Fanconi anemia proteins stabilize replication forks

DNA Repair

Volumn 7, Issue 12, 2008, Pages 1973-1981

  Wang, Lily Chien ^a,b   Stone, Stacie ^c   Hoatlin, Maureen Elizabeth ^c   Gautier, Jean ^a  

^a Howard Hughes Medical Institute   (United States)

^b Integrated Program in Cellular   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Fanconi anemia; Mitomycin C; Replication forks; Replication restart

Indexed keywords

ATR PROTEIN; CAMPTOTHECIN; FANCONI ANEMIA GROUP A PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA GROUP L PROTEIN; FANCONI ANEMIA PROTEIN; MITOMYCIN C;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA CROSS LINKING; DNA REPAIR; DNA REPLICATION; FANCONI ANEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN STABILITY; XENOPUS;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APHIDICOLIN; CAMPTOTHECIN; CELL CYCLE PROTEINS; CELL NUCLEUS; CELL-FREE SYSTEM; CHROMATIN; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ENZYME INHIBITORS; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP L PROTEIN; MITOMYCIN; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 55149115113     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.08.005     Document Type: Article

References (56)

1. German J., Schonberg S., Caskie S., Warburton D., Falk C., and Ray J.H. A test for Fanconi's anemia. Blood 69 (1987) 1637-1641
2. Zou L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548
3. Auerbach A.D. A test for Fanconi's anemia. Blood 72 (1988) 366-367
4. Poll E.H., Arwert F., Joenje H., and Wanamarta A.H. Differential sensitivity of Fanconi anaemia lymphocytes to the clastogenic action of cis-diamminedichloroplatinum (II) and trans-diamminedichloroplatinum (II). Hum. Genet. 71 (1985) 206-210
5. 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., and Joenje H. Identification of the Fanconi anemia complementation group I gene, FANCI. Cell. Oncol. 29 (2007) 211-218
6. 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., and Wang W. FAAP100 is essential for activation of the Fanconi anemia-associated DNA damage response pathway. EMBO J. 26 (2007) 2104-2114
7. 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., and West S.C. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol. Cell 25 (2007) 331-343
8. Garcia-Higuera I., Taniguchi T., Ganesan S., Meyn M.S., Timmers C., Hejna J., Grompe M., and D'Andrea A.D. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7 (2001) 249-262
9. 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., and Wang W. A novel ubiquitin ligase is deficient in Fanconi anemia. Nat. Genet. 35 (2003) 165-170
10. 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., and Wang W. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 37 (2005) 958-963
11. Sims A.E., Spiteri E., Sims III R.J., Arita A.G., Lach F.P., Landers T., Wurm M., Freund M., Neveling K., Hanenberg H., Auerbach A.D., and Huang T.T. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 14 (2007) 564-567
12. Alpi A., Langevin F., Mosedale G., Machida Y.J., Dutta A., and Patel K.J. UBE2T, the FA core complex and FANCD2 are recruited independently to chromatin: a basis for the regulation of FANCD2 monoubiquitination. Mol. Cell. Biol. (2007)
13. 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., and Joenje H. X-linked inheritance of Fanconi anemia complementation group B. Nat. Genet. 36 (2004) 1219-1224
14. Smogorzewska A., Matsuoka S., Vinciguerra P., McDonald III E.R., Hurov K.E., Luo J., Ballif B.A., Gygi S.P., Hofmann K., D'Andrea A.D., and Elledge S.J. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129 (2007) 289-301
15. Wang X., Andreassen P.R., and D'Andrea A.D. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell. Biol. 24 (2004) 5850-5862
16. 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., and Livingston D.M. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 105 (2001) 149-160
17. 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., and Mathew C.G. Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum. Mol. Genet. 13 (2004) 1241-1248
18. 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., and Rahman N. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat. Genet. 39 (2007) 162-164
19. 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., and de Winter J.P. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat. Genet. 39 (2007) 159-161
20. Folias A., Matkovic M., Bruun D., Reid S., Hejna J., Grompe M., D'Andrea A., and Moses R. BRCA1 interacts directly with the Fanconi anemia protein FANCA. Hum. Mol. Genet. 11 (2002) 2591-2597
21. 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., and Joenje H. Heterogeneity in Fanconi anemia: evidence for 2 new genetic subtypes. Blood 103 (2004) 2498-2503
22. Litman R., Peng M., Jin Z., Zhang F., Zhang J., Powell S., Andreassen P.R., and Cantor S.B. BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 8 (2005) 255-265
23. 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., and D'Andrea A.D. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297 (2002) 606-609
24. Kennedy R.D., and D'Andrea A.D. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev. 19 (2005) 2925-2940
25. Akkari Y.M., Bateman R.L., Reifsteck C.A., D'Andrea A.D., Olson S.B., and Grompe M. The 4N cell cycle delay in Fanconi anemia reflects growth arrest in late S phase. Mol. Genet. Metab. 74 (2001) 403-412
26. 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., and Hoatlin M.E. Fanconi anemia proteins are required to prevent accumulation of replication-associated DNA double-strand breaks. Mol. Cell. Biol. 26 (2006) 425-437
27. Mi J., and Kupfer G.M. The Fanconi anemia core complex associates with chromatin during S phase. Blood 105 (2005) 759-766
28. Sobeck A., Stone S., and Hoatlin M.E. DNA structure-induced recruitment and activation of the Fanconi anemia pathway protein FANCD2. Mol. Cell. Biol. 27 (2007) 4283-4292
29. Bell S.P., and Dutta A. DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71 (2002) 333-374
30. Labib K., and Hodgson B. Replication fork barriers: pausing for a break or stalling for time?. EMBO Rep. 8 (2007) 346-353
31. Admire A., Shanks L., Danzl N., Wang M., Weier U., Stevens W., Hunt E., and Weinert T. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev. 20 (2006) 159-173
32. Cha R.S., and Kleckner N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297 (2002) 602-606
33. Lopes M., Cotta-Ramusino C., Pellicioli A., Liberi G., Plevani P., Muzi-Falconi M., Newlon C.S., and Foiani M. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412 (2001) 557-561
34. Tercero J.A., and Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412 (2001) 553-557
35. Liu L.F., Desai S.D., Li T.K., Mao Y., Sun M., and Sim S.P. Mechanism of action of camptothecin. Ann. N.Y. Acad. Sci. 922 (2000) 1-10
36. Trenz K., Smith E., Smith S., and Costanzo V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25 (2006) 1764-1774
37. Stone S., Sobeck A., van Kogelenberg M., de Graaf B., Joenje H., Christian J., and Hoatlin M.E. Identification, developmental expression and regulation of the Xenopus ortholog of human FANCG/XRCC9. Genes Cells 12 (2007) 841-851
38. Ying C.Y., and Gautier J. The ATPase activity of MCM2-7 is dispensable for pre-RC assembly but is required for DNA unwinding. EMBO J. 24 (2005) 4334-4344
39. Montes de Oca R., Andreassen P.R., Margossian S.P., Gregory R.C., Taniguchi T., Wang X., Houghtaling S., Grompe M., and D'Andrea A.D. Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 105 (2005) 1003-1009
40. Stokes M.P., and Michael W.M. DNA damage-induced replication arrest in Xenopus egg extracts. J. Cell Biol. 163 (2003) 245-255
41. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15 (2001) 2177-2196
42. Costanzo V., Robertson K., Bibikova M., Kim E., Grieco D., Gottesman M., Carroll D., and Gautier J. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell. 8 (2001) 137-147
43. Shechter D., Costanzo V., and Gautier J. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell. Biol. 6 (2004) 648-655
44. Ho G.P., Margossian S., Taniguchi T., and D'Andrea A.D. Phosphorylation of FANCD2 on two novel sites is required for mitomycin C resistance. Mol. Cell. Biol. 26 (2006) 7005-7015
45. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald III E.R., Hurov K.E., Luo J., Bakalarski C.E., Zhao Z., Solimini N., Lerenthal Y., Shiloh Y., Gygi S.P., and Elledge S.J. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316 (2007) 1160-1166
46. Qiao F., Mi J., Wilson J.B., Zhi G., Bucheimer N.R., Jones N.J., and Kupfer G.M. Phosphorylation of fanconi anemia (FA) complementation group G protein, FANCG, at serine 7 is important for function of the FA pathway. J. Biol. Chem. 279 (2004) 46035-46045
47. Wang X., Kennedy R.D., Ray K., Stuckert P., Ellenberger T., and D'Andrea A.D. Chk1-mediated phosphorylation of FANCE is required for the Fanconi anemia/BRCA pathway. Mol. Cell Biol. 27 (2007) 3098-3108
48. Yamashita T., Kupfer G.M., Naf D., Suliman A., Joenje H., Asano S., and D'Andrea A.D. The fanconi anemia pathway requires FAA phosphorylation and FAA/FAC nuclear accumulation. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 13085-13090
49. Chirnomas D., Taniguchi T., de la Vega M., Vaidya A.P., Vasserman M., Hartman A.R., Kennedy R., Foster R., Mahoney J., Seiden M.V., and D'Andrea A.D. Chemosensitization to cisplatin by inhibitors of the Fanconi anemia/BRCA pathway. Mol. Cancer Ther. 5 (2006) 952-961
50. Nomura Y., Adachi N., and Koyama H. Human Mus81 and FANCB independently contribute to repair of DNA damage during replication. Genes Cells 12 (2007) 1111-1122
51. Mace G., Bogliolo M., Guervilly J.H., Dugas du Villard J.A., and Rosselli F. 3R coordination by Fanconi anemia proteins. Biochimie 87 (2005) 647-658
52. Pichierri P., and Rosselli F. Fanconi anemia proteins and the s phase checkpoint. Cell Cycle 3 (2004) 698-700
53. Thompson L.H., Hinz J.M., Yamada N.A., and Jones N.J. How Fanconi anemia proteins promote the four Rs: replication, recombination, repair, and recovery. Environ. Mol. Mutagen. 45 (2005) 128-142
54. Pichierri P., Franchitto A., and Rosselli F. BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. EMBO J. 23 (2004) 3154-3163
55. Gupta R., Sharma S., Sommers J.A., Kenny M.K., Cantor S.B., and Brosh Jr. R.M. 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 110 (2007) 2390-2398
56. Wang W. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 8 (2007) 735-748