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http://dx.doi.org/10.14348/molcells.2015.0175

Exploiting the Fanconi Anemia Pathway for Targeted Anti-Cancer Therapy  

Jo, Ukhyun (Department of Pharmacological Sciences, Stony Brook University)
Kim, Hyungjin (Department of Pharmacological Sciences, Stony Brook University)
Publication Information
Molecules and Cells / v.38, no.8, 2015 , pp. 669-676 More about this Journal
Abstract
Genome instability, primarily caused by faulty DNA repair mechanisms, drives tumorigenesis. Therapeutic interventions that exploit deregulated DNA repair in cancer have made considerable progress by targeting tumor-specific alterations of DNA repair factors, which either induces synthetic lethality or augments the efficacy of conventional chemotherapy and radiotherapy. The study of Fanconianemia (FA), a rare inherited blood disorder and cancer predisposition syndrome, has been instrumental in understanding the extent to which DNA repair defects contribute to tumorigenesis. The FA pathway functions to resolve blocked replication forks in response to DNA interstrand cross-links (ICLs), and accumulating knowledge of its activation by the ubiquitin-mediated signaling pathway has provided promising therapeutic opportunities for cancer treatment. Here, we discuss recent advances in our understanding of FA pathway regulation and its potential application for designing tailored therapeutics that take advantage of deregulated DNA ICL repair in cancer.
Keywords
cancer therapeutics; DNA interstrand cross-link; DNA repair; Fanconi anemia; ubiquitin signaling;
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1 Long, D.T., Joukov, V., Budzowska, M., and Walter, J.C. (2014). BRCA1 promotes unloading of the CMG helicase from a stalled DNA replication fork. Mol. Cell 56, 174-185.   DOI   ScienceOn
2 Mateos-Gomez, P.A., Gong, F., Nair, N., Miller, K.M., Lazzerini-Denchi, E., and Sfeir, A. (2015). Mammalian polymerase theta promotes alternative NHEJ and suppresses recombination. Nature 518, 254-257.   DOI   ScienceOn
3 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., et al. (2003). A novel ubiquitin ligase is deficient in Fanconi anemia. Nat. Genet. 35, 165-170.   DOI   ScienceOn
4 Meetei, A.R., Medhurst, A.L., Ling, C., Xue, Y., Singh, T.R., Bier, P., Steltenpool, J., Stone, S., Dokal, I., Mathew, C.G., et al. (2005). A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 37, 958-963.   DOI   ScienceOn
5 Mistry, H., Hsieh, G., Buhrlage, S.J., Huang, M., Park, E., Cuny, G.D., Galinsky, I., Stone, R.M., Gray, N.S., D'Andrea, A.D., et al. (2013). Small-molecule inhibitors of USP1 target ID1 degradation in leukemic cells. Mol. Cancer Ther. 12, 2651-2662.   DOI   ScienceOn
6 Moynahan, M.E., Pierce, A.J., and Jasin, M. (2001). BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 7, 263-272.   DOI   ScienceOn
7 Negrini, S., Gorgoulis, V.G., and Halazonetis, T.D. (2010). Genomic instability--an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 11, 220-228.   DOI   ScienceOn
8 Niedzwiedz, W., Mosedale, G., Johnson, M., Ong, C.Y., Pace, P., and Patel, K.J. (2004). The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell 15, 607-620.   DOI   ScienceOn
9 Nijman, S.M., Huang, T.T., Dirac, A.M., Brummelkamp, T.R., Kerkhoven, R.M., D'Andrea, A.D., and Bernards, R. (2005). The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol. Cell 17, 331-339.   DOI   ScienceOn
10 Polito, D., Cukras, S., Wang, X., Spence, P., Moreau, L., D'Andrea, A.D., and Kee, Y. (2014). The carboxyl terminus of FANCE recruits FANCD2 to the Fanconi Anemia (FA) E3 ligase complex to promote the FA DNA repair pathway. J. Biol. Chem. 289, 7003-7010.   DOI   ScienceOn
11 Psakhye, I., and Jentsch, S. (2012). Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820.   DOI   ScienceOn
12 Rajendra, E., Oestergaard, V.H., Langevin, F., Wang, M., Dornan, G.L., Patel, K.J., and Passmore, L.A. (2014). The genetic and biochemical basis of FANCD2 monoubiquitination. Mol. Cell 54, 858-869.   DOI   ScienceOn
13 Raschle, M., Knipscheer, P., Enoiu, M., Angelov, T., Sun, J., Griffith, J.D., Ellenberger, T.E., Scharer, O.D., and Walter, J.C. (2008). Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134, 969-980.   DOI   ScienceOn
14 Raschle, M., Smeenk, G., Hansen, R.K., Temu, T., Oka, Y., Hein, M.Y., Nagaraj, N., Long, D.T., Walter, J.C., Hofmann, K., et al. (2015). DNA repair. Proteomics reveals dynamic assembly of repair complexes during bypass of DNA cross-links. Science 348, 1253671.   DOI   ScienceOn
15 Sawyer, S.L., Tian, L., Kahkonen, M., Schwartzentruber, J., Kircher, M., University of Washington Centre for Mendelian, G., Consortium, F.C., Majewski, J., Dyment, D.A., Innes, A.M., et al. (2015). Biallelic mutations in BRCA1 cause a new Fanconi anemia subtype. Cancer Discov. 5, 135-142.   DOI   ScienceOn
16 Schwab, R.A., Blackford, A.N., and Niedzwiedz, W. (2010). ATR activation and replication fork restart are defective in FANCMdeficient cells. EMBO J. 29, 806-818.   DOI   ScienceOn
17 Smogorzewska, A., Desetty, R., Saito, T.T., Schlabach, M., Lach, F.P., Sowa, M.E., Clark, A.B., Kunkel, T.A., Harper, J.W., Colaiacovo, M.P., et al. (2010). A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell 39, 36-47.   DOI   ScienceOn
18 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., et al. (2010). MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol. Cell 37, 879-886.   DOI   ScienceOn
19 Singh, T.R., Ali, A.M., Paramasivam, M., Pradhan, A., Wahengbam, K., Seidman, M.M., and Meetei, A.R. (2013). ATR-dependent phosphorylation of FANCM at serine 1045 is essential for FANCM functions. Cancer Res. 73, 4300-4310.   DOI   ScienceOn
20 Smogorzewska, A., Matsuoka, S., Vinciguerra, P., McDonald, E.R., 3rd, 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.   DOI   ScienceOn
21 Tian, Y., Paramasivam, M., Ghosal, G., Chen, D., Shen, X., Huang, Y., Akhter, S., Legerski, R., Chen, J., Seidman, M.M., et al. (2015). UHRF1 Contributes to DNA Damage Repair as a Lesion Recognition Factor and Nuclease Scaffold. Cell Rep. 10, 1957-1966.   DOI   ScienceOn
22 Unno, J., Itaya, A., Taoka, M., Sato, K., Tomida, J., Sakai, W., Sugasawa, K., Ishiai, M., Ikura, T., Isobe, T., et al. (2014). FANCD2 binds CtIP and regulates DNA-end resection during DNA interstrand crosslink repair. Cell Rep. 7, 1039-1047.   DOI   ScienceOn
23 Vaz, F., Hanenberg, H., Schuster, B., Barker, K., Wiek, C., Erven, V., Neveling, K., Endt, D., Kesterton, I., Autore, F., et al. (2010). Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat. Genet. 42, 406-409.   DOI   ScienceOn
24 Wang, A.T., Sengerova, B., Cattell, E., Inagawa, T., Hartley, J.M., Kiakos, K., Burgess-Brown, N.A., Swift, L.P., Enzlin, J.H., Schofield, C.J., et al. (2011). Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev. 25, 1859-1870.   DOI   ScienceOn
25 Walden, H., and Deans, A.J. (2014). The Fanconi anemia DNA repair pathway: structural and functional insights into a complex disorder. Ann. Rev. Biophys. 43, 257-278.   DOI   ScienceOn
26 Wang, X., Kennedy, R.D., Ray, K., Stuckert, P., Ellenberger, T., and D'Andrea, A.D. (2007). Chk1-mediated phosphorylation of FANCE is required for the Fanconi anemia/BRCA pathway. Mol. Cell. Biol. 27, 3098-3108.   DOI   ScienceOn
27 Wang, H., Zhang, S.Y., Wang, S., Lu, J., Wu, W., Weng, L., Chen, D., Zhang, Y., Lu, Z., Yang, J., et al. (2009). REV3L confers chemoresistance to cisplatin in human gliomas: the potential of its RNAi for synergistic therapy. Neuro Oncol. 11, 790-802.   DOI
28 Williams, S.A., Longerich, S., Sung, P., Vaziri, C., and Kupfer, G.M. (2011a). The E3 ubiquitin ligase RAD18 regulates ubiquitylation and chromatin loading of FANCD2 and FANCI. Blood 117, 5078-5087.   DOI   ScienceOn
29 Williams, S.A., Maecker, H.L., French, D.M., Liu, J., Gregg, A., Silverstein, L.B., Cao, T.C., Carano, R.A., and Dixit, V.M. (2011b). USP1 deubiquitinates ID proteins to preserve a mesenchymal stem cell program in osteosarcoma. Cell 146, 918-930.   DOI   ScienceOn
30 Williams, S.A., Wilson, J.B., Clark, A.P., Mitson-Salazar, A., Tomashevski, A., Ananth, S., Glazer, P.M., Semmes, O.J., Bale, A.E., Jones, N.J., et al. (2011c). Functional and physical interaction between the mismatch repair and FA-BRCA pathways. Hum. Mol. Genet. 20, 4395-4410.   DOI   ScienceOn
31 Xie, J., Kim, H., Moreau, L.A., Puhalla, S., Garber, J., Al Abo, M., Takeda, S., and D'Andrea, A.D. (2015). RNF4-mediated polyubiquitination regulates the Fanconi anemia/BRCA pathway. J. Clin. Invest. 125, 1523-1532.   DOI   ScienceOn
32 Wojtaszek, J., Lee, C.J., D'Souza, S., Minesinger, B., Kim, H., D'Andrea, A.D., Walker, G.C., and Zhou, P. (2012). Structural basis of Rev1-mediated assembly of a quaternary vertebrate translesion polymerase complex consisting of Rev1, heterodimeric polymerase (Pol) zeta, and Pol kappa. J. Biol. Chem. 287, 33836-33846.   DOI
33 Xia, B., Sheng, Q., Nakanishi, K., Ohashi, A., Wu, J., Christ, N., Liu, X., Jasin, M., Couch, F.J., and Livingston, D.M. (2006). Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol. Cell 22, 719-729.   DOI   ScienceOn
34 Xie, K., Doles, J., Hemann, M.T., and Walker, G.C. (2010). Errorprone translesion synthesis mediates acquired chemoresistance. Proc. Natl. Acad. Sci. USA 107, 20792-20797.   DOI   ScienceOn
35 Yamamoto, K.N., Kobayashi, S., Tsuda, M., Kurumizaka, H., Takata, M., Kono, K., Jiricny, J., Takeda, S., and Hirota, K. (2011). Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc. Natl. Acad. Sci. USA 108, 6492-6496.   DOI   ScienceOn
36 Yan, Z., Delannoy, M., Ling, C., Daee, D., Osman, F., Muniandy, P.A., Shen, X., Oostra, A.B., Du, H., Steltenpool, J., et al. (2010). A histone-fold complex and FANCM form a conserved DNAremodeling complex to maintain genome stability. Mol. Cell 37, 865-878.   DOI   ScienceOn
37 Yang, K., Moldovan, G.L., Vinciguerra, P., Murai, J., Takeda, S., and D'Andrea, A.D. (2011). Regulation of the Fanconi anemia pathway by a SUMO-like delivery network. Genes Dev. 25, 1847-1858.   DOI   ScienceOn
38 Zhang, J., Dewar, J.M., Budzowska, M., Motnenko, A., Cohn, M.A., and Walter, J.C. (2015). DNA interstrand cross-link repair requires replication-fork convergence. Nat. Struct. Mol. Biol. 22, 242-247.   DOI   ScienceOn
39 Yarde, D.N., Oliveira, V., Mathews, L., Wang, X., Villagra, A., Boulware, D., Shain, K.H., Hazlehurst, L.A., Alsina, M., Chen, D.T., et al. (2009). Targeting the Fanconi anemia/BRCA pathway circumvents drug resistance in multiple myeloma. Cancer Res. 69, 9367-9375.   DOI   ScienceOn
40 Zhang, F., Ma, J., Wu, J., Ye, L., Cai, H., Xia, B., and Yu, X. (2009). PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr. Biol. 19, 524-529.
41 Zhou, W., Otto, E.A., Cluckey, A., Airik, R., Hurd, T.W., Chaki, M., Diaz, K., Lach, F.P., Bennett, G.R., Gee, H.Y., et al. (2012). FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat. Genet. 44, 910-915.   DOI   ScienceOn
42 Bryant, H.E., Schultz, N., Thomas, H.D., Parker, K.M., Flower, D., Lopez, E., Kyle, S., Meuth, M., Curtin, N.J., and Helleday, T. (2005). Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434, 913-917.   DOI   ScienceOn
43 Bartkova, J., Rezaei, N., Liontos, M., Karakaidos, P., Kletsas, D., Issaeva, N., Vassiliou, L.V., Kolettas, E., Niforou, K., Zoumpourlis, V.C., et al. (2006). Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633-637.   DOI   ScienceOn
44 Blackford, A.N., Schwab, R.A., Nieminuszczy, J., Deans, A.J., West, S.C., and Niedzwiedz, W. (2012). The DNA translocase activity of FANCM protects stalled replication forks. Human molecular genetics 21, 2005-2016.   DOI   ScienceOn
45 Bogliolo, M., Schuster, B., Stoepker, C., Derkunt, B., Su, Y., Raams, A., Trujillo, J.P., Minguillon, J., Ramirez, M.J., Pujol, R., et al. (2013). Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. American journal of human genetics 92, 800-806.   DOI   ScienceOn
46 Chang, D.J., and Cimprich, K.A. (2009). DNA damage tolerance:when it's OK to make mistakes. Nat. Chem. Biol. 5, 82-90.   DOI   ScienceOn
47 Budzowska, M., Graham, T.G., Sobeck, A., Waga, S., and Walter, J.C. (2015). Regulation of the Rev1-pol zeta complex during bypass of a DNA interstrand cross-link. EMBO J. pii: e201490878. [Epub ahead of print]
48 Bunting, S.F., Callen, E., Kozak, M.L., Kim, J.M., Wong, N., Lopez-Contreras, A.J., Ludwig, T., Baer, R., Faryabi, R.B., Malhowski, A., et al. (2012). BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair. Mol. Cell 46, 125-135.   DOI   ScienceOn
49 Ceccaldi, R., Liu, J.C., Amunugama, R., Hajdu, I., Primack, B., Petalcorin, M.I., O'Connor, K.W., Konstantinopoulos, P.A., Elledge, S.J., Boulton, S.J., et al. (2015). Homologousrecombination-deficient tumours are dependent on Polthetamediated repair. Nature 518, 258-262.   DOI   ScienceOn
50 Chen, C.C., Kennedy, R.D., Sidi, S., Look, A.T., and D'Andrea, A. (2009). CHK1 inhibition as a strategy for targeting Fanconi Anemia (FA) DNA repair pathway deficient tumors. Mol. Cancer 8, 24.   DOI   ScienceOn
51 Chen, X.B., Melchionna, R., Denis, C.M., Gaillard, P.H., Blasina, A., Van de Weyer, I., Boddy, M.N., Russell, P., Vialard, J., and McGowan, C.H. (2001). Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell 8, 1117-1127.   DOI   ScienceOn
52 Chen, J., Dexheimer, T.S., Ai, Y., Liang, Q., Villamil, M.A., Inglese, J., Maloney, D.J., Jadhav, A., Simeonov, A., and Zhuang, Z. (2011). Selective and cell-active inhibitors of the USP1/UAF1 deubiquitinase complex reverse cisplatin resistance in non-small cell lung cancer cells. Chem. Biol. 18, 1390-1400.   DOI   ScienceOn
53 Collins, N.B., Wilson, J.B., Bush, T., Thomashevski, A., Roberts, K.J., Jones, N.J., and Kupfer, G.M. (2009). ATR-dependent phosphorylation of FANCA on serine 1449 after DNA damage is important for FA pathway function. Blood 113, 2181-2190.   DOI   ScienceOn
54 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., et al. (2006). Chemosensitization to cisplatin by inhibitors of the Fanconi anemia/BRCA pathway. Mol. Cancer Ther. 5, 952-961.   DOI   ScienceOn
55 Clauson, C., Scharer, O.D., and Niedernhofer, L. (2013). Advances in understanding the complex mechanisms of DNA interstrand cross-link repair. Cold Spring Harbor Perspect. Biol. 5, a012732.
56 Cohn, M.A., Kowal, P., Yang, K., Haas, W., Huang, T.T., Gygi, S.P., and D'Andrea, A.D. (2007). A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol. Cell 28, 786-797.   DOI   ScienceOn
57 Collis, S.J., Ciccia, A., Deans, A.J., Horejsi, Z., Martin, J.S., Maslen, S.L., Skehel, J.M., Elledge, S.J., West, S.C., and Boulton, S.J. (2008). FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol. Cell 32, 313-324.   DOI   ScienceOn
58 Cybulski, K.E., and Howlett, N.G. (2011). FANCP/SLX4: a Swiss army knife of DNA interstrand crosslink repair. Cell Cycle 10, 1757-1763.   DOI
59 D'Andrea, A.D. (2010). Susceptibility pathways in Fanconi's anemia and breast cancer. N Engl. J. Med. 362, 1909-1919.   DOI   ScienceOn
60 Deans, A.J., and West, S.C. (2009). FANCM connects the genome instability disorders Bloom's Syndrome and Fanconi Anemia. Mol. Cell 36, 943-953.   DOI   ScienceOn
61 Deans, A.J., and West, S.C. (2011). DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 11, 467-480.   DOI   ScienceOn
62 Gaillard, H., Garcia-Muse, T., and Aguilera, A. (2015). Replication stress and cancer. Nat. Rev. Cancer 15, 276-289.   DOI   ScienceOn
63 Di Micco, R., Fumagalli, M., Cicalese, A., Piccinin, S., Gasparini, P., Luise, C., Schurra, C., Garre, M., Nuciforo, P.G., Bensimon, A., et al. (2006). Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444, 638-642.   DOI   ScienceOn
64 Doles, J., Oliver, T.G., Cameron, E.R., Hsu, G., Jacks, T., Walker, G.C., and Hemann, M.T. (2010). Suppression of Rev3, the catalytic subunit of Pol{zeta}, sensitizes drug-resistant lung tumors to chemotherapy. Proc. Natl. Acad. Sci. USA 107, 20786-20791.   DOI   ScienceOn
65 Farmer, H., McCabe, N., Lord, C.J., Tutt, A.N., Johnson, D.A., Richardson, T.B., Santarosa, M., Dillon, K.J., Hickson, I., Knights, C., et al. (2005). Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917-921.   DOI   ScienceOn
66 Garaycoechea, J.I., and Patel, K.J. (2014). Why does the bone marrow fail in Fanconi anemia? Blood 123, 26-34.   DOI   ScienceOn
67 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.   DOI   ScienceOn
68 Gari, K., Decaillet, C., Delannoy, M., Wu, L., and Constantinou, A. (2008). Remodeling of DNA replication structures by the branch point translocase FANCM. Proc. Natl. Acad. Sci. USA 105, 16107-16112.   DOI   ScienceOn
69 Gibbs-Seymour, I., Oka, Y., Rajendra, E., Weinert, B.T., Passmore, L.A., Patel, K.J., Olsen, J.V., Choudhary, C., Bekker-Jensen, S., and Mailand, N. (2015). Ubiquitin-SUMO circuitry controls activated fanconi anemia ID complex dosage in response to DNA damage. Mol. Cell 57, 150-164.   DOI   ScienceOn
70 Guainazzi, A., and Scharer, O.D. (2010). Using synthetic DNA interstrand crosslinks to elucidate repair pathways and identify new therapeutic targets for cancer chemotherapy. Cell Mol Life Sci. 67, 3683-3697.   DOI
71 Guervilly, J.H., Takedachi, A., Naim, V., Scaglione, S., Chawhan, C., Lovera, Y., Despras, E., Kuraoka, I., Kannouche, P., Rosselli, F., et al. (2015). The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability. Mol. Cell 57, 123-137.   DOI   ScienceOn
72 Hira, A., Yoshida, K., Sato, K., Okuno, Y., Shiraishi, Y., Chiba, K., Tanaka, H., Miyano, S., Shimamoto, A., Tahara, H., et al. (2015). Mutations in the gene encoding the E2 conjugating enzyme UBE2T cause Fanconi Anemia. Am. J. Hum. Genet. 96, 1001-1007.   DOI   ScienceOn
73 Ho, G.P., Margossian, S., Taniguchi, T., and D'Andrea, A.D. (2006). Phosphorylation of FANCD2 on two novel sites is required for mitomycin C resistance. Mol. Cell. Biol. 26, 7005-7015.   DOI   ScienceOn
74 Hodskinson, M.R., Silhan, J., Crossan, G.P., Garaycoechea, J.I., Mukherjee, S., Johnson, C.M., Scharer, O.D., and Patel, K.J. (2014). Mouse SLX4 is a tumor suppressor that stimulates the activity of the nuclease XPF-ERCC1 in DNA crosslink repair. Mol. Cell 54, 472-484.   DOI   ScienceOn
75 Huang, M., Kim, J.M., Shiotani, B., Yang, K., Zou, L., and D'Andrea, A.D. (2010). The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response. Mol. Cell 39, 259-268.   DOI   ScienceOn
76 Huang, M., Kennedy, R., Ali, A.M., Moreau, L.A., Meetei, A.R., D'Andrea, A.D., and Chen, C.C. (2011). Human MutS and FANCM complexes function as redundant DNA damage sensors in the Fanconi Anemia pathway. DNA Repair 10, 1203-1212.   DOI   ScienceOn
77 Johnson, N., Li, Y.C., Walton, Z.E., Cheng, K.A., Li, D., Rodig, S.J., Moreau, L.A., Unitt, C., Bronson, R.T., Thomas, H.D., et al. (2011). Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat. Med. 17, 875-882.   DOI   ScienceOn
78 Huang, Y., Leung, J.W., Lowery, M., Matsushita, N., Wang, Y., Shen, X., Huong, D., Takata, M., Chen, J., and Li, L. (2014). Modularized functions of the Fanconi anemia core complex. Cell Rep. 7, 1849-1857.   DOI   ScienceOn
79 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.   DOI   ScienceOn
80 Jacquemont, C., and Taniguchi, T. (2007). Proteasome function is required for DNA damage response and fanconi anemia pathway activation. Cancer Res. 67, 7395-7405.   DOI   ScienceOn
81 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.   DOI   ScienceOn
82 Kandoth, C., McLellan, M.D., Vandin, F., Ye, K., Niu, B., Lu, C., Xie, M., Zhang, Q., McMichael, J.F., Wyczalkowski, M.A., et al. (2013). Mutational landscape and significance across 12 major cancer types. Nature 502, 333-339.   DOI   ScienceOn
83 Kee, Y., Huang, M., Chang, S., Moreau, L.A., Park, E., Smith, P.G., and D'Andrea, A.D. (2012). Inhibition of the Nedd8 system sensitizes cells to DNA interstrand cross-linking agents. Mol. Cancer Res. 10, 369-377.   DOI
84 Kim, H., and D'Andrea, A.D. (2012). Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev. 26, 1393-1408.   DOI   ScienceOn
85 Kennedy, R.D., Chen, C.C., Stuckert, P., Archila, E.M., De la Vega, M.A., Moreau, L.A., Shimamura, A., and D'Andrea, A.D. (2007). Fanconi anemia pathway-deficient tumor cells are hypersensitive to inhibition of ataxia telangiectasia mutated. J. Clin. Invest. 117, 1440-1449.   DOI   ScienceOn
86 Kikuchi, S., Hara, K., Shimizu, T., Sato, M., and Hashimoto, H. (2012). Structural basis of recruitment of DNA polymerase zeta by interaction between REV1 and REV7 proteins. J. Biol. Chem. 287, 33847-33852.   DOI
87 Kim, Y. (2014). Nuclease delivery: versatile functions of SLX4/FANCP in genome maintenance. Mol. Cells 37, 569-574.   DOI   ScienceOn
88 Kim, J.M., Parmar, K., Huang, M., Weinstock, D.M., Ruit, C.A., Kutok, J.L., and D'Andrea, A.D. (2009). Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype. Dev. Cell 16, 314-320.   DOI   ScienceOn
89 Kim, H., Yang, K., Dejsuphong, D., and D'Andrea, A.D. (2012). Regulation of Rev1 by the Fanconi anemia core complex. Nat. Struct. Mol. Biol. 19, 164-170.   DOI   ScienceOn
90 Klein Douwel, D., Boonen, R.A., Long, D.T., Szypowska, A.A., Raschle, M., Walter, J.C., and Knipscheer, P. (2014). XPFERCC1 acts in Unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol. Cell 54, 460-471.   DOI   ScienceOn
91 Knipscheer, P., Raschle, M., Smogorzewska, A., Enoiu, M., Ho, T.V., Scharer, O.D., Elledge, S.J., and Walter, J.C. (2009). The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 326, 1698-1701.   DOI   ScienceOn
92 Lehmann, A.R., Niimi, A., Ogi, T., Brown, S., Sabbioneda, S., Wing, J.F., Kannouche, P.L., and Green, C.M. (2007). Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair 6, 891-899.   DOI   ScienceOn
93 Kottemann, M.C., and Smogorzewska, A. (2013). Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493, 356-363.   DOI   ScienceOn
94 Landais, I., Sobeck, A., Stone, S., LaChapelle, A., and Hoatlin, M.E. (2009). A novel cell-free screen identifies a potent inhibitor of the Fanconi anemia pathway. Int. J. Cancer 124, 783-792.   DOI   ScienceOn
95 Langevin, F., Crossan, G.P., Rosado, I.V., Arends, M.J., and Patel, K.J. (2011). Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature 475, 53-58.   DOI   ScienceOn
96 Leung, J.W., Wang, Y., Fong, K.W., Huen, M.S., Li, L., and Chen, J. (2012). Fanconi anemia (FA) binding protein FAAP20 stabilizes FA complementation group A (FANCA) and participates in interstrand cross-link repair. Proc. Natl. Acad. Sci. USA 109, 4491-4496.   DOI
97 Liang, Q., Dexheimer, T.S., Zhang, P., Rosenthal, A.S., Villamil, M.A., You, C., Zhang, Q., Chen, J., Ott, C.A., Sun, H., et al. (2014). A selective USP1-UAF1 inhibitor links deubiquitination to DNA damage responses. Nat. Chem. Biol. 10, 298-304.   DOI   ScienceOn
98 Liang, C.C., Zhan, B., Yoshikawa, Y., Haas, W., Gygi, S.P., and Cohn, M.A. (2015). UHRF1 is a sensor for DNA interstrand crosslinks and recruits FANCD2 to initiate the Fanconi anemia pathway. Cell Rep. 10, 1947-1956.   DOI   ScienceOn
99 Liu, Y., Tarsounas, M., O'Regan, P., and West, S.C. (2007). Role of RAD51C and XRCC3 in genetic recombination and DNA repair. J. Biol. Chem. 282, 1973-1979.   DOI   ScienceOn