Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

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)
  • Received : 2015.06.17
  • Accepted : 2015.06.19
  • Published : 2015.08.31
Download PDF
⟨ Previous Next ⟩

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

References

  1. 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. https://doi.org/10.1038/nature05268
  2. 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. https://doi.org/10.1093/hmg/dds013
  3. 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. https://doi.org/10.1016/j.ajhg.2013.04.002
  4. 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. https://doi.org/10.1038/nature03443
  5. 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]
  6. 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. https://doi.org/10.1016/j.molcel.2012.02.015
  7. 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. https://doi.org/10.1038/nature14184
  8. Chang, D.J., and Cimprich, K.A. (2009). DNA damage tolerance:when it's OK to make mistakes. Nat. Chem. Biol. 5, 82-90. https://doi.org/10.1038/nchembio.139
  9. 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. https://doi.org/10.1186/1476-4598-8-24
  10. 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. https://doi.org/10.1016/S1097-2765(01)00375-6
  11. 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. https://doi.org/10.1016/j.chembiol.2011.08.014
  12. 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. https://doi.org/10.1158/1535-7163.MCT-05-0493
  13. 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.
  14. 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. https://doi.org/10.1016/j.molcel.2007.09.031
  15. 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. https://doi.org/10.1182/blood-2008-05-154294
  16. 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. https://doi.org/10.1016/j.molcel.2008.10.014
  17. Cybulski, K.E., and Howlett, N.G. (2011). FANCP/SLX4: a Swiss army knife of DNA interstrand crosslink repair. Cell Cycle 10, 1757-1763. https://doi.org/10.4161/cc.10.11.15818
  18. D'Andrea, A.D. (2010). Susceptibility pathways in Fanconi's anemia and breast cancer. N Engl. J. Med. 362, 1909-1919. https://doi.org/10.1056/NEJMra0809889
  19. 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. https://doi.org/10.1016/j.molcel.2009.12.006
  20. Deans, A.J., and West, S.C. (2011). DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 11, 467-480. https://doi.org/10.1038/nrc3088
  21. 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. https://doi.org/10.1038/nature05327
  22. 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. https://doi.org/10.1073/pnas.1011409107
  23. 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. https://doi.org/10.1038/nature03445
  24. Gaillard, H., Garcia-Muse, T., and Aguilera, A. (2015). Replication stress and cancer. Nat. Rev. Cancer 15, 276-289. https://doi.org/10.1038/nrc3916
  25. Garaycoechea, J.I., and Patel, K.J. (2014). Why does the bone marrow fail in Fanconi anemia? Blood 123, 26-34. https://doi.org/10.1182/blood-2013-09-427740
  26. 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. https://doi.org/10.1016/S1097-2765(01)00173-3
  27. 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. https://doi.org/10.1073/pnas.0804777105
  28. 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. https://doi.org/10.1016/j.molcel.2014.12.001
  29. 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. https://doi.org/10.1007/s00018-010-0492-6
  30. 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. https://doi.org/10.1016/j.molcel.2014.11.014
  31. 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. https://doi.org/10.1016/j.ajhg.2015.04.022
  32. 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. https://doi.org/10.1128/MCB.02018-05
  33. 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. https://doi.org/10.1016/j.molcel.2014.03.014
  34. 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. https://doi.org/10.1016/j.molcel.2010.07.005
  35. 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. https://doi.org/10.1016/j.dnarep.2011.09.006
  36. 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. https://doi.org/10.1016/j.celrep.2014.04.029
  37. 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. https://doi.org/10.1038/nsmb.1504
  38. Jacquemont, C., and Taniguchi, T. (2007). Proteasome function is required for DNA damage response and fanconi anemia pathway activation. Cancer Res. 67, 7395-7405. https://doi.org/10.1158/0008-5472.CAN-07-1015
  39. 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. https://doi.org/10.1038/nm.2377
  40. 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. https://doi.org/10.1126/science.1205805
  41. 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. https://doi.org/10.1038/nature12634
  42. 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. https://doi.org/10.1158/1541-7786.MCR-11-0497
  43. 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. https://doi.org/10.1172/JCI31245
  44. 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. https://doi.org/10.1074/jbc.M112.396838
  45. Kim, Y. (2014). Nuclease delivery: versatile functions of SLX4/FANCP in genome maintenance. Mol. Cells 37, 569-574. https://doi.org/10.14348/molcells.2014.0118
  46. 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. https://doi.org/10.1101/gad.195248.112
  47. 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. https://doi.org/10.1016/j.devcel.2009.01.001
  48. 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. https://doi.org/10.1038/nsmb.2222
  49. 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. https://doi.org/10.1016/j.molcel.2014.03.015
  50. 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. https://doi.org/10.1126/science.1182372
  51. Kottemann, M.C., and Smogorzewska, A. (2013). Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493, 356-363. https://doi.org/10.1038/nature11863
  52. 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. https://doi.org/10.1002/ijc.24039
  53. 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. https://doi.org/10.1038/nature10192
  54. 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. https://doi.org/10.1016/j.dnarep.2007.02.003
  55. 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. https://doi.org/10.1073/pnas.1118720109
  56. 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. https://doi.org/10.1038/nchembio.1455
  57. 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. https://doi.org/10.1016/j.celrep.2015.02.053
  58. 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. https://doi.org/10.1074/jbc.M609066200
  59. 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. https://doi.org/10.1016/j.molcel.2014.08.012
  60. 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. https://doi.org/10.1038/nature14157
  61. 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. https://doi.org/10.1038/ng1241
  62. 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. https://doi.org/10.1038/ng1626
  63. 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. https://doi.org/10.1158/1535-7163.MCT-13-0103-T
  64. 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. https://doi.org/10.1016/S1097-2765(01)00174-5
  65. 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. https://doi.org/10.1038/nrm2858
  66. 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. https://doi.org/10.1016/j.molcel.2004.08.009
  67. 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. https://doi.org/10.1016/j.molcel.2005.01.008
  68. 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. https://doi.org/10.1074/jbc.M113.533976
  69. Psakhye, I., and Jentsch, S. (2012). Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820. https://doi.org/10.1016/j.cell.2012.10.021
  70. 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. https://doi.org/10.1016/j.molcel.2014.05.001
  71. 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. https://doi.org/10.1016/j.cell.2008.08.030
  72. 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. https://doi.org/10.1126/science.1253671
  73. 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. https://doi.org/10.1158/2159-8290.CD-14-1156
  74. 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. https://doi.org/10.1038/emboj.2009.385
  75. 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. https://doi.org/10.1016/j.molcel.2010.01.036
  76. 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. https://doi.org/10.1158/0008-5472.CAN-12-3976
  77. 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. https://doi.org/10.1016/j.cell.2007.03.009
  78. 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. https://doi.org/10.1016/j.molcel.2010.06.023
  79. 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. https://doi.org/10.1016/j.celrep.2015.03.038
  80. 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. https://doi.org/10.1016/j.celrep.2014.04.005
  81. 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. https://doi.org/10.1038/ng.570
  82. 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. https://doi.org/10.1146/annurev-biophys-051013-022737
  83. 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. https://doi.org/10.1128/MCB.02357-06
  84. 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. https://doi.org/10.1215/15228517-2009-015
  85. 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. https://doi.org/10.1101/gad.15699211
  86. 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. https://doi.org/10.1182/blood-2010-10-311761
  87. 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. https://doi.org/10.1016/j.cell.2011.07.040
  88. 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. https://doi.org/10.1093/hmg/ddr366
  89. 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. https://doi.org/10.1074/jbc.M112.394841
  90. 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. https://doi.org/10.1016/j.molcel.2006.05.022
  91. 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. https://doi.org/10.1073/pnas.1011412107
  92. 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. https://doi.org/10.1172/JCI79325
  93. 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. https://doi.org/10.1073/pnas.1018487108
  94. 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. https://doi.org/10.1016/j.molcel.2010.01.039
  95. 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. https://doi.org/10.1101/gad.17020911
  96. 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. https://doi.org/10.1158/0008-5472.CAN-09-2616
  97. 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.
  98. 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. https://doi.org/10.1038/nsmb.2956
  99. 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. https://doi.org/10.1038/ng.2347

Cited by

  1. BRCA1alterations with additional defects in DNA damage response genes may confer chemoresistance to BRCA-like breast cancers treated with neoadjuvant chemotherapy vol.56, pp.5, 2017, https://doi.org/10.1002/gcc.22445
  2. The Emerging Role of Non-traditional Ubiquitination in Oncogenic Pathways vol.292, pp.9, 2017, https://doi.org/10.1074/jbc.R116.755694
  3. Silencing of FANCD2 enhances the radiosensitivity of metastatic cervical lymph node-derived head and neck squamous cell carcinoma HSC-4 cells vol.50, pp.4, 2017, https://doi.org/10.3892/ijo.2017.3902
  4. Synthetic lethal approaches for assessing combinatorial efficacy of chemotherapeutic drugs vol.162, 2016, https://doi.org/10.1016/j.pharmthera.2016.01.014
  5. Involvement of FANCD2 in Energy Metabolism via ATP5α vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-05150-1
  6. Drugging the Cancers Addicted to DNA Repair vol.109, pp.11, 2017, https://doi.org/10.1093/jnci/djx059
  7. Strategic role of the ubiquitin-dependent segregase p97 (VCP or Cdc48) in DNA replication vol.126, pp.1, 2017, https://doi.org/10.1007/s00412-016-0587-4
  8. Paths from DNA damage and signaling to genome rearrangements via homologous recombination 2017, https://doi.org/10.1016/j.mrfmmm.2017.07.008
  9. The FANCD2–FANCI complex is recruited to DNA interstrand crosslinks before monoubiquitination of FANCD2 vol.7, 2016, https://doi.org/10.1038/ncomms12124
  10. New insights into diagnosis and therapeutic options for proliferative hepatoblastoma vol.68, pp.1, 2018, https://doi.org/10.1002/hep.29672
  11. FBW7 regulates DNA interstrand cross-link repair by modulating FAAP20 degradation vol.7, pp.24, 2015, https://doi.org/10.18632/oncotarget.9595
  12. DUOXA1-mediated ROS production promotes cisplatin resistance by activating ATR-Chk1 pathway in ovarian cancer vol.428, pp.None, 2015, https://doi.org/10.1016/j.canlet.2018.04.029
  13. Genome-wide analysis of canine oral malignant melanoma metastasis-associated gene expression vol.9, pp.None, 2015, https://doi.org/10.1038/s41598-019-42839-x
  14. Prolyl isomerization of FAAP20 catalyzed by PIN1 regulates the Fanconi anemia pathway vol.15, pp.2, 2015, https://doi.org/10.1371/journal.pgen.1007983
  15. Fanconi anemia and the underlying causes of genomic instability vol.61, pp.7, 2015, https://doi.org/10.1002/em.22358
  16. Acetylation modulates the Fanconi anemia pathway by protecting FAAP20 from ubiquitin-mediated proteasomal degradation vol.295, pp.40, 2020, https://doi.org/10.1074/jbc.ra120.015288
  17. Structural insight into FANCI–FANCD2 monoubiquitination vol.64, pp.5, 2015, https://doi.org/10.1042/ebc20200001
  18. The ubiquitination machinery of the Fanconi Anemia DNA repair pathway vol.163, pp.None, 2015, https://doi.org/10.1016/j.pbiomolbio.2020.09.009