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Protein & Cell

, Volume 2, Issue 9, pp 704–711 | Cite as

The Fanconi anemia pathway and DNA interstrand cross-link repair

  • Xiaoyu Su
  • Jun HuangEmail author
Review

Abstract

Fanconi anemia (FA) is an autosomal or X-linked recessive disorder characterized by chromosomal instability, bone marrow failure, cancer susceptibility, and a profound sensitivity to agents that produce DNA interstrand cross-link (ICL). To date, 15 genes have been identified that, when mutated, result in FA or an FA-like syndrome. It is believed that cellular resistance to DNA interstrand cross-linking agents requires all 15 FA or FA-like proteins. Here, we review our current understanding of how these FA proteins participate in ICL repair and discuss the molecular mechanisms that regulate the FA pathway to maintain genome stability.

Keywords

Fanconi anemia DNA interstrand crosslink repair FANCD2-FANCI mono-ubiquitylation chromosomal instability 

References

  1. 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.CrossRefGoogle Scholar
  2. Alpi, A.F., Pace, P.E., Babu, M.M., and Patel, K.J. (2008). Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol Cell 32, 767–777.CrossRefGoogle Scholar
  3. Alter, B.P., Greene, M.H., Velazquez, I., and Rosenberg, P.S. (2003). Cancer in Fanconi anemia. Blood 101, 2072.CrossRefGoogle Scholar
  4. Auerbach, A.D. (1988). A test for Fanconi’s anemia. Blood 72, 366–367.Google Scholar
  5. Bandaru, V., Sunkara, S., Wallace, S.S., and Bond, J.P. (2002). A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair (Amst) 1, 517–529.CrossRefGoogle Scholar
  6. Bhagwat, N., Olsen, A.L., Wang, A.T., Hanada, K., Stuckert, P., Kanaar, R., D’Andrea, A., Niedernhofer, L.J., and McHugh, P.J. (2009). XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair. Mol Cell Biol 29, 6427–6437.CrossRefGoogle Scholar
  7. Brown, S., Niimi, A., and Lehmann, A.R. (2009). Ubiquitination and deubiquitination of PCNA in response to stalling of the replication fork. Cell Cycle 8, 689–692.CrossRefGoogle Scholar
  8. Ciccia, A., Ling, C., Coulthard, R., Yan, Z., Xue, Y., Meetei, A.R., Laghmani, H., Joenje, H., McDonald, N., de Winter, J.P., et al. (2007). Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 25, 331–343.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. Cole, R.S. (1973). Repair of DNA containing interstrand crosslinks in Escherichia coli: sequential excision and recombination. Proc Natl Acad Sci U S A 70, 1064–1068.CrossRefGoogle Scholar
  11. Crossan, G.P., van der Weyden, L., Rosado, I.V., Langevin, F., Gaillard, P.H., McIntyre, R.E., Gallagher, F., Kettunen, M.I., Lewis, D.Y., Brindle, K., et al., and the Sanger Mouse Genetics Project. (2011). Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat Genet 43, 147–152.CrossRefGoogle Scholar
  12. D’Andrea, A.D., and Grompe, M. (2003). The Fanconi anaemia/BRCA pathway. Nat Rev Cancer 3, 23–34.CrossRefGoogle Scholar
  13. de Groote, F.H., Jansen, J.G., Masuda, Y., Shah, D.M., Kamiya, K., de Wind, N., and Siegal, G. (2011). The Rev1 translesion synthesis polymerase has multiple distinct DNA binding modes. DNA Repair (Amst) 10, 915–925.CrossRefGoogle Scholar
  14. De Silva, I.U., McHugh, P.J., Clingen, P.H., and Hartley, J.A. (2000). Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol Cell Biol 20, 7980–7990.CrossRefGoogle Scholar
  15. de Winter, J.P., and Joenje, H. (2009). The genetic and molecular basis of Fanconi anemia. Mutat Res 668, 11–19.CrossRefGoogle Scholar
  16. 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.Google Scholar
  17. Dronkert, M.L., and Kanaar, R. (2001). Repair of DNA interstrand cross-links. Mutat Res 486, 217–247.CrossRefGoogle Scholar
  18. Evans, E., Fellows, J., Coffer, A., and Wood, R.D. (1997). Open complex formation around a lesion during nucleotide excision repair provides a structure for cleavage by human XPG protein. EMBO J 16, 625–638.CrossRefGoogle Scholar
  19. Fekairi, S., Scaglione, S., Chahwan, C., Taylor, E.R., Tissier, A., Coulon, S., Dong, M.Q., Ruse, C., Yates, J.R. 3rd, Russell, P., et al. (2009). Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138, 78–89.CrossRefGoogle Scholar
  20. Friedel, A.M., Pike, B.L., and Gasser, S.M. (2009). ATR/Mec1: coordinating fork stability and repair. Curr Opin Cell Biol 21, 237–244.CrossRefGoogle Scholar
  21. Garcia-Higuera, I., Kuang, Y., Denham, J., and D’Andrea, A.D. (2000). The fanconi anemia proteins FANCA and FANCG stabilize each other and promote the nuclear accumulation of the Fanconi anemia complex. Blood 96, 3224–3230.Google Scholar
  22. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M., and D’Andrea, A.D. (2001a). Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7, 249–262.CrossRefGoogle Scholar
  23. Geng, L., Huntoon, C.J., and Karnitz, L.M. (2010). RAD18-mediated ubiquitination of PCNA activates the Fanconi anemia DNA repair network. J Cell Biol 191, 249–257.CrossRefGoogle Scholar
  24. German, J., Schonberg, S., Caskie, S., Warburton, D., Falk, C., and Ray, J.H. (1987). A test for Fanconi’s anemia. Blood 69, 1637–1641.Google Scholar
  25. 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.CrossRefGoogle Scholar
  26. Grossmann, K.F., Ward, A.M., Matkovic, M.E., Folias, A.E., and Moses, R.E. (2001). S. cerevisiae has three pathways for DNA interstrand crosslink repair. Mutat Res 487, 73–83.CrossRefGoogle Scholar
  27. Guo, C., Sonoda, E., Tang, T.S., Parker, J.L., Bielen, A.B., Takeda, S., Ulrich, H.D., and Friedberg, E.C. (2006). REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol Cell 23, 265–271.CrossRefGoogle Scholar
  28. Gurtan, A.M., Stuckert, P., and D’Andrea, A.D. (2006). The WD40 repeats of FANCL are required for Fanconi anemia core complex assembly. J Biol Chem 281, 10896–10905.CrossRefGoogle Scholar
  29. Hanada, K., Budzowska, M., Modesti, M., Maas, A., Wyman, C., Essers, J., and Kanaar, R. (2006). The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J 25, 4921–4932.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. Hodson, C., Cole, A.R., Lewis, L.P., Miles, J.A., Purkiss-Trew, A., and Walden, H. (2011). Structural analysis of human FANCL, the E3 ligase in the fanconi anemia pathway. J Biol Chem Jul 20. [Epub ahead of print].Google Scholar
  32. Howlett, N.G., Harney, J.A., Rego, M.A., Kolling, F.W. 4th, and Glover, T.W. (2009). Functional interaction between the Fanconi Anemia D2 protein and proliferating cell nuclear antigen (PCNA) via a conserved putative PCNA interaction motif. J Biol Chem 284, 28935–28942.CrossRefGoogle Scholar
  33. Huang, T.T., Nijman, S.M., Mirchandani, K.D., Galardy, P.J., Cohn, M. A., Haas, W., Gygi, S.P., Ploegh, H.L., Bernards, R., and D’Andrea, A.D. (2006). Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat Cell Biol 8, 339–347.Google Scholar
  34. Hussain, S., Wilson, J.B., Medhurst, A.L., Hejna, J., Witt, E., Ananth, S., Davies, A., Masson, J.Y., Moses, R., West, S.C., et al. (2004). Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum Mol Genet 13, 1241–1248.CrossRefGoogle Scholar
  35. Ishiai, M., Kitao, H., Smogorzewska, A., Tomida, J., Kinomura, A., Uchida, E., Saberi, A., Kinoshita, E., Kinoshita-Kikuta, E., Koike, T., et al. (2008a). FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat Struct Mol Biol 15, 1138–1146.CrossRefGoogle Scholar
  36. Ishiai, M., Kitao, H., Smogorzewska, A., Tomida, J., Kinomura, A., Uchida, E., Saberi, A., Kinoshita, E., Kinoshita-Kikuta, E., Koike, T., et al. (2008b). FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat Struct Mol Biol 15, 1138–1146.CrossRefGoogle Scholar
  37. Kee, Y., and D’Andrea, A.D. (2010). Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 24, 1680–1694.CrossRefGoogle Scholar
  38. Kennedy, R.D., and D’Andrea, A.D. (2005). The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev 19, 2925–2940.CrossRefGoogle Scholar
  39. Kim, J.M., Kee, Y., Gurtan, A., and D’Andrea, A.D. (2008). Cell cycledependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood 111, 5215–5222.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. Kim, Y., Lach, F.P., Desetty, R., Hanenberg, H., Auerbach, A.D., and Smogorzewska, A. (2011). Mutations of the SLX4 gene in Fanconi anemia. Nat Genet 43, 142–146.CrossRefGoogle Scholar
  42. Knipscheer, P., Räschle, M., Smogorzewska, A., Enoiu, M., Ho, T.V., Schärer, 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.CrossRefGoogle Scholar
  43. Kratz, K., Schöpf, B., Kaden, S., Sendoel, A., Eberhard, R., Lademann, C., Cannavó, E., Sartori, A.A., Hengartner, M.O., and Jiricny, J. (2010). Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142, 77–88.CrossRefGoogle Scholar
  44. Kumaraswamy, E., and Shiekhattar, R. (2007). Activation of BRCA1/BRCA2-associated helicase BACH1 is required for timely progression through S phase. Mol Cell Biol 27, 6733–6741.CrossRefGoogle Scholar
  45. Kuraoka, I., Kobertz, W.R., Ariza, R.R., Biggerstaff, M., Essigmann, J. M., and Wood, R.D. (2000). Repair of an interstrand DNA crosslink initiated by ERCC1-XPF repair/recombination nuclease. J Biol Chem 275, 26632–26636.CrossRefGoogle Scholar
  46. Lehoczký, P., McHugh, P.J., and Chovanec, M. (2007). DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol Rev 31, 109–133.CrossRefGoogle Scholar
  47. Ling, C., Ishiai, M., Ali, A.M., Medhurst, A.L., Neveling, K., Kalb, R., Yan, Z., Xue, Y., Oostra, A.B., Auerbach, A.D., et al. (2007). FAAP100 is essential for activation of the Fanconi anemia-associated DNA damage response pathway. EMBO J 26, 2104–2114.CrossRefGoogle Scholar
  48. Liu, T., Ghosal, G., Yuan, J., Chen, J., and Huang, J. (2010). FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329, 693–696.CrossRefGoogle Scholar
  49. Long, D.T., Räschle, M., Joukov, V., and Walter, J.C. (2011). Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333, 84–87.CrossRefGoogle Scholar
  50. Machida, Y.J., Machida, Y., Chen, Y., Gurtan, A.M., Kupfer, G.M., D’Andrea, A.D., and Dutta, A. (2006). UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation. Mol Cell 23, 589–596.CrossRefGoogle Scholar
  51. MacKay, C., Déclais, A.C., Lundin, C., Agostinho, A., Deans, A.J., MacArtney, T.J., Hofmann, K., Gartner, A., West, S.C., Helleday, T., et al. (2010). Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142, 65–76.CrossRefGoogle Scholar
  52. Medhurst, A.L., Laghmani, H., Steltenpool, J., Ferrer, M., Fontaine, C., de Groot, J., Rooimans, M.A., Scheper, R.J., Meetei, A.R., Wang, W., et al. (2006). Evidence for subcomplexes in the Fanconi anemia pathway. Blood 108, 2072–2080.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. Meindl, A., Hellebrand, H., Wiek, C., Erven, V., Wappenschmidt, B., Niederacher, D., Freund, M., Lichtner, P., Hartmann, L., Schaal, H., et al. (2010). Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet 42, 410–414.CrossRefGoogle Scholar
  55. Mirchandani, K.D., and D’Andrea, A.D. (2006). The Fanconi anemia/BRCA pathway: a coordinator of cross-link repair. Exp Cell Res 312, 2647–2653.CrossRefGoogle Scholar
  56. Moldovan, G.L., and D’Andrea, A.D. (2009). How the fanconi anemia pathway guards the genome. Annu Rev Genet 43, 223–249.CrossRefGoogle Scholar
  57. 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. (2005). Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 105, 1003–1009CrossRefGoogle Scholar
  58. Muñoz, I.M., Hain, K., Déclais, A.C., Gardiner, M., Toh, G.W., Sanchez-Pulido, L., Heuckmann, J.M., Toth, R., Macartney, T., Eppink, B., et al. (2009). Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 35, 116–127.CrossRefGoogle Scholar
  59. Murai, J., Yang, K., Dejsuphong, D., Hirota, K., Takeda, S., and D’Andrea, A.D. (2011). The USP1/UAF1 complex promotes double-strand break repair through homologous recombination. Mol Cell Biol 31, 2462–2469.CrossRefGoogle Scholar
  60. Niedernhofer, L.J., Lalai, A.S., and Hoeijmakers, J.H. (2005). Fanconi anemia (cross)linked to DNA repair. Cell 123, 1191–1198.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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.CrossRefGoogle Scholar
  63. Nojima, K., Hochegger, H., Saberi, A., Fukushima, T., Kikuchi, K., Yoshimura, M., Orelli, B.J., Bishop, D.K., Hirano, S., Ohzeki, M., et al. (2005). Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res 65, 11704–11711.CrossRefGoogle Scholar
  64. Oestergaard, V.H., Langevin, F., Kuiken, H.J., Pace, P., Niedzwiedz, W., Simpson, L.J., Ohzeki, M., Takata, M., Sale, J.E., and Patel, K. J. (2007). Deubiquitination of FANCD2 is required for DNA crosslink repair. Mol Cell 28, 798–809.CrossRefGoogle Scholar
  65. Pace, P., Johnson, M., Tan, W.M., Mosedale, G., Sng, C., Hoatlin, M., de Winter, J., Joenje, H., Gergely, F., and Patel, K.J. (2002). FANCE: the link between Fanconi anaemia complex assembly and activity. EMBO J 21, 3414–3423.CrossRefGoogle Scholar
  66. Ramaekers, C.H., and Wouters, B.G. (2011). Regulatory functions of ubiquitin in diverse DNA damage responses. Curr Mol Med 11, 152–169.CrossRefGoogle Scholar
  67. Rego, M.A., Kolling, F.W. 4th, and Howlett, N.G. (2009). The Fanconi anemia protein interaction network: casting a wide net. Mutat Res 668, 27–41.CrossRefGoogle Scholar
  68. Saffran, W.A., Ahmed, S., Bellevue, S., Pereira, G., Patrick, T., Sanchez, W., Thomas, S., Alberti, M., and Hearst, J.E. (2004). DNA repair defects channel interstrand DNA cross-links into alternate recombinational and error-prone repair pathways. J Biol Chem 279, 36462–36469.CrossRefGoogle Scholar
  69. Sasaki, M.S. (1975). Is Fanconi’s anaemia defective in a process essential to the repair of DNA cross links? Nature 257, 501–503.CrossRefGoogle Scholar
  70. 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.CrossRefGoogle Scholar
  71. Smogorzewska, A., Desetty, R., Saito, T.T., Schlabach, M., Lach, F.P., Sowa, M.E., Clark, A.B., Kunkel, T.A., Harper, J.W., Colaiácovo, 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.CrossRefGoogle Scholar
  72. 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.CrossRefGoogle Scholar
  73. Stoepker, C., Hain, K., Schuster, B., Hilhorst-Hofstee, Y., Rooimans, M.A., Steltenpool, J., Oostra, A.B., Eirich, K., Korthof, E.T., Nieuwint, A.W., et al. (2011). SLX4, a coordinator of structurespecific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet 43, 138–141.CrossRefGoogle Scholar
  74. Svendsen, J.M., Smogorzewska, A., Sowa, M.E., O’Connell, B.C., Gygi, S.P., Elledge, S.J., and Harper, J.W. (2009). Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138, 63–77.CrossRefGoogle Scholar
  75. Sy, S.M., Huen, M.S., and Chen, J. (2009). PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc Natl Acad Sci U S A 106, 7155–7160.CrossRefGoogle Scholar
  76. Taniguchi, T., and D’Andrea, A.D. (2002). The Fanconi anemia protein, FANCE, promotes the nuclear accumulation of FANCC. Blood 100, 2457–2462.CrossRefGoogle Scholar
  77. Thompson, L.H., Hinz, J.M., Yamada, N.A., and Jones, N.J. (2005). How Fanconi anemia proteins promote the four Rs: replication, recombination, repair, and recovery. Environ Mol Mutagen 45, 128–142.CrossRefGoogle Scholar
  78. 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.CrossRefGoogle Scholar
  79. Venkitaraman, A.R. (2004). Tracing the network connecting BRCA and Fanconi anaemia proteins. Nat Rev Cancer 4, 266–276.CrossRefGoogle Scholar
  80. Wang, W. (2007). Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat Rev Genet 8, 735–748.CrossRefGoogle Scholar
  81. Wang, X., Andreassen, P.R., and D’Andrea, A.D. (2004). Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol Cell Biol 24, 5850–5862.CrossRefGoogle Scholar
  82. Wang, X., Peterson, C.A., Zheng, H., Nairn, R.S., Legerski, R.J., and Li, L. (2001). Involvement of nucleotide excision repair in a recombination-independent and error-prone pathway of DNA interstrand cross-link repair. Mol Cell Biol 21, 713–720.CrossRefGoogle Scholar
  83. Waters, L.S., Minesinger, B.K., Wiltrout, M.E., D’souza, S., Woodruff, R.V., and Walker, G.C. (2009). Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Mol Biol Rev 73, 134–154.CrossRefGoogle Scholar
  84. 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.CrossRefGoogle Scholar
  85. Yamamoto, K.N., Kobayashi, S., Tsuda, M., Kurumizaka, H., Takata, M., Kono, K., Jiricny, J., Takeda, S., and Hirota, K. (2011a). Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc Natl Acad Sci U S A 108, 6492–6496.CrossRefGoogle Scholar
  86. Yamamoto, K.N., Kobayashi, S., Tsuda, M., Kurumizaka, H., Takata, M., Kono, K., Jiricny, J., Takeda, S., and Hirota, K. (2011b). Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc Natl Acad Sci U S A 108, 6492–6496.CrossRefGoogle Scholar
  87. 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.CrossRefGoogle Scholar
  88. Zhang, F., Fan, Q., Ren, K., and Andreassen, P.R. (2009). PALB2 functionally connects the breast cancer susceptibility proteins BRCA1 and BRCA2. Mol Cancer Res 7, 1110–1118.CrossRefGoogle Scholar

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© Higher Education Press and Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Life Sciences InstituteZhejiang UniversityHangzhouChina

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