The Rad17 homologue of Arabidopsis is involved in the regulation of DNA damage repair and homologous recombination

Plant Journal

Volumn 38, Issue 6, 2004, Pages 954-968

  Heitzeberg, Fabian ^a   Chen, I Peng ^a,b   Hartung, Frank ^a,b   Orel, Nadiya ^a   Angelis, Karel J ^c   Puchta, Holger ^a,b  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b UNIVERSITY OF KARLSRUHE   (Germany)

^c INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

Author keywords

Arabidopsis; Comet assay; Double strand break repair; Mutagens; RAD17; RAD9

Indexed keywords

CELLS; DNA; GENES; YEAST;

ARABIDOPSIS; DOUBLE-STRAND BREAKS (DSB);

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; COMPLEMENTARY DNA; DNA BINDING PROTEIN; ENDONUCLEASE; HUS1 PROTEIN, S POMBE; PROTEIN RAD9; RAD17 PROTEIN, ARABIDOPSIS; SCHIZOSACCHAROMYCES POMBE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; DNA DAMAGE; DNA REPAIR; GENETIC RECOMBINATION; GENETICS; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPAIR; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; ENDONUCLEASES; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS; EMBRYOPHYTA;

EID: 2942750410     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02097.x     Document Type: Article

References (73)

1. Abraham, R.T. (2001) Cell cycle checkpoint signalling through the ATM and ATR kinases. Genes Dev. 15, 2177-2196.
2. Al-Khodairy, F. and Carr, A.M. (1992) DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe. EMBO J. 11, 1343-1350.
3. Allen, C., Kurimasa, A., Brenneman, M.A., Chen, D.J. and Nickoloff, J.A. (2002) DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl. Acad. Sci. USA, 99, 3758-3763.
4. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
5. Bao, S., Tibbetts, R.S., Brumbaugh, K.M., Fang, Y., Richardson, D.A., Ali, A., Chen, S.M., Abraham, R.T. and Wang, X.F. (2001) ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature, 411, 969-974.
6. Bashkirov, V.I., King, J.S., Bashkirova, E.V., Schmuckli-Maurer, J. and Heyer, W.D. (2000) DNA repair protein Rad55 is a terminal substrate of the DNA damage checkpoints. Mol. Cell Biol. 20, 4393-4404.
7. Britt, A.B. and May, G.D. (2003) Re-engineering plant gene targeting. Trends Plant Sci. 8, 90-95.
8. Burtelow, M.A., Kaufmann, S.H. and Karnitz, L.M. (2000) Retention of the human Rad9 checkpoint complex in extraction-resistant nuclear complexes after DNA damage. J. Biol. Chem. 275, 26343-26348.
9. Carr, A.M. (1997) Control of cell cycle arrest by the Mec1sc/Rad3sp DNA structure checkpoint pathway. Curr. Opin. Genet. Dev. 7, 93-98 (review).
10. Caspari, T., Dahlen, M., Kanter-Smoler, G., Lindsay, H.D., Hofmann, K., Papadimitriou, K., Sunnerhagen, P. and Carr, A.M. (2000) Characterization of Schizosaccharomyces pombe Hus1: a PCNA-related protein that associates with Rad1 and Rad9. Mol. Cell Biol. 20, 1254-1262.
11. Chen, I.P., Haehnel, U., Altschmied, L., Schubert, I. and Puchta, H. (2003) The transcriptional response of Arabidopsis to genotoxic stress - a high-density colony array study (HDCA). Plant J. 35, 771-786.
12. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl. Acad. Sci. USA, 81, 1991-1995.
13. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
14. Cullmann, G., Fien, K., Kobayashi, R. and Stillman, B. (1995) Characterization of the five replication factor C genes of Saccharomyces cerevisiae. Mol. Cell Biol. 15, 4661-4671.
15. Eckardt-Schupp, F., Siede, W. and Game, J.C. (1987) The RAD24 (=Rs1) gene product of Saccharomyces cerevisiae participates in two different pathways of DNA repair. Genetics, 115, 83-90.
16. Elledge, S.J. (1996) Cell cycle checkpoints: preventing an identity crisis. Science, 274, 1664-1672. Review.
17. Enoch, T. and Norbury, C. (1995) Cellular responses to DNA damage: cell-cycle checkpoints, apoptosis and the roles of p53 and ATM. Trends Biochem. Sci. 20, 426-430 (review).
18. Enoch, T., Carr, A.M. and Nurse, P. (1992) Fission yeast genes involved in coupling mitosis to completion of DNA replication. Genes Dev. 6, 2035-2046.
19. Frank, K.M., Sharpless, N.E., Gao, Y., Sekiguchi, J.M., Ferguson, D.O., Zhu, C., Manis, J.P., Horner, J., DePinho, R.A. and Alt, F.W. (2000) DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell. 5, 993-1002.
20. Freire, R., Murguia, J.R., Tarsounas, M., Lowndes, N.F., Moens, P.B. and Jackson, S.P. (1998) Human and mouse homologs of Schizosaccharomyces pombe rad1(+) and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev. 12, 2560-2573.
21. Friedberg, E.C., Walker, G.C. and Siede, W. (1995) DNA Repair and Mutagenesis. Washington DC: ASM.
22. Friesner, J. and Britt, A.B. (2003) Ku80- and DNA ligase IV-deficient plants are sensitive to ionizing radiation and defective in T-DNA integration. Plant J. 34, 427-440.
23. Gallego, F., Fleck, O., Li, A., Wyrzykowska, J. and Tinland, B. (2000) AtRAD1, a plant homologue of human and yeast nucleotide excision repair endonucleases, is involved in dark repair of UV damages and recombination. Plant J. 21, 507-518.
24. Garcia, V., Salanoubat, M., Choisne, N. and Tissier, A. (2000) An ATM homologue from Arabidopsis thaliana: complete genomic organisation and expression analysis. Nucl. Acids Res. 28, 1692-1699.
25. 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.
26. Gherbi, H., Gallego, M.E., Jalut, N., Lucht, J.M., Hohn, B. and White, C.I. (2001) Homologous recombination in planta is stimulated in the absence of Rad50. EMBO Rep. 2, 287-291.
27. Green, C.M., Erdjument-Bromage, H., Tempst, P. and Lowndes, N.F. (2000) A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr. Biol. 10, 39-42.
28. Griffiths, D.J., Barbet, N.C., McCready, S., Lehmann, A.R. and Carr, A.M. (1995) Fission yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins. EMBO J. 14, 5812-5823.
29. Grushcow, J.M., Holzen, T.M., Park, K.J., Weinert, T., Lichten, M. and Bishop, D.K. (1999) Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics, 153, 607-620.
30. Hajdukiewicz, P., Svab, Z. and Maliga, P. (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989-994.
31. Hartung, F. and Puchta, H. (2004) What comparative genomics tells us about the evolution of genes involved in recombination. Curr. Genomics, 5, 109-121.
32. Hartwell, L.H. and Kastan, M.B. (1994) Cell cycle control and cancer. Science, 266, 1821-1828 (review).
33. Hong, E.J. and Roeder, G.S. (2002) A role for Ddc1 in signaling meiotic double-strand breaks at the pachytene checkpoint. Genes Dev. 16, 363-376.
34. Jeggo, P.A. (1998) Identification of genes involved in repair of DNA double-strand breaks in mammalian cells. Radiat. Res. 150 (Suppl. 5), 80-91.
35. Klein, H.L. (2001) Mutations in recombinational repair and in checkpoint control genes suppress the lethal combination of srs2Delta with other DNA repair genes in Saccharomyces cerevisiae. Genetics, 157, 557-565.
36. Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K. and Sugimoto, K. (2001) Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science, 294, 867-870.
37. Kostrub, C.F., Knudsen, K., Subramani, S. and Enoch, T. (1998) Hus1p, a conserved fission yeast checkpoint protein, interacts with Rad1p and is phosphorylated in response to DNA damage. EMBO J. 17, 2055-2066.
38. Lee, S.E., Moore, J.K., Holmes, A., Umezu, K., Kolodner, R.D. and Haber, J.E. (1998) Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell, 94, 399-409.
39. Li, L., Peterson, C.A., Kanter-Smoler, G., Wei, Y.F., Ramagli, LS., Sunnerhagen, P., Siciliano, M.J. and Legerski, R.J. (1999) hRAD17, a structural homolog of the Schizosaccharomyces pombe RAD17 cell cycle checkpoint gene, stimulates p53 accumulation. Oncogene, 18, 1689-1699.
40. Lieberman, H.B., Hopkins, K.M., Nass, M., Demetrick, D. and Davey, S. (1996) A human homolog of the Schizosaccharomyces pombe rad9+ checkpoint control gene. Proc. Natl. Acad. Sci. USA, 93, 13890-13985.
41. Longhese, M.P., Paciotti, V., Fraschini, R., Zaccarini, R., Pievani, P. and Lucchini, G. (1997) The novel DNA damage checkpoint protein ddc1p is phosphorylated periodically during the cell cycle and in response to DNA damage in budding yeast. EMBO J. 16, 5216-5226.
42. Lowndes, N.F. and Murguia, J.R. (2000) Sensing and responding to DNA damage. Curr. Opin. Genet. Dev. 10, 17-25.
43. Martienssen, R. and Springer, P. (1998) Enhancer and Gene Trap Transposon Mutagenesis in Arabidopsis. (http://genetrap.cshl. org/traps.html)
44. Martin, S.G., Laroche, T., Suka, N., Grunstein, M. and Gasser, S.M. (1999) Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell, 97, 621-633.
45. Masson, J.E. and Paszkowski, J. (1997) Arabidopsis thaliana mutants altered in homologous recombination. Proc. Natl. Acad. Sci. USA, 94, 11731-11735.
46. Matz, M., Shagin, D., Bogdanova, E., Britanova, O., Lukyanov, S., Diatchenko, L. and Chenchik, A. (1999) Amplification of cDNA ends based on template-switching effect and step-out PCR. Nucl. Acids Res. 27, 1558-1560.
47. McAinsh, A.D., Scott-Drew, S., Murray, J.A. and Jackson, S.P. (1999) DNA damage triggers disruption of telomeric silencing and Mec1p-dependent relocation of Sir3p. Curr. Biol. 9, 963-966.
48. Melo, J.A., Cohen, J. and Toczyski, D.P. (2001) Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15, 2809-2821.
49. Mills, K.D., Sinclair, D.A. and Guarente, L. (1999) MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell, 97, 609-620.
50. Morrison, C., Sonoda, E., Takao, N., Shinohara, A., Yamamoto, K. and Takeda, S. (2000) The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 19, 463-471.
51. Neuwald, A.F., Aravind, L., Spouge, J.L. and Koonin, E.V. (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43.
52. Orel, N. and Puchta, H. (2003) Differences in the processing of DNA ends in Arabidopsis thaliana and tobacco: possible implications for genome evolution. Plant Mol. Biol. 51, 523-531.
53. Paques, 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. Review.
54. Parker, A.E., Van de Weyer, I., Laus, M.C., Oostveen, I., Yon, J., Verhasselt, P. and Luyten, W.H. (1998) Homologue of the Schizosaccharomyces pombe rad1+ checkpoint gene encodes an exonuclease. J. Biol. Chem. 273, 18332-18339.
55. Paulovich, A.G., Toczyski, D.P. and Hartwell, L.H. (1997) When checkpoints fail. Cell, 88, 315-321. Review.
56. Preuss, S.B. and Britt, A.B. (2003) A DNA-damage-induced cell cycle checkpoint in Arabidopsis. Genetics, 164, 323-334.
57. Puchta, H., Swoboda, P., Gal, S., Blot, M. and Hohn, B. (1995) Somatic intrachromosomal homologous recombination events in populations of plant siblings. Plant Mol. Biol. 28, 281-292.
58. Puchta, H., Dujon, B. and Hohn, B. (1996) Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc. Natl. Acad. Sci. USA, 93, 5055-5060.
59. Roos-Mattjus, P., Vroman, B.T., Burtelow, M.A., Rauen, M., Eape, A.K. and Karnitz, L.M. (2002) Genotoxin-induced Rad9-Hus1-Rad1 (9-1-1) chromatin association is an early checkpoint signaling event. J. Biol. Chem. 277, 43809-43812.
60. Roos-Mattjus, P., Hopkins, K.M., Oestreich, A.J., Vroman, B.T., Johnson, K.L., Naylor, S., Lieberman, H.B. and Karnitz, L.M. (2003) Phosphorylation of human Rad9 is required for genotoxin-activated checkpoint signaling. J. Biol. Chem. 278, 24428-24437.
61. Rouse, J. and Jackson, S.P. (2002) Interfaces between the detection, signaling, and repair of DNA damage. Science, 297, 547-551 (review).
62. Rowley, R., Subramani, S. and Young, P.G. (1992) Checkpoint controls in Schizosaccharomyces pombe: rad1. EMBO J. 11, 1335-1342.
63. Salomon, S. and Puchta, H. (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J, 17, 6086-6095.
64. Schmidt-Puchta, W., Orel, N., Kirik, A. and Puchta, H. (2004) Intrachromosomal homologous recombination in Arabidopsis thaliana. Meth. Mol. Biol. 262, 25-35.
65. Siebert, R. and Puchta, H. (2002) Efficient repair of genomic double-strand breaks by homologous recombination between directly repeated sequences in the plant genome. Plant Cell, 14, 1121-1131.
66. Stewart, E. and Enoch, T. (1996) S-phase and DNA-damage checkpoints: a tale of two yeasts. Curr. Opin. Cell Biol. 8, 781-787 (review).
67. Sundaresan, V., Springer, P., Volpe, T., Haward, S., Jones, J.D., Dean, C., Ma, H. and Martienssen, R. (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9, 1797-1810.
68. Swoboda, P., Gal, S., Hohn, B. and Puchta, H. (1994) Intrachromosomal homologous recombination in whole plants. EMBO J. 13, 484-489.
69. Thelen, M.P., Venclovas, C. and Fidelis, K.A. (1999) Sliding clamp model for the Rad1 family of cell cycle checkpoint proteins. Cell, 96, 769-770
70. de la Torre-Ruiz, M. and Lowndes, N.F. (2000) The Saccharomyces cerevisiae DNA damage checkpoint is required for efficient repair of double strand breaks by non-homologous end joining. FEBS Lett. 467, 311-315.
71. Venclovas, C. and Thelen, M.P. (2000) Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucl Acids Res. 28, 2481-2493.
72. Volkmer, E. and Karnitz, L.M. (1999) Human homologs of Schizosaccharomyces pombe rad1, hus1, and rad9 form a DNA damage-responsive protein complex. J. Biol. Chem. 274, 567-570.
73. Zou, L., Cortez, D. and Elledge, S.J. (2002) Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16, 198-208.