Distinct roles of the ATR kinase and the Mre11-Rad50-Nbs1 complex in the maintenance of chromosomal stability in Arabidopsis

Plant Cell

Volumn 22, Issue 9, 2010, Pages 3020-3033

  Amiard, Simon ^a   Charbonnel, Cyril ^a   Allain, Elisabeth ^a   Depeiges, Annie ^a   White, Charles I ^a   Gallego, Maria Eugenia ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 78049460790     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.078527     Document Type: Article

References (70)

1. Adams, K.E., Medhurst, A.L., Dart, D.A., and Lakin, N.D. (2006). Recruitment of ATR to sites of ionising radiation-induced DNA damage requires ATM and components of the MRN protein complex. Oncogene 25: 3894-3904.
2. Bi, X., Srikanta, D., Fanti, L., Pimpinelli, S., Badugu, R., Kellum, R., and Rong, Y.S. (2005). Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc. Natl. Acad. Sci. USA 102: 15167-15172.
3. Bleuyard, J.-Y., Gallego, M.E., and White, C.I. (2004). Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination. Chromo-soma 113: 197-203.
4. Brown, E.J., and Baltimore, D. (2000). ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14: 397-402.
5. Bundock, P., and Hooykaas, P. (2002). Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants. Plant Cell 14: 2451-2462.
6. Carson, C.T., Schwartz, R.A., Stracker, T.H., Lilley, C.E., Lee, D.V., and Weitzman, M.D. (2003). The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22: 6610-6620.
7. Caryl, A.P., Armstrong, S.J., Jones, G.H., and Franklin, F.C. (2000). A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109: 62-71.
8. Charbonnel, C., Gallego, M.E., and White, C.I. (2010). XRCC1-dependent and KU-dependent DNA double-strand break repair knetics in Arabidopsis plants. Plant J. http://dx.doi.org/10.1111/j.1365-313X.2010.04331.x.
9. Ciapponi, L., Cenci, G., and Gatti, M. (2006). The Drosophila Nbs protein functions in multiple pathways for the maintenance of genome stability. Genetics 173: 1447-1454.
10. Cimprich, K.A., and Cortez, D. (2008). ATR: An essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9: 616-627.
11. Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D., and Gautier, J. (2001). Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell 8: 137-147.
12. Culligan, K., Tissier, A., and Britt, A. (2004). ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16: 1091-1104.
13. Curtis, M.J., and Hays, J.B. (2007). Tolerance of dividing cells to replication stress in UVB-irradiated Arabidopsis roots: requirements for DNA translesion polymerases eta and zeta. DNA Repair (Amst.) 6: 1341-1358.
14. Czornak, K., Chughtai, S., and Chrzanowska, K.H. (2008). Mystery of DNA repair: The role of the MRN complex and ATM kinase in DNA damage repair. J. Appl. Genet. 49: 383-396.
15. D'Amours, D., and Jackson, S.P. (2001). The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15: 2238-2249.
16. Davies, S.L., North, P.S., Dart, A., Lakin, N.D., and Hickson, I.D. (2004). Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol. 24: 1279-1291.
17. Davies, S.L., North, P.S., and Hickson, I.D. (2007). Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nat. Struct. Mol. Biol. 14: 677-679.
18. de Klein, A., Muijtjens, M., van Os, R., Verhoeven, Y., Smit, B., Carr, A.M., Lehmann, A.R., and Hoeijmakers, J.H. (2000). Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10: 479-482.
19. Fernandez-Capetillo, O., Celeste, A., and Nussenzweig, A. (2003). Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle 2: 426-427.
20. Fillingham, J., Keogh, M.-C., and Krogan, N.J. (2006). GammaH2AX and its role in DNA double-strand break repair. Biochem. Cell Biol. 84: 568-577.
21. 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.
22. Friesner, J.D., Liu, B., Culligan, K., and Britt, A.B. (2005). Ionizing radiation-dependent gamma-H2AX focus formation requires ataxia telangiectasia mutated and ataxia telangiectasia mutated and Rad3-related. Mol. Biol. Cell 16: 2566-2576.
23. Fulcher, N., and Sablowski, R. (2009). Hypersensitivity to DNA damage in plant stem cell niches. Proc. Natl. Acad. Sci. USA 106: 20984-20988.
24. Furukawa, T., Curtis, M.J., Tominey, C.M., Duong, Y.H., Wilcox, B. W., Aggoune, D., Hays, J.B., and Britt, A.B. (2010). A shared DNA-damage-response pathway for induction of stem-cell death by UVB and by gamma irradiation. DNA Repair (Amst.) 9: 940-948.
25. Gallego, M.E., Jeanneau, M., Granier, F., Bouchez, D., Bechtold, N., and White, C.I. (2001). Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity. Plant J. 25: 31-41.
26. Gallego, M.E., and White, C.I. (2001). RAD50 function is essential for telomere maintenance in Arabidopsis. Proc. Natl. Acad. Sci. USA 98: 1711-1716.
27. Garcia, V., Bruchet, H., Camescasse, D., Granier, F., Bouchez, D., and Tissier, A. (2003). AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15: 119-132.
28. Harper, J.W., and Elledge, S.J. (2007). The DNA damage response: Ten years after. Mol. Cell 28: 739-745.
29. Hickson, I., Zhao, Y., Richardson, C.J., Green, S.J., Martin, N.M.B., Orr, A.I., Reaper, P.M., Jackson, S.P., Curtin, N.J., and Smith, G.C.M. (2004). Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64: 9152-9159.
30. Horejsí, Z., Falck, J., Bakkenist, C.J., Kastan, M.B., Lukas, J., and Bartek, J. (2004). Distinct functional domains of Nbs1 modulate the timing and magnitude of ATM activation after low doses of ionizing radiation. Oncogene 23: 3122-3127.
31. 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.
32. Kinner, A., Wu, W., Staudt, C., and Iliakis, G. (2008). Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36: 5678-5694.
33. Lamarche, B.J., Orazio, N.I., and Weitzman, M.D. (2010). The MRN complex in double-strand break repair and telomere maintenance. FEBS Lett. 584: 3682-3695.
34. Laurençon, A., Purdy, A., Sekelsky, J., Hawley, R.S., and Su, T.T. (2003). Phenotypic analysis of separation-of-function alleles of MEI-41, Drosophila ATM/ATR. Genetics 164: 589-601.
35. Lee, J.H., and Paull, T.T. (2004). Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304: 93-96.
36. Liu, B., Marc, J., Joshi, H.C., and Palevitz, B.A. (1993). A gamma-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J. Cell Sci. 104: 1217-1228.
37. Liu, J.S., Kuo, S.R., and Melendy, T. (2006). Phosphorylation of replication protein A by S-phase checkpoint kinases. DNA Repair (Amst.) 5: 369-380.
38. Lowndes, N.F., and Toh, G.W. (2005). DNA repair: The importance of phosphorylating histone H2AX. Curr. Biol. 15: R99-R102.
39. Mimitou, E.P., and Symington, L.S. (2009). DNA end resection: Many nucleases make light work. DNA Repair (Amst.) 8: 983-995.
40. Mirzoeva, O.K., and Petrini, J.H.J. (2003). DNA replication-dependent nuclear dynamics of the Mre11 complex. Mol. Cancer Res. 1: 207-218.
41. Mokros, P., Vrbsky, J., and Siroky, J. (2006). Identification of chromosomal fusion sites in Arabidopsis mutants using sequential bi-colour BAC-FISH. Genome 49: 1036-1042.
42. Myers, J.S., and Cortez, D. (2006). Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J. Biol. Chem. 281: 9346-9350.
43. Olson, E., Nievera, C.J., Lee, A.Y., Chen, L., and Wu, X. (2007). The Mre11-Rad50-Nbs1 complex acts both upstream and downstream of ataxia telangiectasia mutated and Rad3-related protein (ATR) to regulate the S-phase checkpoint following UV treatment. J. Biol. Chem. 282: 22939-22952.
44. Paull, T.T., and Gellert, M. (1999). Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13: 1276-1288.
45. Paull, T.T., Rogakou, E.P., Yamazaki, V., Kirchgessner, C.U., Gellert, M., and Bonner, W.M. (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10: 886-895.
46. Pichierri, P., Rosselli, F., and Franchitto, A. (2003). Werner's syndrome protein is phosphorylated in an ATR/ATM-dependent manner following replication arrest and DNA damage induced during the S phase of the cell cycle. Oncogene 22: 1491-1500.
47. Pirzio, L.M., Pichierri, P., Bignami, M., and Franchitto, A. (2008). Werner syndrome helicase activity is essential in maintaining fragile site stability. J. Cell Biol. 180: 305-314.
48. Puizina, J., Siroky, J., Mokros, P., Schweizer, D., and Riha, K. (2004). Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16: 1968-1978.
49. Rich, T., Allen, R.L., and Wyllie, A.H. (2000). Defying death after DNA damage. Nature 407: 777-783.
50. Robison, J.G., Elliott, J., Dixon, K., and Oakley, G.G. (2004). Replication protein A and the Mre11.Rad50.Nbs1 complex co-localize and interact at sites of stalled replication forks. J. Biol. Chem. 279: 34802-34810.
51. Scholl, R.L., May, S.T., and Ware, D.H. (2000). Seed and molecular resources for Arabidopsis. Plant Physiol. 124: 1477-1480.
52. Shiloh, Y. (2006). The ATM-mediated DNA-damage response: Taking shape. Trends Biochem. Sci. 31: 402-410.
53. Shor, E., Gangloff, S., Wagner, M., Weinstein, J., Price, G., and Rothstein, R. (2002). Mutations in homologous recombination genes rescue top3 slow growth in Saccharomyces cerevisiae. Genetics 162: 647-662.
54. Stiff, T., Reis, C., Alderton, G.K., Woodbine, L., O'Driscoll, M., and Jeggo, P.A. (2005). Nbs1 is required for ATR-dependent phosphorylation events. EMBO J. 24: 199-208.
55. Stucki, M., and Jackson, S.P. (2006). GammaH2AX and MDC1: Anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst.) 5: 534-543.
56. Tibbetts, R.S., Cortez, D., Brumbaugh, K.M., Scully, R., Livingston, D., Elledge, S.J., and Abraham, R.T. (2000). Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 14: 2989-3002.
57. Tittel-Elmer, M., Alabert, C., Pasero, P., and Cobb, J.A. (2009). The MRX complex stabilizes the replisome independently of the S phase checkpoint during replication stress. EMBO J. 28: 1142-1156.
58. Tomimatsu, N., Mukherjee, B., and Burma, S. (2009). Distinct roles of ATR and DNA-PKcs in triggering DNA damage responses in ATM-deficient cells. EMBO Rep. 10: 629-635.
59. Trenz, K., Errico, A., and Costanzo, V. (2008). Plx1 is required for chromosomal DNA replication under stressful conditions. EMBO J. 27: 876-885.
60. Trenz, K., Smith, E., Smith, S., and Costanzo, V. (2006). ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25: 1764-1774.
61. Unal, E., Arbel-Eden, A., Sattler, U., Shroff, R., Lichten, M., Haber, J.E., and Koshland, D. (2004). DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16: 991-1002.
62. Uziel, T., Lerenthal, Y., Moyal, L., Andegeko, Y., Mittelman, L., and Shiloh, Y. (2003). Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22: 5612-5621.
63. Vannier, J.-B., Depeiges, A., White, C., and Gallego, M.E. (2006). Two roles for Rad50 in telomere maintenance. EMBO J. 25: 4577-4585.
64. Vannier, J.-B., Depeiges, A., White, C., and Gallego, M.E. (2009). ERCC1/XPF protects short telomeres from homologous recombination in Arabidopsis thaliana. PLoS Genet. 5: e1000380.
65. Vanstraelen, M., Baloban, M., Da Ines, O., Cultrone, A., Lammens, T., Boudolf, V., Brown, S.C., De Veylder, L., Mergaert, P., and Kondorosi, E. (2009). APC/C-CCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl. Acad. Sci. USA 106: 11806-11811.
66. Vespa, L., Couvillion, M., Spangler, E., and Shippen, D.E. (2005). ATM and ATR make distinct contributions to chromosome end protection and the maintenance of telomeric DNA in Arabidopsis. Genes Dev. 19: 2111-2115.
67. Yamaguchi-Iwai, Y., Sonoda, E., Sasaki, M.S., Morrison, C., Haraguchi, T., Hiraoka, Y., Yamashita, Y.M., Yagi, T., Takata, M., Price, C., Kakazu, N., and Takeda, S. (1999). Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 18: 6619-6629.
68. Yoo, H.Y., Shevchenko, A., Shevchenko, A., and Dunphy, W.G. (2004). Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. J. Biol. Chem. 279: 53353-53364.
69. Zhao, S., Renthal, W., and Lee, E.Y. (2002). Functional analysis of FHA and BRCT domains of NBS1 in chromatin association and DNA damage responses. Nucleic Acids Res. 30: 4815-4822.
70. Zhong, H., Bryson, A., Eckersdorff, M., and Ferguson, D.O. (2005). Rad50 depletion impacts upon ATR-dependent DNA damage responses. Hum. Mol. Genet. 14: 2685-2693.