Both ATM and ATR promote the efficient and accurate processing of programmed meiotic double-strand breaks

Plant Journal

Volumn 55, Issue 4, 2008, Pages 629-638

  Culligan, Kevin M ^a   Britt, Anne B ^b  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ATM; ATR; Double strand break; Meiosis; SPO11

Indexed keywords

ARABIDOPSIS PROTEIN; ATM PROTEIN, ARABIDOPSIS; ATR PROTEIN, ARABIDOPSIS; CELL CYCLE PROTEIN; PLANT DNA; PROTEIN SERINE THREONINE KINASE;

APOPTOSIS; ARABIDOPSIS; ARTICLE; CELL CYCLE; CHROMATID; CYTOLOGY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETICS; MEIOSIS; METABOLISM; MUTAGENESIS; PHYSIOLOGY; PLANT CHROMOSOME; POLLEN;

APOPTOSIS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMES, PLANT; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA, PLANT; MEIOSIS; MUTAGENESIS; POLLEN; PROTEIN-SERINE-THREONINE KINASES;

ARABIDOPSIS; MUS; SYNAPSIS;

EID: 49249129345     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03530.x     Document Type: Article

References (40)

1. Abraham, R. (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15, 2177 2196.
2. Akutsu, N., Iijima, K., Hinata, T. Tauchi, H. (2007) Characterization of the plant homolog of Nijmegen breakage syndrome 1: involvement in DNA repair and recombination. Biochem. Biophys. Res. Commun. 353, 394 398.
3. Armstrong, S.J., Franklin, F.C. Jones, G.H. (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114, 4207 4217.
4. Barlow, C., Liyanage, M., Moens, P.B., Deng, C.X., Ried, T. Wynshaw-Boris, A. (1997) Partial rescue of the prophase I defects of Atm-deficient mice by p53 and p21 null alleles. Nat. Genet. 17, 462 466.
5. Barlow, C., Liyanage, M., Moens, P.B. et al. (1998) Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development, 125, 4007 4017.
6. Bellani, M.A., Romanienko, P.J., Cairatti, D.A. Camerini-Otero, R.D. (2005) SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes. J. Cell Sci. 118, 3233 3245.
7. Bleuyard, J.Y. White, C.I. (2004) The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. EMBO J. 23, 439 449.
8. Couteau, F., Belzile, F., Horlow, C., Grandjean, O., Vezon, D. Doutriaux, M.-P. (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell, 11, 1623 1634.
9. Cromie, G.A., Hyppa, R.W., Taylor, A.F., Zakharyevich, K., Hunter, N. Smith, G.R. (2006) Single Holliday junctions are intermediates of meiotic recombination. Cell, 127, 1167 1178.
10. Culligan, K.M., Tissier, A. Britt, A.B. (2004) ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell, 16, 1091 1104.
11. Culligan, K., Robertson, C., Foreman, J., Doerner, P. Britt, A. (2006) ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J. 48, 947 961.
12. D'Amours, D. Jackson, S.P. (2002) The Mre11 complex: At the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3, 317 327.
13. Falck, J., Coates, J. Jackson, S.P. (2005) Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature, 434, 605 611.
14. Friesner, J.D., Liu, B., Culligan, K. 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.
15. Garcia, V., Bruchet, H., Camescasse, D., Fabienne, G., Bouchez, D.L. Tissier, A. (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell, 15, 119 132.
16. Grelon, M., Vezon, D., Gendrot, G. Pelletier, G. (2001) AtSpo11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 20, 589 600.
17. Grushcow, J.M., Holzen, T.M., Park, K.J., Weinert, T., Lichten, M. Bishop, D.K. (1999) Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics, 153, 607 620.
18. Haber, J.E., Ira, G., Malkova, A. Sugawara, N. (2004) Repairing a double-strand chromosome break by homologous recombination: revisiting Robin Holliday's model. Philos. Trans. R. Soc. Lond. 359, 79 86.
19. Hochwagen, A. Amon, A. (2006) Checking your breaks: surveillance mechanisms of meiotic recombination. Curr. Biol. 16, R217 R228.
20. Hunter, N. Kleckner, N. (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell, 106, 59 70.
21. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G.C., Lukas, J. 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.
22. Keegan, K.S., Holtzman, D.A., Plug, A.W. et al. (1996) The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10, 2423 2437.
23. Keeney, S. Neale, M.J. (2006) Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 34, 523 525.
24. Keeney, S., Giroux, C.N. Kleckner, N. (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell, 88, 375 384.
25. Li, W., Chen, C., Markmann-Mulisch, U.L.T., Schmelzer, E., Ma, H. Reiss, B. (2004) The Arabidopsis AtRAD51 gene is dispensible for vegetative development but required for meiosis. Proc. Natl Acad. Sci. USA, 101, 10596 10601.
26. Li, W., Yang, X., Lin, Z., Timofejeva, L., Xiao, R., Makaroff, C.A. 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. Lydall, D., Nikolsky, Y., Bishop, D.K. Weinert, T. (1996) A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature, 383, 840 843.
28. Merker, J.D., Dominska, M. Petes, T.D. (2003) Patterns of heteroduplex formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics, 165, 47 63.
29. Moens, P.B., Tarsounas, M., Morita, T., Habu, T., Rottinghaus, S., Freire, R., Jackson, S., Barlow, C. Wynshaw-Boris, A. (1999) The association of ATR protein with mouse meiotic chromosome cores. Chromosoma, 108, 95 102.
30. Moens, P.B., Kolas, N.K., Tarsounas, M., Marcon, E., Cohen, P.E. Spyropoulos, B. (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J. Cell Sci. 115, 1611 1622.
31. Page, S.L. Hawley, R.S. (2003) Chromosome choreography: the meiotic ballet. Science, 301, 785 789.
32. Perera, D., Perez-Hidalgo, L., Moens, P.B., Reini, K., Lakin, N., Syvaoja, J.E., San-Segundo, P.A. Freire, R. (2004) TopBP1 and ATR colocalization at meiotic chromosomes: role of TopBP1/Cut5 in the meiotic recombination checkpoint. Mol. Biol. Cell, 15, 1568 1579.
33. Puizina, J., Siroky, J., Mokros, P., Schweizer, D. 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.
34. Ross, K.J., Fransz, P. Jones, G.H. (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4, 507 516.
35. Shiloh, Y. (2003) ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer, 3, 155 168.
36. Stacey, N.J., Kuromori, T., Azumi, Y., Roberts, G., Breuer, C., Wada, T., Maxwell, A., Roberts, K. Sugimoto-Shirasu, K. (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J. 48, 206 216.
37. Sun, H., Treco, D., Schultes, N.P. Szostak, J.W. (1989) Double-strand breaks at an initiation site for meiotic gene conversion. Nature, 338, 87 90.
38. Waterworth, W., Altun, C., Armstrong, S., Roberts, N., Dean, P., Young, K., Weil, C., Bray, C. West, C. (2007) NBS1 is involved in DNA repair and plays a synergistic role with ATM in mediating meiotic homologous recombination in plants. Plant J. 52, 41 52.
39. Xu, Y. Baltimore, D. (1996) Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev. 10, 2401 2410.
40. Xu, Y., Ashley, T., Brainerd, E., Bronson, R., Meyn, M. Baltimore, D. (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genens Dev. 10, 2411 2422.