Nuclease Delivery: Versatile Functions of SLX4/FANCP in Genome Maintenance

Molecules and Cells

Volumn 37, Issue 8, 2014, Pages 569-574

  Kim, Yonghwan ^a  

^a Sookmyung Women's University   (South Korea)

Author keywords

Fanconi anemia; Holliday junction; ICL repair; SLX4 FANCP; Telomere maintenance

Indexed keywords

NUCLEASE; SCAFFOLD PROTEIN; SLX4 PROTEIN; UNCLASSIFIED DRUG; CRUCIFORM DNA; PROTEIN BINDING; RECOMBINASE; SLX4 PROTEIN, HUMAN;

CAENORHABDITIS ELEGANS; CROSS LINKING; DISEASE PREDISPOSITION; DNA DAMAGE; DROSOPHILA MELANOGASTER; FANCONI ANEMIA; GENE MUTATION; GENETIC DISORDER; GENOME; GENOMIC INSTABILITY; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; HUMAN; MUS MUSCULUS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SACCHAROMYCES CEREVISIAE; TELOMERE HOMEOSTASIS; ANIMAL; DNA REPAIR; DNA REPLICATION; GENETICS; HUMAN GENOME; METABOLISM; MUTATION; PATHOLOGY; PROTEIN ANALYSIS; SCHIZOSACCHAROMYCES;

ANIMALS; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA, CRUCIFORM; FANCONI ANEMIA; GENOME, HUMAN; GENOMIC INSTABILITY; HUMANS; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RECOMBINASES; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; TELOMERE HOMEOSTASIS;

EID: 84930252372     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2014.0118     Document Type: Review

References (48)

1. Ancelin, K., Brunori, M., Bauwens, S., Koering, C.E., Brun, C., Ricoul, M., Pommier, J.P., Sabatier, L., and Gilson, E. (2002). Targeting assay to study the cis functions of human telomeric proteins: evidence for inhibition of telomerase by TRF1 and for activation of telomere degradation by TRF2. Mol. Cell. Biol. 22, 3474-3487.
2. Andersen, S.L., Bergstralh, D.T., Kohl, K.P., LaRocque, J.R., Moore, C.B., and Sekelsky, J. (2009). Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell 35, 128-135.
3. Andersen, S.L., Kuo, H.K., Savukoski, D., Brodsky, M.H., and Sekelsky, J. (2011). Three structure-selective endonucleases are essential in the absence of BLM helicase in Drosophila. PLoS Genet. 7, e1002315.
4. Bergstralh, D.T., and Sekelsky, J. (2008). Interstrand crosslink repair: can XPF-ERCC1 be let off the hook? Trends Genet. 24, 70-76.
5. Boddy, M.N., Gaillard, P.H., McDonald, W.H., Shanahan, P., Yates, J.R., 3rd, and Russell, P. (2001). Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107, 537-548.
6. 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. Am. J. Hum. Genet. 92, 800-806.
7. Castor, D., Nair, N., Declais, A.C., Lachaud, C., Toth, R., Macartney, T.J., Lilley, D.M., Arthur, J.S., and Rouse, J. (2013). Cooperative control of holliday junction resolution and DNA repair by the SLX1 and MUS81-EME1 nucleases. Mol. Cell 52, 221-233.
8. Cimprich, K.A., and Cortez, D. (2008). ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627.
9. Clerici, M., Paciotti, V., Baldo, V., Romano, M., Lucchini, G., and Longhese, M.P. (2001). Hyperactivation of the yeast DNA damage checkpoint by TEL1 and DDC2 overexpression. EMBO J. 20, 6485-6498.
10. Coulon, S., Gaillard, P.H., Chahwan, C., McDonald, W.H., Yates, J.R., 3rd, and Russell, P. (2004). Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol. Biol. Cell 15, 71-80.
11. D’Andrea, A.D. (2010). Susceptibility pathways in Fanconi’s anemia and breast cancer. N. Engl. J. Med. 362, 1909-1919.
12. 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.
13. Deans, A.J., and West, S.C. (2011). DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 11, 467-480.
14. Dendouga, N., Gao, H., Moechars, D., Janicot, M., Vialard, J., and McGowan, C.H. (2005). Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol. Cell. Biol. 25, 7569-7579.
15. 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.
16. Gaillard, P.H., Noguchi, E., Shanahan, P., and Russell, P. (2003). The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism. Mol. Cell 12, 747-759.
17. Garner, E., and Smogorzewska, A. (2011). Ubiquitylation and the Fanconi anemia pathway. FEBS Lett. 585, 2853-2860.
18. Garner, E., Kim, Y., Lach, F.P., Kottemann, M.C., and Smogorzewska, A. (2013). Human GEN1 and the SLX4-associated nucleases MUS81 and SLX1 are essential for the resolution of replication-induced Holliday junctions. Cell Rep. 5, 207-215.
19. 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.
20. Hollingsworth, N.M., and Brill, S.J. (2004). The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev. 18, 117-125.
21. Kashiyama, K., Nakazawa, Y., Pilz, D.T., Guo, C., Shimada, M., Sasaki, K., Fawcett, H., Wing, J.F., Lewin, S.O., Carr, L., et al. (2013). Malfunction of nuclease ERCC1-XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia. Am. J. Hum. Genet. 92, 807-819.
22. 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.
23. 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.
24. Kim, Y., Spitz, G.S., Veturi, U., Lach, F.P., Auerbach, A.D., and Smogorzewska, A. (2013). Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 121, 54-63.
25. Kottemann, M.C., and Smogorzewska, A. (2013). Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493, 356-363.
26. Kumaresan, K.R., and Lambert, M.W. (2000). Fanconi anemia, complementation group A, cells are defective in ability to produce incisions at sites of psoralen interstrand cross-links. Carcinogenesis 21, 741-751.
27. 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.
28. Li, X., and Heyer, W.D. (2008). Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 18, 99-113.
29. Liu, Y., and West, S.C. (2004). Happy Hollidays: 40th anniversary of the Holliday junction. Nat. Rev. Mol. Cell. Biol. 5, 937-944.
30. Matos, J., Blanco, M.G., Maslen, S., Skehel, J.M., and West, S.C. (2011). Regulatory ontrol of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 147, 158-172.
31. McPherson, J.P., Lemmers, B., Chahwan, R., Pamidi, A., Migon, E., Matysiak-Zablocki, E., Moynahan, M.E., Essers, J., Hanada, K., Poonepalli, A., et al. (2004). Involvement of mammalian Mus81 in genome integrity and tumor suppression. Science 304, 1822-1826.
32. Mullen, J.R., Kaliraman, V., Ibrahim, S.S., and Brill, S.J. (2001). Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157, 103-118.
33. Munoz, I.M., Hain, K., Declais, 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.
34. Ohouo, P.Y., Bastos de Oliveira, F.M., Almeida, B.S., and Smolka, M.B. (2010). DNA damage signaling recruits the Rtt107-Slx4 scaffolds via Dpb11 to mediate replication stress response. Mol. Cell 39, 300-306.
35. Ohouo, P.Y., Bastos de Oliveira, F.M., Liu, Y., Ma, C.J., and Smolka, M.B. (2013). DNA-repair scaffolds dampen checkpoint signaling by counteracting the adaptor Rad9. Nature 493, 120-124.
36. Rothfuss, A., and Grompe, M. (2004). Repair kinetics of genomic interstrand DNA cross-links: evidence for DNA double-strand break-dependent activation of the Fanconi anemia/BRCA pathway. Mol. Cell. Biol. 24, 123-134.
37. Saito, T.T., Youds, J.L., Boulton, S.J., and Colaiacovo, M.P. (2009). Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet. 5, e1000735.
38. Saito, T.T., Lui, D.Y., Kim, H.M., Meyer, K., and Colaiacovo, M.P. (2013). Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLoS Genet. 9, e1003586.
39. Smogorzewska, A., van Steensel, B., Bianchi, A., Oelmann, S.,Schaefer, M.R., Schnapp, G., and de Lange, T. (2000). Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol. 20, 1659-1668.
40. 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.
41. Sung, P., and Klein, H. (2006). Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7, 739-750.
42. Svendsen, J.M., and Harper, J.W. (2010). GEN1/Yen1 and the SLX4 complex: Solutions to the problem of Holliday junction resolution. Genes Dev. 24, 521-536.
43. Svendsen, J.M., Smogorzewska, A., Swa, 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.
44. Wan, B., Yin, J., Horvath, K., Sarkar, J., Chen, Y., Wu, J., Wan, K., Lu, J., Gu, P., Yu, E.Y., et al. (2013). SLX4 assembles a telomere maintenance toolkit by bridging multiple endonucleases with telomeres. Cell Rep. 4, 861-869.
45. Wilson, J.S., Tejera, A.M., Castor, D., Toth, R., Blasco, M.A., and Rouse, J. (2013). Localization-dependent and –independent roles of SLX4 in regulating telomeres. Cell Rep. 4, 853-860.
46. Wu, L., and Hickson, I.D. (2006). DNA helicases required for homologous recombination and repair of damaged replication forks. Ann. Rev. Genet. 40, 279-306.
47. Wyatt, H.D., Sarbajna, S., Matos, J., and West, S.C. (2013). Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol. Cell 52, 234-247.
48. 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. USA108, 6492-6496.