 759-766.
197. Luo, Y.; Leverson, J. D. New opportunities in chemosensitization and radiosensitization: modulating the DNA-damage response. Expert Rev. Anticancer Ther. 2005, 5, 333-342.
198. Wacheck, V.; Zangemeister-Wittke, U. Antisense molecules for targeted cancer therapy. Crit. Rev. Oncol. Hematol. 2006, 59, 65-73.
199. Takeshita, F.; Ochiya, T. Therapeutic potential of RNA interference against cancer. Cancer Sci. 2006, 97, 689-696.
200. Dykxhoorn, D. M.; Lieberman, J. Running interference: prospects and obstacles to using small interfering RNAs as small molecule drugs. Annu. Rev. Biomed. Eng. 2006, 8, 377-402.
201. Wang, Q.; Fan, S.; Eastman, A.; Worland, P. J.; Sausville, E. A.; O'Connor, P. M. UCN-01: a potent abrogator of G2 checkpoint function in cancer cells with disrupted p53. J. Natl. Cancer Inst. 1996, 88, 956-965.
202. Mandic, A.; Viktorsson, K.; Heiden, T.; Hansson, J.; Shoshan, M. C. The MEK1 inhibitor PD98059 sensitizes C8161 melanoma cells to cisplatin-induced apoptosis. Melanoma Res. 2001, 11, 11-19.
203. Beuvink, I.; Boulay, A.; Fumagalli, S.; Zilbermann, F.; Ruetz, S.; O'Reilly, T.; Natt, F.; Hall, J.; Lane, H. A.; Thomas, G. The mTOR inhibitor RAD001 sensitizes tumor cells to DNA-damaged induced apoptosis through inhibition of p21 translation. Cell 2005, 120, 747-759.
204. Chirnomas, D.; Taniguchi, T.; de la Vega, M.; Vaidya, A. P.; Vasserman, M.; Hartman, A. R.; Kennedy, R.; Foster, R.; Ma-honey, J.; Seiden, M. V.; D'Andrea, A. D. Chemosensitization to cisplatin by inhibitors of the Fanconi anemia/BRCA pathway. Mol. Cancer Ther. 2006, 5, 952-961.
205. Gallmeier, E.; Calhoun, E. S.; Rago, C.; Brody, J. R.; Cunningham, S. C.; Hucl, T.; Gorospe, M.; Kohli, M.; Lengauer, C.; Kern, S. E. Targeted disruption of FANCC and FANCG in human cancer provides a preclinical model for specific therapeutic options. Gastroenterology 2006, 130, 2145-2154.
206. Selvakumaran, M.; Pisarcik, D. A.; Bao, R.; Yeung, A. T.; Hamilton, T. C. Enhanced cisplatin cytotoxicity by disturbing the nucleotide excision repair pathway in ovarian cancer cell lines. Cancer Res. 2003, 63, 1311-1316.
207. Chen, Q.; Van der Sluis, P. C.; Boulware, D.; Hazlehurst, L. A.; Dalton, W. S. The FA/BRCA pathway is involved in melphalaninduced DNA interstrand cross-link repair and accounts for melphalan resistance in multiple myeloma cells. Blood 2005, 106, 698-705.
208. Ferrer, M.; de Winter, J. P.; Mastenbroek, D. C.; Curiel, D. T.; Gerritsen, W. R.; Giaccone, G.; Kruyt, F. A. Chemosensitizing tumor cells by targeting the Fanconi anemia pathway with an adenovirus overexpressing dominant-negative FANCA. Cancer Gene Ther. 2004, 11, 539-546.
209. Bartz, S. R.; Zhang, Z.; Burchard, J.; Imakura, M.; Martin, M.; Palmieri, A.; Needham, R.; Guo, J.; Gordon, M.; Chung, N.; Warrener, P.; Jackson, A. L.; Carleton, M.; Oatley, M.; Locco, L.; Santini, F.; Smith, T.; Kunapuli, P.; Ferrer, M.; Strulovici, B.; Friend, S. H.; Linsley, P. S. Small interfering RNA screens reveal enhanced cisplatin cytotoxicity in tumor cells having both BRCA network and TP53 disruptions. Mol. Cell. Biol. 2006, 26, 9377-9386.
210. Inagaki, M.; Watanabe, M.; Hidaka, H. N-(2-Aminoethyl)-5- isoquinolinesulfonamide, a newly synthesized protein kinase inhibitor, functions as a ligand in affinity chromatography. Purification of Ca2+-activated, phospholipid-dependent and other protein kinases. J. Biol. Chem. 1985, 260, 2922-2925.
211. Ito, M.; Tanabe, F.; Sato, A.; Takami, Y.; Shigeta, S. A potent inhibitor of protein kinase C inhibits natural killer activity. Int. J. Immunopharmacol. 1988, 10, 211-216.
212. Schultz, C.; Link, A.; Leost, M.; Zaharevitz, D. W.; Gussio, R.; Sausville, E. A.; Meijer, L.; Kunick, C. Paullones, a series of cyclin-dependent kinase inhibitors: synthesis, evaluation of CDK1/cyclin B inhibition, and in vitro antitumor activity. J. Med. Chem. 1999, 42, 2909-2919.
213. Sausville, E. A.; Johnson, J.; Alley, M.; Zaharevitz, D.; Senderowicz, A. M. Inhibition of CDKs as a therapeutic modality. Ann. N.Y. Acad. Sci. 2000, 910, 207-21; discussion 221-222.
214. Sharma, R. A.; Gescher, A. J.; Steward, W. P. Curcumin: the story so far. Eur. J. Cancer 2005, 41, 1955-1968.
215. McCabe, N.; Turner, N. C.; Lord, C. J.; Kluzek, K.; Bialkowska, A.; Swift, S.; Giavara, S.; O'Connor, M. J.; Tutt, A. N.; Zdzienicka, M. Z.; Smith, G. C.; Ashworth, A. Deficiency in the Repair of DNA Damage by Homologous Recombination and Sensitivity to Poly(ADP-Ribose) Polymerase Inhibition. Cancer Res. 2006, 66, 8109-8115.
216. Farmer, H.; McCabe, N.; Lord, C. J.; Tutt, A. N.; Johnson, D. A.; Richardson, T. B.; Santarosa, M.; Dillon, K. J.; Hickson, I.; Knights, C.; Martin, N. M.; Jackson, S. P.; Smith, G. C.; Ashworth, A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434, 917-921.
217. Bryant, H. E.; Schultz, N.; Thomas, H. D.; Parker, K. M.; Flower, D.; Lopez, E.; Kyle, S.; Meuth, M.; Curtin, N. J.; Helleday, T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434, 913-917.
218. Schmitt, C. A. Senescence, apoptosis and therapy-cutting the lifelines of cancer. Nat. Rev. Cancer 2003, 3, 286-295.
219. Mathew, C. G. Fanconi anaemia genes and susceptibility to cancer. Oncogene 2006, 25, 5875-5884.
220. Lyakhovich, A.; Surralles, J. Disruption of the Fanconi anemia/BRCA pathway in sporadic cancer. Cancer Lett. 2006, 232, 99-106.
221. Casey, G. The BRCA1 and BRCA2 breast cancer genes. Curr. Opin. Oncol. 1997, 9, 88-93.
222. Berwick, M.; Satagopan, J. M.; Ben-Porat, L.; Carlson, A.; Mah, K.; Henry, R.; Diotti, R.; Milton, K.; Pujara, K.; Landers, T.; Dev Batish, S.; Morales, J.; Schindler, D.; Hanenberg, H.; Hromas, R.; Levran, O.; Auerbach, A. D. Genetic heterogeneity among Fanconi anemia heterozygotes and risk of cancer. Cancer Res. 2007, 67, 9591-9596.
223. Cass, I.; Baldwin, R. L.; Varkey, T.; Moslehi, R.; Narod, S. A.; Karlan, B. Y. Improved survival in women with BRCA-associated ovarian carcinoma. Cancer 2003, 97, 2187-2195.
224. Chen, F.; Medhurst, A. L.; de Winter, J. P.; Waisfisz, Q.; Rooimans, M. A.; Oostra, A. B.; Meyer, S.; Zhang, K. J.; Xia, B.; Pals, G.; Arwert, F.; Zwaan, C. M.; Joenje, H. Apparent absence of BRCA2 protein in a proportion of acute myeloid leukemia cell lines. Leukemia 2004, 18, 1918-1920.
225. Tischkowitz, M. D.; Morgan, N. V.; Grimwade, D.; Eddy, C.; Ball, S.; Vorechovsky, I.; Langabeer, S.; Stoger, R.; Hodgson, S. V.; Mathew, C. G. Deletion and reduced expression of the Fanconi anemia FANCA gene in sporadic acute myeloid leukemia. Leukemia 2004, 18, 420-425.
226. Condie, A.; Powles, R. L.; Hudson, C. D.; Shepherd, V.; Bevan, S.; Yuille, M. R.; Houlston, R. S. Analysis of the Fanconi anaemia complementation group A gene in acute myeloid leukaemia. Leuk. Lymphoma 2002, 43, 1849-1853.
227. Taniguchi, T.; Tischkowitz, M.; Ameziane, N.; Hodgson, S. V.; Mathew, C. G.; Joenje, H.; Mok, S. C.; D'Andrea, A. D. Disruption of the Fanconi anemia-BRCA pathway in cisplatin-sensitive ovarian tumors. Nat. Med. 2003, 9, 568-574.
228. Narayan, G.; Arias-Pulido, H.; Nandula, S. V.; Basso, K.; Sugirtharaj, D. D.; Vargas, H.; Mansukhani, M.; Villella, J.; Meyer, L.; Schneider, A.; Gissmann, L.; Durst, M.; Pothuri, B.; Murty, V. V. Promoter hypermethylation of FANCF: disruption of Fanconi Anemia-BRCA pathway in cervical cancer. Cancer Res. 2004, 64, 2994-2997.
229. Marsit, C. J.; Liu, M.; Nelson, H. H.; Posner, M.; Suzuki, M.; Kelsey, K. T. Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: implications for treatment and survival. Oncogene 2004, 23, 1000-1004.
230. Neveling, K.; Kalb, R.; Florl, A. R.; Herterich, S.; Friedl, R.; Hoehn, H.; Hader, C.; Hartmann, F. H.; Nanda, I.; Steinlein, C.; Schmid, M.; Tonnies, H.; Hurst, C. D.; Knowles, M. A.; Hanenberg, H.; Schulz, W. A.; Schindler, D. Disruption of the FA/BRCA pathway in bladder cancer. Cytogenet. Genome Res. 2007, 118, 166-176.
231. Tischkowitz, M.; Ameziane, N.; Waisfisz, Q.; De Winter, J. P.; Harris, R.; Taniguchi, T.; D'Andrea, A.; Hodgson, S. V.; Mathew, C. G.; Joenje, H. Bi-allelic silencing of the Fanconi anaemia gene FANCF in acute myeloid leukaemia. Br. J. Haematol. 2003, 123, 469-471.
232. Potapova, A.; Hoffman, A. M.; Godwin, A. K.; Al-Saleem, T.; Cairns, P. Promoter hypermethylation of the PALB2 susceptibility gene in inherited and sporadic breast and ovarian cancer. Cancer Res. 2008, 68, 998-1002.
233. Gupta, R.; Sharma, S.; Sommers, J. A.; Kenny, M. K.; Cantor, S. B.; Brosh, R. M., Jr. FANCJ (BACH1) helicase forms DNA damage inducible foci with replication protein A and interacts physically and functionally with the single-stranded DNA-binding protein. Blood 2007, 110, 2390-2398.