Mouse SLX4 Is a Tumor Suppressor that Stimulates the Activity of the Nuclease XPF-ERCC1 in DNA Crosslink Repair

Molecular Cell

Volumn 54, Issue 3, 2014, Pages 472-484

  Hodskinson, Michael R G ^a   Silhan, Jan ^a   Crossan, Gerry P ^a   Garaycoechea, Juan I ^a   Mukherjee, Shivam ^b   Johnson, Christopher M ^a   Schärer, Orlando D ^b   Patel, Ketan J ^a,c  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; MITOMYCIN; NUCLEASE; SLX4 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; XPF ERCC1 PROTEIN COMPLEX;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA CROSS LINKING; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; EPITHELIAL CANCER CELL LINE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MOUSE; NEOPLASM; NONHUMAN; PROTEIN BINDING; PROTEIN FOLDING; VERTEBRATE;

MUS; VERTEBRATA;

ANIMALS; BASE SEQUENCE; BONE MARROW CELLS; DNA ADDUCTS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; ENDONUCLEASES; HEMATOPOIETIC STEM CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASMS; NUCLEIC ACID CONFORMATION; RECOMBINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84899918056     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.03.014     Document Type: Article

References (56)

1. Al-Minawi A.Z., Saleh-Gohari N., Helleday T. The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res. 2008, 36:1-9.
2. Andersen S.L., Bergstralh D.T., Kohl K.P., LaRocque J.R., Moore C.B., Sekelsky J. Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell 2009, 35:128-135.
3. Angelov T., Guainazzi A., Schärer O.D. Generation of DNA interstrand cross-links by post-synthetic reductive amination. Org. Lett. 2009, 11:661-664.
4. Auerbach A.D., Wolman S.R. Susceptibility of Fanconi's anaemia fibroblasts to chromosome damage by carcinogens. Nature 1976, 261:494-496.
5. Barnes D.E., Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 2004, 38:445-476.
6. Bhagwat N., Olsen A.L., Wang A.T., Hanada K., Stuckert P., Kanaar R., D'Andrea A., Niedernhofer L.J., McHugh P.J. XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair. Mol. Cell. Biol. 2009, 29:6427-6437.
7. Bogliolo M., Schuster B., Stoepker C., Derkunt B., Su Y., Raams A., Trujillo J.P., Minguillón J., Ramírez M.J., Pujol R., et al. Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. Am. J. Hum. Genet. 2013, 92:800-806.
8. Bowles M., Lally J., Fadden A.J., Mouilleron S., Hammonds T., McDonald N.Q. Fluorescence-based incision assay for human XPF-ERCC1 activity identifies important elements of DNA junction recognition. Nucleic Acids Res. 2012, 40:e101.
9. Castor D., Nair N., Declais A.C., Lachaud C., Toth R., Macartney T.J., Lilley D.M., Arthur J.S., Rouse J. Cooperative control of Holliday junction resolution and DNA repair by the SLX1 and MUS81-EME1 nucleases. Mol Cell 2013.
10. Ceccaldi R., Parmar K., Mouly E., Delord M., Kim J.M., Regairaz M., Pla M., Vasquez N., Zhang Q.S., Pondarre C., et al. Bone marrow failure in Fanconi anemia is triggered by an exacerbated p53/p21 DNA damage response that impairs hematopoietic stem and progenitor cells. Cell Stem Cell 2012, 11:36-49.
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. Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat. Genet. 2011, 43:147-152. Sanger Mouse Genetics Project.
12. de Laat W.L., Appeldoorn E., Jaspers N.G., Hoeijmakers J.H. DNA structural elements required for ERCC1-XPF endonuclease activity. J.Biol. Chem. 1998, 273:7835-7842.
13. De Silva I.U., McHugh P.J., Clingen P.H., Hartley J.A. Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol. Cell. Biol. 2000, 20:7980-7990.
14. Demuth I., Digweed M., Concannon P. Human SNM1B is required for normal cellular response to both DNA interstrand crosslink-inducing agents and ionizing radiation. Oncogene 2004, 23:8611-8618.
15. Dendouga N., Gao H., Moechars D., Janicot M., Vialard J., McGowan C.H. Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol. Cell. Biol. 2005, 25:7569-7579.
16. Enzlin J.H., Schärer O.D. The active site of the DNA repair endonuclease XPF-ERCC1 forms a highly conserved nuclease motif. EMBO J. 2002, 21:2045-2053.
17. Evans E., Fellows J., Coffer A., Wood R.D. Open complex formation around a lesion during nucleotide excision repair provides a structure for cleavage by human XPG protein. EMBO J. 1997, 16:625-638.
18. Fekairi S., Scaglione S., Chahwan C., Taylor E.R., Tissier A., Coulon S., Dong M.Q., Ruse C., Yates J.R., Russell P., et al. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 2009, 138:78-89.
19. Fisher L.A., Bessho M., Bessho T. Processing of a psoralen DNA interstrand cross-link by XPF-ERCC1 complex invitro. J.Biol. Chem. 2008, 283:1275-1281.
20. Garaycoechea J.I., Patel K.J. Why does the bone marrow fail in Fanconi anemia?. Blood 2014, 123:26-34.
21. Garaycoechea J.I., Crossan G.P., Langevin F., Daly M., Arends M.J., Patel K.J. Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature 2012, 489:571-575.
22. Garcia-Higuera I., Taniguchi T., Ganesan S., Meyn M.S., Timmers C., Hejna J., Grompe M., D'Andrea A.D. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 2001, 7:249-262.
23. Guainazzi A., Campbell A.J., Angelov T., Simmerling C., Schärer O.D. Synthesis and molecular modeling of a nitrogen mustard DNA interstrand crosslink. Chemistry 2010, 16:12100-12103.
24. Hsia K.T., Millar M.R., King S., Selfridge J., Redhead N.J., Melton D.W., Saunders P.T. DNA repair gene Ercc1 is essential for normal spermatogenesis and oogenesis and for functional integrity of germ cell DNA in the mouse. Development 2003, 130:369-378.
25. 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. Malfunction of nuclease ERCC1-XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia. Am. J. Hum. Genet. 2013, 92:807-819.
26. Kim Y., Lach F.P., Desetty R., Hanenberg H., Auerbach A.D., Smogorzewska A. Mutations of the SLX4 gene in Fanconi anemia. Nat. Genet. 2011, 43:142-146.
27. Kim Y., Spitz G.S., Veturi U., Lach F.P., Auerbach A.D., Smogorzewska A. Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 2013, 121:54-63.
28. Klein Douwel D., Boonen R.A.C.M., Long D.T., Szypowska A.A., Räschle M., Walter J.C., Knipscheer P. XPF-ERCC1 Acts in Unhooking DNA Interstrand Crosslinks in Cooperation with FANCD2 and FANCP/SLX4. Mol. Cell 2014, 54. Published online May 8, 2014. 10.1016/j.molcel.2014.03.015.
29. Knipscheer P., Räschle M., Smogorzewska A., Enoiu M., Ho T.V., Schärer O.D., Elledge S.J., Walter J.C. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009, 326:1698-1701.
30. Kratz K., Schöpf B., Kaden S., Sendoel A., Eberhard R., Lademann C., Cannavó E., Sartori A.A., Hengartner M.O., Jiricny J. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 2010, 142:77-88.
31. Kuraoka I., Kobertz W.R., Ariza R.R., Biggerstaff M., Essigmann J.M., Wood R.D. Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J.Biol. Chem. 2000, 275:26632-26636.
32. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362:709-715.
33. Liu T., Ghosal G., Yuan J., Chen J., Huang J. FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 2010, 329:693-696.
34. Long D.T., Räschle M., Joukov V., Walter J.C. Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 2011, 333:84-87.
35. 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. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 2010, 142:65-76.
36. 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. Involvement of mammalian Mus81 in genome integrity and tumor suppression. Science 2004, 304:1822-1826.
37. McWhir J., Selfridge J., Harrison D.J., Squires S., Melton D.W. Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat. Genet. 1993, 5:217-224.
38. 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. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 2009, 35:116-127.
39. Niedernhofer L.J., Essers J., Weeda G., Beverloo B., de Wit J., Muijtjens M., Odijk H., Hoeijmakers J.H., Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J. 2001, 20:6540-6549.
40. Niedzwiedz W., Mosedale G., Johnson M., Ong C.Y., Pace P., Patel K.J. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell 2004, 15:607-620.
41. Prasher J.M., Lalai A.S., Heijmans-Antonissen C., Ploemacher R.E., Hoeijmakers J.H., Touw I.P., Niedernhofer L.J. Reduced hematopoietic reserves in DNA interstrand crosslink repair-deficient Ercc1-/- mice. EMBO J. 2005, 24:861-871.
42. Räschle M., Knipscheer P., Enoiu M., Angelov T., Sun J., Griffith J.D., Ellenberger T.E., Schärer O.D., Walter J.C. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 2008, 134:969-980.
43. Sengerová B., Allerston C.K., Abu M., Lee S.Y., Hartley J., Kiakos K., Schofield C.J., Hartley J.A., Gileadi O., McHugh P.J. Characterization of the human SNM1A and SNM1B/Apollo DNA repair exonucleases. J.Biol. Chem. 2012, 287:26254-26267.
44. Sijbers A.M., de Laat W.L., Ariza R.R., Biggerstaff M., Wei Y.F., Moggs J.G., Carter K.C., Shell B.K., Evans E., de Jong M.C., et al. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 1996, 86:811-822.
45. Simpson L.J., Sale J.E. Rev1 is essential for DNA damage tolerance and non-templated immunoglobulin gene mutation in a vertebrate cell line. EMBO J. 2003, 22:1654-1664.
46. Smogorzewska A., Matsuoka S., Vinciguerra P., McDonald E.R., Hurov K.E., Luo J., Ballif B.A., Gygi S.P., Hofmann K., D'Andrea A.D., Elledge S.J. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007, 129:289-301.
47. 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., Elledge S.J. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell 2010, 39:36-47.
48. 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. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat. Genet. 2011, 43:138-141.
49. Su Y., Orelli B., Madireddy A., Niedernhofer L.J., Schärer O.D. Multiple DNA binding domains mediate the function of the ERCC1-XPF protein in nucleotide excision repair. J.Biol. Chem. 2012, 287:21846-21855.
50. Svendsen J.M., Smogorzewska A., Sowa M.E., O'Connell B.C., Gygi S.P., Elledge S.J., Harper J.W. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 2009, 138:63-77.
51. Trujillo J.P., Mina L.B., Pujol R., Bogliolo M., Andrieux J., Holder M., Schuster B., Schindler D., Surrallés J. On the role of FAN1 in Fanconi anemia. Blood 2012, 120:86-89.
52. Wang A.T., Sengerová 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. Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev. 2011, 25:1859-1870.
53. Wyatt H.D., Sarbajna S., Matos J., West S.C. Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol. Cell 2013, 52:234-247.
54. Yamamoto K.N., Kobayashi S., Tsuda M., Kurumizaka H., Takata M., Kono K., Jiricny J., Takeda S., Hirota K. Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc. Natl. Acad. Sci. USA 2011, 108:6492-6496.
55. Yoshikiyo K., Kratz K., Hirota K., Nishihara K., Takata M., Kurumizaka H., Horimoto S., Takeda S., Jiricny J. KIAA1018/FAN1 nuclease protects cells against genomic instability induced by interstrand cross-linking agents. Proc. Natl. Acad. Sci. USA 2010, 107:21553-21557.
56. 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. FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat. Genet. 2012, 44:910-915.