Perturbed gap-filling synthesis in nucleotide excision repair causes histone H2AX phosphorylation in human quiescent cells

Journal of Cell Science

Volumn 120, Issue 6, 2007, Pages 1104-1112

  Matsumoto, Megumi ^a   Yaginuma, Kie ^a   Igarashi, Ai ^a   Imura, Mayumi ^a   Hasegawa, Mizuho ^a   Iwabuchi, Kuniyoshi ^b   Date, Takayasu ^b   Mori, Toshio ^c   Ishizaki, Kanji ^d   Yamashita, Katsumi ^a   Inobe, Manabu ^a   Matsunaga, Tsukasa ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

^c NARA MEDICAL UNIVERSITY   (Japan)

^d AICHI CANCER CENTER HOSPITAL   (Japan)

Author keywords

ATM and Rad3 related (ATR); Histone H2AX; Nucleotide excision repair

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; CYCLINE; CYTARABINE; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE EPSILON; DOUBLE STRANDED DNA; HISTONE H2AX; HYDROXYUREA; REPLICATION PROTEIN A; SERINE; SINGLE STRANDED DNA;

ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL DAMAGE; CELL GROWTH; CELL NUCLEUS; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; EXCISION REPAIR; FIBROBLAST; GROWTH INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; CYTARABINE; DNA DAMAGE; DNA POLYMERASE II; DNA POLYMERASE III; DNA REPAIR; DNA, SINGLE-STRANDED; FIBROBLASTS; HISTONES; HUMANS; PHOSPHORYLATION; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; REPLICATION PROTEIN A; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS;

ATAXIA TELANGIECTASIA;

EID: 34247354227     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03391     Document Type: Article

References (43)

1. Aboussekhra, A., Biggerstaff, M., Shivji, M. K. K., Vilpo, J. A., Moncollin, V., Podust, V. N., Protic, M., Hubscher, U., Egly, J.-M. and Wood, R. D. (1995). Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80, 859-868.
2. Bomgarden, R. D., Lupardus, P. J., Soni, D. V., Yee, M.-C., Ford, J. M. and Cimprich, K. A. (2006). Opposing effects of the UV lesion repair protein XPA and UV bypass polymerase h on ATR checkpoint signaling. EMBO J. 25, 2605-2614.
3. Chini, C. C. S. and Chen, J. (2003). Human Claspin is required for replication checkpoint control. J. Biol. Chem. 278, 30057-30062.
4. Coverley, D., Kenny, M. K., Munn, M., Rupp, W. D., Lane, D. P. and Wood, R. D. (1991). Requirement for the replication protein SSB in human DNA excision repair. Nature 349, 538-541.
5. Fernandez-Capetillo, O., Lee, A., Nussenzweig, M. and Nussenzweig, A. (2004). H2AX: the histone guardian of the genome. DNA Repair 3, 959-967.
6. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A. and Ellenberger, T. (2006). DNA Repair and Mutagenesis. Washington, DC: ASM Press.
7. Garinis, G. A., Mitchell, J. R., Moorhouse, M. J., Hanada, K., de Waard, H., Vandeputte, D., Jans, J., Brand, K., Smid, M., van der Spek, P. J. et al. (2005). Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UV-induced DNA breaks. EMBO J. 24, 3952-3962.
8. Giannattasio, M., Lazzaro, F., Longhese, M. P., Plevani, P. and Muzi-Falconi, M. (2004). Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint. EMBO J. 23, 429-438.
9. Goldberg, M., Stucki, M., Falck, J., D'Amours, D., Rahman, D., Pappin, D., Bartek, J. and Jackson, S. P. (2003). MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421, 952-956.
10. Iwabuchi, K., Basu, B. P., Kysela, B., Kurihara, T., Shibata, M., Guan, D., Cao, Y., Hamada, T., Imamura, K., Jeggo, P. A. et al. (2003). Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J. Biol. Chem. 278, 36487-36495.
11. Jiang, G. and Sancar, A. (2006). Recruitment of DNA damage checkpoint proteins to damage in transcribed and nontranscribed sequences. Mol. Cell. Biol. 26, 39-49.
12. Katsumi, S., Kobayashi, N., Imoto, K., Nakagawa, A., Yamashina, Y., Muramatsu, T., Shirai, T., Miyagawa, S., Sugiura, S., Hanaoka, F. et al. (2001). In situ visualization of ultraviolet-light-induced DNA damage repair in locally irradiated human fibroblasts. J. Invest. Dermatol. 117, 1156-1161.
13. Ljungman, M. and Zhang, F. (1996). Blockage of RNA polymerase as a possible trigger for u.v. light-induced apoptosis. Oncogene 13, 823-831.
14. Lou, Z., Minter-Dykhouse, K., Wu, X. and Chen, J. (2003). MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421, 957-961.
15. Marti, T. M., Hefner, E., Feeney, L., Natale, V. and Cleaver, J. E. (2006). H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 103, 9891-9896.
16. Mori, T., Nakane, M., Hattori, T., Matsunaga, T., Ihara, M. and Nikaido, O. (1991). Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4)photoproduct from the same mouse immunized with ultraviolet-irradiated DNA. Photochem. Photobiol. 54, 225-232.
17. Morris, G. F. and Mathews, M. B. (1989). Regulation of proliferating cell nuclear antigen during the cell cycle. J. Biol. Chem. 264, 13856-13864.
18. Mu, D., Park, C.-H., Matsunaga, T., Hsu, D. S., Reardon, J. T. and Sancar, A. (1995). Reconstitution of human DNA repair excision nuclease in a highly defined system. J. Biol. Chem. 270, 2415-2418.
19. Nakamura, H., Fukami, H., Hayashi, Y., Kiyono, T., Nakatsugawa, S., Hamaguchi, M. and Ishizaki, K. (2002). Establishment of immortal normal and ataxia telangiectasia fibroblast cell lines by introduction of the hTERT gene. J. Radiat. Res. 43, 167-174.
20. Nichols, A. F. and Sancar, A. (1992). Purification of PCNA as a nucleotide excision repair protein. Nucleic Acids Res. 20, 2441-2446.
21. O'Driscoll, M., Ruiz-Perez, V. L., Woods, C. G., Jeggo, P. A. and Goodship, J. A. (2003). A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 33, 497-501.
22. Paull, T. T., Rogakou, E. P., Yamazaki, V., Kirchgessner, C. U., Gellert, M. and Bonner, W. M. (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10, 886-895.
23. Rappold, I., Iwabuchi, K., Date, T. and Chen, J. (2001). Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153, 613-620.
24. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. and Bonner, W. M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868.
25. Schultz, L. B., Chehab, N. H., Malikzay, A. and Halazonetis, T. D. (2000). p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151, 1381-1390.
26. Shivji, M. K. K., Kenny, M. K. and Wood, R. D. (1992). Proliferating cell nuclear antigen is required for DNA excision repair. Cell 69, 367-374.
27. Shivji, M. K. K., Podust, V. N., Hubscher, U. and Wood, R. D. (1995). Nucleotide excision repair DNA synthesis by DNA polymerase e in the presence of PCNA, RFC, and RPA. Biochemistry 34, 5011-5017.
28. Stewart, G. S., Wang, B., Bignell, C. R., Taylor, A. M. and Elledge, S. J. (2003). MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961-966.
29. Stiff, T., O'Driscoll, M., Rief, N., Iwabuchi, K., Lobrich, M. and Jeggo, P. A. (2004). ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64, 2390-2396.
30. Stiff, T., Reis, C., Alderton, G. K., Woodbine, L., O'Driscoll, M. and Jeggo, P. A. (2005). Nbs1 is required for ATR-dependent phosphorylation events. EMBO J. 24, 199-208.
31. Takebe, H., Miki, Y., Kozuka, T., Furuyama, J., Tanaka, K., Sasaki, M. S., Fujiwara, Y. and Akiba, H. (1977). DNA repair characteristics and skin cancers of xeroderma pigmentosum patients in Japan. Cancer Res. 37, 490-495.
32. Tuusa, J., Uitto, L. and Syvaoja, J. E. (1995). Human DNA polymerase e is expressed during cell proliferation in a manner characteristic of replicative DNA polymerases. Nucleic Acids Res. 23, 2178-2183.
33. Volker, M., Mone, M. J., Karmakar, P., van Hoffen, A., Schul, W., Vermeulen, W., Hoeijmakers, J. H., van Driel, R., van Zeeland, A. A. and Mullenders, L. H. (2001). Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8, 213-224.
34. Wang, Y., Kobayashi, K., Chang, H. R., Zeng, Y., Ishizaki, K., Dai, H., Kuan, Y. Z. and Ikenaga, M. (1991). Assignment of a Chinese xeroderma pigmentosum patient from Taiwan to complementation group C. J. Radiat. Res. 32, 181-190.
35. Ward, I. M. and Chen, J. (2001). Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276, 47759-47762.
36. Ward, I. M., Minn, K. and Chen, J. (2004). UV-induced ataxia-telangiectasia-mutated and Rad3-related (ATR) activation requires replication stress. J. Biol. Chem. 279, 9677-9680.
37. West, M. H. P. and Bonner, W. M. (1980). Histone 2A, a heteromorphous family of eight protein species. Biochemistry 19, 3238-3245.
38. Wood, R. D. and Shivji, M. K. K. (1997). Which DNA polymerases are used for DNA-repair in eukaryotes? Carcinogenesis 18, 605-610.
39. Yamaizumi, M. and Sugano, T. (1994). U.v.-induced nuclear accumulation of p53 is evoked through DNA damage of actively transcribed genes independent of the cell cycle. Oncogene 9, 2775-2784.
40. Yang, C.-L., Chang, L.-S., Zhang, P., Hao, H., Zhu, L., Toomey, N. L. and Lee, M. Y. (1992). Molecular cloning of the cDNA for the catalytic subunit of human DNA polymerase d. Nucleic Acids Res. 20, 735-745.
41. Zeng, X. R., Jiang, Y., Zhang, S. J., Hao, H. and Lee, M. Y. (1994a). DNA polymerase d is involved in the cellular response to UV damage in human cells. J. Biol. Chem. 269, 13748-13751.
42. Zeng, X. R., Hao, H., Jiang, Y. and Lee, M. Y. (1994b). Regulation of human DNA polymerase d during the cell cycle. J. Biol. Chem. 269, 24027-24033.
43. Zou, L. and Elledge, S. J. (2003). Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548.