This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow An erratum has been published
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Okano, S.
Right arrow Articles by Yasui, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Okano, S.
Right arrow Articles by Yasui, A.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, June 2003, p. 3974-3981, Vol. 23, No. 11
0270-7306/03/$08.00+0     DOI: 10.1128/MCB.23.11.3974-3981.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Spatial and Temporal Cellular Responses to Single-Strand Breaks in Human Cells

Satoshi Okano,1 Li Lan,1 Keith W. Caldecott,2 Toshio Mori,3 and Akira Yasui1*

Department of Molecular Genetics, Institute of Development, Aging and Cancer, Tohoku University, 980-8575 Sendai,1 Radioisotope Research Center, Nara Medical University, 634-8521 Nara, Japan,3 Genome Damage and Stability Centre, University of Sussex, Falmer, Brighton BN1 9RQ, United Kingdom2

Received 23 December 2002/ Returned for modification 10 February 2003/ Accepted 13 March 2003

DNA single-strand breaks (SSB) are one of the most frequent DNA lesions produced by reactive oxygen species and during DNA metabolism, but the analysis of cellular responses to SSB remains difficult due to the lack of an experimental method to produce SSB alone in cells. By using human cells expressing a foreign UV damage endonuclease (UVDE) and irradiating the cells with UV through tiny pores in membrane filters, we created SSB in restricted areas in the nucleus by the immediate action of UVDE on UV-induced DNA lesions. Cellular responses to the SSB were characterized by using antibodies and fluorescence microscopy. Upon UV irradiation, poly(ADP-ribose) synthesis occurred immediately in the irradiated area. Simultaneously, but dependent on poly(ADP-ribosyl)ation, XRCC1 was translocated from throughout the nucleus, including nucleoli, to the SSB. The BRCT1 domain of XRCC1 protein was indispensable for its poly(ADP-ribose)-dependent recruitment to the SSB. Proliferating cell nuclear antigen and the p150 subunit of chromatin assembly factor 1 also accumulated at the SSB in a detergent-resistant form, which was significantly reduced by inhibition of poly(ADP-ribose) synthesis. Our results show the importance of poly(ADP-ribosyl)ation in sequential cellular responses to SSB.

* Corresponding author. Mailing address: Department of Molecular Genetics, Institute of Development, Aging and Cancer, Tohoku University, 980-8575 Sendai, Japan. Phone: 81 22 717 8465. Fax: 81 22 717 8470. E-mail: ayasui{at}idac.tohoku.ac.jp.

Molecular and Cellular Biology, June 2003, p. 3974-3981, Vol. 23, No. 11
0022-538X/03/$08.00+0     DOI: 10.1128/MCB.23.11.3974-3981.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Trautlein, D., Deibler, M., Leitenstorfer, A., Ferrando-May, E. (2009). Specific local induction of DNA strand breaks by infrared multi-photon absorption. Nucleic Acids Res 0: gkp932v1-gkp932 [Abstract] [Full Text]  
  • Ame, J.-C., Fouquerel, E., Gauthier, L. R., Biard, D., Boussin, F. D., Dantzer, F., de Murcia, G., Schreiber, V. (2009). Radiation-induced mitotic catastrophe in PARG-deficient cells. J. Cell Sci. 122: 1990-2002 [Abstract] [Full Text]  
  • Levy, N., Oehlmann, M., Delalande, F., Nasheuer, H. P., Van Dorsselaer, A., Schreiber, V., de Murcia, G., Menissier-de Murcia, J., Maiorano, D., Bresson, A. (2009). XRCC1 interacts with the p58 subunit of DNA Pol {alpha}-primase and may coordinate DNA repair and replication during S phase. Nucleic Acids Res 37: 3177-3188 [Abstract] [Full Text]  
  • Kong, X., Mohanty, S. K., Stephens, J., Heale, J. T., Gomez-Godinez, V., Shi, L. Z., Kim, J.-S., Yokomori, K., Berns, M. W. (2009). Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells. Nucleic Acids Res 37: e68-e68 [Abstract] [Full Text]  
  • Wang, S., Gong, Z., Chen, R., Liu, Y., Li, A., Li, G., Zhou, J. (2009). JWA regulates XRCC1 and functions as a novel base excision repair protein in oxidative-stress-induced DNA single-strand breaks. Nucleic Acids Res 37: 1936-1950 [Abstract] [Full Text]  
  • Hong, Z., Jiang, J., Hashiguchi, K., Hoshi, M., Lan, L., Yasui, A. (2008). Recruitment of mismatch repair proteins to the site of DNA damage in human cells. J. Cell Sci. 121: 3146-3154 [Abstract] [Full Text]  
  • Rulten, S. L., Cortes-Ledesma, F., Guo, L., Iles, N. J., Caldecott, K. W. (2008). APLF (C2orf13) Is a Novel Component of Poly(ADP-Ribose) Signaling in Mammalian Cells. Mol. Cell. Biol. 28: 4620-4628 [Abstract] [Full Text]  
  • Fahrer, J., Kranaster, R., Altmeyer, M., Marx, A., Burkle, A. (2007). Quantitative analysis of the binding affinity of poly(ADP-ribose) to specific binding proteins as a function of chain length. Nucleic Acids Res 35: e143-e143 [Abstract] [Full Text]  
  • Mortusewicz, O., Ame, J.-C., Schreiber, V., Leonhardt, H. (2007). Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res 35: 7665-7675 [Abstract] [Full Text]  
  • Albert, J. M., Cao, C., Kim, K. W., Willey, C. D., Geng, L., Xiao, D., Wang, H., Sandler, A., Johnson, D. H., Colevas, A. D., Low, J., Rothenberg, M. L., Lu, B. (2007). Inhibition of Poly(ADP-Ribose) Polymerase Enhances Cell Death and Improves Tumor Growth Delay in Irradiated Lung Cancer Models. Clin. Cancer Res. 13: 3033-3042 [Abstract] [Full Text]  
  • Hashiguchi, K., Matsumoto, Y., Yasui, A. (2007). Recruitment of DNA repair synthesis machinery to sites of DNA damage/repair in living human cells. Nucleic Acids Res 35: 2913-2923 [Abstract] [Full Text]  
  • Parlanti, E., Locatelli, G., Maga, G., Dogliotti, E. (2007). Human base excision repair complex is physically associated to DNA replication and cell cycle regulatory proteins. Nucleic Acids Res 35: 1569-1577 [Abstract] [Full Text]  
  • Berger, F., Lau, C., Ziegler, M. (2007). Regulation of poly(ADP-ribose) polymerase 1 activity by the phosphorylation state of the nuclear NAD biosynthetic enzyme NMN adenylyl transferase 1. Proc. Natl. Acad. Sci. USA 104: 3765-3770 [Abstract] [Full Text]  
  • Campalans, A., Amouroux, R., Bravard, A., Epe, B., Radicella, J. P. (2007). UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. J. Cell Sci. 120: 23-32 [Abstract] [Full Text]  
  • Wang, M., Wu, W., Wu, W., Rosidi, B., Zhang, L., Wang, H., Iliakis, G. (2006). PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 34: 6170-6182 [Abstract] [Full Text]  
  • Keil, C., Grobe, T., Li Oei, S. (2006). MNNG-induced Cell Death Is Controlled by Interactions between PARP-1, Poly(ADP-ribose) Glycohydrolase, and XRCC1. J. Biol. Chem. 281: 34394-34405 [Abstract] [Full Text]  
  • Nakajima, S., Lan, L., Kanno, S.-i., Usami, N., Kobayashi, K., Mori, M., Shiomi, T., Yasui, A. (2006). Replication-dependent and -independent Responses of RAD18 to DNA Damage in Human Cells. J. Biol. Chem. 281: 34687-34695 [Abstract] [Full Text]  
  • van der Straaten, T., Kweekel, D., Tiller, M., Bogaartz, J., Guchelaar, H.-J. (2006). Multiplex Pyrosequencing of Two Polymorphisms in DNA Repair Gene XRCC1. J. Mol. Diagn. 8: 444-448 [Abstract] [Full Text]  
  • Semighini, C. P., Savoldi, M., Goldman, G. H., Harris, S. D. (2006). Functional Characterization of the Putative Aspergillus nidulans Poly(ADP-Ribose) Polymerase Homolog PrpA. Genetics 173: 87-98 [Abstract] [Full Text]  
  • Nabatiyan, A., Szuts, D., Krude, T. (2006). Induction of CAF-1 Expression in Response to DNA Strand Breaks in Quiescent Human Cells.. Mol. Cell. Biol. 26: 1839-1849 [Abstract] [Full Text]  
  • Noel, G., Godon, C., Fernet, M., Giocanti, N., Megnin-Chanet, F., Favaudon, V. (2006). Radiosensitization by the poly(ADP-ribose) polymerase inhibitor 4-amino-1,8-naphthalimide is specific of the S phase of the cell cycle and involves arrest of DNA synthesis.. Molecular Cancer Therapeutics 5: 564-574 [Abstract] [Full Text]  
  • Hirano, M., Furiya, Y., Asai, H., Yasui, A., Ueno, S. (2006). ALADINI482S causes selective failure of nuclear protein import and hypersensitivity to oxidative stress in triple A syndrome. Proc. Natl. Acad. Sci. USA 103: 2298-2303 [Abstract] [Full Text]  
  • Levy, N., Martz, A., Bresson, A., Spenlehauer, C., de Murcia, G., Menissier-de Murcia, J. (2006). XRCC1 is phosphorylated by DNA-dependent protein kinase in response to DNA damage. Nucleic Acids Res 34: 32-41 [Abstract] [Full Text]  
  • Lan, L., Nakajima, S., Komatsu, K., Nussenzweig, A., Shimamoto, A., Oshima, J., Yasui, A. (2005). Accumulation of Werner protein at DNA double-strand breaks in human cells. J. Cell Sci. 118: 4153-4162 [Abstract] [Full Text]  
  • Thorslund, T., von Kobbe, C., Harrigan, J. A., Indig, F. E., Christiansen, M., Stevnsner, T., Bohr, V. A. (2005). Cooperation of the Cockayne Syndrome Group B Protein and Poly(ADP-Ribose) Polymerase 1 in the Response to Oxidative Stress. Mol. Cell. Biol. 25: 7625-7636 [Abstract] [Full Text]  
  • Kim, M. Y., Zhang, T., Kraus, W. L. (2005). Poly(ADP-ribosyl)ation by PARP-1: `PAR-laying' NAD+ into a nuclear signal. Genes Dev. 19: 1951-1967 [Abstract] [Full Text]  
  • Liu, X., Guo, Y., Li, Y., Jiang, Y., Chubb, S., Azuma, A., Huang, P., Matsuda, A., Hittelman, W., Plunkett, W. (2005). Molecular Basis for G2 Arrest Induced by 2'-C-Cyano-2'-Deoxy-1-{beta}-D-Arabino-Pentofuranosylcytosine and Consequences of Checkpoint Abrogation. Cancer Res. 65: 6874-6881 [Abstract] [Full Text]  
  • Mortusewicz, O., Schermelleh, L., Walter, J., Cardoso, M. C., Leonhardt, H. (2005). Recruitment of DNA methyltransferase I to DNA repair sites. Proc. Natl. Acad. Sci. USA 102: 8905-8909 [Abstract] [Full Text]  
  • Brem, R., Hall, J. (2005). XRCC1 is required for DNA single-strand break repair in human cells. Nucleic Acids Res 33: 2512-2520 [Abstract] [Full Text]  
  • Luna, L., Rolseth, V., Hildrestrand, G. A., Otterlei, M., Dantzer, F., Bjoras, M., Seeberg, E. (2005). Dynamic relocalization of hOGG1 during the cell cycle is disrupted in cells harbouring the hOGG1-Cys326 polymorphic variant. Nucleic Acids Res 33: 1813-1824 [Abstract] [Full Text]  
  • Ismail, I. H., Nystrom, S., Nygren, J., Hammarsten, O. (2005). Activation of Ataxia Telangiectasia Mutated by DNA Strand Break-inducing Agents Correlates Closely with the Number of DNA Double Strand Breaks. J. Biol. Chem. 280: 4649-4655 [Abstract] [Full Text]  
  • Vodenicharov, M. D., Ghodgaonkar, M. M., Halappanavar, S. S., Shah, R. G., Shah, G. M. (2005). Mechanism of early biphasic activation of poly(ADP-ribose) polymerase-1 in response to ultraviolet B radiation. J. Cell Sci. 118: 589-599 [Abstract] [Full Text]  
  • Okano, S., Lan, L., Tomkinson, A. E., Yasui, A. (2005). Translocation of XRCC1 and DNA ligase III{alpha} from centrosomes to chromosomes in response to DNA damage in mitotic human cells. Nucleic Acids Res 33: 422-429 [Abstract] [Full Text]  
  • Meder, V. S., Boeglin, M., de Murcia, G., Schreiber, V. (2005). PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J. Cell Sci. 118: 211-222 [Abstract] [Full Text]  
  • Audebert, M., Salles, B., Calsou, P. (2004). Involvement of Poly(ADP-ribose) Polymerase-1 and XRCC1/DNA Ligase III in an Alternative Route for DNA Double-strand Breaks Rejoining. J. Biol. Chem. 279: 55117-55126 [Abstract] [Full Text]  
  • Lan, L., Nakajima, S., Oohata, Y., Takao, M., Okano, S., Masutani, M., Wilson, S. H., Yasui, A. (2004). In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc. Natl. Acad. Sci. USA 101: 13738-13743 [Abstract] [Full Text]  
  • Dianova, I. I., Sleeth, K. M., Allinson, S. L., Parsons, J. L., Breslin, C., Caldecott, K. W., Dianov, G. L. (2004). XRCC1-DNA polymerase {beta} interaction is required for efficient base excision repair. Nucleic Acids Res 32: 2550-2555 [Abstract] [Full Text]  
  • Fan, J., Otterlei, M., Wong, H.-K., Tomkinson, A. E., Wilson, D. M. III (2004). XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res 32: 2193-2201 [Abstract] [Full Text]  
  • Rouleau, M., Aubin, R. A., Poirier, G. G. (2004). Poly(ADP-ribosyl)ated chromatin domains: access granted. J. Cell Sci. 117: 815-825 [Abstract] [Full Text]  
  • Malanga, M., Althaus, F. R. (2004). Poly(ADP-ribose) Reactivates Stalled DNA Topoisomerase I and Induces DNA Strand Break Resealing. J. Biol. Chem. 279: 5244-5248 [Abstract] [Full Text]  
  • Oliver, A. W., Ame, J.-C., Roe, S. M., Good, V., de Murcia, G., Pearl, L. H. (2004). Crystal structure of the catalytic fragment of murine poly(ADP-ribose) polymerase-2. Nucleic Acids Res 32: 456-464 [Abstract] [Full Text]  
  • Petrucco, S. (2003). Sensing DNA damage by PARP-like fingers. Nucleic Acids Res 31: 6689-6699 [Abstract] [Full Text]  
  • Haoudi, A., Daniels, R. C., Wong, E., Kupfer, G., Semmes, O. J. (2003). Human T-cell Leukemia Virus-I Tax Oncoprotein Functionally Targets a Subnuclear Complex Involved in Cellular DNA Damage-Response. J. Biol. Chem. 278: 37736-37744 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»