Regulation of FANCD2 and FANCI monoubiquitination by their interaction and by DNA

Nucleic Acids Research

Volumn 42, Issue 9, 2014, Pages 5657-5670

  Longerich, Simonne ^a   Kwon, Youngho ^a   Tsai, Miaw Sheue ^b   Hlaing, Aye Su ^b   Kupfer, Gary M ^c   Sung, Patrick ^a  

^a YALE UNIVERSITY   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DOUBLE STRANDED DNA; FANCONI ANEMIA GROUP D2 PROTEIN; INHIBITOR OF DIFFERENTIATION 2; LYSINE; PROTEIN FANCI; PROTEIN UBE2T; SINGLE STRANDED DNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; DNA MODIFICATION; ENZYME ACTIVATION; ENZYME SUBSTRATE; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; UBIQUITINATION;

AMINO ACID SUBSTITUTION; ANIMALS; DNA, CIRCULAR; DNA, VIRAL; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP L PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 2; NUCLEOSOMES; PLASMIDS; PROTEIN BINDING; SF9 CELLS; SPODOPTERA; SUBSTRATE SPECIFICITY; UBIQUITINATION;

EID: 84901319029     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku198     Document Type: Article

References (33)

1. Kitao, H. and Takata, M. (2011) Fanconi anemia: A disorder defective in the DNA damage response. Int. J. Hematol., 93, 417-424
2. Kottemann, M.C. and Smogorzewska, A. (2013) Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature, 493, 356-363
3. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M. and D'Andrea, A.D. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. cell, 7, 249-262. (Pubitemid 32206493
4. Taniguchi, T., Garcia-Higuera, I., Andreassen, P.R., Gregory, R.C., Grompe, M. and D'Andrea, A.D. (2002) S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood, 100, 2414-2420
5. Thompson, L.H. and Hinz, J.M. (2009) Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: Mechanistic insights. Mutat. Res., 668, 54-72
6. Fu, D., Dudimah, F.D., Zhang, J., Pickering, A., Paneerselvam, J., Palrasu, M., Wang, H. and Fei, P. (2013) Recruitment of DNA polymerase eta by FANCD2 in the early response to DNA damage. Cell Cycle, 12, 803-809
7. Huang, M. and D'Andrea, A.D. (2010) A new nuclease member of the FAN club. Nat. Struct. Mol. Biol., 17, 926-928
8. Garner, E. and Smogorzewska, A. (2011) Ubiquitylation and the Fanconi anemia pathway. FEBS Lett., 585, 2853-2860
9. Cybulski, K.E. and Howlett, N.G. (2011) FANCP/SLX4: A swiss army knife of DNA interstrand crosslink repair. Cell Cycle, 10, 1757-1763
10. Joo, W., Xu, G., Persky, N.S., Smogorzewska, A., Rudge, D.G., Buzovetsky, O., Elledge, S.J. and Pavletich, N.P. (2011) Structure of the FANCI-FANCD2 complex: Insights into the Fanconi anemia DNA repair pathway. Science, 333, 312-316
11. Yuan, F., El Hokayem, J., Zhou, W. and Zhang, Y. (2009) FANCI protein binds to DNA and interacts with FANCD2 to recognize branched structures. J. Biol. Chem., 284, 24443-24452
12. Smogorzewska, A., Matsuoka, S., Vinciguerra, P., McDonald, E.R. III, Hurov, K.E., Luo, J., Ballif, B.A., Gygi, S.P., Hofmann, K., D'Andrea, A.D. et al. (2007) Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell, 129, 289-301. (Pubitemid 46584733
13. Sims, A.E., Spiteri, E., Sims, R.J. III, Arita, A.G., Lach, F.P., Landers, T., Wurm, M., Freund, M., Neveling, K., Hanenberg, H. et al. (2007) FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol., 14, 564-567
14. Dorsman, J.C., Levitus, M., Rockx, D., Rooimans, M.A., Oostra, A.B., Haitjema, A., Bakker, S.T., Steltenpool, J., Schuler, D., Mohan, S. et al. (2007) Identification of the Fanconi anemia complementation group I gene, FANCI. Cell. Oncol., 29, 211-218. (Pubitemid 46855710
15. Longerich, S., San Filippo, J., Liu, D. and Sung, P. (2009) FANCI binds branched DNA and is monoubiquitinated by UBE2T-FANCL. J. Biol. Chem., 284, 23182-23186
16. Sato, K., Toda, K., Ishiai, M., Takata, M. and Kurumizaka, H. (2012) DNA robustly stimulates FANCD2 monoubiquitylation in the complex with FANCI. Nucleic Acids Res., 40, 4553-4561
17. Singh, T.R., Ali, A.M., Busygina, V., Raynard, S., Fan, Q., Du, C.H., Andreassen, P.R., Sung, P. and Meetei, A.R. (2008) BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes Dev., 22, 2856-2868
18. Gordon, S.M. and Buchwald, M. (2003) Fanconi anemia protein complex: Mapping protein interactions in the yeast 2-And 3-hybrid systems. Blood, 102, 136-141. (Pubitemid 36759646
19. Kwon, Y., Chi, P., Roh, D.H., Klein, H. and Sung, P. (2007) Synergistic action of the Saccharomyces cerevisiae homologous recombination factors Rad54 and Rad51 in chromatin remodeling. DNA Repair (Amst), 6, 1496-1506. (Pubitemid 47385402
20. Beard, B.C., Wilson, S.H. and Smerdon, M.J. (2003) Suppressed catalytic activity of base excision repair enzymes on rotationally positioned uracil in nucleosomes. Proc. Natl. Acad. Sci. U.S.A., 100, 7465-7470
21. Park, W.H., Margossian, S., Horwitz, A.A., Simons, A.M., D'Andrea, A.D. and Parvin, J.D. (2005) Direct DNA binding activity of the Fanconi anemia D2 protein. J. Biol. Chem., 280, 23593-23598
22. Hodson, C., Cole, A.R., Lewis, L.P., Miles, J.A., Purkiss, A. and Walden, H. (2011) Structural analysis of human FANCL, the E3 ligase in the Fanconi anemia pathway. J. Biol. Chem., 286, 32628-32637
23. Sato, K., Ishiai, M., Toda, K., Furukoshi, S., Osakabe, A., Tachiwana, H., Takizawa, Y., Kagawa, W., Kitao, H., Dohmae, N. et al. (2012) Histone chaperone activity of Fanconi anemia proteins, FANCD2 and FANCI, is required for DNA crosslink repair. EMBO J., 31, 3524-3536
24. Knipscheer, P., Raschle, M., Smogorzewska, A., Enoiu, M., Ho, T.V., Scharer, O.D., Elledge, S.J. andWalter, J.C. (2009) The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science, 326, 1698-1701
25. Fanconi Anemia Mutation Database Rockefeller University, New York. http://www.rockefeller.edu/fanconi/ (6 March 2014, date last accessed
26. Sareen, A., Chaudhury, I., Adams, N. and Sobeck, A. (2012) Fanconi anemia proteins FANCD2 and FANCI exhibit different DNA damage responses during S-phase. Nucleic Acids Res., 40, 8425-8439
27. Ishiai, M., Kitao, H., Smogorzewska, A., Tomida, J., Kinomura, A., Uchida, E., Saberi, A., Kinoshita, E., Kinoshita-Kikuta, E., Koike, T. et al. (2008) FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat. Struct. Mol. Biol., 15, 1138-1146
28. Sobeck, A., Stone, S. and Hoatlin, M.E. (2007) DNA structure-induced recruitment and activation of the Fanconi anemia pathway protein FANCD2. Mol. Cell. Biol., 27, 4283-4292
29. Shigechi, T., Tomida, J., Sato, K., Kobayashi, M., Eykelenboom, J.K., Pessina, F., Zhang, Y., Uchida, E., Ishiai, M., Lowndes, N.F. et al. (2012) ATR-ATRIP kinase complex triggers activation of the Fanconi anemia DNA repair pathway. Cancer Res., 72, 1149-1156
30. Zhi, G., Wilson, J.B., Chen, X., Krause, D.S., Xiao, Y., Jones, N.J. and Kupfer, G.M. (2009) Fanconi anemia complementation group FANCD2 protein serine 331 phosphorylation is important for fanconi anemia pathway function and BRCA2 interaction. Cancer Res., 69, 8775-8783
31. Alpi, A., Langevin, F., Mosedale, G., Machida, Y.J., Dutta, A. and Patel, K.J. (2007) 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, 8421-8430
32. Parker, J.L., Bucceri, A., Davies, A.A., Heidrich, K., Windecker, H. and Ulrich, H.D. (2008) SUMO modification of PCNA is controlled by DNA. EMBO J., 27, 2422-2431
33. Sorkin, A. (2007) Ubiquitination without E3. Mol. Cell, 26, 771-773