Werner Protein Protects Nonproliferating Cells from Oxidative DNA Damage

REFERENCES

• Atamna, H., A. Paler-Martinez, and B. N. Ames. 2000. N-t-butyl hydroxylamine, a hydrolysis product of alpha-phenyl-N-t-butyl nitrone, is more potent in delaying senescence in human lung fibroblasts. J. Biol. Chem. 275:6741–6748.
   PubMed Web of Science ®Google Scholar
• Atamna, H., C. Robinson, R. Ingersoll, H. Elliott, and B. N. Ames. 2001. N-t-Butyl hydroxylamine is an antioxidant that reverses age-related changes in mitochondria in vivo and in vitro. FASEB J. 15:2196–2204.
   PubMed Web of Science ®Google Scholar
• Beckman, K. B., and B. N. Ames. 1998. The free radical theory of aging matures. Physiol. Rev. 78:547–581.
   PubMed Web of Science ®Google Scholar
• Bischof, O., S. H. Kim, J. Irving, S. Beresten, N. A. Ellis, and J. Campisi. 2001. Regulation and localization of the Bloom syndrome protein in response to DNA damage. J. Cell Biol. 153:367–380.
   PubMed Web of Science ®Google Scholar
• Blander, G., N. Zalle, J. F. Leal, R. L. Bar-Or, C. E. Yu, and M. Oren. 2000. The Werner syndrome protein contributes to induction of p53 by DNA damage. FASEB J. 14:2138–2140.
   PubMedGoogle Scholar
• Bradshaw, P. S., D. J. Stavropoulos, and M. S. Meyn. 2005. Human telomeric protein TRF2 associates with genomic double-strand breaks as an early response to DNA damage. Nat. Genet. 37:193–197.
   PubMed Web of Science ®Google Scholar
• Celeste, A., S. Petersen, P. J. Romanienko, O. Fernandez-Capetillo, H. T. Chen, O. A. Sedelnikova, B. Reina-San-Martin, V. Coppola, E. Meffre, M. J. Difilippantonio, C. Redon, D. R. Pilch, A. Olaru, M. Eckhaus, R. D. Camerini-Otero, L. Tessarollo, F. Livak, K. Manova, W. M. Bonner, M. C. Nussenzweig, and A. Nussenzweig. 2002. Genomic instability in mice lacking histone H2AX. Science 296:922–927.
   PubMed Web of Science ®Google Scholar
• Chang, S., A. S. Multani, N. G. Cabrera, M. L. Naylor, P. Laud, D. Lombard, S. Pathak, L. Guarente, and R. A. DePinho. 2004. Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat. Genet. 36:877–882.
   PubMed Web of Science ®Google Scholar
• Chen, Q., A. Fischer, J. D. Reagan, L. J. Yan, and B. N. Ames. 1995. Oxidative DNA damage and senescence of human diploid fibroblast cells. Proc. Natl. Acad. Sci. USA 92:4337–4341.
   PubMed Web of Science ®Google Scholar
• Choi, D., P. S. Whittier, J. Oshima, and W. D. Funk. 2001. Telomerase expression prevents replicative senescence but does not fully reset mRNA expression patterns in Werner syndrome cell strains. FASEB J. 15:1014–1020.
   PubMedGoogle Scholar
• Cooke, M. S., M. D. Evans, M. Dizdaroglu, and J. Lunec. 2003. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 17:1195–1214.
   PubMed Web of Science ®Google Scholar
• d'Adda di Fagagna, F., P. M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N. P. Carter, and S. P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426:194–198.
   PubMed Web of Science ®Google Scholar
• Davalos, A. R., and J. Campisi. 2003. Bloom syndrome cells undergo p53-dependent apoptosis and delayed assembly of BRCA1 and NBS1 repair complexes at stalled replication forks. J. Cell Biol. 162:1197–1209.
   PubMed Web of Science ®Google Scholar
• Davies, S. L., P. S. North, A. Dart, N. D. Lakin, and I. D. Hickson. 2004. Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol. 24:1279–1291.
   PubMed Web of Science ®Google Scholar
• Dimri, G. P., X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. E. Medrano, M. Linskens, I. Rubelj, O. Pereira-Smith, et al. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92:9363–9367.
   PubMed Web of Science ®Google Scholar
• Du, X., J. Shen, N. Kugan, E. E. Furth, D. B. Lombard, C. Cheung, S. Pak, G. Luo, R. J. Pignolo, R. A. DePinho, L. Guarente, and F. B. Johnson. 2004. Telomere shortening exposes functions for the mouse Werner and Bloom syndrome genes. Mol. Cell. Biol. 24:8437–8446.
   PubMedGoogle Scholar
• Dutertre, S., M. Ababou, R. Onclercq, J. Delic, B. Chatton, C. Jaulin, and M. Amor-Gueret. 2000. Cell cycle regulation of the endogenous wild type Bloom's syndrome DNA helicase. Oncogene 19:2731–2738.
   PubMed Web of Science ®Google Scholar
• Elbashir, S. M., J. Harborth, K. Weber, and T. Tuschl. 2002. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26:199–213.
   PubMed Web of Science ®Google Scholar
• Ellis, N. A., J. Groden, T. Z. Ye, J. Straughen, D. J. Lennon, S. Ciocci, M. Proytcheva, and J. German. 1995. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83:655–666.
   PubMed Web of Science ®Google Scholar
• Epstein, C. J., and A. G. Motulsky. 1996. Werner syndrome: entering the helicase era. Bioessays 18:1025–1027.
   PubMedGoogle Scholar
• Evans, M. D., M. Dizdaroglu, and M. S. Cooke. 2004. Oxidative DNA damage and disease: induction, repair and significance. Mutat. Res. 567:1–61.
   PubMed Web of Science ®Google Scholar
• Fernandez-Capetillo, O., A. Lee, M. Nussenzweig, and A. Nussenzweig. 2004. H2AX: the histone guardian of the genome. DNA Repair 3:959–967.
   PubMed Web of Science ®Google Scholar
• Fukuchi, K., G. M. Martin, and R. J. Monnat, Jr. 1989 Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc. Natl. Acad. Sci. USA 86:5893–5897.
   PubMedGoogle Scholar
• Harrigan, J. A., P. L. Opresko, C. von Kobbe, P. S. Kedar, R. Prasad, S. H. Wilson, and V. A. Bohr. 2003. The Werner syndrome protein stimulates DNA polymerase beta strand displacement synthesis via its helicase activity. J. Biol. Chem. 278:22686–22695.
   PubMedGoogle Scholar
• Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169–178.
   PubMed Web of Science ®Google Scholar
• Hisama, F. M., Y. H. Chen, M. S. Meyn, J. Oshima, and S. M. Weissman. 2000. WRN or telomerase constructs reverse 4-nitroquinoline 1-oxide sensitivity in transformed Werner syndrome fibroblasts. Cancer Res. 60:2372–2376.
   PubMedGoogle Scholar
• Huschtscha, L. I., K. V. Thompson, and R. Holliday. 1986. The susceptibility of Werner's syndrome and other human skin fibroblasts to SV40-induced transformation and immortalization. Proc. R. Soc. Lond. B Biol. Sci. 229:1–12.
   PubMedGoogle Scholar
• Karanjawala, Z. E., N. Murphy, D. R. Hinton, C. L. Hsieh, and M. R. Lieber. 2002. Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Curr. Biol. 12:397–402.
   PubMed Web of Science ®Google Scholar
• Karlseder, J., A. Smogorzewska, and T. de Lange. 2002. Senescence induced by altered telomere state, not telomere loss. Science 295:2446–2449.
   PubMed Web of Science ®Google Scholar
• Kitao, S., A. Shimamoto, M. Goto, R. W. Miller, W. A. Smithson, N. M. Lindor, and Y. Furuichi. 1999. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet. 22:82–84.
   PubMed Web of Science ®Google Scholar
• Lombard, D. B., C. Beard, B. Johnson, R. A. Marciniak, J. Dausman, R. Bronson, J. E. Buhlmann, R. Lipman, R. Curry, A. Sharpe, R. Jaenisch, and L. Guarente. 2000. Mutations in the WRN gene in mice accelerate mortality in a p53-null background. Mol. Cell. Biol. 20:3286–3291.
   PubMedGoogle Scholar
• Martin, G. M., and J. Oshima. 2000. Lessons from human progeroid syndromes. Nature 408:263–266.
   PubMedGoogle Scholar
• Martin, G. M., J. Oshima, M. D. Gray, and M. Poot. 1999. What geriatricians should know about the Werner syndrome. J. Am. Geriatr. Soc. 47:1136–1144.
   PubMedGoogle Scholar
• Mochan, T. A., M. Venere, R. A. DiTullio, Jr., and T. D. Halazonetis. 2004. 53BP1, an activator of ATM in response to DNA damage. DNA Repair 3:945–952.
   PubMed Web of Science ®Google Scholar
• Monnat, R. J., Jr., and Y. Saintigny. 2004. Werner syndrome protein-unwinding function to explain disease. Sci. Aging Knowledge Environ. 13:1–10.
   Google Scholar
• Neff, N. F., N. A. Ellis, T. Z. Ye, J. Noonan, K. Huang, M. Sanz, and M. Proytcheva. 1999. The DNA helicase activity of BLM is necessary for the correction of the genomic instability of bloom syndrome cells. Mol. Biol. Cell 10:665–676.
   PubMed Web of Science ®Google Scholar
• Opresko, P. L., W. H. Cheng, and V. A. Bohr. 2004. Junction of RecQ helicase biochemistry and human disease. J. Biol. Chem. 279:18099–18102.
   PubMed Web of Science ®Google Scholar
• Opresko, P. L., M. Otterlei, J. Graakjaer, P. Bruheim, L. Dawut, S. Kolvraa, A. May, M. M. Seidman, and V. A. Bohr. 2004. The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol. Cell 14:763–774.
   PubMed Web of Science ®Google Scholar
• Opresko, P. L., C. von Kobbe, J. P. Laine, J. Harrigan, I. D. Hickson, and V. A. Bohr. 2002. Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem. 277:41110–41119.
   PubMed Web of Science ®Google Scholar
• Parrinello, S., E. Samper, A. Krtolica, J. Goldstein, S. Melov, and J. Campisi. 2003. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5:741–747.
   PubMed Web of Science ®Google Scholar
• Reynolds, T. Y., S. Rockwell, and P. M. Glazer. 1996. Genetic instability induced by the tumor microenvironment. Cancer Res 56:5754–5757.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Lopez, A. M., D. A. Jackson, F. Iborra, and L. S. Cox. 2002. Asymmetry of DNA replication fork progression in Werner's syndrome. Aging Cell 1:30–39.
   PubMed Web of Science ®Google Scholar
• Rogakou, E. P., C. Boon, C. Redon, and W. M. Bonner. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905–916.
   PubMed Web of Science ®Google Scholar
• Rothkamm, K., and M. Lobrich. 2003. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proc. Natl. Acad. Sci. USA 100:5057–5062.
   PubMed Web of Science ®Google Scholar
• Sage, J., A. L. Miller, P. A. Perez-Mancera, J. M. Wysocki, and T. Jacks. 2003. Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry. Nature 424:223–228.
   PubMed Web of Science ®Google Scholar
• Salk, D. 1982. Werner's syndrome: a review of recent research with an analysis of connective tissue metabolism, growth control of cultured cells, and chromosomal aberrations. Hum. Genet. 62:1–5.
   PubMed Web of Science ®Google Scholar
• Salk, D., K. Au, H. Hoehn, M. R. Stenchever, and G. M. Martin. 1981. Evidence of clonal attenuation, clonal succession, and clonal expansion in mass cultures of aging Werner's syndrome skin fibroblasts. Cytogenet. Cell Genet. 30:108–117.
   PubMedGoogle Scholar
• Schultz, L. B., N. H. Chehab, A. Malikzay, and T. D. Halazonetis. 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.
   PubMed Web of Science ®Google Scholar
• Senderowicz, A. M. 2003. Small-molecule cyclin-dependent kinase modulators. Oncogene 22:6609–6620.
   PubMed Web of Science ®Google Scholar
• Siitonen, H. A., O. Kopra, H. Kaariainen, H. Haravuori, R. M. Winter, A. M. Saamanen, L. Peltonen, and M. Kestila. 2003. Molecular defect of RAPADILINO syndrome expands the phenotype spectrum of RECQL diseases. Hum. Mol. Genet. 12:2837–2844.
   PubMed Web of Science ®Google Scholar
• Smogorzewska, A., and T. de Lange. 2004. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73:177–208.
   PubMed Web of Science ®Google Scholar
• Spillare, E. A., A. I. Robles, X. W. Wang, J. C. Shen, C. E. Yu, G. D. Schellenberg, and C. C. Harris. 1999. p53-mediated apoptosis is attenuated in Werner syndrome cells. Genes Dev. 13:1355–1360.
   PubMed Web of Science ®Google Scholar
• Szekely, A. M., Y. H. Chen, C. Zhang, J. Oshima, and S. M. Weissman. 2000. Werner protein recruits DNA polymerase delta to the nucleolus. Proc. Natl. Acad. Sci. USA 97:11365–11370.
   PubMedGoogle Scholar
• Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549–1556.
   PubMed Web of Science ®Google Scholar
• von Kobbe, C., J. A. Harrigan, V. Schreiber, P. Stiegler, J. Piotrowski, L. Dawut, and V. A. Bohr. 2004. Poly(ADP-ribose) polymerase 1 regulates both the exonuclease and helicase activities of the Werner syndrome protein. Nucleic Acids Res. 32:4003–4014.
   PubMed Web of Science ®Google Scholar
• von Kobbe, C., P. Karmakar, L. Dawut, P. Opresko, X. Zeng, R. M. Brosh, Jr., I. D. Hickson, and V. A. Bohr. 2002. Colocalization, physical, and functional interaction between Werner and Bloom syndrome proteins. J. Biol. Chem. 277:22035–22044.
   PubMed Web of Science ®Google Scholar
• Von Kobbe, C., A. May, C. Grandori, and V. A. Bohr. 2004. Werner syndrome cells escape hydrogen peroxide-induced cell proliferation arrest. FASEB J. 18:1970–1972.
   PubMed Web of Science ®Google Scholar
• von Zglinicki, T. 2002. Oxidative stress shortens telomeres. Trends Biochem. Sci. 27:339–344.
   PubMed Web of Science ®Google Scholar
• Ward, I. M., K. Minn, K. G. Jorda, and J. Chen. 2003. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278:19579–19582.
   PubMed Web of Science ®Google Scholar
• Wyllie, F. S., C. J. Jones, J. W. Skinner, M. F. Haughton, C. Wallis, D. Wynford-Thomas, R. G. Faragher, and D. Kipling. 2000. Telomerase prevents the accelerated cell ageing of Werner syndrome fibroblasts. Nat. Genet. 24:16–17.
   PubMed Web of Science ®Google Scholar
• Yang, H. S., and P. W. Hinds. 2003. Increased ezrin expression and activation by CDK5 coincident with acquisition of the senescent phenotype. Mol. Cell 11:1163–1176.
   PubMedGoogle Scholar