DNA double-strand breaks trigger apoptosis in p53-deficient fibroblasts

Friedberg,E.C., Walker,G.C. and Siede,W. (1995) DNA Repair and Mutagenesis. ASM Press, Washington, DC.

Obe,G., Johannes,C. and Schulte-Frohlinde,D. (1992) DNA double-strand breaks induced by sparsely ionizing radiation and endonucleases as critical lesions for cell death, chromosomal aberrations, mutations and oncogenic transformation. Mutagenesis, 7, 3–12.

Dominguez,I., Boel,J.J.W.A., Balajee,A.S. and Natarajan,A.T. (1996) Analysis of radiation-induced chromosome aberrations in Chinese hamster cells by FISH using chromosome specific DNA libraries. Int. J. Radiat. Biol., 70, 199–208.

Kaina,B. (1998) Critical steps in alkylation-induced aberration formation. Mutat. Res., 404, 119–124.

Natarajan,A.T. and Zwanenburg,T.S.B. (1982) Mechanisms for chromo- somal aberrations in mammalian cells. Mutat. Res., 95, 1–6.

Schwartz,J.L., Rotmensch,J., Giovanazzi,S., Cohen,M.B. and Weichselbaum, R.R. (1988) Faster repair of DNA double-strand breaks in radioresistant human tumor cells. Int. J. Radiat. Oncol. Biol. Phys., 15, 907–912.

Whitacker,S.J., Ung,Y.C. and McMillan,T.J. (1995) DNA double-strand break induction and rejoining as determinants of human tumour cell radiosensitivity. A pulse-field gel electrophoresis study. Int. J. Radiat. Biol., 67, 7–18.

Wurm,R., Burnet,N.G., Duggal,N., Yarnold,J.R. and Peacock,J.H. (1994) Cellular radiosensitivity and DNA damage in primary human fibroblasts. Int. J. Radiat. Oncol. Biol. Phys., 30, 625–633.

Olive,P.L., Banath,J.P. and MacPhail,H.S. (1994) Lack of correlation between radiosensitivity and DNA double strand-break induction or rejoining in six human tumour cell lines. Cancer Res., 54, 3939–3946.

Woudstra,E.C., Roesink,J.M., Rosemann,M., Brunsting,J.F., Driessen,C., Orta,C., Konings,A.W.T., Peacock,J.H. and Kampinga,H.H. (1996) Chromatin structure and cellular radiosensitivity: a comparison of two human tumour cell lines. Int. J. Radiat. Biol., 70, 693–703.

Dikomey,E., Dahm-Daphi,J., Brammer,I., Martensen,R. and Kaina,B. (1998) Correlation between cellular radiosensitivity and non-repaired double-strand breaks studied in nine mammalian cell lines. Int. J. Radiat. Biol., 73, 269–278.

Cornforth,M.N. and Bedford,J.S. (1987) A quantitative comparison of potentially lethal damage repair and the rejoining of interphase chromosome breaks in low passage normal human fibroblasts. Radiat. Res., 111, 385–405.

Ashkenazi,A. and Dixit,V.M. (1998) Death receptors: signaling and modulation. Science, 281, 1305–1308.

Basu,S. and Kolesnick,R. (1998) Stress signals for apoptosis: ceramide and c-Jun kinase. Oncogene, 17, 3277–3285.

Costa,N.D. and Bryant,P.E. (1991) Differences in accumulation of blunt- and cohesive-ended double-strand breaks generated by restriction endonucleases in electroporated CHO cells. Mutat. Res., 254, 239–246.

Winegar,R.A., Philips,J.W., Youngblom,J.H. and Morgan,W.F. (1989) Cell electroporation is a highly efficient method for introducing restriction endonucleases into cells. Mutat. Res., 225, 49–53.

Bryant,P.E. (1984) Enzymatic restriction of mammalian cell DNA using PvuII and BamH1: evidence for the double-strand break origin of chromosomal aberrations. Int. J. Radiat. Biol., 46, 57–65.

Obe,G., Palitti,F., Tanzarella,C., Degrassi,F. and De Salvia,R. (1985) Chromosomal aberrations induced by restriction endonucleases. Mutat. Res., 150, 359–368.

Winegar,R.A. and Preston,R.J. (1988) The induction of chromosome aberrations by restriction endonucleases that produce blunt-end or cohesice-end double-strand breaks. Mutat. Res., 197.

Donehower,L.A., Harvey,M., Slagle,B.L., McArthur,M.J., Montgomery, C.A., Butel,J.S. and Bradley,A. (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature, 356, 215–221.

Obe,G., Eke,P. and Johannes,C. (1995) Exposure of CHO cells to AluI: comparison of chromosomal aberrations and cell survival. Mutat. Res., 326, 171–174.

Singh,N.P., McCoy,M.T., Tice,R.R. and Schneider,E.L. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell. Res., 175, 184–191.

Olive,P.L., Wlodek,D. and Banath,J.P. (1991) DNA double-strand breaks measured in individual cells subjected to gel electrophoresis. Cancer Res., 51, 4671–4676.

Ochs,K., Sobol,R.W., Wilson,S.H. and Kaina,B. (1999) Cells deficient in DNA polymerase β are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res., 59, 1544–1551.

Vermes,I., Haanen,C., Steffens-Nakken,H. and Reutelingsberger,C. (1995) A novel assay for apoptosis: flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods, 184, 39–51.

Ioannou,Y.A. and Chen,F. (1996) Quantitation of DNA fragmentation in apoptosis. Nucleic Acids Res., 24, 992–993.

Ochs,K. and Kaina,B. (2000) Apoptosis induced by DNA damage O6-methylguanine is Bcl-2 and caspase-9/-3 regulated and Fas/caspase-8 independent. Cancer Res., 60, 5815–5824.

von Sonntag,C. (1987) The Chemical Basis of Radiation Biology. London, UK.

Hallahan,D.E., Sukhatme,V.P., Sherman,M.L., Virudachalam,S., Kufe,D. and Weichselbaum,R.R. (1991) Protein kinase C mediates X-ray inducibility of nuclear signal transducers EGR1 and Jun. Proc. Natl Acad. Sci. USA, 88, 2156–2160.

Weaver,D.T. (1995) What to do at an end: DNA double-strand break repair. Trends Genet., 11, 388–392.

Takata,M., Sasaki,M.S., Sonoda,E., Morrison,C., Hashimoto,M., Utsumi,H., Yamaguchi-Iwai,Y., Shinohara,A. and Takeda,S. (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J., 17, 5497–5508.

Jeggo,P.A. (1997) DNA-PK: at the crossroads of biochemistry and genetics. Mutat. Res., 384, 1–14.

Li,Z., Otevrel,T., Gao,Y., Cheng,H.-L., Seed,B., Stamato,T.D., Taccioli,E. and Alt,F.W. (1995) The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V (D)J recombination. Cell, 83, 1079–1089.

Grawunder,U., Wilm,M., Wu,X., Kulesza,P., Wilson,T.E., Mann,M. and Lieber,M.R. (1997) Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature, 388, 492–495.

Wang,S., Guo,M., Ouyang,H., Li,X., Cordon-Cardo,C., Kurimasa,A., Chen,D.J., Fuks,Z., Ling,C.C. and Li,G.C. (2000) The catalytic subunit of DNA-dependent protein kinase selectively regulates p53-dependent apoptosis but not cell-cycle arrest. Proc. Natl Acad. Sci. USA, 97, 1584–1588.

Süsse,S., Janz,C., Janus,F., Deppert,W. and Wiesmüller,L. (2000) Role of heteroduplex joints in the functional interactions between human Rad51 and wild-type p53. Oncogene, 19, 4500–4512.

Stürzbecher,H.-W., Donzelmann,B., Henning,W., Knippschild,U. and Buchop,S. (1996) p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction. EMBO J., 15, 1992–2002.

Mummenbrauer,T., Janus,F., Muller,B., Wiesmüller,L., Deppert,W. and Grosse,F. (1996) p53 protein exhibits 3′-to-5′ exonuclease activity. Cell, 85, 1089–1099.

Ford,J.M. and Hanawalt,P.C. (1997) Expression of wild-type p53 is required for efficient global genomic nucleotide excision repair in UV-irradiated human fibroblasts. J. Biol. Chem., 272, 28073–28080.

Smith,M.L., Ford,J.M., Hollander,C., Bortnick,R.A., Amundson,S.A., Seo,Y.R., Deng,C.X., Hanawalt,P.C. and Fornace,A.J. (2000) p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21 and/or gadd45 genes. Mol. Cell. Biol., 20, 3705–3714.

Tang,W., Willers,H. and Powell,S.N. (1999) p53 directly enhances rejoining of DNA double-strand breaks with cohesive ends in γ-irradiated mouse fibroblasts. Cancer Res., 59, 2562–2565.

Lackinger,D. and Kaina,B. (2000) Primary mouse fibroblasts deficient for c-Fos, p53 or for both proteins are hypersensitive to UV light and alkylating agent-induced chromosomal breakage and apoptosis. Mutat. Res., 9042, 1–11.

Kuerbitz,S.J., Plunkett,B.S., Walsh,W.V. and Kastan,M.B. (1992) Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl Acad. Sci. USA, 89, 7491–7495.

Lowe,S.W., Schmitt,E.M., Smith,S.W., Osborne,B.A. and Jacks,T. (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature, 362, 847–849.

Lee,J.M. and Bernstein,A. (1993) p53 mutations increase resistance to ionizing radiation. Proc. Natl Acad. Sci. USA, 90, 5742–5746.

Muller,M., Wilder,S., Bannasch, et al. (1998) p53 activates the CD95 (Apo-1/Fas) gene in response to DNA damage by anticancer drugs. J. Exp. Med., 188, 2033–2045.

Miyashita,T., Krajewsky,S., Krajewska,M., Wang,H.G., Lin,H.K., Liebermann,D.A., Hoffman,B. and Reed,J.C. (1994) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene, 9, 1799–1805.

Haldar,S., Chintapalli,J. and Croce,C.M. (1996) Taxol induces Bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res., 56, 1253–1255.

Uberti,D., Schwartz,D., Almog,N., Goldfinger,N., Harmelin,A., Memo,M. and Rotter,V. (1999) Epithelial cells of different organs exhibits distinct patterns of p53-dependent and p53-independent apoptosis following DNA insult. Exp. Cell Res., 252, 123–133.

Unger,C., Buchmann,A., Buenemann,C.L., Kress,S. and Schwarz,M. (1998) Wild-type function of the p53 tumor suppressor protein is not required for apoptosis of mouse hepatoma cells. Cell Death Differ., 5, 87–95.

Thust,R., Tomicic,M., Klöcking,R., Voutilainen,N., Wutzler,P. and Kaina,B. (2000) Comparison of the genotoxic and apoptosis-inducing properties of ganciclovir and penciclovir in Chinese hamster ovary cells transfected with the thymidine kinase gene of herpes simplex virus-1: implications for gene therapeutic approaches. Cancer Gene Ther., 7, 107–117.

Reed,J.C. (1998) Bcl-2 family proteins. Oncogene, 17, 3225–3236.