Drosophila ATR in double-strand break repair

Genetics

Volumn 175, Issue 3, 2007, Pages 1023-1033

  LaRocque, Jeannine R ^a   Jaklevic, Burnley ^b,c   Tin, Tin Su ^b   Sekelsky, Jeff ^a,d  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLINE;

ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DROSOPHILA; GENE; GENE INSERTION; GENOMIC INSTABILITY; MALE; MEI 41 GENE; MITOSIS; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; DNA REPAIR; DROSOPHILA; DROSOPHILA PROTEINS; GENES, CDC; MODELS, GENETIC; MUTATION; NUCLEAR PROTEINS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, DNA;

ATAXIA TELANGIECTASIA;

EID: 34249008981     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.067330     Document Type: Article

References (75)

1. ABRAHAM, R. T., 2001 Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15: 2177-2196.
2. ADAMS, M. D., M. MCVEY and J. SEKELSKY, 2003 Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299: 265-267.
3. BANGA, S. S., A. VELAZQUEZ and J. B. BOYD, 1991 P transposition in Drosophila provides a new tool for analyzing postreplication repair and double-strand break repair. Mutat. Res. 255: 79-88.
4. BASSING, C. H., K. F. CHUA, J. SEKIGUCHI, H. SUH, S. R. WHITLOW et al., 2002 Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. USA 99: 8173-8178.
5. BEALL, E. L., and D. C. RIO, 1997 Drosophila P-element transposase is a novel site-specific endonuclease. Genes Dev. 11: 2137-2151.
6. BI, X., S. C. WEI and Y. S. RONG, 2004 Telomere protection without a telomerase; the role of ATM and Mre11 in Drosophila telomere maintenance. Curr. Biol. 14: 1348-1353.
7. 2/M checkpoint induced by low-dose irradiation. Genetics 171: 845-847.
8. BI, X., D. SRIKANTA, L. FANTI, S. PIMPINELLI, R. BADUGU et al., 2005b Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc. Natl. Acad. Sci. USA 102: 15167-15172.
9. BIER, E., H. VAESSIN, S. SHEPHERD, K. LEE, K. MCCALL et al., 1989 Searching for pattern and mutation in the Drosophila genome with P-lacZ vector. Genes Dev. 3: 1273-1287.
10. BODDY, M. N., B. FURNARI, O. MONDESERT and P. RUSSELL, 1998 Replication checkpoint enforced by kinases Cds1 and Chk1. Science 280: 909-912.
11. BOYD, J. B., M. D. GOLINO, T. D. NGUYEN and M. M. GREEN, 1976 Isolation and characterization of X-linked mutants of Drosophila melanogaster which are sensitive to mutagens. Genetics 84: 485-506.
12. BRODSKY, M. H., J. SEKELSKY, G. TSANG, R. S. HAWLEY and G. M. RUBIN, 2000 mus304 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 14: 666-678.
13. BRODSKY, M. H., B. T. WEINERT, G. TSANG, Y. S. RONG, N. M. MCGINNIS et al., 2004 Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol. Cell. Biol. 24: 1219-1231.
14. BROWN, E. J., and D. BALTIMORE, 2003 Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 17: 615-628.
15. CANMAN, C. E., D.-S. LIN, K. A. CIMPRICH, Y. TAYA, K. TAMAI et al., 1998 Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281: 1677-1679.
16. CELESTE, A., S. PETERSEN, P. J. ROMANIENKO, O. FERNANDEZ-CAPETILLO, H. T. CHEN et al., 2002 Genomic instability in mice lacking histone H2AX. Science 296: 922-927.
17. CHEN, Y., and Y. SANCHEZ, 2004 Chk1 in the DNA damage response: conserved roles from yeasts to mammals. DNA Repair 3: 1025-1032.
18. CLIBY, W. A., C. J. ROBERTS, K. A. CIMPRICH, C. M. STRINGER, J. R. LAMB et al., 1998 Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17: 159-169.
19. DAS, K. C., and R. DASHNAMOORTHY, 2004 Hyperoxia activates the ATR-Chk1 pathway and phosphorylates p53 at multiple sites. Am. J. Physiol. Lung Cell Mol. Physiol. 286: L87-L97.
20. DE VRIES, H. I., L. UYETAKE, W. LEMSTRA, J. F. BRUNSTING, T. T. SU et al., 2005 Grp/DChk1 is required for G2-M checkpoint activation in Drosophila S2 cells, whereas Dmnk/DChk2 is dispensable. J. Cell Sci. 118: 1833-1842.
21. EDGAR, B. A., F. SPRENGER, R. J. DURONIO, P. LEOPOLD and P. H. O'FARRELL, 1994 Distinct molecular mechanisms regulate cell cycle timing at successive stages of Drosophila embryogenesis. Genes Dev. 8: 440-452.
22. ENGELS, W. R., W. K. BENZ, C. R. PRESTON, P. L. GRAHAM, R. W. PHILLIS et al., 1987 Somatic effects of P element activity in Drosophila melanogaster: pupal lethality. Genetics 117: 745-757.
23. FOGARTY, P., R. F. KALPIN and W. SULLIVAN, 1994 The Drosophila maternal-effect mutation grapes causes a metaphase arrest at nuclear cycle 13. Development 120: 2131-2142.
24. FOGARTY, P., S. D. CAMPBELL, R. ABU- SHUMAYS, B. DE SAINT PHALLE, K. R. YU et al., 1997 The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr. Biol. 7: 418-426.
25. FRANKENBERG-SCHWAGER, M., 1990 Induction, repair and biological relevance of radiation-induced DNA lesions in eukaryotic cells. Radiat. Environ. Biophys. 29: 273-292.
26. GARNER, M., S. VAN KREEVELD and T. T. SU, 2001 mei-41 and bub1 block mitosis at two distinct steps in response to incomplete DNA replication in Drosophila embryos. Curr. Biol. 11: 1595-1599.
27. GLOOR, G. B., J. MORETTI, J. MOUYAL and K. J. KEELER, 2000 Distinct P-element excision products in somatic and germline cells of Drosophila melanogaster. Genetics 155: 1821-1830.
28. HARI, K. L., A. SANTERRE, J. SEKELSKY, K. S. MCKIM, J. B. BOYD et al., 1995 The mei-41 gene of D. melanogaster is a structural and functional homolog of the human ataxia telangiectasia gene. Cell 82: 815-821.
29. HELT, C. E., W. A. CLIBY, P. C. KENG, R. A. BAMBARA and M. A. O'REILLY, 2005 Ataxia telangiectasia mutated (ATM) and ATM and Rad3-related protein exhibit selective target specificities in response to different forms of DNA damage. J. Biol. Chem. 280: 1186-1192.
30. HUTCHINSON, F., 1985 Chemical changes induced in DNA by ionizing radiation. Prog. Nucleic Acid Res. Mol. Biol. 32: 115-154.
31. IRA, G., A. PELLICIOLI, A. BALIJJA, X. WANG, S. FIORANI et al., 2004 DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431: 1011-1017.
32. IVANOV, E. L., N. SUGAWARA, J. FISHMAN- LOBELL and J. E. HABER, 1996 Genetic requirements for the single-strand annealing pathway for double-strand break repair in Saccharomyces cerevisiae. Genetics 142: 693-704.
33. JACOBS, H. W., J. A. KNOBLICH and C. F. LEHNER, 1998 Drosophila Cyclin B3 is required for female fertility and is dispensable for mitosis like Cyclin B. Genes Dev. 12: 3741-3751.
34. JAKLEVIC, B. R., and T. T. SU, 2004 Relative contribution of DNA repair, cell cycle checkpoints, and cell death to survival after DNA damage in Drosophila larvae. Curr. Biol. 14: 23-32.
35. JEGGO, P. A., and M. LOBRICH, 2005 Artemis links ATM to double strand break rejoining. Cell Cycle 4: 359-362.
36. JEGGO, P. A., and M. LOBRICH, 2006 Contribution of DNA repair and cell cycle checkpoint arrest to the maintenance of genomic stability. DNA Repair 5: 1192-1198.
37. JEGGO, P. A., A. M. CARR and A. R. LEHMANN, 1998 Splitting the ATM: distinct repair and checkpoint defects in ataxia-telangiectasia. Trends Genet. 14: 312-316.
38. KOUNDAKJIAN, E. J., D. M. COWAN, R. W. HARDY and A. H. BECKER, 2004 The Zuker collection: a resource for the analysis of autosomal gene function in Drosophila melanogaster. Genetics 167: 203-206.
39. KUHNE, M., E. RIBALLO, N. RIEF, K. ROTHKAMM, P. A. JEGGO et al., 2004 A double-strand break repair defect in ATM-deficient cells contributes to radiosensitivity. Cancer Res. 64: 500-508.
40. KURKULOS, M., J. M. WEINBERG, D. ROY and S. M. MOUNT, 1994 P element-mediated in vivo deletion analysis of white-apricot: deletions between direct repeats are strongly favored. Genetics 136: 1001-1011.
41. LAURENCON, A., A. PURDY, J. SEKELSKY, R. S. HAWLEY and T. T. SU, 2003 Phenotypic analysis of separation-of-function alleles of MEI-41, Drosophila ATM/ATR. Genetics 164: 589-601.
42. LIU, Q., S. GUNTUKU, X. S. CUI, S. MATSUOKA, D. CORTEZ et al., 2000 Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14: 1448-1459.
43. LOBRICH, M., and P. A. JEGGO, 2005 Harmonising the response to DSBs: a new string in the ATM bow. DNA Repair 4: 749-759.
44. MASROUHA, N., L. YANG, S. HIJAL, S. LAROCHELLE and B. SUTER, 2003 The Drosophila chk2 gene loki is essential for embryonic DNA double-strand-break checkpoints induced in S phase or G2. Genetics 163: 973-982.
45. MCVEY, M., M. D. ADAMS, E. STAEVA-VIEIRA and J. SEKELSKY, 2004a Evidence for multiple cycles of strand invasion during repair of double-strand gaps in Drosophila. Genetics 167: 699-705.
46. MCVEY, M., D. RADUT and J. SEKELSKY, 2004b End-joining repair of double-strand breaks in Drosophila is largely DNA ligase IV-independent. Genetics 168: 2067-2076.
47. MILLS, K. D., D. A. SINCLAIR and L. GUARENTE, 1999 MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell 97: 609-620.
48. MORRISON, C., E. SONODA, N. TAKAO, A. SHINOHARA, K. YAMAMOTO et al., 2000 The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 19: 463-471.
49. NASSIF, N., and W. R. ENGELS, 1993 DNA homology requirements for mitotic gap repair in Drosophila. Proc. Natl. Acad. Sci. USA 90: 1262-1266.
50. O'DRISCOLL, M., and P. A. JEGGO, 2006 The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet. 7: 45-54.
51. OIKEMUS, S. R., J. QUEIROZ-MACHADO, K. LAI, N. MCGINNIS, C. SUNKEL et al., 2006 Epigenetic telomere protection by Drosophila DNA damage response pathways. PLoS Genet. 2: e71.
52. PAULL, T. T., E. P. ROGAKOU, V. YAMAZAKI, C. U. KIRCHGESSNER, M. GELLERT et al., 2000 A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10: 886-895.
53. PRICE, A., 1993 The repair of ionising radiation-induced damage to DNA. Semin. Cancer Biol. 4: 61-71.
54. RIBALLO, E., M. KUHNE, N. RIEF, A. DOHERTY, G. C. SMITH et al., 2004 A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 16: 715-724.
55. ROMEIJN, R. J., M. M. GORSKI, M. A. VAN SCHIE, J. N. NOORDERMEER, L. H. MULLENDERS et al., 2005 Lig4 and rad54 are required for repair of DNA double-strand breaks induced by P-element excision in Drosophila. Genetics 169: 795-806.
56. RONG, Y. S., and K. G. GOLIC, 2000 Gene targeting by homologous recombination in Drosophila. Science 288: 2013-2018.
57. ROYOU, A., H. MACIAS and W. SULLIVAN, 2005 The Drosophila Grp/Chk1 DNA damage checkpoint controls entry into anaphase. Curr. Biol. 15: 334-339.
58. SANCAR, A., L. A. LINDSEY-BOLTZ, K. UNSAL-KACMAZ and S. LINN, 2004 Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73: 39-85.
59. SANCHEZ, Y., B. A. DESANY, W. J. JONES, Q. LIU, B. WANG et al., 1996 Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271: 357-360.
60. SHILOH, Y., 2003 ATM: ready, set, go. Cell Cycle 2: 116-117.
61. SIBON, O. C., A. LAURENCON, R. HAWLEY and W. E. THEURKAUF, 1999 The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr. Biol. 9: 302-312.
62. SIGRIST, S. J., and C. F. LEHNER, 1997 Drosophila fizzy-related down-regulates mitotic cyclins and is required for cell proliferation arrest and entry into endocycles. Cell 90: 671-681.
63. SILVA, E., S. TIONG, M. PEDERSEN, E. HOMOLA, A. ROYOU et al., 2004 ATM is required for telomere maintenance and chromosome stability during Drosophila development. Curr. Biol. 14: 1341-1347.
64. SONG, Y. H., G. MIREY, M. BETSON, D. A. HABER and J. SETTLEMAN, 2004 The Drosophila ATM ortholog, dATM, mediates the response to ionizing radiation and to spontaneous DNA damage during development. Curr. Biol. 14: 1354-1359.
65. STAEVA-VIEIRA, E., S. YOO and R. LEHMANN, 2003 An essential role of DmRad51/SpnA in DNA repair and meiotic checkpoint control. EMBO J. 22: 5863-5874.
66. SU, T. T., S. D. CAMPBELL and P. H. O'FARRELL, 1999 Drosophila grapes/CHK1 mutants are defective in cyclin proteolysis and coordination of mitotic events. Curr. Biol. 9: 919-922.
67. TAYLOR, A. M. R., D. G. HARNDEN, C. F. ARLETT, C. F. HARCOURT, A. R. LEHMANN et al., 1975 Ataxia telangiectasia: a human mutation with abnormal radiation sensitivity. Nature 258: 427-429.
68. UNSAL-KACMAZ, K., A. M. MAKHOV, J. D. GRIFFITH and A. SANCAR, 2002 Preferential binding of ATR protein to UV-damaged DNA. Proc. Natl. Acad. Sci. USA 99: 6673-6678.
69. WANG, X., J. KHADPE, B. HU, G. ILIAKIS and Y. WANG, 2003 An overactivated ATR/CHK1 pathway is responsible for the prolonged G2 accumulation in irradiated AT cells. J. Biol. Chem. 278: 30869-30874.
70. WARD, I. M., and J. CHEN, 2001 Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276: 47759-47762.
71. WARD, J. F., 1990 The yield of DNA double-strand breaks produced intracellularly by ionizing radiation: a review. Int. J. Radiat. Biol. 57: 1141-1150.
72. WRIGHT, J. A., K. S. KEEGAN, D. R. HERENDEEN, N. J. BENTLEY, A. M. CARR et al., 1998 Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc. Natl. Acad. Sci. USA 95: 7445-7450.
73. XU, J., S. XIN and W. DU, 2001 Drosophila Chk2 is required for DNA damage-mediated cell cycle arrest and apoptosis. FEBS Lett. 508: 394-398.
74. YOO, H. Y., A. SHEVCHENKO, A. SHEVCHENKO and W. G. DUNPHY, 2004 Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. J. Biol. Chem. 279: 53353-53364.
75. YU, K. R., R. B. SAINT and W. SULLIVAN, 2000 The Grapes checkpoint coordinates nuclear envelope breakdown and chromosome condensation. Nat. Cell Biol. 2: 609-615.