Arabidopsis replication protein a 70a is required for DNA damage response and telomere length homeostasis

Plant and Cell Physiology

Volumn 50, Issue 11, 2009, Pages 1965-1976

  Takashi, Yoshiyuki ^a   Kobayashi, Yuki ^a   Tanaka, Kan ^a   Tamura, Katsunori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Arabidopsis thaliana; Cell cycle checkpoint; DNA repair; Telomere maintenance

Indexed keywords

ARABIDOPSIS PROTEIN; BACTERIAL DNA; PLANT RNA; PROTEIN SUBUNIT; REPLICATION FACTOR A; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; DOUBLE STRANDED DNA BREAK; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; SEQUENCE HOMOLOGY; TELOMERE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CLONING, MOLECULAR; DNA BREAKS, DOUBLE-STRANDED; DNA, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; MUTAGENESIS, INSERTIONAL; PROTEIN SUBUNITS; REPLICATION PROTEIN A; RNA, PLANT; SEQUENCE HOMOLOGY, AMINO ACID; TELOMERE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 70450265395     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcp140     Document Type: Article

References (62)

1. Ball, H.L., Myers, J.S. and Cortez, D. (2005) ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Mol. Biol. Cell 16: 2372-2381.
2. Bechtold, N. and Pelletier, G. (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol. 82: 259-266.
3. Becker, D. (1990) Binary vectors which allow the exchange of plant selectable markers and reporter genes. Nucleic Acids Res. 18: 203.
4. Binz, S.K., Sheehan, A.M. and Wold, M.S. (2004) Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair 3: 1015-1024.
5. Bochkareva, E., Belegu, V., Korolev,S.and Bochkarev, A.(2001) Structure of the major single stranded DNA-binding domain of replication protein A suggests a dynamic mechanism for DNA binding. EMBO J. 20: 612-618.
6. Bochkareva, E., Korolev, S. and Bochkarev, A. (2000) The role for zinc in replication protein A. J. Biol. Chem. 275: 27332-27338.
7. Braun, K.A., Lao, Y., He, Z., Ingles, C.J. and Wold, M.S. (1997) Role of protein-protein interactions in the function of replication protein A (RPA): RPA modulates the activity of DNA polymerase alpha by multiple mechanisms. Biochemistry 36: 8443-8454.
8. Bullock, P.A. (1997) The initiation of simian virus 40 DNA replication in vitro. Crit. Rev. Biochem. Mol. Biol. 32: 503-568.
9. 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.
10. Cahill, D., Connor, B. and Carney, J.P. (2006) Mechanisms of eukaryotic DNA double strand break repair. Front. Biosci. 11: 1958-1976.
11. Cohen, S., Jacob, E. and Manor, H. (2004) Effects of single-stranded DNA binding proteins on primer extension by telomerase. Biochim. Biophys. Acta 1679: 129-140.
12. Daniely, Y. and Borowiec, J.A. (2000) Formation of a complex between nucleolin and replication protein A after cell stress prevents initiation of DNA replication. J. Cell Biol. 149: 799-810.
13. Doherty, K.M., Sommers, J.A., Gray, M.D., Lee, J.W., von Kobbe, C., Thoma, N.H., et al. (2005) Physical and functional mapping of the replication protein A interaction domain of the Werner and Bloom syndrome helicases. J. Biol. Chem. 280: 29494-29505.
14. Fanning, E., Klimovich, V. and Nager, A.R. (2006) A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34: 4126-4137.
15. Fields, S. and Sternglanz, R. (1994) The two-hybrid system: an assay for protein-protein interactions. Trends Genet. 10: 286-292.
16. Fitzgerald, M.S., Riha, K., Gao, F., Ren, S., McKnight, T.D. and Shippen, D.E. ( 1999 ) Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc. Natl Acad. Sci. USA 96: 14813-14818.
17. Frank-Vaillant, M. and Marcand, S. (2002) Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol. Cell 10: 1189-1199.
18. Gallego, M.E., Jalut, N. and White, C.I. (2002) Telomerase dependence of telomere lengthening in ku80 mutant Arabidopsis. Plant Cell 15: 782-789.
19. 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
20. Garcia-Maya,M.M.andBuck,K.W.(1997)Isolationandcharacterization of replication protein A (RPA) from tobacco cells. FEBS Lett. 413: 181-184.
21. Grandin, N. and Charbonneau, M. ( 2007 ) Control of the yeast telomeric senescence survival pathways of recombination by the Mec1 and Mec3 DNA damage sensors and RPA. Nucleic Acids Res. 35: 822-838.
22. Henson, J.D., Neumann, A.A., Yeager, T.R. and Reddle, R.R. (2002) Alternative lengthening of telomeres in mammalian cells. Oncogene 21: 598-610.
23. Ishibashi, T., Kimura, S., Furukawa, T., Hatanaka, M., Hashimoto, J. and Sakaguchi, K. (2001) Two types of replication protein A 70kDa subunit in rice, Oryza sativa: molecular cloning, characterization and cellular and tissue distribution. Gene 272: 335-343.
24. Ishibashi, T., Koga, A., Yamamoto, T., Uchiyama, Y., Mori, Y., Hashimoto, J., et al. (2005). Two types of replication protein A in seed plants. FEBS J. 272: 3270-3281.
25. Iftode, C., Daniely, Y. and Borowiec, J.A. (1999) Replication protein A (RPA): the eukaryotic SSB. Crit. Rev. Biochem. Mol. Biol. 34: 141-180.
26. Keshav, K.F., Chen, C. and Dutta, A. (1995) Rpa4, a homolog of the 34-kilodalton subunit of the replication protein A complex. Mol. Cell. Biol. 15: 3119-3128.
27. Kim, K., Dimitrova, D.D., Carta, K.M., Saxena, A., Daras, M. and Borowiec, J.A. (2005) Novel checkpoint response to genotoxic stress mediated by nucleolin-replication protein A complex formation. Mol. Cell. Biol. 25: 2463-2474.
28. Kim, C., Paulus, B.F. and Wold, M.S. (1994) Interactions of human replication protein A with oligonucleotides. Biochemistry 33: 14197-14206.
29. Longhese, M.P., Neecke, H., Paciotti, V., Lucchini, G. and Plevani, P. ( 1996 ) The 70 kDa subunit of replication protein A is required for the G1/S and intra-S DNA damage checkpoints in budding yeast. Nucleic Acids Res. 24: 3533-3537.
30. Lundblad, V. (2002) Telomere maintenance without telomerase. Oncogene 21: 522-531.
31. Namiki, Y. and Zou, L. (2006) ATRIP associates with replication protein A-coated ssDNA through multiple interactions. Proc. Natl Acad. Sci. USA 103: 580-585.
32. Oguchi, K., Liu, H., Tamura, K. and Takahashi, H. (1999) Molecular cloning and characterization of AtTERT, a telomerase reverse transcriptase homolog in Arabidopsis thaliana. FEBS Lett. 457: 465-469.
33. Ono, Y., Tomita, K., Matsuura, A., Nakagawa, T., Masukata, H., Uritani, M., et al. (2003) A novel allele of fission yeast rad11 that causes defects in DNA repair and telomere length regulation. Nucleic Acids Res. 31: 7141-7149. (Pubitemid 38008445)
34. Opresko, P.L., von Kobbe, C., Laine, J.P., Harrigan, J., Hickson, I.D. and Bohr, V.A. (2002) Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem. 277: 41110-41119.
35. Pacher, M., Schmidt-Puchta, W. and Puchta, H. (2007) Two unlinked double-strand breaks can induce reciprocal exchanges in plant genomes via homologous recombination and nonhomologous end joining. Genetics 175: 21-29.
36. Riha, K., Watson, J.M., Parkey, J. and Shippen, D.E. (2001) Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants defi cient in Ku70. EMBO J. 21: 2819-2826.
37. 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.
38. Salas, T.R., Petruseva, I., Lavrik, O., Bourdoncle, A., Mergny, J.L., Favre, A., et al. (2006) Human replication protein A unfolds telomeric G-quadruplexes. Nucleic Acids Res. 34: 4857-4865.
39. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Schramke, V., Luciano, P., Brevet, V., Guillot, S., Corda, Y., Longhese, M.P., et al. ( 2004 ) RPA regulates telomerase action by providing Est1p access to chromosome ends. Nat. Genet. 36: 46-54.
41. Smith, J., Zou, H. and Rothstein, R. (2000) Characterization of genetic interactions with RFA1: the role of RPA in DNA replication and telomere maintenance. Biochimie 82: 71-78.
42. Sogo, J.M., Lopes, M. and Foiani, M. (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602
43. Song, B.and Sung, P. (2000) Functional interactions among yeast Rad51 recombinase, Rad52 mediator and replication protein A in DNA strand exchange. J. Biol. Chem. 275: 15895-15904.
44. Stenlund, A. (2003) Initiation of DNA replication: lessons from viral initiator proteins. Nat. Rev. Mol. Cell Biol. 4: 777-785.
45. Sugiyama, T. and Kowalczykowski, S.C. (2002) Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem. 277: 31663-31672.
46. Symington, L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66: 630-670.
47. Tamura, K., Adachi, Y., Chiba, K., Oguchi, K. and Takahashi, H. (2002) Identifi cation of Ku70 and Ku80 homologues in Arabidopsis thaliana: evidence for a role in the repair of DNA double-strand breaks. Plant J. 29: 771-781.
48. Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
49. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specifi c gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
50. Tuteja, N., Singh, M.B., Misra, M.K., Bhalla, P.L. and Tuteja, R. (2001) Molecular mechanisms of DNA damage and repair: progress in plants. Crit. Rev. Biochem. Mol. Biol. 36: 337-397.
51. van der Knaap, E., Jagoueix, S. and Kende, H. (1997) Expression of an ortholog of replication protein A1 (RPA1) is induced by gibberellin in deepwater rice. Proc. Natl Acad. Sci. USA 94: 9979-9983.
52. Verdun, R.E. and Karlseder, J. (2006) The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127: 709-720.
53. Viscardi, V., Clerici, M., Cartagena-Lirola, H. and Longhese, M.P. (2005) Telomeres and DNA damage checkpoints. Biochimie 87: 613-624.
54. Wold, M.S. (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66: 61-92.
55. Wong, J.M.S., Ionescu, D. and Ingles, C.J. (2003) Interaction between BRCA2 and replication protein A is compromised by a cancer-predisposing mutation in BRCA2. Oncogene 22: 28-33.
56. Wu, X., Shell, S.M. and Zou, Y. (2005) Interaction and colocalization of Rad9/Rad1/Hus1 checkpoint complex with replication protein A in human cells. Oncogene 24: 4728-4735.
57. Xia, R., Wang, J., Liu, C., Wang, Y., Wang, Y., Zhai, J., et al. (2006) ROR1/ RPA2A, a putative replication protein A2, functions in epigenetic gene silencing and in regulation of meristem development in Arabidopsis. Plant Cell 18: 85-103.
58. Yoo, E., Kim, B.U., Lee, S.Y., Cho, C.H., Chung, J.H. and Lee, C.-H. (2005) 53BP1 is associated with replication protein A and is required for RPA2 hyperphosphorylation following DNA damage. Oncogene 24: 5423-5430.
59. Zaug, A.J., Podell, E.R. and Cech, T.R. (2005) Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc. Natl Acad. Sci. USA 102: 10864-10869.
60. Zhang, L., Tamura, K., Shin-ya, K. and Takahashi, T. (2006) The telomerase inhibitor telomestatin induces telomere shortening and cell death in Arabidopsis. Biochim. Biophys. Acta 1763: 39-44.
61. Zou, L. and Elledge, S.J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
62. Zou, L., Liu, D. and Elledge, S.J. (2003) Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl Acad. Sci. USA 100: 13827-13832.