Evidence for complete epistasis of null mutations in murine Fanconi anemia genes Fanca and Fancg

DNA Repair

Volumn 10, Issue 12, 2011, Pages 1252-1261

  Van de Vrugt, Henri J ^a,b   Koomen, Mireille ^a   Bakker, Sietske ^b   Berns, Mariska A D ^a   Cheng, Ngan Ching ^a   van der Valk, Martin A ^b   de Vries, Yne ^a   Rooimans, Martin A ^a   Oostra, Anneke B ^a   Hoatlin, Maureen E ^c   te Riele, Hein ^b   Joenje, Hans ^a   Arwert, Fré ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Crosslink repair; Fanca; Fancg; Fanconi anemia; Knockout mice

Indexed keywords

KU 0058948; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL HYPERPLASIA; CELL SURVIVAL; CELL VACUOLE; CHROMOSOME BREAKAGE; DNA REPAIR; DRUG EFFECT; ENZYME ACTIVITY; EPISTASIS; FANCA GENE; FANCG GENE; FANCONI ANEMIA; FEMALE; FEMALE FERTILITY; FOLLICLE CYST; GENE; GENE FREQUENCY; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; GENOMICS; GENOTYPE; GONAD; LEYDIG CELL; MALE; MALE FERTILITY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; OVARY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION; SERTOLI CELL; STEM CELL; TESTIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BONE MARROW CELLS; CELL LINE; CELL NUCLEUS; CHROMOSOME BREAKAGE; EMBRYO, MAMMALIAN; EPISTASIS, GENETIC; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP A PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP G PROTEIN; FEMALE; FERTILITY; FIBROBLASTS; FLUOROBENZENES; HEMATOLOGIC TESTS; HUMANS; MALE; MICE; MUTATION; OVARY; PHTHALAZINES; POLY(ADP-RIBOSE) POLYMERASES; STEM CELLS; TESTIS;

MURINAE; MUS;

EID: 82555168322     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2011.09.015     Document Type: Article

References (42)

1. van de Vrugt H.J., Grompe M. Fanconi anemia. Inborn Errors of Development 2008, 1230-1236. Oxford University Press, New York. second ed. C.J. Epstein, R.P. Erickson, A. Wynshaw-Boris (Eds.).
2. Kee Y., D'Andrea A.D. Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev. 2010, 24:1680-1694.
3. Stoepker C., Hain K., Schuster B., Hilhorst-Hofstee Y., Rooimans M.A., Steltenpool J., Oostra A.B., Eirich K., Korthof E.T., Nieuwint A.W.M., Jaspers N.G.J., Bettecken T., Joenje H., Schindler D., Rouse J., de Winter J.P. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat. Genet. 2011, 43:138-141.
4. Kim Y., Lach F.P., Desetty R., Hanenberg H., Auerbach A.D., Smogorzewska A. Mutations of the SLX4 gene in Fanconi anemia. Nat. Genet. 2011, 43:142-146.
5. Huang M., Kim J.M., Shiotani B., Yang K., Zou L., D'Andrea A.D. The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response. Mol. Cell 2010, 39:259-268.
6. Gong Z., Kim J.E., Leung C.C.Y., Glover J.N.M., Chen J. BACH1/FANCJ acts with TopBP1 and participates early in DNA replication checkpoint control. Mol. Cell 2010, 37:438-446.
7. Ishiai M., Kitao H., Smogorzewska A., Tomida J., Kinomura A., Uchida E., Saberi A., Kinoshita E., Kinoshita-Kikuta E., Koike T., Tashiro S., Elledge S.J., Takata M. FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 2008, 15:1138-1146.
8. Deans A.J., West S.C. FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Mol. Cell 2009, 36:943-953.
9. 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.
10. Singh T.R., Saro D., Ali A.M., Zheng X.-F., Du C.-h., Killen M.W., Sachpatzidis A., Wahengbam K., Pierce A.J., Xiong Y., Sung P., Meetei A.R. MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol. Cell 2010, 37:879-886.
11. Yan Z., Delannoy M., Ling C., Daee D., Osman F., Muniandy P.A., Shen X., Oostra A.B., Du H., Steltenpool J., Lin T., Schuster B., Décaillet C., Stasiak A., Stasiak A.Z., Stone S., Hoatlin M.E., Schindler D., Woodcock C.L., Joenje H., Sen R., de Winter J.P., Li L., Seidman M.M., Whitby M.C., Myung K., Constantinou A., Wang W. A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol. Cell 2010, 37:865-878.
12. Knipscheer P., Räschle M., Smogorzewska A., Enoiu M., Ho T.V., Schärer O.D., Elledge S.J., Walter J.C. The Fanconi anemia pathway promotes replication-dependent DNA interstrand crosslink repair. Science 2009, 326:1698-1701.
13. Blom E., van de Vrugt H.J., de Winter J.P., Arwert F., Joenje H. Evolutionary clues to the molecular function of Fanconi anemia genes. Acta Haematol. 2002, 108:231-236.
14. 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.
15. Wilson J.B., Blom E., Cunningham R., Xiao Y., Kupfer G.M., Jones N.J. Several tetratricopeptide repeat (TPR) motifs of FANCG are required for assembly of the BRCA2/D1-D2-G-X3 complex, FANCD2 monoubiquitylation and phleomycin resistance. Mutat. Res. 2010, 689:12-20.
16. Collis S.J., Ciccia A., Deans A.J., Horejsí Z., Martin J.S., Maslen S.L., Skehel J.M., Elledge S.J., West S.C., Boulton S.J. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol. Cell 2008, 32:313-324.
17. Hoatlin M.E., Christianson T.A., Keeble W.W., Hammond A.T., Zhi Y., Heinrich M.C., Tower P.A., Bagby G.C. The Fanconi anemia group C gene product is located in both the nucleus and cytoplasm of human cells. Blood 1998, 91:1418-1425.
18. Du W., Li J., Sipple J., Chen J., Pang Q. Cytoplasmic FANCA-FANCC complex interacts and stabilizes the cytoplasm-dislocalized leukemic nucleophosmin protein (NPMc). J. Biol. Chem. 2010, 285:37436-37444.
19. Cordell H.J. Epistasis: what it means, what it doesn't mean, and statistical methods to detect it in humans. Hum. Mol. Genet. 2002, 11:2463-2468.
20. van de Vrugt H.J., Cheng N.C., de Vries Y., Rooimans M.A., de Groot J., Schepers R.J., Zhi Y., Hoatlin M.E., Joenje H., Arwert F. Cloning and characterization of murine Fanconi anemia group A gene: Fanca protein is expressed in lymphoid tissues, testis, and ovary. Mamm. Genome 2000, 11:326-331.
21. Van de Vrugt H.J., Koomen M., Berns M.A.D., de Vries Y., Rooimans M.A., van der Weel L., Blom E., de Groot J., Schepers R.J., Stone S., Hoatlin M.E., Cheng N.C., Joenje H., Arwert F. Characterization, expression and complex formation of the murine Fanconi anaemia gene product Fancg. Genes Cell 2002, 7:333-342.
22. Cheng N.C., van de Vrugt H.J., van der Valk M.A., Oostra A.B., Krimpenfort P., de Vries Y., Joenje H., Berns A., Arwert F. Mice with a targeted disruption of the Fanconi anemia homolog Fanca. Hum. Mol. Genet. 2000, 9:1805-1811.
23. Koomen M., Cheng N.C., van de Vrugt H.J., Godthelp B.C., van der Valk M.A., Oostra A.B., Zdzienicka M.Z., Joenje H., Arwert F. Reduced fertility and hypersensitivity to mitomycin C characterize Fancg/Xrcc9 null mice. Hum. Mol. Genet. 2002, 11:273-281.
24. Noll M., Battaile K.P., Bateman R., Lax T.P., Rathbun K., Reifsteck C., Bagby G., Finegold M., Olson S., Grompe M. Fanconi anemia group A and C double-mutant mice: functional evidence for a multi-protein Fanconi anemia complex. Exp. Hematol. 2002, 30:679-688.
25. Pulliam-Leath A.C., Ciccone S.L., Nalepa G., Li X., Si Y., Miravalle L., Smith D., Yuan J., Li J., Anur P., Orazi A., Vance G.H., Yang F.-C., Hanenberg H., Bagby G.C., Clapp D.W. Genetic disruption of both Fancc and Fancg in mice recapitulates the hematopoietic manifestations of Fanconi anemia. Blood 2010, 116:2915-2920.
26. van de Vrugt H.J., Eaton L., Hanlon Newell A., Al-Dhalimy M., Liskay R.M., Olson S.B., Grompe M. Embryonic lethality after combined inactivation of Fancd2 and Mlh1 in mice. Cancer Res. 2009, 69:9431-9438.
27. Bakker S.T., van de Vrugt H.J., Rooimans M.A., Oostra A.B., Steltenpool J., Delzenne-Goette E., van der Wal A., van der Valk M., Joenje H., te Riele H., de Winter J.P. Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M. Hum. Mol. Genet. 2009, 18:3484-3495.
28. Whitney M.A., Royle G., Low M.J., Kelly M.A., Axthelm M.K., Reifsteck C., Olson S., Braun R.E., Heinrich M.C., Rathbun R.K., Bagby G.C., Grompe M. Germ cell defects and hematopoietic hypersensitivity to gamma-interferon in mice with a targeted disruption of the Fanconi anemia C gene. Blood 1996, 88:49-58.
29. 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.
30. Agoulnik A.I., Lu B., Zhu Q., Truong C., Ty M.T., Arango N., Chada K.K., Bishop C.E. A novel gene, Pog, is necessary for primordial germ cell proliferation in the mouse and underlies the germ cell deficient mutation, gcd. Hum. Mol. Genet. 2002, 11:3047-3053.
31. Parmar K., D'Andrea A., Niedernhofer L.J. Mouse models of Fanconi anemia. Mutat. Res. 2009, 668:133-140.
32. Wirth-Dziciołowska E., Karaszewska J., Pyśniak K., Smolińska M., Gajewska M. Selected peripheral blood cell parameters in twelve inbred strains of laboratory mice. Anim. Sci. Pap. Rep. 2009, 27:69-77.
33. Neveling K., Endt D., Hoehn H., Schindler D. Genotype-phenotype correlations in Fanconi anemia. Mutat. Res. 2009, 668:73-91.
34. 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.M., 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.
35. Waisfisz Q., de Winter J.P., Kruyt F.A.E., de Groot J., van der Weel L., Dijkmans L.M., Zhi Y., Arwert F., Scheper R.J., Youssoufian H., Hoatlin M.E., Joenje H. A physical complex of the Fanconi anemia proteins FANCG/XRCC9 and FANCA. P. N. A. S. 1999, 96:10320-10325.
36. Léveillé F., Ferrer M., Medhurst A.L., Laghmani E.H., Rooimans M.A., Bier P., Steltenpool J., Titus T.A., Postlethwait J.H., Hoatlin M.E., Joenje H., de Winter J.P. The nuclear accumulation of the Fanconi anemia protein FANCE depends on FANCC. DNA Repair 2006, 5:556-565.
37. de Winter J.P., van der Weel L., de Groot J., Stone S., Waisfisz Q., Arwert F., Scheper R.J., Kruyt F.A.E., Hoatlin M.E., Joenje H. The Fanconi anemia protein FANCF forms a nuclear complex with FANCA, FANCC and FANCG. Hum. Mol. Genet. 2000, 9:2665-2674.
38. Léveillé F., Blom E., Medhurst A.L., Bier P., Laghmani E.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.
39. de Winter J.P., Rooimans M.A., van der Weel L., van Berkel C.G.M., 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.
40. Reliene R., Yamamoto M.L., Rao P.N., Schiestl R.H. Genomic instability in mice is greater in Fanconi anemia caused by deficiency of Fancd2 than Fancg. Cancer Res. 2010, 70:9703-9710.
41. 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.
42. Medhurst A.L., Laghmani E.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 subcomplexes in the Fanconi anemia pathway. Blood 2006, 108:2072-2080.