Recent discoveries in the molecular pathogenesis of the inherited bone marrow failure syndrome Fanconi anemia

Blood Reviews

Volumn 31, Issue 3, 2017, Pages 93-99

  Mamrak, Nicholas E ^a   Shimamura, Akiko ^b   Howlett, Niall G ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

DNA repair; Fanconi anemia; Genome instability; Homologous recombination; Ubiquitin

Indexed keywords

BRCA1 PROTEIN; RAD51 PROTEIN; BRCA1 PROTEIN, HUMAN; DNA BINDING PROTEIN; FANCONI ANEMIA PROTEIN; MAD2L2 PROTEIN, HUMAN; PROTEIN MAD2; UBE2T PROTEIN, HUMAN; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; XRCC2 PROTEIN, HUMAN;

BONE MARROW DEPRESSION; CAUSAL ATTRIBUTION; CELL LINEAGE; DNA REPAIR; FANCONI ANEMIA; FANCR GENE; FANCS GENE; FANCT GENE; FANCU GENE; FANCV GENE; GENE; GENE FUNCTION; GENE MUTATION; GENETIC CODE; GENOMIC INSTABILITY; HUMAN; MOLECULAR PATHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAD51 GENE; REV7 GENE; REVIEW; TUMOR SUPPRESSOR GENE; UBE2T GENE; UPREGULATION; XRCC2 GENE; BONE MARROW; DNA DAMAGE; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; MUTATION; PATHOLOGY; SIGNAL TRANSDUCTION;

BONE MARROW; BRCA1 PROTEIN; DNA DAMAGE; DNA-BINDING PROTEINS; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMANS; MAD2 PROTEINS; MUTATION; RAD51 RECOMBINASE; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84994391673     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2016.10.002     Document Type: Review

References (103)

1. Lobitz, S., Velleuer, E., Guido Fanconi (1892–1979): a jack of all trades. Nat Rev Cancer 6 (2006), 893–898.
2. Fanconi, G., Familiare, infantile, perniziosaartige anamie (pernizioses blutbild und konstitution). Jahrb Kinderheilkd 117 (1927), 257–280.
3. Fanconi Anemia Research Fund, Inc, Fanconi anemia: guidelines for diagnosis and management. 2014, 1–429.
4. Rosenberg, P.S., Tamary, H., Alter, B.P., How high are carrier frequencies of rare recessive syndromes? Contemporary estimates for Fanconi anemia in the United States and Israel. Am J Med Genet A 155a (2011), 1877–1883.
5. Alter, B.P., Fanconi anemia and the development of leukemia. Best Pract Res Clin Haematol 27 (2014), 214–221.
6. Alter, B.P., Greene, M.H., Velazquez, I., Rosenberg, P.S., Cancer in Fanconi anemia. Blood, 101, 2003, 2072.
7. Strathdee, C.A., Duncan, A.M., Buchwald, M., Evidence for at least four Fanconi anaemia genes including FACC on chromosome 9. Nat Genet 1 (1992), 196–198.
8. Strathdee, C.A., Gavish, H., Shannon, W.R., Buchwald, M., Cloning of cDNAs for Fanconi's anaemia by functional complementation. Nature 356 (1992), 763–767.
9. Positional cloning of the Fanconi anaemia group A gene. Nat Genet, 14, 1996, 324–328.
10. Lo Ten Foe, J.R., Rooimans, M.A., Bosnoyan-Collins, L., et al. Expression cloning of a cDNA for the major Fanconi anemia gene, FAA. Nat Genet 14 (1996), 320–323.
11. de Winter, J.P., Waisfisz, Q., Rooimans, M.A., van Berkel, C.G.M., Bosnoyan-Collins, L., Alon, N., et al. The Fanconi anaemia group G gene is identical with human XRCC9. Nat Genet 20 (1998), 281–283.
12. de Winter, J.P., Leveille, F., van Berkel, C.G.M., Rooimans, M.A., van der Weel, L., Steltenpool, J., et al. Isolation of a cDNA representing the Fanconi anemia complementation group E gene. Am J Hum Genet 67 (2000), 1306–1308.
13. de Winter, J.P., Rooimans, M.A., van der Weel, L., Van Berkel, C.M., Alon, N., Bosnoyan-Collins, L., et al. The Fanconi anemia complementation gene FANCF encodes a novel protein with homology to ROM. Nat Genet 24 (2000), 15–16.
14. Timmers, C., Taniguchi, T., Hejna, J., Reifsteck, C., Lucas, L., Bruun, D., et al. Positional cloning of a novel Fanconi anemia gene, FANCD2. Mol Cell 7 (2001), 241–248.
15. Joenje, H., Levitus, M., Waisfisz, Q., D'Andrea, A., Garcia-Higuera, I., Pearson, T., et al. Complementation analysis in Fanconi anemia: assignment of the reference FA-H patient to group A. Am J Hum Genet 67 (2000), 759–762.
16. Joenje, H., Oostra, A.B., Wijker, M., di Summa, F.M., van Berkel, C.G., Rooimans, M.A., et al. Evidence for at least eight Fanconi anemia genes. Am J Hum Genet 61 (1997), 940–944.
17. Kottemann, M.C., Smogorzewska, A., Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493 (2013), 356–363.
18. Walden, H., Deans, A.J., The Fanconi anemia DNA repair pathway: structural and functional insights into a complex disorder. Annu Rev Biophys 43 (2014), 257–278.
19. Auerbach, A.D., Fanconi anemia diagnosis and the diepoxybutane (DEB) test. Exp Hematol 21 (1993), 731–733.
20. Alpi, A., Langevin, F., Mosedale, G., Machida, Y.J., Dutta, A., Patel, K.J., UBE2T, the Fanconi anemia core complex, and FANCD2 are recruited independently to chromatin: a basis for the regulation of FANCD2 monoubiquitination. Mol Cell Biol 27 (2007), 8421–8430.
21. Gurtan, A.M., D'Andrea, A.D., Dedicated to the core: understanding the Fanconi anemia complex. DNA Repair (Amst) 5 (2006), 1119–1125.
22. Huang, Y., Leung, J.W., Lowery, M., Matsushita, N., Wang, Y., Shen, X., et al. Modularized functions of the Fanconi anemia core complex. Cell Rep 7 (2014), 1849–1857.
23. Rajendra, E., Oestergaard, V.H., Langevin, F., Wang, M., Dornan, G.L., Patel, K.J., et al. The genetic and biochemical basis of FANCD2 monoubiquitination. Mol Cell 54 (2014), 858–869.
24. Ciccia, A., Ling, C., Coulthard, R., Yan, Z., Xue, Y., Meetei, A.R., et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 25 (2007), 331–343.
25. Coulthard, R., Deans, A.J., Swuec, P., Bowles, M., Costa, A., West, S.C., et al. Architecture and DNA recognition elements of the Fanconi anemia FANCM–FAAP24 complex. Structure 21 (2013), 1648–1658.
26. 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 111 (2008), 5215–5222.
27. Singh, T.R., Saro, D., Ali, A.M., Zheng, X.F., Du, C.H., Killen, M.W., et al. MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol Cell 37 (2010), 879–886.
28. Alpi, A.F., Pace, P.E., Babu, M.M., Patel, K.J., Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol Cell 32 (2008), 767–777.
29. Machida, Y.J., Machida, Y., Chen, Y., Gurtan, A.M., Kupfer, G.M., D'Andrea, A.D., et al. UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation. Mol Cell 23 (2006), 589–596.
30. Meetei, A.R., de Winter, J.P., Medhurst, A.L., Wallisch, M., Waisfisz, Q., van de Vrugt, H.J., et al. A novel ubiquitin ligase is deficient in Fanconi anemia. Nat Genet 35 (2003), 165–170.
31. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7 (2001), 249–262.
32. Sims, A.E., Spiteri, E., Sims, R.J. III, Arita, A.G., Lach, F.P., Landers, T., et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat Struct Mol Biol 14 (2007), 564–567.
33. Smogorzewska, A., Matsuoka, S., Vinciguerra, P., McDonald, E.R. III, Hurov, K.E., Luo, J., et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129 (2007), 289–301.
34. Joo, W., Xu, G., Persky, N.S., Smogorzewska, A., Rudge, D.G., Buzovetsky, O., et al. Structure of the FANCI–FANCD2 complex: insights into the Fanconi anemia DNA repair pathway. Science 333 (2011), 312–316.
35. Hicke, L., Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2 (2001), 195–201.
36. 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 100 (2002), 2414–2420.
37. Wang, X., Andreassen, P.R., D'Andrea, A.D., Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol Cell Biol 24 (2004), 5850–5862.
38. Kim, Y., Spitz, G.S., Veturi, U., Lach, F.P., Auerbach, A.D., Smogorzewska, A., Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 121 (2013), 54–63.
39. Klein Douwel, D., Boonen, R.A., Long, D.T., Szypowska, A.A., Raschle, M., Walter, J.C., et al. XPF-ERCC1 acts in unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol Cell 54 (2014), 460–471.
40. Kratz, K., Schopf, B., Kaden, S., Sendoel, A., Eberhard, R., Lademann, C., et al. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142 (2010), 77–88.
41. MacKay, C., Declais, A.C., Lundin, C., Agostinho, A., Deans, A.J., MacArtney, T.J., et al. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142 (2010), 65–76.
42. Murina, O., von Aesch, C., Karakus, U., Ferretti, L.P., Bolck, H.A., Hanggi, K., et al. FANCD2 and CtIP cooperate to repair DNA interstrand crosslinks. Cell Rep 7 (2014), 1030–1038.
43. Smogorzewska, A., Desetty, R., Saito, T.T., Schlabach, M., Lach, F.P., Sowa, M.E., et al. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39 (2010), 36–47.
44. Unno, J., Itaya, A., Taoka, M., Sato, K., Tomida, J., Sakai, W., et al. FANCD2 binds CtIP and regulates DNA-end resection during DNA interstrand crosslink repair. Cell Rep 7 (2014), 1039–1047.
45. Budzowska, M., Graham, T.G., Sobeck, A., Waga, S., Walter, J.C., Regulation of the Rev1–pol zeta complex during bypass of a DNA interstrand cross-link. EMBO J 34 (2015), 1971–1985.
46. Zhang, J., Walter, J.C., Mechanism and regulation of incisions during DNA interstrand cross-link repair. DNA Repair (Amst) 19 (2014), 135–142.
47. Haber, J.E., Partners and pathways: repairing a double-strand break. Trends Genet 16 (2000), 259–264.
48. Mazon, G., Mimitou, E.P., Symington, L.S., SnapShot: homologous recombination in DNA double-strand break repair. Cell, 142, 2011, 646 [e1].
49. Boulton, S.J., Cellular functions of the BRCA tumour-suppressor proteins. Biochem Soc Trans 34 (2006), 633–645.
50. Park, J.Y., Zhang, F., Andreassen, P.R., PALB2: the hub of a network of tumor suppressors involved in DNA damage responses. Biochim Biophys Acta 2014 (1846), 263–275.
51. Suwaki, N., Klare, K., Tarsounas, M., RAD51 paralogs: roles in DNA damage signalling, recombinational repair and tumorigenesis. Semin Cell Dev Biol 22 (2011), 898–905.
52. Adamo, A., Collis, S.J., Adelman, C.A., Silva, N., Horejsi, Z., Ward, J.D., et al. Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol Cell 39 (2010), 25–35.
53. Lieber, M.R., Wilson, T.E., SnapShot: nonhomologous DNA end joining (NHEJ). Cell, 142, 2010 496–496.e1.
54. Pace, P., Mosedale, G., Hodskinson, M.R., Rosado, I.V., Sivasubramaniam, M., Patel, K.J., Ku70 corrupts DNA repair in the absence of the Fanconi anemia pathway. Science 329 (2010), 219–223.
55. Hershko, A., Ciechanover, A., The ubiquitin system. Annu Rev Biochem 67 (1998), 425–479.
56. Longerich, S., San Filippo, J., Liu, D., Sung, P., FANCI binds branched DNA and is mono-ubiquitinated by UBE2T–FANCL. J Biol Chem 284 (2009), 23182–23186.
57. Zhang, Q.H., Ye, M., Wu, X.Y., Ren, S.X., Zhao, M., Zhao, C.J., et al. Cloning and functional analysis of cDNAs with open reading frames for 300 previously undefined genes expressed in CD34 + hematopoietic stem/progenitor cells. Genome Res 10 (2000), 1546–1560.
58. Corson, T.W., Huang, A., Tsao, M.S., Gallie, B.L., KIF14 is a candidate oncogene in the 1q minimal region of genomic gain in multiple cancers. Oncogene 24 (2005), 4741–4753.
59. Hira, A., Yoshida, K., Sato, K., Okuno, Y., Shiraishi, Y., Chiba, K., et al. Mutations in the gene encoding the E2 conjugating enzyme UBE2T cause Fanconi anemia. Am J Hum Genet 96 (2015), 1001–1007.
60. Hodson, C., Purkiss, A., Miles, J.A., Walden, H., Structure of the human FANCL RING-Ube2T complex reveals determinants of cognate E3–E2 selection. Structure 22 (2014), 337–344.
61. Rickman, K.A., Lach, F.P., Abhyankar, A., Donovan, F.X., Sanborn, E.M., Kennedy, J.A., et al. Deficiency of UBE2T, the E2 ubiquitin ligase necessary for FANCD2 and FANCI ubiquitination, causes FA-T subtype of Fanconi anemia. Cell Rep 12 (2015), 35–41.
62. Virts, E.L., Jankowska, A., MacKay, C., Glaas, M.F., Wiek, C., Kelich, S.L., et al. AluY-mediated germline deletion, duplication and somatic stem cell reversion in UBE2T defines a new subtype of Fanconi anemia. Hum Mol Genet 24 (2015), 5093–5108.
63. Sharma, S., Helchowski, C.M., Canman, C.E., The roles of DNA polymerase zeta and the Y family DNA polymerases in promoting or preventing genome instability. Mutat Res 743–744 (2013), 97–110.
64. Tomida, J., Takata, K., Lange, S.S., Schibler, A.C., Yousefzadeh, M.J., Bhetawal, S., et al. REV7 is essential for DNA damage tolerance via two REV3L binding sites in mammalian DNA polymerase zeta. Nucleic Acids Res 43 (2015), 1000–1011.
65. Okada, T., Sonoda, E., Yoshimura, M., Kawano, Y., Saya, H., Kohzaki, M., et al. Multiple roles of vertebrate REV genes in DNA repair and recombination. Mol Cell Biol 25 (2005), 6103–6111.
66. Bluteau, D., Masliah-Planchon, J., Clairmont, C., Rousseau, A., Ceccaldi, R., Dubois d'Enghien, C., et al. Biallelic inactivation of REV7 is associated with Fanconi anemia. J Clin Invest 126 (2016), 3580–3584.
67. Hall, J.M., Lee, M.K., Newman, B., Morrow, J.E., Anderson, L.A., Huey, B., et al. Linkage of early-onset familial breast cancer to chromosome 17q21. Science 250 (1990), 1684–1689.
68. Miki, Y., Swensen, J., Shattuck-Eidens, D., Futreal, P.A., Harshman, K., Tavtigian, S., et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266 (1994), 66–71.
69. Domchek, S.M., Tang, J., Stopfer, J., Lilli, D.R., Hamel, N., Tischkowitz, M., et al. Biallelic deleterious BRCA1 mutations in a woman with early-onset ovarian cancer. Cancer Discov 3 (2013), 399–405.
70. Yu, X., Chini, C.C., He, M., Mer, G., Chen, J., The BRCT domain is a phospho-protein binding domain. Science 302 (2003), 639–642.
71. Sawyer, S.L., Tian, L., Kahkonen, M., Schwartzentruber, J., Kircher, M., University of Washington Centre for Mendelian G, et al. Biallelic mutations in BRCA1 cause a new Fanconi anemia subtype. Cancer Discov 5 (2015), 135–142.
72. Coquelle, N., Green, R., Glover, J.N., Impact of BRCA1 BRCT domain missense substitutions on phosphopeptide recognition. Biochemistry 50 (2011), 4579–4589.
73. Cantor, S.B., Bell, D.W., Ganesan, S., Kass, E.M., Drapkin, R., Grossman, S., et al. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 105 (2001), 149–160.
74. Chen, J., Silver, D.P., Walpita, D., Cantor, S.B., Gazdar, A.F., Tomlinson, G., et al. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol Cell 2 (1998), 317–328.
75. Chen, J.J., Silver, D., Cantor, S., Livingston, D.M., Scully, R., BRCA1, BRCA2, and Rad51 operate in a common DNA damage response pathway. Cancer Res 59 (1999), 1752s–1756s.
76. Fullbright, G., Rycenga, H.B., Gruber, J.D., Long, D.T., p97 promotes a conserved mechanism of helicase unloading during DNA crosslink repair. Mol Cell Biol, 2016 [Epub ahead of print].
77. Bunting, S.F., Callen, E., Kozak, M.L., Kim, J.M., Wong, N., Lopez-Contreras, A.J., et al. BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair. Mol Cell 46 (2012), 125–135.
78. Bunting, S.F., Callen, E., Wong, N., Chen, H.T., Polato, F., Gunn, A., et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141 (2010), 243–254.
79. Chen, Z., Yang, H., Pavletich, N.P., Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453 (2008), 489–494.
80. San Filippo, J., Sung, P., Klein, H., Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77 (2008), 229–257.
81. Abe, H., Wada, M., Kohno, K., Kuwano, M., Altered drug sensitivities to anticancer agents in radiation-sensitive DNA repair deficient yeast mutants. Anticancer Res 14 (1994), 1807–1810.
82. Slupianek, A., Schmutte, C., Tombline, G., Nieborowska-Skorska, M., Hoser, G., Nowicki, M.O., et al. BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol Cell 8 (2001), 795–806.
83. Dong, Y., Hakimi, M.A., Chen, X., Kumaraswamy, E., Cooch, N.S., Godwin, A.K., et al. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol Cell 12 (2003), 1087–1099.
84. Lim, D.S., Hasty, P., A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol Cell Biol 16 (1996), 7133–7143.
85. Ameziane, N., May, P., Haitjema, A., van de Vrugt, H.J., van Rossum-Fikkert, S.E., Ristic, D., et al. A novel Fanconi anaemia subtype associated with a dominant-negative mutation in RAD51. Nat Commun, 6, 2015, 8829.
86. Wang, A.T., Kim, T., Wagner, J.E., Conti, B.A., Lach, F.P., Huang, A.L., et al. A dominant mutation in human RAD51 reveals its function in DNA interstrand crosslink repair independent of homologous recombination. Mol Cell 59 (2015), 478–490.
87. Hashimoto, Y., Chaudhuri, A.R., Lopes, M., Costanzo, V., Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nat Struct Mol Biol 17 (2010), 1305–1311.
88. Long, D.T., Raschle, M., Joukov, V., Walter, J.C., Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333 (2011), 84–87.
89. Schlacher, K., Wu, H., Jasin, M., A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 22 (2012), 106–116.
90. Park, J.Y., Virts, E.L., Jankowska, A., Wiek, C., Othman, M., Chakraborty, S.C., et al. Complementation of hypersensitivity to DNA interstrand crosslinking agents demonstrates that XRCC2 is a Fanconi anaemia gene. J Med Genet 53:10 (2016), 672–680 [Epub ahead of print].
91. Masson, J.Y., Tarsounas, M.C., Stasiak, A.Z., Stasiak, A., Shah, R., McIlwraith, M.J., et al. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev 15 (2001), 3296–3307.
92. Takata, M., Sasaki, M.S., Tachiiri, S., Fukushima, T., Sonoda, E., Schild, D., et al. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol Cell Biol 21 (2001), 2858–2866.
93. Deans, B., Griffin, C.S., Maconochie, M., Thacker, J., Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice. EMBO J 19 (2000), 6675–6685.
94. Shamseldin, H.E., Elfaki, M., Alkuraya, F.S., Exome sequencing reveals a novel Fanconi group defined by XRCC2 mutation. J Med Genet 49 (2012), 184–186.
95. Park, D.J., Lesueur, F., Nguyen-Dumont, T., Pertesi, M., Odefrey, F., Hammet, F., et al. Rare mutations in XRCC2 increase the risk of breast cancer. Am J Hum Genet 90 (2012), 734–739.
96. Erkko, H., Xia, B., Nikkila, J., Schleutker, J., Syrjakoski, K., Mannermaa, A., et al. A recurrent mutation in PALB2 in Finnish cancer families. Nature 446 (2007), 316–319.
97. Futreal, P.A., Liu, Q., Shattuck-Eidens, D., Cochran, C., Harshman, K., Tavtigian, S., et al. BRCA1 mutations in primary breast and ovarian carcinomas. Science 266 (1994), 120–122.
98. Lux, M.P., Fasching, P.A., Beckmann, M.W., Hereditary breast and ovarian cancer: review and future perspectives. J Mol Med 84 (2006), 16–28.
99. Meindl, A., Hellebrand, H., Wiek, C., Erven, V., Wappenschmidt, B., Niederacher, D., et al. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet 42 (2010), 410–414.
100. Melchor, L., Benitez, J., The complex genetic landscape of familial breast cancer. Hum Genet 132 (2013), 845–863.
101. Rahman, N., Seal, S., Thompson, D., Kelly, P., Renwick, A., Elliott, A., et al. PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat Genet 39 (2007), 165–167.
102. Seal, S., Thompson, D., Renwick, A., Elliott, A., Kelly, P., Barfoot, R., et al. Truncating mutations in the Fanconi anemia J gene BRIP1 are low-penetrance breast cancer susceptibility alleles. Nat Genet 38 (2006), 1239–1241.
103. Vaz, F., Hanenberg, H., Schuster, B., Barker, K., Wiek, C., Erven, V., et al. Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat Genet 42 (2010), 406–409.