Complementation of hypersensitivity to DNA interstrand crosslinking agents demonstrates that XRCC2 is a Fanconi anaemia gene

Journal of Medical Genetics

Volumn 53, Issue 10, 2016, Pages 672-680

  Park, Jung Young ^a   Virts, Elizabeth L ^b   Jankowska, Anna ^b   Wiek, Constanze ^c   Othman, Mohamed ^d   Chakraborty, Sujata C ^b   Vance, Gail H ^b   Alkuraya, Fowzan S ^e,f   Hanenberg, Helmut ^b,c,g   Andreassen, Paul R ^a,h  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

^e KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^f ALFAISAL UNIVERSITY   (Saudi Arabia)

^g UNIVERSITY HOSPITAL ESSEN   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; FORMALDEHYDE; MELPHALAN; MITOMYCIN; NUCLEAR PROTEIN; OLAPARIB; RAD51 PROTEIN; UNCLASSIFIED DRUG; XRCC2 PROTEIN; DNA ADDUCT; DNA BINDING PROTEIN; RAD51B PROTEIN, HUMAN; RAD51C PROTEIN, HUMAN; RAD51D PROTEIN, HUMAN; XRCC2 PROTEIN, HUMAN;

ARTICLE; CASE REPORT; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CHILD; CHROMOSOME BREAKAGE; COMPLEX FORMATION; CONTROLLED STUDY; DISEASE PREDISPOSITION; DNA CROSS LINKING; DRUG SENSITIVITY; FANCONI ANEMIA; GENE; GENE FREQUENCY; GENE MUTATION; GENETIC COMPLEMENTATION; HUMAN; HUMAN CELL; IONIZING RADIATION; MALE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; WILD TYPE; DNA ADDUCT; DNA DAMAGE; DNA REPAIR; GENETICS; METABOLISM; MUTATION;

CHILD; DNA ADDUCTS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; FANCONI ANEMIA; HUMANS; MALE; MUTATION;

EID: 84969945397     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmedgenet-2016-103847     Document Type: Article

References (51)

1. Auerbach AD. Fanconi anemia and its diagnosis. Mutat Res 2009;668:4-10.
2. Longerich S, Li J, Xiong Y, Sung P, Kupfer GM. Stress and DNA repair biology of the Fanconi anemia pathway. Blood 2014;124:2812-19.
3. Kutler DI, Singh B, Satagopan J, Batish SD, Berwick M, Giampietro PF, Hanenberg H, Auerbach AD. A 20-year perspective on the International Fanconi Anemia Registry (IFAR). Blood 2003;101:1249-56.
4. Faivre L, Guardiola P, Lewis C, Dokal I, Ebell W, Zatterale A, Altay C, Poole J, Stones D, Kwee ML, van Weel-Sipman M, Havenga C, Morgan N, de Winter J, Digweed M, Savoia A, Pronk J, de Ravel T, Jansen S, Joenje H, Gluckman E, Mathew CG. Association of complementation group and mutation type with clinical outcome in Fanconi anemia. European Fanconi Anemia Research Group. Blood 2000;96:4064-70.
5. Grompe M, D'Andrea A. Fanconi anemia and DNA repair. Human Mol Genet 2001;10:2253-9.
6. Andreassen PR, Ren K. Fanconi anemia proteins, DNA interstrand crosslink repair pathways, and cancer therapy. Curr Cancer Drug Targets 2009;9:101-17.
7. Hira A, Yoshida K, Sato K, Okuno Y, Shiraishi Y, Chiba K, Tanaka H, Miyano S, Shimamoto A, Tahara H, Ito E, Kojima S, Kurumizaka H, Ogawa S, Takata M, Yabe H, Yabe M. Mutations in the Gene Encoding the E2 Conjugating Enzyme UBE2T Cause Fanconi Anemia. Am J Hum Genet 2015;96:1001-7.
8. Rickman KA, Lach FP, Abhyankar A, Donovan FX, Sanborn EM, Kennedy JA, Sougnez C, Gabriel SB, Elemento O, Chandrasekharappa SC, Schindler D, Auerbach AD, Smogorzewska A. Deficiency of UBE2T, the E2 Ubiquitin Ligase Necessary for FANCD2 and FANCI Ubiquitination, Causes FA-T Subtype of Fanconi Anemia. Cell Rep 2015;12:35-41.
9. Virts EL, Jankowska A, Mackay C, Glaas MF, Wiek C, Kelich SL, Lottmann N, Kennedy FM, Marchal C, Lehnert E, Scharf RE, Dufour C, Lanciotti M, Farruggia P, Santoro A, Savasan S, Scheckenbach K, Schipper J, Wagenmann M, Lewis T, Leffak M, Farlow JL, Foroud TM, Honisch E, Niederacher D, Chakraborty SC, Vance GH, Pruss D, Timms KM, Lanchbury JS, Alpi AF, Hanenberg H. AluY-mediated germline deletion, duplication and somatic stem cell reversion in UBE2T defines a new subtype of Fanconi anemia. Human Mol Genet 2015;24:5093-108.
10. Sawyer SL, Tian L, Kähkönen M, Schwartzentruber J, Kircher M, University of Washington Centre for Mendelian Genetics, FORGE Canada Consortium, Majewski J, Dyment DA, Innes AM, Boycott KM, Moreau LA, Moilanen JS, Greenberg RA. Biallelic Mutations in BRCA1 Cause a New Fanconi Anemia Subtype. Cancer Discov 2015;5:135-42.
11. Wang AT, Kim T, Wagner JE, Conti BA, Lach FP, Huang AL, Molina H, Sanborn EM, Zierhut H, Cornes BK, Abhyankar A, Sougnez C, Gabriel SB, Auerbach AD, Kowalczykowski SC, Smorgorzewska A. A Dominant Mutation in Human RAD51 Reveals Its Function in DNA Interstrand Crosslink Repair Independent of Homologous Recombination. Mol Cell 2015;59:478-90.
12. Ameziane N, May P, Haitjema A, van de Vrugt HJ, van Rossum-Fikkert SE, Ristic D, Williams GJ, Balk J, Rockx D, Li H, Rooimans MA, Oostra AB, Velleuer E, Dietrich R, Bleijerveld OB, Maarten Altelaar AF, Meijers-Heijboer H, Joenje H, Glusman G, Roach J, Hood L, Galas D, Wyman C, Balling R, den Dunnen J, de Winter JP, Kanaar R, Gelinas R, Dorsman C. A novel Fanconi anaemia subtype associated with a dominant-negative mutation in RAD51. Nat Commun 2015;6:8829.
13. Walden H, Deans AJ. The Fanconi anemia DNA repair pathway: structural and functional insights into a complex disorder. Annu Rev Biophys 2014;43:257-78.
14. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, Grompe M, D'Andrea AD. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 2001;7:249-62.
15. Sims AE, Spiteri E, Sims RJ III, Arita AG, Lach FP, Landers T, Wurm M, Freund M, Neveling K, Hanenberg H, Auerbach AD, Huang TT. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat Struct Mol Biol 2007;14:564-7.
16. Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald ER III, Hurov KE, Luo J, Ballif BA, Gygi SP, Hofmann K, D'Andrea AD, Elledge SJ. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007;129:289-301.
17. Yuan SS, Lee SY, Chen G, Song M, Tomlinson GE, Lee EY. BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo. Cancer Res 1999;59:3547-51.
18. Vaz F, Hanenberg H, Schuster B, Barker K, Wiek C, Erven V, Neveling K, Endt D, Kesterton I, Autore F, Fraternali F, Freund M, Hartmann L, Grimwade D, Roberts RG, Schaal H, Mohammed S, Rahman N, Schindler D, Mathew CG. Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat Genet 2010;42:406-9.
19. Xia B, Dorsman JC, Ameziane N, de Vries Y, Rooimans MA, Sheng Q, Pals G, Errami A, Gluckman E, Llera J, Wang W, Livingston DM, Joenje H, de Winter JP. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat Genet 2007;39:159-61.
20. Shamseldin HE, Elfaki M, Alkuraya FS. Exome sequencing reveals a novel Fanconi group defined by XRCC2 mutation. J Med Genet 2012;49:184-6.
21. Zhang F, Fan Q, Ren K, Andreassen PR. PALB2 functionally connects the breast cancer susceptibility proteins BRCA1 and BRCA2. Mol Cancer Res 2009;7:1110-18.
22. Zhang F, Fan Q, Ren K, Andreassen PR. FANCJ/BRIP1 recruitment and regulation of FANCD2 in DNA damage responses. Chromosoma 2010;119:637-49.
23. Fan Q, Zhang F, Barrett B, Ren K, Andreassen PR. A role for monoubiquitinated FANCD2 at telomeres in ALT cells. Nucleic Acids Res 2009;37:1740-54.
24. Park JY, Singh TR, Nassar N, Zhang F, Freund M, Hanenberg H, Meetei AR, Andreassen PR. Breast cancer-associated missense mutants of the PALB2 WD40 domain, which directly binds RAD51C, RAD51 and BRCA2, disrupt DNA repair. Oncogene 2014;33:4803-12.
25. Andreassen PR, D'Andrea AD, Taniguchi T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev 2004;18:1958-63. 26 Oostra AB, Nieuwint AW, Joenje H, de Winter JP. Diagnosis of Fanconi anemia: chromosomal breakage analysis. Anemia 2012;2012:238731.
26. Oostra AB, Nieuwint AW, Joenje H, de Winter JP. Diagnosis of Fanconi anemia: chromosomal breakage analysis. Anemia 2012;2012:238731
27. Chandra S, Levran O, Jurickova I, Maas C, Kapur R, Schindler D, Henry R, Milton K, Batish SD, Cancelas JA, Hanenberg H, Auerbach AD, Williams DA. A rapid method for retrovirus-mediated identification of complementation groups in Fanconi anemia patients. Mol Ther 2005;12:976-84.
28. Joenje H, Levitus M, Waisfisz Q, D'Andrea A, Garcia-Higuera I, Pearson T, van Berkel CG, Rooimans MA, Morgan N, Mathew CG, Arwert F. Complementation analysis in Fanconi anemia: assignment of the reference FA-H patient to group A. Am J Hum Genet 2000;67:759-62.
29. Kupfer GM, D'Andrea AD. The effect of the Fanconi anemia polypeptide, FAC, upon p53 induction and G2 checkpoint regulation. Blood 1996;88:1019-25.
30. 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.
31. Buisson R, Dion-Côté AM, Coulombe Y, Launay H, Cai H, Stasiak AZ, Stasiak A, Xia B, Masson JY. Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination. Nat Struct Mol Biol 2010;17: 1247-54.
32. Ren X, Ji Z, McHale CM, Yuh J, Bersonda J, Tang M, Smith MT, Xhang L. The impact of FANCD2 deficiency on formaldehyde-induced toxicity in human lymphoblastoid cell lines. Arch Toxicol 2013;87:189-96.
33. Karanja KK, Lee EH, Hendrickson EA, Campbell JL. Preventing over-resection by DNA2 helicase/nuclease suppresses repair defects in Fanconi anemia cells. Cell Cycle 2014;13:1540-50.
34. Godthelp BC, Artwert F, Joenje H, Zdzienicka MZ. Impaired DNA damage-induced nuclear Rad51 foci formation uniquely characterizes Fanconi anemia group D1. Oncogene 2002;21:5002-5.
35. Masson JY, Tarsounas MC, Stasiak AZ, Stasiak A, Shah R, McIlwraith MJ, Benson FE, West SC. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev 2001;15:3296-307.
36. Liu N, Schild D, Thelen MP, Thompson LH. Involvement of Rad51C in two distinct protein complexes of Rad51 paralogs in human cells. Nucleic Acids Res 2002;30:1009-15.
37. Takata M, Sasaki MS, Tachiiri S, Fukushima T, Sonoda E, Schild D, Thompson LH, Takeda S. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol Cell Biol 2001;21:2858-66.
38. Fanconi G. Familial constitutional panmyelocytopathy, Fanconi's anemia (F.A.). I. Clinical aspects. Semin Hematol 1967;4:233-40.
39. Park JY, Zhang F, Andreassen PR. PALB2: the hub of a network of tumor suppressors involved in DNA damage responses. Biochim Biophys Acta 2014;1846:263-75.
40. Rosado IV, Langevin F, Crossan GP, Takata M, Patel KJ. Formaldehyde catabolism is essential in cells deficient for the Fanconi anemia DNA-repair pathway. Nat Struct Mol Biol 2011;18:1432-4.
41. Ridpath JR, Nakamura A, Tano K, Luke AM, Sonoda E, Arakawa H, Buerstedde JM, Gillespie DA, Sale JE, Yamazoe M, Bishop DK, Takata M, Takeda S, Watanabe M, Swenberg JA, Nakamura J. Cells deficient in the FANC/BRCA pathway are hypersensitive to plasma levels of formaldehyde. Cancer Res 2007;67:11117-22.
42. Ghosh S, Sur S, Yerram SR, Rago C, Bhunia AK, Hossain MZ, Paun BC, Ren YR, Iacobuzio-Donahue CA, Azad NA, Kern SE. Hypersensitivities for acetaldehyde and other agents among cancer cells null for clinically relevant Fanconi anemia genes. Am J Pathol 2014;184:260-70.
43. Garaycoechea JI, Crossan GP, Langevin F, Daly M, Arends MJ, Patel KJ. Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature 2012;489:571-5.
44. Dang Y, Low WK, Xu J, Gehring NH, Dietz HC, Romo D, Liu JO. Inhibition of nonsense-mediated mRNA decay by the natural product pateamine A through eukaryotic initiation factor 4AIII. J Biol Chem 2009;284:23613-21.
45. Schild D, Lio YC, Collins DW, Tsomondo T, Chen DJ. Evidence for simultaneous protein interactions between human Rad51 paralogs. J Biol Chem 2000;275:16443-9.
46. Chun J, Buechelmaier ES, Powell SN. Rad51 paralog complexes BCDX2 and CX3 act at different stages in the BRCA1-BRCA2-dependent homologous recombination pathway. Mol Cell Biol 2013;33:387-95.
47. Johnson RD, Liu N, Jasin M. Mammalian XRCC2 promotes the repair of DNA double-strand breaks by homologous recombination. Nature 1999;401:397-9. 48 Park DJ, Lesueur F, Nguyen-Dumont T, Pertesi M, Odefrey F, Hammet F, Neuhausen S, John EM, Andrulis IL, Terry MB, Daly M, Buys S, Le Calvez-Kelm F, Lonie A, Pope BJ, Tsimiklis H, Voegele C, Hilbers FM, Hoogerbrugge N, Barroso A, Osorio A, Breast Cancer Family Registry, Kathleen Cunningham Foundation Consortium for Research into Familial Breast Cancer, Giles GG, Devilee P, Benitez J, Hopper JL, Tavtigian SV, Goldgar DE, Southey MC. Rare mutations in XRCC2 increase the risk of breast cancer. Am J Hum Genet 2012;90:734-9.
48. Park DJ, Lesueur F, Nguyen-Dumont T, Pertesi M, Odefrey F, Hammet F, Neuhausen S, John EM, Andrulis IL, Terry MB, Daly M, Buys S, Le Calvez-Kelm F, Lonie A, Pope BJ, Tsimiklis H, Voegele C, Hilbers FM, Hoogerbrugge N, Barroso A, Osorio A, Breast Cancer Family Registry, Kathleen Cunningham Foundation Consortium for Research into Familial Breast Cancer, Giles GG, Devilee P, Benitez J, Hopper JL, Tavtigian SV, Goldgar DE, Southey MC. Rare mutations in XRCC2 increase the risk of breast cancer. Am J Hum Genet 2012;90:734-9
49. Meindl A, Hellebrand H, Wiek C, Erven C, Wappenschmidt B, Niederacher D, Freund M, Lichtner P, Hartmann L, Schaal H, Ramser J, Honisch E, Kubisch C, Wichmann HE, Kast K, Deissler H, Engel C, Muller-Myhsok B, Neveling K, Kiechle M, Mathew CG, Schindler D, Schmutzler RK, Hanenberg H. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet 2010;42:410-14.
50. Miki Y, Swensen J, Shattuck-Eidens D, Futreal PA, Harshman K, Tavtigian S, Liu Q, Cochran C, Bennett LM, Ding W, Bell R, Rosenthal JS, Hussey C, Tran T, McClure M, Frye C, Hattier T, Phelps R, Haugen-Strano A, Katcher H, Yakumo K, Gholami Z, Shaffer D, Stone S, Bayer S, Wray C, Bogden R, Dayananth P, Ward JH, Tonin P, Narod S, Bristow PK, Norris FH, Helvering LM, Morrison P, Rosteck P, Lai M, Barrett C, Lewis C, Neuhausen SL, Cannon-Albright LA, Goldgar D, Wiseman RW, Kamb A., Skolnick MH. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 1994;266:66-71.
51. Berwick M, Satagopan JM, 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 AD. Genetic heterogeneity among Fanconi anemia heterozygotes and risk of cancer. Cancer Res 2007;67:9591-6.