The involvement of FANCM, FANCI, and checkpoint proteins in the interstrand DNA crosslink repair pathway is conserved in C. elegans

DNA Repair

Volumn 9, Issue 4, 2010, Pages 374-382

  Lee, Kyong Yun ^a   Chung, Kee Yang ^b   Koo, Hyeon Sook ^a  

^a Yonsei University   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

Cell cycle checkpoint; FANCI; FANCM; Fanconi anemia; Nuclear foci

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA PROTEIN; PROTEIN FANCI; PROTEIN FANCM; PROTEIN RPA; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CROSS LINKING; DNA REPAIR; DNA STRAND; GENE STRUCTURE; GENETIC CODE; GENETIC CONSERVATION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; CAENORHABDITIS ELEGANS; DNA; DNA DAMAGE; DNA HELICASES; DNA REPAIR; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; PHOSPHORYLATION;

CAENORHABDITIS ELEGANS;

EID: 77949658531     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2009.12.018     Document Type: Article

References (58)

1. Dronkert M.L., and Kanaar R. Repair of DNA interstrand cross-links. Mutat. Res. 486 (2001) 217-247
2. Beljanski V., Marzilli L.G., and Doetsch P.W. DNA damage-processing pathways involved in the eukaryotic cellular response to anticancer DNA cross-linking drugs. Mol. Pharmacol. 65 (2004) 1496-1506
3. Nojima K., Hochegger H., Saberi A., Fukushima T., Kikuchi K., Yoshimura M., Orelli B.J., Bishop D.K., Hirano S., Ohzeki M., Ishiai M., Yamamoto K., Takata M., Arakawa H., Buerstedde J.M., Yamazoe M., Kawamoto T., Araki K., Takahashi J.A., Hashimoto N., Takeda S., and Sonoda E. Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res. 65 (2005) 11704-11711
4. Joenje H., and Patel K.J. The emerging genetic and molecular basis of Fanconi anaemia. Nat. Rev. Genet. 2 (2001) 446-457
5. D'Andrea A.D., and Grompe M. The Fanconi anaemia/BRCA pathway. Nat. Rev. Cancer 3 (2003) 23-34
6. Jacquemont C., and Taniguchi T. The Fanconi anemia pathway and ubiquitin. BMC Biochem. 8 (2007) S10
7. Wang W. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 8 (2007) 735-748
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., Sechi S., Wallisch M., Yang D., Young M.K., Joenje H., Hoatlin M.E., and Wang W. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol. Cell. Biol. 23 (2003) 3417-3426
10. 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
11. Alpi A.F., Pace R.E., Babu M.M., and Patel K.J. Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol. Cell 32 (2008) 767-777
12. Taniguchi T., Garcia-Higuera I., Andreassen P.R., Gregory R.C., Grompe M., and D'Andrea A.D. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100 (2002) 2414-2420
13. 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
14. 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
15. Mosedale G., Niedzwiedz W., Alpi A., Perrina F., Pereira-Leal J.B., Johnson M., Langevin F., Pace P., and Patel K.J. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat. Struct. Mol. Biol. 12 (2005) 763-771
16. Gari K., Décaillet C., Stasiak A.Z., Stasiak A., and Constantinou A. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell 29 (2008) 141-148
17. 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
18. Smogorzewska A., Matsuoka S., Vinciguerra P., McDonald S E.R. III, 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
19. Yuan F., Hokayem J.E., Zhou W., and Zhang Y. FANCI protein binds to DNA and interacts with FANCD2 to recognize branched structures. J. Biol. Chem. 284 (2009) 24443-24452
20. 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 (2008) 255-265
21. Levitus M., Waisfisz Q., Godthelp B.C., de Vries Y., Hussain S., Wiegant W.W., Elghalbzouri-Maghrani E., Steltenpool J., Rooimans M.A., Pals G., Arwert F., Mathew C.G., Zdzienicka M.Z., Hiom K., De Winter J.P., and Joenje H. The DNA helicase BRIP1 is defective in Fanconi anemia complementation group J. Nat. Genet. 37 (2005) 934-935
22. Levran O., Attwooll C., Henry R.T., Milton K.L., Neveling K., Rio P., Batish S.D., Kalb R., Velleuer E., Barral S., Ott J., Petrini J., Schindler D., Hanenberg H., and Auerbach A.D. The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia. Nat. Genet. 37 (2005) 931-933
23. Xia B., Sheng Q., Nakanishi K., Ohashi A., Wu J., Christ N., Liu X., Jasin M., Couch F.J., and Livingston D.M. Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol. Cell 22 (2006) 719-729
24. 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 D.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
25. 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
26. Ciccia A., Ling C., Coulthard R., Yan Z., Xue Y., Meetei A.R., Laghmani E.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
27. 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
28. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15 (2001) 2177-2196
29. Zou L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548
30. Andreassen P.R., D'Andrea A.D., and Taniguchi T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev. 18 (2004) 1958-1963
31. 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., and Takata M. FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 15 (2008) 1138-1146
32. Pichierri P., and Rosselli F. The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J. 23 (2004) 1178-1187
33. 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., and Boulton S.J. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the fanconi anemia core complex. Mol. Cell 32 (2008) 313-324
34. Liu Q., Guntuku S., Cui X.S., Matsuoka S., Cortez D., Tamai K., Luo G., Carattini-Rivera S., DeMayo F., Bradley A., Donehower L.A., and Elledge S.J. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14 (2000) 1448-1459
35. 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
36. Banerjee S., Smith S., Oum J.H., Liaw H.J., Hwang J.Y., Sikdar N., Motegi A., Lee S.E., and Myung K. Mph1p promotes gross chromosomal rearrangement through partial inhibition of homologous recombination. J. Cell Biol. 181 (2008) 1083-1093
37. Sun W., Nandi S., Osman F., Ahn J.S., Jakovleska J., Lorenz A., and Whitby M.C. The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol. Cell 32 (2008) 118-128
38. Youds J.L., Barber L.J., and Boulton S.J. C. elegans: a model of Fanconi anemia and ICL repair. Mutat. Res. 668 (2009) 103-116
39. Collis S.J., Barber L.J., Ward J.D., Martin J.S., and Boulton S.J. C. elegans FANCD2 responds to replication stress and functions in interstrand cross-link repair. DNA Repair 5 (2006) 1398-1406
40. Lee K.Y., Yang I., Park J.-E., Baek O.-R., Chung K.Y., and Koo H.-S. Developmental stage- and DNA damage-specific functions of C. elegans FANCD2. Biochem. Biophys. Res. Commun. 352 (2007) 479-485
41. Youds J.L., Barber L.J., Ward J.D., Collis S.J., O'Neil N.J., Boulton S.J., and Rose A.M. DOG-1 is the Caenorhabditis elegans BRIP1/FANCJ homologue and functions in interstrand cross-link repair. Mol. Cell. Biol. 28 (2008) 1470-1479
42. Martin J.S., Winkelmann N., Petalcorin M.I., McIlwraith M.J., and Boulton S.J. RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair. Mol. Cell. Biol. 25 (2005) 3127-3139
43. Tabara H., Yigit E., Siomi H., and Mello C.C. The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 109 (2002) 861-871
44. Duchaine T.F., Wohlschlegel J.A., Kennedy S., Bei Y., Conte Jr. D., Pang K., Brownell D.R., Harding S., Mitani S., Ruvkun G., Yates III J.R., and Mello C.C. Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 124 (2006) 343-354
45. Nakamura M., Ando R., Nakazawa T., Yudazono T., Tsutsumi N., Hatanaka N., Ohgake T., Hanaoka F., and Eki T. Dicer-related drh-3 gene functions in germ-line development by maintenance of chromosomal integrity in Caenorhabditis elegans. Genes Cells 12 (2007) 997-1010
46. Rothfuss A., and Grompe M. Repair kinetics of genomic interstrand DNA cross-links: evidence for DNA double-strand break-dependent activation of the Fanconi anemia/BRCA pathway. Mol. Cell. Biol. 24 (2004) 123-134
47. McCabe K.M., Hemphill A., Akkari Y., Jakobs P.M., Pauw D., Olson S.B., Moses R.E., and Grompe M. ERCC1 is required for FANCD2 focus formation. Mol. Genet. Metab. 95 (2008) 66-73
48. Guervilly J.H., Macé-Aimé G., and Rosselli F. Loss of CHK1 function impedes DNA damage-induced FANCD2 monoubiquitination but normalizes the abnormal G2 arrest in Fanconi anemia. Hum. Mol. Genet. 17 (2008) 679-689
49. Kim J.M., Kee Y., Gurtan A., and D'Andrea A.D. Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood 111 (2008) 5215-5222
50. Sobeck A., Stone S., Landais I., de Graaf B., and Hoatlin M.E. The Fanconi anemia protein FANCM is controlled by FANCD2 and the ATR/ATM pathways. J. Biol. Chem. 284 (2009) 25560-25568
51. Digweed M., Rothe S., Demuth I., Scholz R., Schindler D., Stumm M., Grompe M., Jordan A., and Sperling K. Attenuation of the formation of DNA-repair foci containing RAD51 in Fanconi anaemia. Carcinogenesis 23 (2002) 1121-1126
52. Godthelp B.C., Wiegant W.W., Waisfisz Q., Medhurst A.L., Arwert F., Joenje H., and Zdzienicka M.Z. Inducibility of nuclear Rad51 foci after DNA damage distinguishes all Fanconi anemia complementation groups from D1/BRCA2. Mutat. Res. 594 (2006) 39-48
53. Ohashi A., Zdzienicka M.Z., Chen J., and Couch F.J. Fanconi anemia complementation group D2 (FANCD2) functions independently of BRCA2- and RAD51-associated homologous recombination in response to DNA damage. J. Biol. Chem. 280 (2005) 14877-14883
54. Xue Y., Li Y., Guo R., Ling C., and Wang W. FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair. Hum. Mol. Genet. 17 (2008) 1641-1652
55. Singh T.R., Bakker S.T., Agarwal S., Jansen M., Grassman E., Godthelp B.C., Ali A.M., Du C.H., Rooimans M.A., Fan Q., Wahengbam K., Steltenpool J., Andreassen P.R., Williams D.A., Joenje H., de Winter J.P., and Meetei A.R. Impaired FANCD2 monoubiquitination and hypersensitivity to camptothecin uniquely characterize Fanconi anemia complementation group M. Blood 114 (2009) 174-180
56. Rosado I.V., Niedzwiedz W., Alpi A.F., and Patel K.J. The Walker B motif in avian FANCM is required to limit sister chromatid exchanges but is dispensable for DNA crosslink repair. Nucleic Acids Res. 37 (2009) 4360-4370
57. 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., and de Winter J.P. Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M. Hum. Mol. Genet. 18 (2009) 3484-3495
58. Sørensen C.S., Hansen L.T., Dziegielewski J., Syljuåsen R.G., Lundin C., Bartek J., and Helleday T. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol. 7 (2005) 195-201