ATM and ATR homologes of Neurospora crassa are essential for normal cell growth and maintenance of chromosome integrity

Fungal Genetics and Biology

Volumn 47, Issue 10, 2010, Pages 809-817

  Wakabayashi, Michiyoshi ^a   Ishii, Chizu ^a   Hatakeyama, Shin ^a   Inoue, Hirokazu ^a   Tanaka, Shuuitsu ^a  

^a SAITAMA UNIVERSITY   (Japan)

Author keywords

ATM; ATR; Checkpoint; DNA repair; Genome instability; Neurospora crassa

Indexed keywords

ATM PROTEIN; ATR PROTEIN;

ALLELE; ARTICLE; CELL GROWTH; CELL VIABILITY; CHROMOSOME ANALYSIS; CONIDIUM; CONTROLLED STUDY; DNA DAMAGE; FUNGAL CELL; FUNGAL STRAIN; FUNGUS HYPHAE; GENE; GENE CONSTRUCT; GENE CONTROL; GENE FUNCTION; GENETIC ANALYSIS; HETEROZYGOSITY; MUS 21 GENE; MUS 9 GENE; MUTATIONAL ANALYSIS; NEUROSPORA CRASSA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE HOMOLOGY; TEMPERATURE SENSITIVITY;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CHROMOSOMES, FUNGAL; DNA-BINDING PROTEINS; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NEUROSPORA CRASSA; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE ALIGNMENT; TUMOR SUPPRESSOR PROTEINS;

EUKARYOTA; FUNGI; MAMMALIA; NEUROSPORA CRASSA;

EID: 77956342893     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.05.010     Document Type: Article

References (64)

1. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001, 15:2177-2196.
2. Alcasabas A.A., Osborn A.J., Bachant J., Hu F., Werler P.J., Bousset K., Furuya K., Diffley J.F., Carr A.M., Elledge S.J. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 2001, 3:958-965.
3. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M., Collins F., Shiloh Y., Crawley J.N., Ried T., Tagle D., Wynshaw-Boris A. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996, 86:159-171.
4. Bhanoori M., Venkateswerlu G. The alkaline single cell gel electrophoresis: a new test for assessing DNA single strand breaks in Neurospora crassa. Mutat. Res. 1998, 405:29-34.
5. Brown E.J., Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 2000, 14:397-402.
6. Bryant P.E., Jones N.J., Liu N. Radiosensitive Chinese hamster irs2 cells show enhanced chromosomal sensitivity to ionizing radiation and restriction endonuclease induced blunt-ended double-strand breaks. Mutagenesis 1993, 8:141-147.
7. Carroll A.M., Sweigard J.A., Valent B. Improved vectors for selecting resistance to hygromycin. Fungal Genet. Newslett. 1994, 41:20-21.
8. Chanoux R.A., Yin B., Urtishak K.A., Asare A., Bassing C.H., Brown E.J. ATR and H2AX cooperate in maintaining genome stability under replication stress. J. Biol. Chem. 2009, 284:5994-6003.
9. Cimprich K.A., Cortez D. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 2008, 9:616-627.
10. Cliby W.A., Roberts C.J., Cimprich K.A., Stringer C.M., Lamb J.R., Schreiber S.L., Friend S.H. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 1998, 17:159-169.
11. Colot H.V., Park G., Turner G.E., Ringelberg C., Crew C.M., Litvinkova L., Weiss R.L., Borkovich K.A., Dunlap J.C. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. USA 2006, 103:10352-10357.
12. Davis R.H., de Serres F.J. Genetic and microbiological research techniques for Neurospora crassa. Meth. Enzymol. 1970, 17:79-143.
13. de Klein A., Muijtjens M., van Os R., Verhoeven Y., Smit B., Carr A.M., Lehmann A.R., Hoeijmakers J.H. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 2000, 10:479-482.
14. Downs J.A., Lowndes N.F., Jackson S.P. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 2000, 408:1001-1004.
15. Dudasova Z., Dudas A., Chovanec M. Non-homologous end-joining factors of Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2004, 28:581-601.
16. Fabre F., Chan A., Heyer W.D., Gangloff S. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. USA 2002, 99:16887-16892.
17. NBS1 genes show genetic interactions during recovery from replication stress and DNA damage. Eukaryot. Cell 2005, 4:1239-1252.
18. Fairbairn D.W., Olive P.L., O'Neill K.L. The comet assay: a comprehensive review. Mutat. Res. 1995, 339:37-59.
19. Fenech M. The in vitro micronucleus technique. Mutat. Res. 2000, 455:81-95.
20. Foster E.R., Downs J.A. Histone H2A phosphorylation in DNA double-strand break repair. FEBS J. 2005, 272:3231-3240.
21. Garner E., Costanzo V. Studying the DNA damage response using in vitro model systems. DNA Repair (Amst) 2009, 8:1025-1037.
22. Harrison J.C., Haber J.E. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 2006, 40:209-235.
23. Hekmat-Nejad M., You Z., Yee M.C., Newport J.W., Cimprich K.A. Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr. Biol. 2000, 10:1565-1573.
24. Hofmann A.F., Harris S.D. The Aspergillus nidulans uvsB gene encodes an ATM-related kinase required for multiple facets of the DNA damage response. Genetics 2000, 154:1577-1586.
25. Ishibashi K., Suzuki K., Ando Y., Takakura C., Inoue H. Nonhomologous chromosomal integration of foreign DNA is completelydependent on MUS-53 (human Lig4 homolog) in Neurospora. Proc. Natl. Acad. Sci. USA 2006, 103:14871-14876.
26. Itakura E., Sawada I., Matsuura A. Dimerization of the ATRIP protein through the coiled-coil motif and its implication to the maintenance of stalled replication forks. Mol. Biol. Cell 2005, 16:5551-5562.
27. Ivessa A.S., Zhou J.Q., Schulz V.P., Monson E.K., Zakian V.A. Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 2002, 16:1383-1396.
28. Kafer E., Luk D. Properties and strains of additional DNA repair-defective mutants in known and new genes of Neurospora crassa. Fungal Genet. Newslett. 1988, 35:11-13.
29. Kato A., Inoue H. Growth defect and mutator phenotypes of RecQ-deficient Neurospora crassa mutants separately result from homologous recombination and nonhomologous end joining during repair of DNA double-strand breaks. Genetics 2006, 172:113-125.
30. Kawabata T., Kato A., Suzuki K., Inoue H. Neurosprora crassa RAD5 homologue, mus-41, inactivation results in higher sensitivity to mutagens but has little effect on PCNA-ubiquitylation in response to UV-irradiation. Curr. Genet. 2007, 52:125-135.
31. Kazama Y., Ishii C., Schroeder A.L., Shimada H., Wakabayashi M., Inoue H. The Neurospora crassa UVS-3 epistasis group encodes homologues of the ATR/ATRIP checkpoint control system. DNA Repair (Amst) 2007, 7:213-229.
32. Kumagai A., Dunphy W.G. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell 2000, 6:839-849.
33. Lee H.C., Chang S.S., Choudhary S., Aalto A.P., Maiti M., Bamford D.H., Liu Y. QiRNA is a new type of small interfering RNA induced by DNA damage. Nature 2009, 459:274-277.
34. Lee R.F., Steinert S. Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat. Res. 2003, 544:43-64.
35. Lobrich M., Jeggo P.A. Harmonising the response to DSBs: a new string in the ATM bow. DNA Repair (Amst) 2005, 4:749-759.
36. MacDougall C.A., Byun T.S., Van C., Yee M.C., Cimprich K.A. The structural determinants of checkpoint activation. Genes Dev. 2007, 21:898-903.
37. ATM homolog with different components of the DNA damage response pathway. Genetics 2008, 178:675-691.
38. Malavazi I., Semighini C.P., Kress M.R., Harris S.D., Goldman G.H. Regulation of hyphal morphogenesis and the DNA damage response by the Aspergillus nidulans ATM homolog AtmA. Genetics 2006, 173:99-109.
39. Martinho R.G., Lindsay H.D., Flaggs G., DeMaggio A.J., Hoekstra M.F., Carr A.M., Bentley N.J. Analysis of Rad3 and Chk1 protein kinases defines different checkpoint responses. EMBO J. 1998, 17:7239-7249.
40. Matsuura A., Naito T., Ishikawa F. Genetic control of telomere integrity in Schizosaccharomyces pombe: rad3(+) and tel1(+) are parts of two regulatory networks independent of the downstream protein kinases chk1(+) and cds1(+). Genetics 1999, 152:1501-1512.
41. Morrow D.M., Tagle D.A., Shiloh Y., Collins F.S., Hieter P. TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell 1995, 82:831-840.
42. Moses S.A., Christie A.F., Bryant P.E. Clastogenicity of PvuII and EcoRI in electroporated CHO cells assayed by metaphase chromosomal aberrations and by micronuclei using the cytokinesis-block technique. Mutagenesis 1990, 5:599-603.
43. Ninomiya Y., Suzuki K., Ishii C., Inoue H. Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc. Natl. Acad. Sci. USA 2004, 101:12248-12253.
44. Ostling O., Johanson K.J. Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem. Biophys. Res. Commun. 1984, 123:291-298.
45. Ozeri-Galai E., Schwartz M., Rahat A., Kerem B. Interplay between ATM and ATR in the regulation of common fragile site stability. Oncogene 2008, 27:2109-2117.
46. Pankratz D.G., Forsburg S.L. Meiotic S-phase damage activates recombination without checkpoint arrest. Mol. Biol. Cell 2005, 16:1651-1660.
47. Paulsen R.D., Cimprich K.A. The ATR pathway: fine-tuning the fork. DNA Repair (Amst) 2007, 6:953-966.
48. Pregueiro A.M., Liu Q., Baker C.L., Dunlap J.C., Loros J.J. The Neurospora checkpoint kinase 2: a regulatory link between the circadian and cell cycles. Science 2006, 313:644-649.
49. Schmidt K.H., Kolodner R.D. Requirement of Rrm3 helicase for repair of spontaneous DNA lesions in cells lacking Srs2 or Sgs1 helicase. Mol. Cell. Biol. 2004, 24:3213-3226.
50. Schroeder A.L. Use of Neurospora to study DNA repair. DNA Repair A Laboratory Manual of Research Procedures 1988, vol. 3:77-98. Dekker, New York.
51. Schroeder A.L., Inoue H., Sachs M.S. DNA repair in Neurospora. DNA Damage and Repair 1998, vol. 1:503-538. Humana Press, New Jersey.
52. Song Y.H. Drosophila melanogaster: a model for the study of DNA damage checkpoint response. Mol. Cells 2005, 19:167-179.
53. Staben C., Jensen B., Singer M., Pollock J., Schechtman M., Kinsey J., Selker E. Use of a bacterial hygromycin B resistance gene as a dominant selectable marker in Neurospora crassa transformation. Fungal Genet. Newslett. 1989, 36:79-81.
54. Stiff T., O'Driscoll M., Rief N., Iwabuchi K., Lobrich M., Jeggo P.A. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 2004, 64:2390-2396.
55. Suzuki K., Kato A., Sakuraba Y., Inoue H. Srs2 and RecQ homologs cooperate in mei-3-mediated homologous recombination repair of Neurospora crassa. Nucleic Acids Res. 2005, 33:1848-1858.
56. Szyjka S.J., Viggiani C.J., Aparicio O.M. Mrc1 is required for normal progression of replication forks throughout chromatin in S. Cerevisiae. Mol. Cell 2005, 19:691-697.
57. Tamaru H., Inoue H. Isolation and characterization of a laccase-derepressed mutant of Neurospora crassa. J. Bacteriol. 1989, 171:6288-6293.
58. Tanaka S., Takayanagi N., Murasawa K., Ishii C., Inoue H. Genetic and molecular analysis of the temperature-sensitive mutant un-17 carrying a mutation in the gene encoding poly(A)-polymerase in Neurospora crassa. Genes Genet. Syst. 2007, 82:447-454.
59. Tong A.H., Evangelista M., Parsons A.B., Xu H., Bader G.D., Page N., Robinson M., Raghibizadeh S., Hogue C.W., Bussey H., Andrews B., Tyers M., Boone C. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 2001, 294:2364-2368.
60. Wakabayashi M., Ishii C., Inoue H., Tanaka S. Genetic analysis of CHK1 and CHK2 homologues revealed a unique cross talk between ATM and ATR pathways in Neurospora crassa. DNA Repair (Amst) 2008, 7:1951-1961.
61. Wang W., Seki M., Otsuki M., Tada S., Takao N., Yamamoto K., Hayashi M., Honma M., Enomoto T. The absence of a functional relationship between ATM and BLM, the components of BASC, in DT40 cells. Biochim. Biophys. Acta 2004, 1688:137-144.
62. Wright J.A., Keegan K.S., Herendeen D.R., Bentley N.J., Carr A.M., Hoekstra M.F., Concannon P. Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc. Natl. Acad. Sci. USA 1998, 95:7445-7450.
63. Xu H., Boone C., Klein H.L. Mrc1 is required for sister chromatid cohesion to aid in recombination repair of spontaneous damage. Mol. Cell. Biol. 2004, 24:7082-7090.
64. Yoo H.Y., Shevchenko A., Shevchenko A., Dunphy W.G. Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. J. Biol. Chem. 2004, 279:53353-53364.