Oxidative DNA damage bypass in Arabidopsis thaliana requires DNA polymerase λ and proliferating cell nuclear antigen 2

Plant Cell

Volumn 23, Issue 2, 2011, Pages 806-822

  Amoroso, Alessandra ^a   Concia, Lorenzo ^b   Maggio, Caterina ^b   Raynaud, Cécile ^c   Bergounioux, Catherine ^c   Crespan, Emmanuele ^a   Cella, Rino ^b   Maga, Giovanni ^a  

^a CNR   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 79953072603     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.081455     Document Type: Article

References (57)

1. Anderson, H.J., et al. (2008). Arabidopsis thaliana Y-family DNA polymerase eta catalyses translesion synthesis and interacts functionally with PCNA2. Plant J. 55: 895-908.
2. Blanc, G., Hokamp, K., and Wolfe, K.H. (2003). A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 13: 137-144.
3. Bray, C.M., and West, C.E. (2005). DNA repair mechanisms in plants: Crucial sensors and effectors for the maintenance of genome integrity. New Phytol. 168: 511-528.
4. Britt, A.B. (1999). Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 4: 20-25.
5. Chan, C.S., Guo, L., and Shih, M.C. (2001). Promoter analysis of the nuclear gene encoding the chloroplast glyceraldehyde-3-phosphate dehydrogenase B subunit of Arabidopsis thaliana. Plant Mol. Biol. 46: 131-141.
6. Chang, W.C., Lee, T.Y., Huang, H.D., Huang, H.Y., and Pan, R.L. (2008). PlantPAN: Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 9: 561.
7. Chen, J., Ai, Y., Wang, J., Haracska, L., and Zhuang, Z. (2010). Chemically ubiquitylated PCNA as a probe for eukaryotic translesion DNA synthesis. Nat. Chem. Biol. 6: 270-272.
8. Chen, W., et al. (2002). Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14: 559-574.
9. 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.
10. Collins, A.R. (1999). Oxidative DNA damage, antioxidants, and cancer. Bioessays 21: 238-246.
11. Crespan, E., Zanoli, S., Khandazhinskaya, A., Shevelev, I., Jasko, M., Alexandrova, L., Kukhanova, M., Blanca, G., Villani, G., Hübscher, U., Spadari, S., and Maga, G. (2005). Incorporation of non-nucleoside triphosphate analogues opposite to an abasic site by human DNA polymerases beta and lambda. Nucleic Acids Res. 33: 4117-4127.
12. Curtis, M.J., and Hays, J.B. (2007). Tolerance of dividing cells to replication stress in UVB-irradiated Arabidopsis roots: Requirements for DNA translesion polymerases h and z. DNA Repair (Amst.) 6: 1341-1358.
13. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
14. Das-Bradoo, S., Nguyen, H.D., and Bielinsky, A.K. (2010). Damagespecific modification of PCNA. Cell Cycle 9: 3674-3679.
15. 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.
16. García-Ortiz, M.V., Roldán-Arjona, T., and Ariza, R.R. (2007). The noncatalytic C-terminus of AtPOLK Y-family DNA polymerase affects synthesis fidelity, mismatch extension and translesion replication. FEBS J. 274: 3340-3350.
17. Gary, R., Kim, K., Cornelius, H.L., Park, M.S., and Matsumoto, Y. (1999). Proliferating cell nuclear antigen facilitates excision in longpatch base excision repair. J. Biol. Chem. 274: 4354-4363.
18. Guilley, H., Dudley, R.K., Jonard, G., Balàzs, E., and Richards, K.E. (1982). Transcription of Cauliflower mosaic virus DNA: Detection of promoter sequences, and characterization of transcripts. Cell 30: 763-773.
19. Harrison, S.J., Mott, E.K., Parsley, K., Aspinall, S., Gray, J.C., and Cottage, A. (2006). A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2: 1-7.
20. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., and Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8: R19.
21. Hudson, M.E., and Quail, P.H. (2003). Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol. 133: 1605-1616.
22. Iftode, C., Daniely, Y., and Borowiec, J.A. (1999). Replication protein A (RPA): The eukaryotic SSB. Crit. Rev. Biochem. Mol. Biol. 34: 141-180.
23. Ishibashi, K., Suzuki, K., Ando, Y., Takakura, C., and Inoue, H. (2006). Nonhomologous chromosomal integration of foreign DNA is completely dependent on MUS-53 (human Lig4 homolog) in Neurospora. Proc. Natl. Acad. Sci. USA 103: 14871-14876.
24. Jin, H., Cominelli, E., Bailey, P., Parr, A., Mehrtens, F., Jones, J., Tonelli, C., Weisshaar, B., and Martin, C. (2000). Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J. 19: 6150-6161.
25. Kamiya, H. (2003). Mutagenic potentials of damaged nucleic acids produced by reactive oxygen/nitrogen species: Approaches using synthetic oligonucleotides and nucleotides: Survey and summary. Nucleic Acids Res. 31: 517-531.
26. Kamiya, H. (2004). Mutagenicities of 8-hydroxyguanine and 2-hydroxyadenine produced by reactive oxygen species. Biol. Pharm. Bull. 27: 475-479.
27. Karimi, M., De Meyer, B., and Hilson, P. (2005). Modular cloning in plant cells. Trends Plant Sci. 10: 103-105.
28. Kimura, S., and Sakaguchi, K. (2006). DNA repair in plants. Chem. Rev. 106: 753-766.
29. Kimura, S., Tahira, Y., Ishibashi, T., Mori, Y., Mori, T., Hashimoto, J., and Sakaguchi, K. (2004). DNA repair in higher plants; photoreactivation is the major DNA repair pathway in non-proliferating cells while excision repair (nucleotide excision repair and base excision repair) is active in proliferating cells. Nucleic Acids Res. 32: 2760-2767.
30. Kraft, E., Stone, S.L., Ma, L., Su, N., Gao, Y., Lau, O.S., Deng, X.W., and Callis, J. (2005). Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol. 139: 1597-1611.
31. Krishna, T.S., Fenyö, D., Kong, X.P., Gary, S., Chait, B.T., Burgers, P., and Kuriyan, J. (1994b). Crystallization of proliferating cell nuclear antigen (PCNA) from Saccharomyces cerevisiae. J. Mol. Biol. 241: 265-268.
32. Krishna, T.S., Kong, X.P., Gary, S., Burgers, P.M., and Kuriyan, J. (1994a). Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79: 1233-1243.
33. Kunz, B.A. (2008). A role for PCNA2 in translesion synthesis by Arabidopsis thaliana DNA polymerase eta. Plant Signal. Behav. 3: 897-898.
34. Macpherson, P., Barone, F., Maga, G., Mazzei, F., Karran, P., and Bignami, M. (2005). 8-Oxoguanine incorporation into DNA repeats in vitro and mismatch recognition by MutSalpha. Nucleic Acids Res. 33: 5094-5105.
35. Maga, G., Blanca, G., Shevelev, I., Frouin, I., Ramadan, K., Spadari, S., Villani, G., and Hübscher, U. (2004). The human DNA polymerase lambda interacts with PCNA through a domain important for DNA primer binding and the interaction is inhibited by p21/WAF1/CIP1. FASEB J. 18: 1743-1745.
36. Maga, G., Crespan, E., Wimmer, U., van Loon, B., Amoroso, A., Mondello, C., Belgiovine, C., Ferrari, E., Locatelli, G., Villani, G., and Hübscher, U. (2008). Replication protein A and proliferating cell nuclear antigen coordinate DNA polymerase selection in 8-oxo-guanine repair. Proc. Natl. Acad. Sci. USA 105: 20689-20694.
37. Maga, G., and Hubscher, U. (2003). Proliferating cell nuclear antigen (PCNA): A dancer with many partners. J. Cell Sci. 116: 3051-3060.
38. Maga, G., van Loon, B., Crespan, E., Villani, G., and Hübscher, U. (2009). The block of DNA polymerase delta strand displacement activity by an abasic site can be rescued by the concerted action of DNA polymerase beta and Flap endonuclease 1. J. Biol. Chem. 284: 14267-14275.
39. Maga, G., Villani, G., Crespan, E., Wimmer, U., Ferrari, E., Bertocci, B., and Hübscher, U. (2007). 8-Oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. Nature 447: 606-608.
40. Menges, M., and Murray, J.A.H. (2002). Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J. 30: 203-212.
41. Potuschak, T., Stary, S., Schlögelhofer, P., Becker, F., Nejinskaia, V., and Bachmair, A. (1998). PRT1 of Arabidopsis thaliana encodes a component of the plant N-end rule pathway. Proc. Natl. Acad. Sci. USA 95: 7904-7908.
42. Raynaud, C., Sozzani, R., Glab, N., Domenichini, S., Perennes, C., Cella, R., Kondorosi, E., and Bergounioux, C. (2006). Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J. 47: 395-407.
43. Ruijter, J.M., Ramakers, C., Hoogaars, W.M., Karlen, Y., Bakker, O., van den Hoff, M.J., and Moorman, A.F. (2009). Amplification efficiency: Linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37: e45.
44. Sakamoto, A., Lan, V.T., Hase, Y., Shikazono, N., Matsunaga, T., and Tanaka, A. (2003). Disruption of the AtREV3 gene causes hypersensitivity to ultraviolet B light and gamma-rays in Arabidopsis: Implication of the presence of a translesion synthesis mechanism in plants. Plant Cell 15: 2042-2057.
45. Santiago, M.J., Alejandre-Durán, E., and Ruiz-Rubio, M. (2006). Analysis of UV-induced mutation spectra in Escherichia coli by DNA polymerase eta from Arabidopsis thaliana. Mutat. Res. 601: 51-60.
46. Shultz, R.W., Tatineni, V.M., Hanley-Bowdoin, L., and Thompson, W.F. (2007). Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiol. 144: 1697-1714.
47. Singhal, R.K., and Wilson, S.H. (1993). Short gap-filling synthesis by DNA polymerase beta is processive. J. Biol. Chem. 268: 15906-15911.
48. Strzalka, W., Oyama, T., Tori, K., and Morikawa, K. (2009). Crystal structures of the Arabidopsis thaliana proliferating cell nuclear antigen 1 and 2 proteins complexed with the human p21 C-terminal segment. Protein Sci. 18: 1072-1080.
49. Takahashi, S., Sakamoto, A., Sato, S., Kato, T., Tabata, S., and Tanaka, A. (2005). Roles of Arabidopsis AtREV1 and AtREV7 in translesion synthesis. Plant Physiol. 138: 870-881.
50. Timmermans, M.C., Maliga, P., Vieira, J., and Messing, J. (1990). The pFF plasmids: Cassettes utilising CaMV sequences for expression of foreign genes in plants. J. Biotechnol. 14: 333-344.
51. Uchiyama, Y., Kimura, S., Yamamoto, T., Ishibashi, T., and Sakaguchi, K. (2004). Plant DNA polymerase lambda, a DNA repair enzyme that functions in plant meristematic and meiotic tissues. Eur. J. Biochem. 271: 2799-2807.
52. Umar, A., Buermeyer, A.B., Simon, J.A., Thomas, D.C., Clark, A.B., Liskay, R.M., and Kunkel, T.A. (1996). Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell 87: 65-73.
53. van der Kemp, P.A., de Padula, M., Burguiere-Slezak, G., Ulrich, H.D., and Boiteux, S. (2009). PCNA monoubiquitylation and DNA polymerase eta ubiquitin-binding domain are required to prevent 8-oxoguanine-induced mutagenesis in Saccharomyces cerevisiae. Nucleic Acids Res. 37: 2549-2559.
54. Walter, M., Chaban, C., Schütze, K., Batistic, O., Weckermann, K., Näke, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., Harter, K., and Kudla, J. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
55. Warbrick, E. (1998). PCNA binding through a conserved motif. Bioessays 20: 195-199.
56. Wimmer, U., Ferrari, E., Hunziker, P., and Hübscher, U. (2008). Control of DNA polymerase lambda stability by phosphorylation and ubiquitination during the cell cycle. EMBO Rep. 9: 1027-1033.
57. Zou, J., Zhang, S., Zhang, W., Li, G., Chen, Z., Zhai, W., Zhao, X., Pan, X., Xie, Q., and Zhu, L. (2006). The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J. 48: 687-698.