The Fanconi anemia pathway and DNA interstrand cross-link repair

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 cross-link 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 17938197.
[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 19111657.
[3] Alter, B.P., Greene, M.H., Velazquez, I., and Rosenberg, P.S. (2003). Cancer in Fanconi anemia. Blood 101, 207212584146.
[4] Auerbach, A.D. (1988). A test for Fanconi’s anemia. Blood 72, 366-367 3291985.
[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 12509226.
[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 19805513.
[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 19221475.
[8] Ciccia, A., Ling, C., Coulthard, R., Yan, Z., Xue, Y., Meetei, A.R., Laghmani, H., Joenje, H., McDonald, N., de Winter, J.P., (2007). Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 25, 331-343 17289582.
[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 18082604.
[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 4577788.
[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., , 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 21240276.
[12] D’Andrea, A.D., and Grompe, M. (2003). The Fanconi anaemia/BRCA pathway. Nat Rev Cancer 3, 23-34 12509764.
[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 21752727.
[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 11027268.
[15] de Winter, J.P., and Joenje, H. (2009). The genetic and molecular basis of Fanconi anemia. Mutat Res 668, 11-19 19061902.
[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., (2007). Identification of the Fanconi anemia complementation group I gene, FANCI. Cell Oncol 29, 211-218 17452773.
[17] Dronkert, M.L., and Kanaar, R. (2001). Repair of DNA interstrand cross-links. Mutat Res 486, 217-247 11516927.
[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 9034344.
[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., (2009). Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138, 78-89 19596236.
[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 19230642.
[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 11050007.
[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 11239454.
[23] Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M., and D’Andrea, A.D. (2001b). Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7, 249-262 11239454.
[24] 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 20937699.
[25] 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 3107630.
[26] 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 12649160.
[27] 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 11738934.
[28] 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 16857592.
[29] 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 16474167.
[30] 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 17036055.
[31] 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 16943440.
[32] 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].
[33] 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 19704162.
[34] 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 16531995.
[35] Hussain, S., Wilson, J.B., Medhurst, A.L., Hejna, J., Witt, E., Ananth, S., Davies, A., Masson, J.Y., Moses, R., West, S.C., (2004). Direct interaction of FANCD2 with BRCA2 in DNA damage response pathways. Hum Mol Genet 13, 1241-1248 15115758.
[36] Ishiai, M., Kitao, H., Smogorzewska, A., Tomida, J., Kinomura, A., Uchida, E., Saberi, A., Kinoshita, E., Kinoshita-Kikuta, E., Koike, T., (2008a). FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat Struct Mol Biol 15, 1138-1146 18931676.
[37] Ishiai, M., Kitao, H., Smogorzewska, A., Tomida, J., Kinomura, A., Uchida, E., Saberi, A., Kinoshita, E., Kinoshita-Kikuta, E., Koike, T., (2008b). FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat Struct Mol Biol 15, 1138-1146 18931676.
[38] Kee, Y., and D’Andrea, A.D. (2010). Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 24, 1680-1694 20713514.
[39] Kennedy, R.D., and D’Andrea, A.D. (2005). The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev 19, 2925-2940 16357213.
[40] Kim, J.M., Kee, Y., Gurtan, A., and D’Andrea, A.D. (2008). Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood 111, 5215-5222 18174376.
[41] 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 19217432.
[42] 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 21240275.
[43] Knipscheer, P., R?schle, M., Smogorzewska, A., Enoiu, M., Ho, T.V., Sch?rer, 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 19965384.
[44] Kratz, K., Sch?pf, 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 20603016.
[45] 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 17664283.
[46] Kuraoka, I., Kobertz, W.R., Ariza, R.R., Biggerstaff, M., Essigmann, J.M., and Wood, R.D. (2000). Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J Biol Chem 275, 26632-26636 10882712.
[47] Lehoczky, P., McHugh, P.J., and Chovanec, M. (2007). DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol Rev 31, 109-133 17096663.
[48] Ling, C., Ishiai, M., Ali, A.M., Medhurst, A.L., Neveling, K., Kalb, R., Yan, Z., Xue, Y., Oostra, A.B., Auerbach, A.D., (2007). FAAP100 is essential for activation of the Fanconi anemia-associated DNA damage response pathway. EMBO J 26, 2104-2114 17396147.
[49] 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 20671156.
[50] Long, D.T., R?schle, M., Joukov, V., and Walter, J.C. (2011). Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333, 84-87 21719678.
[51] 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 16916645.
[52] MacKay, C., Déclais, A.C., Lundin, C., Agostinho, A., Deans, A.J., MacArtney, T.J., Hofmann, K., Gartner, A., West, S.C., Helleday, T., (2010). Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142, 65-76 20603015.
[53] 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., (2006). Evidence for subcomplexes in the Fanconi anemia pathway. Blood 108, 2072-2080 16720839.
[54] 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., (2003). A novel ubiquitin ligase is deficient in Fanconi anemia. Nat Genet 35, 165-170 12973351.
[55] Meindl, A., Hellebrand, H., Wiek, C., Erven, V., Wappenschmidt, B., Niederacher, D., Freund, M., Lichtner, P., Hartmann, L., Schaal, H., (2010). Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat Genet 42, 410-414 20400964.
[56] 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 16859679.
[57] Moldovan, G.L., and D’Andrea, A.D. (2009). How the fanconi anemia pathway guards the genome. Annu Rev Genet 43, 223-249 19686080.
[58] 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, 1003-1009 15454491
[59] Mu?oz, I.M., Hain, K., Déclais, A.C., Gardiner, M., Toh, G.W., Sanchez-Pulido, L., Heuckmann, J.M., Toth, R., Macartney, T., Eppink, B., (2009). Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 35, 116-127 19595721.
[60] 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 21482670.
[61] Niedernhofer, L.J., Lalai, A.S., and Hoeijmakers, J.H. (2005). Fanconi anemia (cross)linked to DNA repair. Cell 123, 1191-1198 16377561.
[62] 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 15327776.
[63] 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 15694335.
[64] Nojima, K., Hochegger, H., Saberi, A., Fukushima, T., Kikuchi, K., Yoshimura, M., Orelli, B.J., Bishop, D.K., Hirano, S., Ohzeki, M., (2005). Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res 65, 11704-11711 16357182.
[65] 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 18082605.
[66] 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 12093742.
[67] Ramaekers, C.H., and Wouters, B.G. (2011). Regulatory functions of ubiquitin in diverse DNA damage responses. Curr Mol Med 11, 152-169 21342128.
[68] 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 19101576.
[69] 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 15213235.
[70] Sasaki, M.S. (1975). Is Fanconi’s anaemia defective in a process essential to the repair of DNA cross links? Nature 257, 501-503 1178054.
[71] 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., (2010). MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol Cell 37, 879-886 20347429.
[72] 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., (2010). A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39, 36-47 20603073.
[73] 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., (2007). Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129, 289-301 17412408.
[74] 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., (2011). SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet 43, 138-141 21240277.
[75] 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 19596235.
[76] 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 19369211.
[77] Taniguchi, T., and D’Andrea, A.D. (2002). The Fanconi anemia protein, FANCE, promotes the nuclear accumulation of FANCC. Blood 100, 2457-2462 12239156.
[78] 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 15668941.
[79] Vaz, F., Hanenberg, H., Schuster, B., Barker, K., Wiek, C., Erven, V., Neveling, K., Endt, D., Kesterton, I., Autore, F., (2010). Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat Genet 42, 406-409 20400963.
[80] Venkitaraman, A.R. (2004). Tracing the network connecting BRCA and Fanconi anaemia proteins. Nat Rev Cancer 4, 266-276 15057286.
[81] Wang, W. (2007). Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat Rev Genet 8, 735-748 17768402.
[82] 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 15199141.
[83] 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 11154259.
[84] 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 19258535.
[85] 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 16793542.
[86] 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 21464321.
[87] 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 21464321.
[88] Yan, Z., Delannoy, M., Ling, C., Daee, D., Osman, F., Muniandy, P.A., Shen, X., Oostra, A.B., Du, H., Steltenpool, J., (2010). A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol Cell 37, 865-878 20347428.
[89] 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 19584259.