Targeting fanconi anemia/BRCA2 pathway defects in cancer: The significance of preclinical pharmacogenomic models

Clinical Cancer Research

Volumn 13, Issue 1, 2007, Pages 4-10

  Gallmeier, Eike ^a   Kern, Scott E ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA2 PROTEIN; CARBOPLATIN; FANCONI ANEMIA PROTEIN; MELPHALAN; MITOMYCIN C;

CANCER; CELL CYCLE REGULATION; GENE FUNCTION; GENE MUTATION; GENETIC DISORDER; HUMAN; NONHUMAN; PHARMACOGENOMICS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REVIEW; RNA INTERFERENCE; RNA TRANSLATION;

ANIMALS; BRCA2 PROTEIN; CELL LINE, TUMOR; CROSS-LINKING REAGENTS; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MODELS, BIOLOGICAL; MUTATION; NEOPLASMS; PHARMACOGENETICS;

EID: 33846333535     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-06-1637     Document Type: Review

References (102)

1. de Winter JP, Waisfisz Q, Rooimans MA, et al. The Fanconi anaemia group G gene FANCG is identical with XRCC9. Nat Genet 1998;20:281-3.
2. de Winter JP, Rooimans MA, van DerWeel L, et al. The Fanconi anaemia gene FANCF encodes a novel protein with homology to ROM. Nat Genet 2000;24:15-6.
3. de Winter JP, Leveille F, van Berkel CG, et al. Isolation of a cDNA representing the Fanconi anemia complementation group E gene. Am J Hum Genet 2000;67:1306-8.
4. Lo Ten Foe JR, Rooimans MA, Bosnoyan-Collins L, et al. Expression cloning of a cDNA for the major Fanconi anaemia gene, FAA. Nat Genet 1996;14:320-3.
5. Strathdee CA, Gavish H, Shannon WR, Buchwald M. Cloning of cDNAs for Fanconi's anaemia by functional complementation. Nature 1992;356:763-7.
6. Meetei AR, de Winter JP, Medhurst AL, et al. A novel ubiquitin ligase is deficient in Fanconi anemia. Nat Genet 2003;35:165-70. Epub 2003 Sep 14.
7. Meetei AR, Levitus M, Xue Y, et al. X-linked inheritance of Fanconi anemia complementation group B. Nat Genet 2004;36:1219-24.
8. Howlett NG, Taniguchi T, Olson S, et al. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 2002;297:606-9.
9. Timmers C, Taniguchi T, Hejna J, et al. Positional cloning of a novel Fanconi anemia gene, FANCD2. Mol Cell 2001;7:241-8.
10. Levitus M, Waisfisz Q, Godthelp BC, et al. The DNA helicase BRIP1 is defective in Fanconi anemia complementation group J. Nat Genet 2005;37:934-5.
11. Meetei AR, Medhurst AL, Ling C, 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.
12. Levitus M, Rooimans MA, Steltenpool J, et al. Heterogeneity in Fanconi anemia: evidence for 2 new genetic subtypes. Blood 2004;103:2498-503.
13. D'Andrea AD, Grompe M. The Fanconi anaemia/BRCA pathway. Nat Rev Cancer 2003;3:23-34.
14. van der Heijden MS, Yeo CJ, Hruban RH, Kern SE. Fanconi anemia gene mutations in young-onset pancreatic cancer. Cancer Res 2003;63:2585-8.
15. van der Heijden MS, Brody JR, Gallmeier E, et al. Functional defects in the Fanconi anemia pathway in pancreatic cancer cells. Am J Pathol 2004;165:651-7.
16. Couch FJ, Johnson MR, Rabe K, et al. Germ line Fanconi anemia complementation group C mutations and pancreatic cancer. Cancer Res 2005;65:383-6.
17. Marsit CJ, Liu M, Nelson HH, Posner M, Suzuki M, Kelsey KT. Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: implications for treatment and survival. Oncogene 2004;23:1000-4.
18. Narayan G, Arias-Pulido H, Nandula SV, et al. Promoter hypermethylation of FANCF: disruption of Fanconi anemia-BRCA pathway in cervical cancer. Cancer Res 2004;64:2994-7.
19. Taniguchi T, Tischkowitz M, Ameziane N, et al. Disruption of the Fanconi anemia-BRCA pathway in cisplatin-sensitive ovarian tumors. Nat Med 2003;9:568-74.
20. Fei P, Yin J, Wang W. New advances in the DNA damage response network of Fanconi anemia and BRCA proteins. FAAP95 replaces BRCA2 as the true FANCB protein. Cell Cycle 2005;4:80-6.
21. Thomashevski A, High AA, Drozd M, et al. The Fanconi anemia core complex forms four complexes of different sizes in different subcellular compartments. J Biol Chem 2004;279:26201-9.
22. Andreassen PR, D'Andrea AD, Taniguchi T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev 2004;18:1958-63.
23. Taniguchi T, Garcia-Higuera I, Xu B, et al. Convergence of the Fanconi anemia and ataxia telangiectasia signaling pathways. Cell 2002;109:459-72.
24. Wang X, D'Andrea AD. The interplay of Fanconi anemia proteins in the DNA damage response. DNA Repair (Amst) 2004;3:1063-9.
25. Pichierri P, Rosselli F. The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-2 pathways. EMBO J 2004;23:1178-87.
26. Garcia-Higuera I, Taniguchi T, et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 2001;7:249-62.
27. Wang X, Andreassen PR, D'Andrea AD. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol Cell Biol 2004;24:5850-62.
28. Montes de Oca R, Andreassen PR, Margossian SP, et al. Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 2005;105:1003-9.
29. 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;23:3154-63.
30. Nakanishi K, Taniguchi T, Ranganathan V, et al. Interaction of FANCD2 and NBS1 in the DNA damage response. Nat Cell Biol 2002;4:913-20.
31. Pichierri P, Averbeck D, Rosselli F. DNA cross-link-dependent RAD50/MRE11/NBS1 subnuclear assembly requires the Fanconi anemia C protein. Hum Mol Genet 2002;11:2531-46.
32. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M, DAndrea AD. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 2002;100:2414-20.
33. Hussain S, Wilson JB, Medhurst AL, et al. Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum Mol Genet 2004;13:1241-8.
34. Howlett NG, Taniguchi T, Durkin SG, D'Andrea AD, Glover TW. 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.
35. Levran O, Attwooll C, Henry RT, et al. The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia. Nat Genet 2005;37:931-3.
36. Bridge WL, Vandenberg CJ, Franklin RJ, Hiom K. The BRIP1 helicase functions independently of BRCA1 in the Fanconi anemia pathway for DNA crosslink repair. Nat Genet 2005;37:953-7.
37. Mosedale G, Niedzwiedz W, Alpi A, et al. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat Struct Mol Biol 2005;12:763-71.
38. Hahn SA, Hoque AT, Moskaluk CA, et al. Homozygous deletion map at 18q21.1 in pancreatic cancer. Cancer Res 1996;56:490-4.
39. McCabe N, Lord CJ, Tutt AN, Martin NM, Smith GC, Ashworth A. BRCA2-deficient CAPAN-1 cells are extremely sensitive to the inhibition of poly (ADP-ribose) polymerase: an issue of potency. Cancer Biol Ther 2005;4:934-6.
40. Gallmeier E, Kern SE. Absence of specific cell killing of the BRCA2-deficient human cancer cell line CAPAN1 by poly(ADP-ribose) polymerase inhibition. Cancer Biol Ther 2005;4:703-6.
41. Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly (ADP-ribose) polymerase. Nature 2005;434:913-7.
42. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005;434:917-21.
43. De Soto JA, Wang X, Tominaga Y, et al. The inhibition and treatment of breast cancer with poly (ADP-ribose) polymerase (PARP-1) inhibitors. Int J Biol Sci 2006;2:179-85.
44. De Soto JA, Deng CX. PARP-1 inhibitors: are they the long-sought genetically specific drugs for BRCA1/2-associated breast cancers? Int J Med Sci 2006;3:117-23.
45. Kalb R, Duerr M, Wagner M, et al. Lack of sensitivity of primary Fanconi's anemia fibroblasts to UV and ionizing radiation. Radiat Res 2004;161:318-25.
46. Gallmeier E, Calhoun ES, Rago C, et al. Targeted disruption of FANCC and FANCG in human cancer provides a preclinical model for specific therapeutic options. Gastroenterology 2006;130:2145-54.
47. Benson JD, Chen YN, Cornell-Kennon SA, et al. Validating cancer drug targets. Nature 2006;441:451-6.
48. Yamamoto K, Ishiai M, Matsushita N, et al. Fanconi anemia FANCG protein in mitigating radiation- and enzyme-induced DNA double-strand breaks by homologous recombination in vertebrate cells. Mol Cell Biol 2003;23:5421-30.
49. Sharan SK, Bradley A. Murine Brca2: sequence, map position, and expression pattern. Genomics 1997;40:234-41.
50. Cunningham SC, Gallmeier E, Hucl T, et al. A detrimental phenotype as a counterweight to the evolution of tumor-suppressor loss in tumorigenesis: explorations in MKK4-Null cancer cells. Cancer Res 2006;66:5560-4.
51. Van der Heijden MS, Brody JR, Elghalbzouri-Maghrani E, Zdzienicka MZ, Kern SE. Does tumorigenesis select for or against mutations of the DNA repair-associated genes BRCA2 and MRE11? Considerations from somatic mutations in microsatellite unstable (MSI) gastrointestinal cancers. BMC Genet 2006;7:3.
52. Chen M, Tomkins DJ, Auerbach W, et al. Inactivation of Fac in mice produces inducible chromosomal instability and reduced fertility reminiscent of Fanconi anaemia. Nat Genet 1996;12:448-51.
53. Cheng NC, van de Vrugt HJ, van der Valk MA, et al. Mice with a targeted disruption of the Fanconi anemia homolog Fanca. Hum Mol Genet 2000;9:1805-11.
54. Koomen M, Cheng NC, van de Vrugt HJ, et al. Reduced fertility and hypersensitivity to mitomycin C characterize Fancg/Xrcc9 null mice. Hum Mol Genet 2002;11:273-81.
55. Whitney MA, Royle G, Low MJ, et al. Germ cell defects and hematopoietic hypersensitivity to γ-interferon in mice with a targeted disruption of the Fanconi anemia C gene. Blood 1996;88:49-58.
56. Wong JC, Alon N, McKerlie C, Huang JR, Meyn MS, Buchwald M. Targeted disruption of exons 1 to 6 of the Fanconi Anemia group A gene leads to growth retardation, strain-specific microphthalmia, meiotic defects and primordial germ cell hypoplasia. Hum Mol Genet 2003;12:2063-76.
57. Yang Y, Kuang Y, De Oca RM, et al. Targeted disruption of the murine Fanconi anemia gene, Fancg/Xrcc9. Blood 2001;98:3435-40.
58. Bennett LM, McAllister KA, Blackshear PE, et al. BRCA2-null embryonic survival is prolonged on the BALB/c genetic background. Mol Carcinog 2000;28:174-83.
59. Connor F, Bertwistle D, Mee PJ, et al. Tumorigenesis and a DNA repair defect in mice with a truncating Brca2 mutation. Nat Genet 1997;17:423-30.
60. Friedman LS, Thistlethwaite FC, Patel KJ, et al. Thymic lymphomas in mice with a truncating mutation in Brca2. Cancer Res 1998;58:1338-43.
61. Ludwig T, Chapman DL, Papaioannou VE, Efstratiadis A. Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev 1997;11:1226-41.
62. McAllister KA, Bennett LM, Houle CD, et al. Cancer susceptibility of mice with a homozygous deletion in the COOH-terminal domain of the Brca2 gene. Cancer Res 2002;62:990-4.
63. Sharan SK, Morimatsu M, Albrecht U, et al. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 1997;386:804-10.
64. Suzuki A, de la Pompa JL, Hakem R, et al. Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev 1997;11:1242-52.
65. Moughtaling S, Timmers C, Noll M, et al. Epithelial cancer in Fanconi anemia complementation group D2 (Fancd2) knockout mice. Genes Dev 2003;17:2021-35. Epub 2003 Jul 2031.
66. Liu TX, Howlett NG, Deng M, et al. Knockdown of zebrafish Fancd2 causes developmental abnormalities via p53-dependent apoptosis. Dev Cell 2003;5:903-14.
67. Daniels MJ, Wang Y, Lee M, Venkitaraman AR. Abnormal cytokinesis in cells deficient in the breast cancer susceptibility protein BRCA2. Science 2004;306:876-9.
68. Goggins M, Hruban RH, Kern SE. BRCA2 is inactivated late in the development of pancreatic intraepithelial neoplasia: evidence and implications. Am J Pathol 2000;156:1767-71.
69. Goggins M, Schutte M, Lu J, et al. Germline BRCA2 gene mutations in patients with apparently sporadic pancreatic carcinomas. Cancer Res 1996;56:5360-4.
70. Hahn SA, Greenhalf B, Ellis I, et al. BRCA2 germline mutations in familial pancreatic carcinoma. J Natl Cancer Inst 2003;95:214-21.
71. Murphy KM, Brune KA, Griffin C, et al. Evaluation of candidate genes MAP2K4, MADH4, ACVR1B, BRCA2 in familial pancreatic cancer: deleterious BRCA2 mutations in 17%. Cancer Res 2002;62:3789-93.
72. Ozcelik H, Schmocker B, Di Nicola N, et al. Germline BRCA2 6174delT mutations in Ashkenazi Jewish pancreatic cancer patients. Nat Genet 1997;16:17-8.
73. Topaloglu O, Hurley PJ, Yildirim O, Civin CI, Bunz F. Improved methods for the generation of human gene knockout and knockin cell lines. Nucleic Acids Res 2005;33:e158.
74. Kohli M, Rago C, Lengauer C, Kinzler KW, Vogelstein B. Facile methods for generating human somatic cell gene knockouts using recombinant adenoassociated viruses. Nucleic Acids Res 2004;32:e3.
75. Hudson DF, Morrison C, Ruchaud S, Earnshaw WC. Reverse genetics of essential genes in tissue-culture cells: "dead cells talking." Trends Cell Biol 2002;12:281-7.
76. Arwert F, Rooimans MA, Westerveld A, Simons JW, Zdzienicka MZ. The Chinese hamster cell mutant V-H4 is homologous to Fanconi anemia (complementation group A). Cytogenet Cell Genet 1991;56:23-6.
77. Zdzienicka MZ, Simons JW. Mutagen-sensitive cell lines are obtained with a high frequency in V79 Chinese hamster cells. Mutat Res 1987;178:235-44.
78. Overkamp WJ, Rooimans MA, Neuteboom I, Telleman P, Arwert F, Zdzienicka MZ. Genetic diversity of mitomycin C-hypersensitive Chinese hamster cell mutants: a new complementation group with chromosomal instability. Somat Cell Mol Genet 1993;19:431-7.
79. Kraakman-van der Zwei M, Overkamp WJ, van Lange RE, et al. Brca2 (XRCC11) deficiency results in radioresistant DNA synthesis and a higher frequency of spontaneous deletions. Mol Cell Biol 2002;22:669-79.
80. Liu N, Lamerdin JE, Tucker JD, et al. The human XRCC9 gene corrects chromosomal instability and mutagen sensitivities in CHO UV40 cells. Proc Natl Acad Sci U S A 1997;94:9232-7.
81. Wilson JB, Johnson MA, Stuckert AP, et al. The Chinese hamster FANCG/XRCC9 mutant NM3 fails to express the monoubiquitinated form of the FANCD2 protein, is hypersensitive to a range of DNA damaging agents and exhibits a normal level of spontaneous sister chromatid exchange. Carcinogenesis 2001;22:1939-46.
82. Wiegant WW, Overmeer RM, Godthelp BC, van Buul PP, Zdzienicka MZ. Chinese hamster cell mutant, V-C8, a model for analysis of Brca2 function. Mutat Res 2006;600:79-88.
83. Harborth J, Elbashir SM, Bechert K, Tuschl T, Weber K. Identification of essential genes in cultured mammalian cells using small interfering RNAs. J Cell Sci 2001;114:4557-65.
84. Birmingham A, Anderson EM, Reynolds A, et al. 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat Methods 2006;3:199-204.
85. Fedorov Y, Anderson EM, Birmingham A, et al. Off-target effects by siRNA can induce toxic phenotype. RNA 2006;12:1188-96.
86. van der Heijden MS, Brody JR, Dezentje DA, et al. In vivo therapeutic responses contingent upon Fanconi/BRCA2 tumor status. Clin Cancer Res 2005;11:7508-15.
87. Abbott DW, Freeman ML, Holt JT. Double-strand break repair deficiency and radiation sensitivity in BRCA2 mutant cancer cells. J Natl Cancer Inst 1998;90:978-85.
88. Wang SC, Shao R, Pao AY, Zhang S, Hung MC, Su LK. Inhibition of cancer cell growth by BRCA2. Cancer Res 2002;62:1311-4.
89. Wang H, Han H, Von Hoff DD. Targeting a loss-of-function mutation in the BRCA2 gene in pancreatic cancer. In: 97th AACR Annual Meeting, Washington DC, April 1-5, 2006.
90. Warren M, Lord CJ, Masabanda J, Griffin D, Ashworth A. Phenotypic effects of heterozygosity for a BRCA2 mutation. Hum Mol Genet 2003;12:2645-56.
91. Hatanaka A, Yamazoe M, Sale JE, et al. Similar effects of Brca2 truncation and Rad51 paralog deficiency on immunoglobulin V gene diversification in DT40 cells support an early role for Rad51 paralogs in homologous recombination. Mol Cell Biol 2005;25:1124-34.
92. Ludwig T, Fisher P, Murty V, Efstratiadis A. Development of mammary adenocarcinomas by tissue-specific knockout of Brca2 in mice. Oncogene 2001;20:3937-48.
93. Morgan NV, Tipping AJ, Joenje H, Mathew CG. High frequency of large intragenic deletions in the Fanconi anemia group A gene. Am J Hum Genet 1999;65:1330-41.
94. Tischkowitz M, Ameziane N, Waisfisz Q, et al. Biallelic silencing of the Fanconi anaemia gene FANCF in acute myeloid leukaemia. Br J Haematol 2003;123:469-71.
95. Druker BJ, Tamura S, Buchdunger E, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996;2:561-6.
96. Druker BJ, Talpaz M, Resta DJ, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001;344:1031-7.
97. Lynch TJ, Bell DW, Sordella R, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004;350:2129-39.
98. Paez JG, Janne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500.
99. Gurtan AM, D'Andrea AD. Dedicated to the core: understanding the Fanconi anemia complex. DNA Repair (Amst) 2006;5:1119-25.
100. van Zeeburg HJ, Snijders PJ, Pals G, et al. Generation and molecular characterization of head and neck squamous cell lines of Fanconi anemia patients. Cancer Res 2005;65:1271-6.
101. Ikeda H, Matsushita M, Waisfisz Q, et al. Genetic reversion in an acute myelogenous leukemia cell line from a Fanconi anemia patient with biallelic mutations in BRCA2. Cancer Res 2003;63:2688-94.
102. Meyer S, Fergusson WD, Oostra AB, et al. A cross-linker-sensitive myeloid leukemia cell line from a 2-year-old boy with severe Fanconi anemia and biallelic FANCD1/BRCA2 mutations. Genes Chromosomes Cancer 2005;42:404-15.