The RAD51 paralogs ensure cellular protection against mitotic defects and aneuploidy

Journal of Cell Science

Volumn 126, Issue 1, 2013, Pages 348-359

  Rodrigue, Amélie ^a   Coulombe, Yan ^a   Jacquet, Karine ^a   Gagné, Jean Phillipe ^b   Roques, Cé line ^a   Gobeil, Stéphane ^b   Poirier, Guy ^b   Masson, Jean Yves ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Holliday junction; Mitosis; Mitotic recombination; RAD51 paralogs

Indexed keywords

NUCLEIC ACID BINDING PROTEIN; PROTEIN RAD51B; PROTEIN RAD51C; PROTEIN RAD51D; PROTEIN XRCC2; RAD51 PROTEIN; UNCLASSIFIED DRUG; XRCC3 PROTEIN;

ANAPHASE; ANEUPLOIDY; ARTICLE; CELL PROTECTION; CENTROSOME; CONTROLLED STUDY; DNA RECOMBINATION; G2 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; HELA CELL; HOLLIDAY JUNCTION; HUMAN; HUMAN CELL; MITOSIS; PARALOGY; PRIORITY JOURNAL; SPINDLE CELL;

ANEUPLOIDY; BLOTTING, WESTERN; DNA, CRUCIFORM; DNA-BINDING PROTEINS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HOLLIDAY JUNCTION RESOLVASES; HUMANS; MITOSIS; RNA INTERFERENCE;

EID: 84875579247     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.114595     Document Type: Article

References (71)

1. Bailly, A. P., Freeman, A., Hall, J., Déclais, A. C., Alpi, A., Lilley, D. M., Ahmed, S. and Gartner, A. (2010). The Caenorhabditis elegans homolog of Gen1/Yen1 resolvases links DNA damage signaling to DNA double-strand break repair. PLoS Genet. 6, e1001025.
2. Baumann, C., Körner, R., Hofmann, K. and Nigg, E. A. (2007). PICH, a centromereassociated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 128, 101-114.
3. Bishop, D. K., Ear, U., Bhattacharyya, A., Calderone, C., Beckett, M., Weichselbaum, R. R. and Shinohara, A. (1998). Xrcc3 is required for assembly of Rad51 complexes in vivo. J. Biol. Chem. 273, 21482-21488.
4. Boddy, M. N., Gaillard, P. H. L., 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.
5. Brenneman, M. A., Wagener, B. M., Miller, C. A., Allen, C. and Nickoloff, J. A. (2002). XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Mol. Cell 10, 387-395.
6. Buisson, R., Dion-Côté, A. M., Coulombe, Y., Launay, H., Cai, H., Stasiak, A. Z., Stasiak, A., Xia, B. and Masson, J. Y. (2010). Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination. Nat. Struct. Mol. Biol. 17, 1247-1254.
7. Bzymek, M., Thayer, N. H., Oh, S. D., Kleckner, N. and Hunter, N. (2010). Double Holliday junctions are intermediates of DNA break repair. Nature 464, 937-941.
8. Chan, S. N., Harris, L., Bolt, E. L., Whitby, M. C. and Lloyd, R. G. (1997). Sequence specificity and biochemical characterization of the RusA Holliday junction resolvase of Escherichia coli. J. Biol. Chem. 272, 14873-14882.
9. Chan, K. L., North, P. S. and Hickson, I. D. (2007). BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 26, 3397-3409.
10. Chapman, J. R., Taylor, M. R. and Boulton, S. J. (2012). Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47, 497-510.
11. Chen, X. B., Melchionna, R., Denis, C. M., Gaillard, P. H. L., Blasina, A., Van de Weyer, I., Boddy, M. N., Russell, P., Vialard, J. and McGowan, C. H. (2001). Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell 8, 1117-1127.
12. Compton, S. A., Ozgür, S. and Griffith, J. D. (2010). Ring-shaped Rad51 paralog protein complexes bind Holliday junctions and replication forks as visualized by electron microscopy. J. Biol. Chem. 285, 13349-13356.
13. Dodson, H., Bourke, E., Jeffers, L. J., Vagnarelli, P., Sonoda, E., Takeda, S., Earnshaw, W. C., Merdes, A. and Morrison, C. (2004). Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J. 23, 3864-3873.
14. Doxsey, S. J., Stein, P., Evans, L., Calarco, P. D. and Kirschner, M. (1994). Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76, 639-650.
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. French, C. A., Masson, J. Y., Griffin, C. S., O'Regan, P., West, S. C. and Thacker, J. (2002). Role of mammalian RAD51L2 (RAD51C) in recombination and genetic stability. J. Biol. Chem. 277, 19322-19330.
17. Giraud-Panis, M. J. E. and Lilley, D. M. J. (1998). Structural recognition and distortion by the DNA junction-resolving enzyme RusA. J. Mol. Biol. 278, 117-133.
18. Godthelp, B. C., Wiegant, W. W., van Duijn-Goedhart, A., Schärer, O. D., van Buul, P. P., Kanaar, R. and Zdzienicka, M. Z. (2002). Mammalian Rad51C contributes to DNA cross-link resistance, sister chromatid cohesion and genomic stability. Nucleic Acids Res. 30, 2172-2182.
19. Griffin, C. S., Simpson, P. J., Wilson, C. R. and Thacker, J. (2000). Mammalian recombination-repair genes XRCC2 and XRCC3 promote correct chromosome segregation. Nat. Cell Biol. 2, 757-761.
20. Holliday, R. (1964). A mechanism for gene conversion in fungi. Genet. Res. (Camb). 5, 282-304.
21. Ip, S. C., Rass, U., Blanco, M. G., Flynn, H. R., Skehel, J. M. and West, S. C. (2008). Identification of Holliday junction resolvases from humans and yeast. Nature 456, 357-361.
22. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C., Lukas, J. and Jackson, S. P. (2006). ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8, 37-45.
23. Jeffery, J. M., Urquhart, A. J., Subramaniam, V. N., Parton, R. G. and Khanna, K. K. (2010). Centrobin regulates the assembly of functional mitotic spindles. Oncogene 29, 2649-2658.
24. Kao, G. D., McKenna, W. G. and Yen, T. J. (2001). Detection of repair activity during the DNA damage-induced G2 delay in human cancer cells. Oncogene 20, 3486-3496.
25. Kuznetsov, S., Pellegrini, M., Shuda, K., Fernandez-Capetillo, O., Liu, Y., Martin, B. K., Burkett, S., Southon, E., Pati, D., Tessarollo, L. et al. (2007). RAD51C deficiency in mice results in early prophase I arrest in males and sister chromatid separation at metaphase II in females. J. Cell Biol. 176, 581-592.
26. Li, W., Yang, X., Lin, Z., Timofejeva, L., Xiao, R., Makaroff, C. A. and Ma, H. (2005). The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol. 138, 965-976.
27. Lio, Y. C., Mazin, A. V., Kowalczykowski, S. C. and Chen, D. J. (2003). Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro. J. Biol. Chem. 278, 2469-2478.
28. Liu, N., Schild, D., Thelen, M. P. and Thompson, L. H. (2002). Involvement of Rad51C in two distinct protein complexes of Rad51 paralogs in human cells. Nucleic Acids Res. 30, 1009-1015.
29. Liu, Y., Masson, J. Y., Shah, R., O'Regan, P. and West, S. C. (2004). RAD51C is required for Holliday junction processing in mammalian cells. Science 303, 243-246.
30. Liu, Y., Tarsounas, M., O'Regan, P. and West, S. C. (2007). Role of RAD51C and XRCC3 in genetic recombination and DNA repair. J. Biol. Chem. 282, 1973-1979.
31. Loveday, C., Turnbull, C., Ramsay, E., Hughes, D., Ruark, E., Frankum, J. R., Bowden, G., Kalmyrzaev, B., Warren-Perry, M., Snape, K. et al. (2011). Germline mutations in RAD51D confer susceptibility to ovarian cancer. Nat. Genet. 43, 879-882.
32. Loveday, C., Turnbull, C., Ruark, E., Xicola, R. M. M., Ramsay, E., Hughes, D., Warren-Perry, M., Snape, K., Eccles, D., Evans, D. G. et al. (2012). Germline RAD51C mutations confer susceptibility to ovarian cancer. Nat. Genet. 44, 475-476.
33. Mandal, T. N., Mahdi, A. A., Sharples, G. J. and Lloyd, R. G. (1993). Resolution of Holliday intermediates in recombination and DNA repair: indirect suppression of ruvA, ruvB, and ruvC mutations. J. Bacteriol. 175, 4325-4334.
34. Masson, J.-Y., Stasiak, A. Z., Stasiak, A., Benson, F. E. and West, S. C. (2001a). Complex formation by the human RAD51C and XRCC3 recombination repair proteins. Proc. Natl. Acad. Sci. USA 98, 8440-8446.
35. Masson, J.-Y., Tarsounas, M. C., Stasiak, A. Z., Stasiak, A., Shah, R., McIlwraith, M. J., Benson, F. E. and West, S. C. (2001b). Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev. 15, 3296-3307.
36. Miller, K. A., Yoshikawa, D. M., McConnell, I. R., Clark, R., Schild, D. and Albala, J. S. (2002). RAD51C interacts with RAD51B and is central to a larger protein complex in vivo exclusive of RAD51. J. Biol. Chem. 277, 8406-8411.
37. Mimitou, E. P. and Symington, L. S. (2009). DNA end resection: many nucleases make light work. DNA Repair (Amst.) 8, 983-995.
38. Muñ 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. et al. (2009). Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 35, 116-127.
39. Nassif, N., Penney, J., Pal, S., Engels, W. R. and Gloor, G. B. (1994). Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14, 1613-1625.
40. Nimonkar, A. V., Ozsoy, A. Z., Genschel, J., Modrich, P. and Kowalczykowski, S. C. (2008). Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl. Acad. Sci. USA 105, 16906-16911.
41. Nogales-Cadenas, R., Abascal, F., Díez-Pérez, J., Carazo, J. M. and Pascual- Montano, A. (2009). CentrosomeDB: a human centrosomal proteins database. Nucleic Acids Res. 37, D175-D180.
42. O'Regan, P., Wilson, C. R., Townsend, S. and Thacker, J. (2001). XRCC2 is a nuclear RAD51-like protein required for damage-dependent RAD51 focus formation without the need for ATP binding. J. Biol. Chem. 276, 22148-22153.
43. Orr, N., Lemnrau, A., Cooke, R., Fletcher, O., Tomczyk, K., Jones, M., Johnson, N., Lord, C. J., Mitsopoulos, C., Zvelebil, M. et al. (2012). Genome-wide association study identifies a common variant in RAD51B associated with male breast cancer risk. Nat. Genet. 44, 1182-1184.
44. Pâques, F. and Haber, J. E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349-404.
45. Pierce, A. J., Johnson, R. D., Thompson, L. H. and Jasin, M. (1999). XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 13, 2633-2638.
46. Rass, U., Compton, S. A., Matos, J., Singleton, M. R., Ip, S. C., Blanco, M. G., Griffith, J. D. and West, S. C. (2010). Mechanism of Holliday junction resolution by the human GEN1 protein. Genes Dev. 24, 1559-1569.
47. Renglin Lindh, A., Schultz, N., Saleh-Gohari, N. and Helleday, T. (2007). RAD51C (RAD51L2) is involved in maintaining centrosome number in mitosis. Cytogenet. Genome Res. 116, 38-45.
48. Rodrigue, A., Lafrance, M., Gauthier, M. C., McDonald, D., Hendzel, M., West, S. C., Jasin, M. and Masson, J. Y. (2006). Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J. 25, 222-231.
49. Saintigny, Y., Makienko, K., Swanson, C., Emond, M. J. and Monnat, R. J., Jr (2002). Homologous recombination resolution defect in Werner syndrome. Mol. Cell. Biol. 22, 6971-6978.
50. Sakaue-Sawano, A., Kurokawa, H., Morimura, T., Hanyu, A., Hama, H., Osawa, H., Kashiwagi, S., Fukami, K., Miyata, T., Miyoshi, H. et al. (2008). Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487-498.
51. Sartori, A. A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J. and Jackson, S. P. (2007). Human CtIP promotes DNA end resection. Nature 450, 509-514.
52. Sigurdsson, S., Van Komen, S., Bussen, W., Schild, D., Albala, J. S. and Sung, P. (2001). Mediator function of the human Rad51B-Rad51C complex in Rad51/RPAcatalyzed DNA strand exchange. Genes Dev. 15, 3308-3318.
53. Starita, L. M., Machida, Y., Sankaran, S., Elias, J. E., Griffin, K., Schlegel, B. P., Gygi, S. P. and Parvin, J. D. (2004). BRCA1-dependent ubiquitination of c-tubulin regulates centrosome number. Mol. Cell. Biol. 24, 8457-8466.
54. Suwaki, N., Klare, K. and Tarsounas, M. (2011). RAD51 paralogs: roles in DNA damage signalling, recombinational repair and tumorigenesis. Semin. Cell Dev. Biol. 22, 898-905.
55. 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.
56. 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.
57. Takata, M., Sasaki, M. S., Tachiiri, S., Fukushima, T., Sonoda, E., Schild, D., Thompson, L. H. and Takeda, S. (2001). Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 21, 2858-2866.
58. Tarsounas, M., Muñ oz, P., Claas, A., Smiraldo, P. G., Pittman, D. L., Blasco, M. A. and West, S. C. (2004). Telomere maintenance requires the RAD51D recombination/ repair protein. Cell 117, 337-347.
59. Vignard, J., Siwiec, T., Chelysheva, L., Vrielynck, N., Gonord, F., Armstrong, S. J., Schlögelhofer, P. and Mercier, R. (2007). The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet. 3, 1894-1906.
60. Wang, L. H., Mayer, B., Stemmann, O. and Nigg, E. A. (2010). Centromere DNA decatenation depends on cohesin removal and is required for mammalian cell division. J. Cell Sci. 123, 806-813.
61. Watanabe, N., Broome, M. and Hunter, T. (1995). Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J. 14, 1878-1891.
62. Wechsler, T., Newman, S. and West, S. C. (2011). Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 471, 642-646.
63. West, S. C. (2003). Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4, 435-445.
64. Whitfield, M. L., Sherlock, G., Saldanha, A. J., Murray, J. I., Ball, C. A., Alexander, K. E., Matese, J. C., Perou, C. M., Hurt, M. M., Brown, P. O. et al. (2002). Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell 13, 1977-2000.
65. Wiese, C., Collins, D. W., Albala, J. S., Thompson, L. H., Kronenberg, A. and Schild, D. (2002). Interactions involving the Rad51 paralogs Rad51C and XRCC3 in human cells. Nucleic Acids Res. 30, 1001-1008.
66. Wong, J. and Fang, G. (2006). HURP controls spindle dynamics to promote proper interkinetochore tension and efficient kinetochore capture. J. Cell Biol. 173, 879-891.
67. Wu, L. and Hickson, I. D. (2003). The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874.
68. Yang, H., Li, Q., Fan, J., Holloman, W. K. and Pavletich, N. P. (2005). The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 433, 653-657.
69. Yang, Z., Kenny, A. E., Brito, D. A. and Rieder, C. L. (2009). Cells satisfy the mitotic checkpoint in Taxol, and do so faster in concentrations that stabilize syntelic attachments. J. Cell Biol. 186, 675-684.
70. Zhu, X. D., Küster, B., Mann, M., Petrini, J. H. J. and de Lange, T. (2000). Cellcycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25, 347-352.
71. Zou, C., Li, J., Bai, Y., Gunning, W. T., Wazer, D. E., Band, V. and Gao, Q. (2005). Centrobin: a novel daughter centriole-associated protein that is required for centriole duplication. J. Cell Biol. 171, 437-445.