Tolerance of dividing cells to replication stress in UVB-irradiated Arabidopsis roots: Requirements for DNA translesion polymerases η and ζ

DNA Repair

Volumn 6, Issue 9, 2007, Pages 1341-1358

  Curtis, Marc J ^a   Hays, John B ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis; DNA damage tolerance; Root meristem; Stem cells; Translesion polymerase; Ultraviolet radiation

Indexed keywords

DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE ETA; PYRIMIDINE DERIVATIVE;

ARABIDOPSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL GROWTH; CELL PROLIFERATION; CELL TYPE; DNA DAMAGE; LETHALITY; MERISTEM; MICROSCOPY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT ROOT; PRIORITY JOURNAL; ROOT GROWTH; STEM CELL; STRESS; TISSUE GROWTH; ULTRAVIOLET B RADIATION; YEAST;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIVISION; DNA DAMAGE; DNA REPLICATION; DNA, PLANT; DNA-DIRECTED DNA POLYMERASE; HUMANS; MOLECULAR SEQUENCE DATA; PLANT ROOTS; PYRIMIDINE DIMERS; SEQUENCE HOMOLOGY, AMINO ACID; ULTRAVIOLET RAYS; XENOPUS LAEVIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MUS;

EID: 34547743317     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.03.004     Document Type: Article

References (79)

1. Moore K.A., and Lemischka I.R. Stem cells and their niches. Science 311 (2006) 1880-1885
2. Morasso M.I., and Tomic-Canic M. Epidermal stem cells: the cradle of epidermal determination, differentiation and wound healing. Biol. Cell 97 (2005) 173-183
3. Scadden D.T. The stem-cell niche as an entity of action. Nature 441 (2006) 1075-1080
4. Singh M.B., and Bhalla P.L. Plant stem cells carve their own niche. Trends Plant Sci. 11 (2006) 241-245
5. Branzei D., and Foiani M. The DNA damage response during DNA replication. Curr. Opin. Cell Biol. 17 (2005) 568-575
6. Heller R.C., and Marians K.J. Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439 (2006) 557-562
7. Lopes M., Foiani M., and Sogo J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21 (2006) 15-27
8. Hochegger H., Sonoda E., and Takeda S. Post-replication repair in DT40 cells: translesion polymerases versus recombinases. Bioessays 26 (2004) 151-158
9. Li Z., Xiao W., McCormick J., and Maher V.M. Identification of a protein essential for a major pathway used by human cells to avoid UV-induced DNA damage. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 4459-4464
10. Torres-Ramos C.A., Prakash S., and Prakash L. Requirement of RAD5 and MMS2 for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 22 (2002) 2419-2426
11. Zhang H., and Lawrence C.W. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 15954-15959
12. Lehmann A.R. Replication of damaged DNA in mammalian cells: new solutions to an old problem. Mut. Res. 509 (2002) 23-34
13. Prakash S., Johnson R.E., and Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74 (2005) 317-353
14. Cha R.S., and Kleckner N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297 (2002) 602-606
15. Lambert S., and Carr A.M. Checkpoint responses to replication fork barriers. Biochimie 87 (2005) 591-602
16. Niida H., and Nakanishi M. DNA damage checkpoints in mammals. Mutagenesis 21 (2005) 3-9
17. Shimada K., Pasero P., and Gasser S.M. ORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phase. Genes Dev. 16 (2002) 3236-3252
18. Zuo L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548
19. Lehmann A.R., Kirk-Bell S., Arlett C.F., Paterson M.C., Lohman P.H.M., De Weerd-Kastelein E.A., and Bootsma D. Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. Proc. Natl. Acad. Sci. U.S.A. 72 (1975) 219-223
20. Johnson R.E., Knodratick C.M., Prakash S., and Prakash L. hRAD30 mutations in the variant form of Xeroderma pigmentosum. Science 285 (1999) 263-265
21. Masutani C., Araki M., Yamada A., Kusumoto R., Nogimori T., Maekawa T., Iwai S., and Hanaoka F. Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J. 18 (1999) 3491-3501
22. Masutani C., Kusumoto R., Yamada A., Dohmae N., Yokoi M., Yuasa M., Araki M., Iwai S., Takio K., and Hanaoka F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399 (1999) 700-704
23. Cordeiro-Stone M., Frank A., Bryant M., Oguejiofor I., Hatch S.B., McDaniel L.D., and Kaufmann W.K. DNA damage responses protect xeroderma pigmentosum variant from UVC-induced clastogenesis. Carcinogenesis 23 (2002) 959-965
24. Cordonnier A.M., and Fuchs R.P.P. Replication of damaged DNA: molecular defect in Xeroderma pigmentosum variant cells. Mut. Res. 435 (1999) 111-119
25. Maher V.M., Ouellette L.M., Curren R.D., and McCormick J.J. Frequency of ultraviolet light-induced mutations is higher in xeroderma pigmentosum variant cells than in normal cells. Nature 261 (1976) 593-595
26. McDonald J.P., Levine A.S., and Woodgate R. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics 147 (1997) 1557-1568
27. Roush A.A., Suarez M., Friedberg E.C., Radman M., and Siede W. Deletion of the Saccharomyces cerevisiae gene RAD30 encoding an Escherichia coli DinB homolog confers UV radiation sensitivity and altered mutability. Mol. Gen. Genet. 257 (1998) 686-692
28. Lawrence C.W., and Christensen R. UV mutagenesis in radiation-sensitive strains of yeast. Genetics 82 (1976) 207-232
29. Lemontt J.F. Mutations of yeast defective in mutation induced by ultraviolet light. Genetics 68 (1971) 21-33
30. Quah S.K., von Borstel R.C., and Hastings P.J. The origin of spontaneous mutation in Saccharomyces cerevisiae. Genetics 96 (1980) 819-839
31. Prakash L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3, and rad52 mutations. Mol. Gen. Genet. 184 (1981) 471-478
32. Sonoda E., Okada T., Zhao G.Y., Tateishi S., Araki K., Yamaizumi M., Yagi T., Verkaik N.S., van Gent D.C., Takata M., and Takeda S. Multiple roles of Rev3, the catalytic subunit of polζ in maintaining genome stability in vertebrates. EMBO J. 22 (2003) 3188-3197
33. Van Sloun P.P.H., Varlet I., Sonneveld E., Boei J.J.W.A., Romeijn R.J., Eeken J.C.J., and De Wind N. Involvement of mouse Rev3 in tolerance of endogenous and exogenous DNA damage. Mol. Cell. Biol. 22 (2002) 2159-2169
34. Yu S.-L., Johnson R.E., Prakash S., and Prakash L. Requirement of DNA polymerase η for error-free bypass of UV-induced CC and TC photoproducts. Mol. Cell. Biol. 21 (2001) 185-188
35. Gibbs P.E.M., McDonald J., Woodgate R., and Lawrence C.W. The relative roles in vivo of Saccharomyces cerevisiae Pol η, Pol ζ, Rev1 protein and Pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer. Genetics 169 (2005) 575-582
36. Cadet J., Sage E., and Douki T. Ultraviolet radiation-mediated damage to cellular DNA. Mut. Res. 571 (2005) 3-17
37. Perdiz D., Grof P., Mezzina M., Nikaido O., Moustacchi E., and Sage E. Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. J. Biol. Chem. 275 (2000) 26732-26742
38. Johnson R.E., Prakash S., and Prakash L. Efficient bypass of thymine-thymine dimmer by yeast DNA polymerase, Polη. Science 283 (1999) 1001-1004
39. Johnson R.E., Washington M.T., Prakash S., and Prakash L. Fidelity of human DNA polymerase η. J. Biol. Chem. 275 (2000) 7447-7450
40. Johnson R.E., Haracska L., Prakash S., and Prakash L. Role of DNA polymerase η in the bypass of a (6-4) TT photoproduct. Mol. Cell. Biol. 21 (2001) 3558-3563
41. Prakash S., and Prakash L. Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev. 16 (2002) 1872-1883
42. Hays J.B. Arabidopsis thaliana, a versatile model system for study of eukaryotic genome-maintenance functions. DNA Rep. 1 (2002) 579-600
43. Britt A.B. Repair of DNA damage induced by solar UV. Photosynth. Res. 81 (2004) 105-112
44. Jiang C.Z., Yee J., Mitchell D.L., and Britt A.B. Photorepair mutants of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7441-7445
45. Pang Q., and Hays J.B. UV-B-inducible and temperature-sensitive photoreactivation of cyclobutane pyrmidine dimers in Arabidopsis thaliana. Plant Physiol. 95 (1991) 536-543
46. Sakamoto A., Lan V.T.T., Hase Y., Shikazono N., Matsunaga T., and Tanaka A. Disruption of the AtREV3 gene causes hypersensitivity to ultraviolet B light and γ-rays in Arabidopsis: implication of the presence of a translesion synthesis mechanism in plants. Plant Cell 15 (2003) 2042-2057
47. Takahashi S., Sakamoto A., Sato S., Kato T., Tabata S., and Tanaka A. Roles of Arabidopsis AtREV1 and AtREV7 in translesion synthesis. Plant Physiol. 138 (2005) 870-881
48. Santiago M.J., Alejandre-Duran E., and Ruiz-Rubio M. Analysis of UV-induced mutation spectra in Escherichia coli by DNA polymerase η from Arabidopsis thaliana. Mut. Res. 601 (2006) 51-60
49. Hefner E., Huefner N., and Britt A.B. Tissue-specific regulation of cell-cycle responses to DNA damage in Arabidoposis seedlings. DNA Rep. 5 (2006) 102-110
50. Beemster G.T.S., and Baskin T.I. Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol. 116 (1998) 1515-1526
51. Blilou I., Xu J., Wildwater M., Willemsen V., Paponov I., Friml J., Heidstra R., Aida M., Palme K., and Scheres B. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433 (2005) 39-44
52. Kramer E.M., and Bennett M.J. Auxin transport: a field in flux. Trends Plant Sci. 11 (2006) 382-386
53. Scheres, B., Benfey, P., Dolan, L. Root development. In: Somerville, C.R., Meyerowitz, E.M. (Eds.), The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD (2002), doi:10.1199/tab.0009, www.aspb.org/publications/arabidopsis/.
54. Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R., et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 (2003) 653-657
55. Edwards K., Johnstone C., and Thompson C. A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19 (1991) 1349-1350
56. Draper C.K., and Hays J.B. Replication of chloroplast, mitochondrial and nuclear DNA during growth of unirradiated and UVB-irradiated Arabidopsis leaves. Plant J. 23 (2000) 255-265
57. Trincao J., Johnson R.E., Escalante C.R., Prakash S., Prakash L., and Aggarwal A.K. Structure of the catalytic core of S. cerevisiae DNA polymerase η: implications for translesion DNA synthesis. Mol. Cell 8 (2001) 417-426
58. Fleck O., and Schar P. Translesion DNA synthesis: little fingers teach tolerance. Curr. Biol. 14 (2004) R389-R391
59. Bienko M., Green C.M., Crosetto N., Rudolf F., Zapart G., Coull B., Kannouche P., Wider G., Peter M., Lehmann A.R., Hofmann K., and Dikic I. Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310 (2005) 1821-1824
60. Plosky B.S., Vidal A.E., Fernández de Henestrosa A.R., McLenigan M.P., McDonald J.P., Mead S., and Woodgate R. Controlling the subcellular localization of DNA polymerases ι and η via interactions with ubiquitin. EMBO J. (2006) 2847-2855
61. Jónsson Z.O., Hindges R., and Hübscher U. Regulation of DNA replication and repair proteins through interaction with the front side of proliferating cell nuclear antigen. EMBO J. 17 (1998) 2412-2425
62. Maga G., and Hübscher U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell Sci. 116 (2003) 3051-3060
63. Kannouche P., Broughton B.C., Volker M., Hanaoka F., Mullenders L.H.F., and Lehmann A.R. Domain structure, localization, and function of DNA polymerase η, defective in xeroderma pigmentosum variant cells. Genes Dev. 15 (2001) 158-172
64. van den Berg C., Willemsen V., Hendriks G., Weisbeek P., and Scheres B. Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390 (1997) 287-289
65. Doerner P. Root development: quiescent center not so mute after all. Curr. Biol. 8 (1998) R42-R44
66. Mouret S., Baudouin C., Charveron M., Favier A., Cadet J., and Douki T. Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13765-13770
67. Bernerd F., and Asselineau D. Successive alteration and recovery of epidermal differentiation and morphogenesis after specific UVB-damages in skin reconstructed in vitro. Dev. Biol. 183 (1997) 123-138
68. Unrau P., Wheatcroft R., Cox B., and Olive T. The formation of pyrimidine dimers in the DNA of fungi and bacteria. Biochim. Biophys. Acta 312 (1973) 626-632
69. Zander L., and Bemark M. Immortalized mouse cell lines that lack a functional Rev3 gene are hypersensitive to UV irradiation and cisplatin treatment. DNA Rep. 3 (2004) 743-752
70. Shechter D., Costanzo V., and Gautier J. Regulation of DNA replication by ATR: signaling in response to DNA intermediates. DNA Rep. 3 (2004) 901-908
71. Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends Biochem. Sci. 31 (2006) 402-410
72. Culligan K., Tissier A., and Britt A. ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16 (2004) 1091-1104
73. Garcia V., Bruchet H., Camescasse D., Granier F., Bouchez D., and Tissier A. AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15 (2003) 119-132
74. Johnson R.E., Washington M.T., Haracska L., Prakash S., and Prakash L. Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature 406 (2000) 1015-1019
75. Acharya N., Johnson R.E., Prakash S., and Prakash L. Complex formation with Rev1 enhances the proficiency of Saccharomyces cerevisiae DNA polymerase ζ for mismatch extension and for extension opposite from DNA lesions. Mol. Cell. Biol. 26 (2006) 9555-9563
76. Ponce G., Barlow P.W., Feldman L.J., and Cassab G.I. Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant Cell Environ. 28 (2005) 719-732
77. Jans J., Garinis G.A., Schul W., van Oudenaren A., Moorhouse M., Smid M., Sert Y.-G., van der Velde A., Rijksen Y., de Gruijl F.R., et al. Differential role of basal keratinocytes in UV-induced immunosuppression and skin cancer. Mol. Cell. Biol. 26 (2006) 8515-8526
78. Bach S.P., Renehan A.G., and Potten C.S. Stem cells: the intestinal stem cell as a paradigm. Carcinogenesis 21 (2000) 469-476
79. Potten C.S. The significance of spontaneous and induced apoptosis in the gastrointestinal tract of mice. Cancer Metastasis Rev. 11 (1992) 179-195