Snm1B/Apollo functions in the fanconi anemia pathway in response to DNA interstrand crosslinks

Human Molecular Genetics

Volumn 20, Issue 13, 2011, Pages 2549-2559

  Mason, Jennifer M ^a   Sekiguchi, JoAnn M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; BRCA1 PROTEIN; DOUBLE STRANDED DNA; METALLO BETA LACTAMASE; MITOMYCIN C; NUCLEASE; RAD51 PROTEIN;

ARTICLE; CELL SURVIVAL; CHROMOSOME ABERRATION; DNA CROSS LINKING; DNA REPAIR; FANCONI ANEMIA; GENE FUNCTION; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ALKYLATING AGENTS; CHROMOSOMAL INSTABILITY; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA REPAIR ENZYMES; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MITOMYCIN; NUCLEAR PROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 79958702602     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr153     Document Type: Article

References (70)

1. Moldovan, G.L. and D'Andrea, A.D. (2009) How the fanconi anemia pathway guards the genome. Annu. Rev. Genet., 43, 223-249.
2. 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.
3. 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 structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat. Genet., 43, 138-141.
4. 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. (2011) Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat. Genet., 43, 147-152.
5. Thompson, L.H. and Hinz, J.M. (2009) Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: mechanistic insights. Mutat. Res., 668, 54-72.
6. 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.
7. 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.
8. Taniguchi, T. and D'Andrea, A.D. (2006) Molecular pathogenesis of Fanconi anemia: recent progress. Blood, 107, 4223-4233.
9. 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.
10. 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.
11. 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.
12. Kratz, K., Schopf, B., Kaden, S., Sendoel, A., Eberhard, R., Lademann, C., Cannavo, 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.
13. MacKay, C., Declais, 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.
14. Li, X. and Moses, R.E. (2003) The beta-lactamase motif in Snm1 is required for repair of DNA double-strand breaks caused by interstrand crosslinks in S. cerevisiae. DNA Repair (Amst.), 2, 121-129.
15. Callebaut, I., Moshous, D., Mornon, J.-P. and de Villartay, J.-P. (2002) Metallo-β-lactamase fold within nucleic acids processing enzymes: the b-CASP family. Nucleic Acids Res., 30, 3592-3601.
16. Dronkert, M.L., de Wit, J., Boeve, M., Vasconcelos, M.L., van Steeg, H., Tan, T.L., Hoeijmakers, J.H. and Kanaar, R. (2000) Disruption of mouse SNM1 causes increased sensitivity to the DNA interstrand cross-linking agent mitomycin C. Mol. Cell Biol., 20, 4553-4561.
17. Hemphill, A.W., Bruun, D., Thrun, L., Akkari, Y., Torimaru, Y., Hejna, K., Jakobs, P.M., Hejna, J., Jones, S., Olson, S.B. et al. (2008) Mammalian SNM1 is required for genome stability. Mol. Genet. Metab., 94, 38-45.
18. Yang, K., Moldovan, G.L. and D'Andrea, A.D. (2010) RAD18-dependent recruitment of SNM1A to DNA repair complexes by a ubiquitin-binding zinc finger. J. Biol. Chem., 285, 19085-19091.
19. Ma, Y., Pannicke, U., Schwarz, K. and Lieber, M.R. (2002) Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell, 108, 781-794.
20. Moshous, D., Callebaut, I., de Chasseval, R., Corneo, B., Cavazzana-Calvo, M., Le Deist, F., Tezcan, I., Sanal, O., Bertrand, Y., Philippe, N. et al. (2001) Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell, 105, 177-186.
21. Rooney, S., Alt, F.W., Lombard, D., Whitlow, S., Eckersdorff, M., Fleming, J., Fugmann, S., Ferguson, D.O., Schatz, D.G. and Sekiguchi, J. (2003) Defective DNA repair and increased genomic instability in Artemis-deficient murine cells. J. Exp. Med., 197, 553-565.
22. Lam, Y.C., Akhter, S., Gu, P., Ye, J., Poulet, A., Giraud-Panis, M.J., Bailey, S.M., Gilson, E., Legerski, R.J. and Chang, S. (2010) SNM1B/Apollo protects leading-strand telomeres against NHEJ-mediated repair. EMBO J., 29, 2230-2241.
23. Wu, P., van Overbeek, M., Rooney, S. and de Lange, T. (2010) Apollo contributes to G overhang maintenance and protects leading-end telomeres. Mol. Cell, 39, 606-617.
24. Bae, J.B., Mukhopadhyay, S.S., Liu, L., Zhang, N., Tan, J., Akhter, S., Liu, X., Shen, X., Li, L. and Legerski, R.J. (2008) Snm1B/Apollo mediates replication fork collapse and S Phase checkpoint activation in response to DNA interstrand cross-links. Oncogene, 27, 5045-5056.
25. Demuth, I., Bradshaw, P.S., Lindner, A., Anders, M., Heinrich, S., Kallenbach, J., Schmelz, K., Digweed, M., Meyn, M.S. and Concannon, P. (2008) Endogenous hSNM1B/Apollo interacts with TRF2 and stimulates ATM in response to ionizing radiation. DNA Repair (Amst.), 7, 1192-1201.
26. Demuth, I., Digweed, M. and Concannon, P. (2004) Human SNM1B is required for normal cellular response to both DNA interstrand crosslink-inducing agents and ionizing radiation. Oncogene, 23, 8611-8618.
27. Lenain, C., Bauwens, S., Amiard, S., Brunori, M., Giraud-Panis, M.J. and Gilson, E. (2006) The Apollo 5′ exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol., 16, 1303-1310.
28. Ye, J., Lenain, C., Bauwens, S., Rizzo, A., Saint-Leger, A., Poulet, A., Benarroch, D., Magdinier, F., Morere, J., Amiard, S. et al. (2010) TRF2 and apollo cooperate with topoisomerase 2alpha to protect human telomeres from replicative damage. Cell, 142, 230-242.
29. Akhter, S., Lam, Y.C., Chang, S. and Legerski, R.J. (2010) The telomeric protein SNM1B/Apollo is required for normal cell proliferation and embryonic development. Aging Cell, 9, 1047-1056.
30. Touzot, F., Callebaut, I., Soulier, J., Gaillard, L., Azerrad, C., Durandy, A., Fischer, A., de Villartay, J.P. and Revy, P. (2010) Function of Apollo (SNM1B) at telomere highlighted by a splice variant identified in a patient with Hoyeraal-Hreidarsson syndrome. Proc. Natl Acad. Sci. USA, 107, 10097-10102.
31. Timmers, C., Taniguchi, T., Hejna, J., Reifsteck, C., Lucas, L., Bruun, D., Thayer, M., Cox, B., Olson, S., D'Andrea, A.D. et al. (2001) Positional cloning of a novel Fanconi anemia gene, FANCD2. Mol. Cell, 7, 241-248.
32. Godthelp, B.C., van Buul, P.P., Jaspers, N.G., Elghalbzouri-Maghrani, E., van Duijn-Goedhart, A., Arwert, F., Joenje, H. and Zdzienicka, M.Z. (2006) Cellular characterization of cells from the Fanconi anemia complementation group, FA-D1/BRCA2. Mutat. Res., 601, 191-201.
33. Taniguchi, T., Garcia-Higuera, I., Xu, B., Andreassen, P.R., Gregory, R.C., Kim, S.T., Lane, W.S., Kastan, M.B. and D'Andrea, A.D. (2002) Convergence of the fanconi anemia and ataxia telangiectasia signaling pathways. Cell, 109, 459-472.
34. 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.
35. 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.
36. 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.
37. 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.
38. Auerbach, A.D. and Wolman, S.R. (1976) Susceptibility of Fanconi's anaemia fibroblasts to chromosome damage by carcinogens. Nature, 261, 494-496.
39. Yuan, F., El Hokayem, J., Zhou, W. and Zhang, Y. (2009) FANCI protein binds to DNA and interacts with FANCD2 to recognize branched structures. J. Biol. Chem., 284, 24443-24452.
40. Sims, A.E., Spiteri, E., Sims, R.J. 3rd, Arita, A.G., Lach, F.P., Landers, T., Wurm, M., Freund, M., Neveling, K., Hanenberg, H. et al. (2007) FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol., 14, 564-567.
41. Gudmundsdottir, K. and Ashworth, A. (2006) The roles of BRCA1 and BRCA2 and associated proteins in the maintenance of genomic stability. Oncogene, 25, 5864-5874.
42. Nakanishi, K., Yang, Y.G., Pierce, A.J., Taniguchi, T., Digweed, M., D'Andrea, A.D., Wang, Z.Q. and Jasin, M. (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc. Natl Acad. Sci. USA, 102, 1110-1115.
43. Taniguchi, T., Garcia-Higuera, I., Andreassen, P.R., Gregory, R.C., Grompe, M. and D'Andrea, A.D. (2002) S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood, 100, 2414-2420.
44. 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.
45. Vandenberg, C.J., Gergely, F., Ong, C.Y., Pace, P., Mallery, D.L., Hiom, K. and Patel, K.J. (2003) BRCA1-independent ubiquitination of FANCD2. Mol. Cell, 12, 247-254.
46. Bhattacharyya, A., Ear, U.S., Koller, B.H., Weichselbaum, R.R. and Bishop, D.K. (2000) The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin. J. Biol. Chem., 275, 23899-23903.
47. Huber, L.J., Yang, T.W., Sarkisian, C.J., Master, S.R., Deng, C.X. and Chodosh, L.A. (2001) Impaired DNA damage response in cells expressing an exon 11-deleted murine Brca1 variant that localizes to nuclear foci. Mol. Cell Biol., 21, 4005-4015.
48. 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.
49. Moldovan, G.L., Madhavan, M.V., Mirchandani, K.D., McCaffrey, R.M., Vinciguerra, P. and D'Andrea, A.D. (2010) DNA polymerase POLN participates in cross-link repair and homologous recombination. Mol. Cell Biol., 30, 1088-1096.
50. Pierce, A.J. and Jasin, M. (2005) Measuring recombination proficiency in mouse embryonic stem cells. Methods Mol. Biol., 291, 373-384.
51. Weinstock, D.M., Nakanishi, K., Helgadottir, H.R. and Jasin, M. (2006) Assaying double-strand break repair pathway choice in mammalian cells using a targeted endonuclease or the RAG recombinase. Methods Enzymol., 409, 524-540.
52. van Overbeek, M. and de Lange, T. (2006) Apollo, an Artemis-related nuclease, interacts with TRF2 and protects human telomeres in S phase. Curr. Biol., 16, 1295-1302.
53. Mladenov, E., Tsaneva, I. and Anachkova, B. (2007) Activation of the S phase DNA damage checkpoint by mitomycin C. J. Cell Physiol., 211, 468-476.
54. Costanzo, V., Shechter, D., Lupardus, P.J., Cimprich, K.A., Gottesman, M. and Gautier, J. (2003) An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell, 11, 203-213.
55. Pichierri, P. and Rosselli, F. (2004) The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J., 23, 1178-1187.
56. 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.
57. 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.
58. Pichierri, P., Averbeck, D. and Rosselli, F. (2002) DNA cross-link-dependent RAD50/MRE11/NBS1 subnuclear assembly requires the Fanconi anemia C protein. Hum. Mol. Genet., 11, 2531-2546.
59. 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.
60. 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.
61. 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.
62. Roques, C., Coulombe, Y., Delannoy, M., Vignard, J., Grossi, S., Brodeur, I., Rodrigue, A., Gautier, J., Stasiak, A.Z., Stasiak, A. et al. (2009) MRE11-RAD50-NBS1 is a critical regulator of FANCD2 stability and function during DNA double-strand break repair. EMBO J., 28, 2400-2413.
63. 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.
64. Kimm, L.R., deLeeuw, R.J., Savage, K.J., Rosenwald, A., Campo, E., Delabie, J., Ott, G., Muller-Hermelink, H.K., Jaffe, E.S., Rimsza, L.M. et al. (2007) Frequent occurrence of deletions in primary mediastinal B-cell lymphoma. Genes Chromosomes Cancer, 46, 1090-1097.
65. Mathew, C.G. (2006) Fanconi anaemia genes and susceptibility to cancer. Oncogene, 25, 5875-5884.
66. Patel, K.J. and Joenje, H. (2007) Fanconi anemia and DNA replication repair. DNA Repair (Amst.), 6, 885-890.
67. Hicks, J.K., Chute, C.L., Paulsen, M.T., Ragland, R.L., Howlett, N.G., Gueranger, Q., Glover, T.W. and Canman, C.E. (2009) Differential roles for DNA polymerases eta, zeta, and REV1 in lesion bypass of intrastrand versus interstrand DNA cross-links. Mol. Cell Biol., 30, 1217-1230.
68. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J.P., Sedivy, J.M., Kinzler, K.W. and Vogelstein, B. (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science, 282, 1497-1501.
69. Bruun, D., Folias, A., Akkari, Y., Cox, Y., Olson, S. and Moses, R. (2003) siRNA depletion of BRCA1, but not BRCA2, causes increased genome instability in Fanconi anemia cells. DNA Repair (Amst.), 2, 1007-1013.
70. 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.