Evidence for DNA-PK-Dependent and -Independent DNA Double-Strand Break Repair Pathways in Mammalian Cells as a Function of the Cell Cycle

REFERENCES

• Ager, D. D., and W. C. Dewey. 1990. Calibration of pulsed field gel electrophoresis for measurement of DNA double-strand breaks. Int. J. Radiat. Biol. 58:249–259.
   PubMed Web of Science ®Google Scholar
• Alt, F., N. Rosenberg, S. Lewis, E. Thomas, and D. Baltimore. 1981. Organization and reorganization of immunoglobulin genes in A-MuLV-transformed cells: rearrangement of heavy but not light chain genes. Cell 27:381–390.
   PubMed Web of Science ®Google Scholar
• Anderson, C. W. 1994. Protein kinases and the response to cell damage. Semin. Cell Biol. 5:427–436.
   PubMedGoogle Scholar
• Anderson, C. W., and T. H. Carter. 1996. The DNA-activated protein kinase, DNA-PK. Curr. Top. Microbiol. Immunol. 217:91–111.
   PubMedGoogle Scholar
• Anderson, C. W., and S. P. Lees-Miller. 1992. The nuclear serine/threonine protein kinase DNA-PK. Crit. Rev. Eukaryotic Gene Expr. 2:283–314.
   PubMedGoogle Scholar
• Bianchi, V., E. Pontis, and P. Reichard. 1986. Changes of deoxyribonucleo-side triphosphate pools induced by hydroxyurea and their relation to DNA synthesis. J. Biol. Chem. 261:16037–16042.
   PubMed Web of Science ®Google Scholar
• Biedermann, K. A., J. Sun, A. J. Giaccia, L. M. Tosto, and J. M. Brown. 1991. scid mutation in mice confers hypersensitivity to ionizing radiation and a deficiency in DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 88:1394–1397.
   PubMed Web of Science ®Google Scholar
• Blocher, D., M. Nusse, and P. E. Bryant. 1983. Kinetics of double strand break repair in the DNA of X-irradiated synchronized mammalian cells. Int. J. Radiat. Biol. 43:579–584.
   Web of Science ®Google Scholar
• Blunt, T., N. J. Finnie, G. E. Taccioli, G. C. M. Smith, J. Demengeot, T. Gottlieb, R. Mizuta, A. J. Varghese, F. W. Alt, P. A. Jeggo, and S. P. Jackson. 1995. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80:813–823.
   PubMed Web of Science ®Google Scholar
• Bosma, M. J., and A. M. Carroll. 1991. The scid mouse mutant: definition, characterization and potential uses. Annu. Rev. Immunol. 9:323–350.
   PubMed Web of Science ®Google Scholar
• Boubnov, N. V., and D. T. Weaver. 1995. scid cells are deficient in Ku and replication protein A phosphorylation by the DNA-dependent protein kinase. Mol. Cell. Biol. 15:5700–5706.
   PubMedGoogle Scholar
• Boulton, S. J., and S. P. Jackson. 1996. Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15:5093–5103.
   PubMed Web of Science ®Google Scholar
• Brush, G. S., C. W. Anderson, and T. J. Kelly. 1994. The DNA-activated protein kinase is required for the phosphorylation of replication protein A during simian virus 40 DNA replication. Proc. Natl. Acad. Sci. USA 91:12520–12524.
   PubMedGoogle Scholar
• Cao, Q. P., S. Pitt, J. Leszyk, and E. F. Baril. 1994. DNA-dependent ATPase from HeLa cells is related to human Ku autoantigen. Biochemistry 33:8548–8557.
   PubMedGoogle Scholar
• Carr, A. M. 1996. Checkpoints take the next step. Science 271:314–315.
   PubMedGoogle Scholar
• Carter, T., I. Vancurova, I. Sun, W. Lou, and S. DeLeon. 1990. A DNA-activated protein kinase from HeLa cell nuclei. Mol. Cell. Biol. 10:6460–6471.
   PubMedGoogle Scholar
• Chan, D. W., and S. P. Lees-Miller. 1996. The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J. Biol. Chem. 271:8936–8941.
   PubMed Web of Science ®Google Scholar
• Chen, F., S. R. Peterson, M. D. Story, and D. J. Chen. 1996. Disruption of DNA-PK in Ku80 mutant xrs-6 and the implications in DNA double-strand break repair. Mutat. Res. 362:9–19.
   PubMedGoogle Scholar
• Danska, J. S., D. P. Holland, S. Mariathasan, K. M. Williams, and C. J. Guidos. 1996. Biochemical and genetic defects in the DNA-dependent protein kinase in murine scid lymphocytes. Mol. Cell. Biol. 16:5507–5517.
   PubMed Web of Science ®Google Scholar
• Eastman, Q. M., T. M. Leu, and D. G. Schatz. 1996. Initiation of V(D)J recombination in vitro obeying the 12/23 rule. Nature 380:85–88.
   PubMedGoogle Scholar
• Errami, A., V. Smider, W. K. Rathmell, D. M. He, E. A. Hendrickson, M. Z. Zdzienicka, and G. Chu. 1996. Ku86 defines the genetic defect and restores X-ray resistance and V(D)J recombination to complementation group 5 hamster cell mutants. Mol. Cell. Biol. 16:1519–1526.
   PubMedGoogle Scholar
• Evans, H. H., M. Ricanati, M.-F. Horng, Q. Jiang, J. Mencl, and P. Olive. 1993. DNA double-strand break rejoining deficiency in TK6 and other human B-lymphoblast cell lines. Radiat. Res. 134:307–315.
   PubMed Web of Science ®Google Scholar
• Finnie, N. J., T. M. Gottlieb, T. Blunt, P. A. Jeggo, and S. P. Jackson. 1995. DNA-dependent protein kinase activity is absent in xrs-6 cells: implications for site-specific recombination and DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 92:320–324.
   PubMed Web of Science ®Google Scholar
• Fulop, G. M., and R. A. Phillips. 1990. The scid mutation in mice causes a general defect in DNA repair. Nature 347:479–482.
   PubMed Web of Science ®Google Scholar
• Giaccia, A., R. Weinstein, J. Hu, and T. D. Stamato. 1985. Cell cycle-dependent repair of double-strand DNA breaks in a gamma-ray-sensitive Chinese hamster cell. Somatic Cell Mol. Genet. 11:485–491.
   PubMedGoogle Scholar
• Han, Z., D. Chatterjee, D. M. He, J. Early, P. Pantazis, J. H. Wyche, and E. A. Hendrickson. 1995. Evidence for a G2 checkpoint in p53-independent apoptosis induction by X-irradiation. Mol. Cell. Biol. 15:5849–5857.
   PubMedGoogle Scholar
• Han, Z., C. Johnston, W. H. Reeves, T. Carter, J. H. Wyche, and E. A. Hendrickson. 1996. Characterization of a Ku86 variant protein that results in altered DNA binding and diminished DNA-dependent protein kinase activity. J. Biol. Chem. 271:14098–14104.
   PubMedGoogle Scholar
• Hartley, K. O., D. Gell, G. C. M. Smith, H. Zhang, N. Divecha, M. A. Connelly, A. Admon, S. P. Lees-Miller, C. W. Anderson, and S. P. Jackson. 1995. DNA-dependent protein kinase catalytic subunit: a relative of phos-phatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82:849–856.
   PubMed Web of Science ®Google Scholar
• Hartwell, L. H., and M. B. Kastan. 1994. Cell cycle control and cancer. Science 266:1821–1828.
   PubMed Web of Science ®Google Scholar
• He, D. M., S. E. Lee, and E. A. Hendrickson. 1996. Restoration of x-ray and etoposide resistance, Ku-end binding activity and V(D)J recombination to the Chinese hamster sxi-3 mutant by a hamster Ku86 cDNA. Mutat. Res. 363:43–56.
   PubMedGoogle Scholar
• Hendrickson, E. A. 1993. The SCID mouse: relevance as an animal model system for studying human disease. Am. J. Pathol. 143:1511–1522.
   PubMed Web of Science ®Google Scholar
• Hendrickson, E. A., X.-Q. Qin, E. A. Bump, D. G. Schatz, M. Oettinger, and D. T. Weaver. 1991. A link between double-strand break-related repair and V(D)J recombination: the scid mutation. Proc. Natl. Acad. Sci. USA 88:4061–4065.
   PubMed Web of Science ®Google Scholar
• Hendrickson, E. A., D. G. Schatz, and D. T. Weaver. 1988. The scid gene encodes a trans-acting factor that mediates the rejoining event of Ig gene rearrangement. Genes Dev. 2:817–829.
   PubMed Web of Science ®Google Scholar
• Huang, L.-C., K. C. Clarkin, and G. M. Wahl. 1996. p53-dependent cell cycle arrests are preserved in DNA-activated protein kinase-deficient mouse fibroblasts. Cancer Res. 56:2940–2944.
   PubMedGoogle Scholar
• Jeggo, P. A. 1990. Studies on mammalian mutants defective in rejoining double-strand breaks in DNA. Mutat. Res. 239:1–16.
   PubMed Web of Science ®Google Scholar
• Jeggo, P. A., G. E. Taccioli, and S. P. Jackson. 1995. Menage a trois: double strand break repair, V(D)J recombination and DNA-PK. Bioessays 17:949–957.
   PubMed Web of Science ®Google Scholar
• Kadyk, L. C., and L. H. Hartwell. 1992. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387–402.
   PubMed Web of Science ®Google Scholar
• Kemp, L. M., S. G. Sedgwick, and P. A. Jeggo. 1984. X-ray sensitive mutants of Chinese hamster ovary cells defective in double-strand break rejoining. Mutat. Res. 132:189–196.
   PubMed Web of Science ®Google Scholar
• Kirchgessner, C. U., C. K. Patil, J. W. Evans, C. A. Cuomo, L. M. Fried, T. Carter, M. A. Oettinger, and J. M. Brown. 1995. DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267:1178–1183.
   PubMed Web of Science ®Google Scholar
• Krek, W., and E. A. Nigg. 1991. Differential phosphorylation of vertebrate p34cdc2 kinase at the G1/S and G2/M transitions of the cell cycle: identification of major phosphorylation sites. EMBO J. 10:305–316.
   PubMed Web of Science ®Google Scholar
• Kuhn, A., T. M. Gottlieb, S. P. Jackson, and I. Grummt. 1995. DNA-dependent protein kinase: a potent inhibitor of transcription by RNA polymerase I. Genes Dev. 9:193–203.
   PubMed Web of Science ®Google Scholar
• Kysela, B. P., B. D. Michael, and J. E. Arrand. 1993. Relative contributions of levels of initial DNA damage and repair of double strand breaks to the ionizing radiation-sensitive phenotype of the Chinese hamster cell mutant, XR-V15B. Part I. X-rays. Int. J. Radiat. Biol. 63:609–616.
   PubMed Web of Science ®Google Scholar
• Lee, S. E., C. R. Pulaski, D. M. He, D. M. Benjamin, M. J. Voss, J. Urn, and E. A. Hendrickson. 1995. Isolation of mammalian cell mutants that are x-ray sensitive, impaired in DNA double-strand break repair and defective for V(D)J recombination. Mutat. Res. 336:279–291.
   PubMedGoogle Scholar
• Lees-Miller, S. P., Y.-R. Chen, and C. W. Anderson. 1990. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell. Biol. 10:6472–6481.
   PubMed Web of Science ®Google Scholar
• Lees-Miller, S. P., K. Sakaguchi, S. J. Ullrich, E. Appella, and C. W. Anderson. 1992. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the ammo-terminal transactivation domain of human p53. Mol. Cell. Biol. 12:5041–5049.
   PubMed Web of Science ®Google Scholar
• Lewis, S. M. 1994. The mechanism of V(D)J joining: lessons from molecular, immunological, and comparative analyses. Adv. Immunol. 56:27–150.
   PubMed Web of Science ®Google Scholar
• Lin, W.-C., and S. Desiderio. 1993. Regulation of V(D)J recombination activator protein RAG-2 by phosphorylation. Science 260:953–959.
   PubMed Web of Science ®Google Scholar
• Lin, W. C., and S. Desiderio. 1994. Cell cycle regulation of V(D)J recombi-nation-activating protein RAG-2. Proc. Natl. Acad. Sci. USA 91:2733–2737.
   PubMed Web of Science ®Google Scholar
• Mages, G. J., H. M. Feldmann, and E.-L. Winnacker. 1996. Involvement of the Saccharomyces cerevisiae HDF1 gene in DNA double-strand break repair and recombination. J. Biol. Chem. 271:7910–7915.
   PubMedGoogle Scholar
• Mateos, S., P. Slijepcevic, R. A. F. MacLeod, and P. E. Bryant. 1994. DNA double-strand break rejoining inxrs5 cells is more rapid in the G2 than in the G1 phase of the cell cycle. Mutat. Res. 315:181–187.
   PubMedGoogle Scholar
• McBlane, J. F., D. C. van Gent, D. A. Ramsden, C. Romeo, C. A. Cuomo, M. Gellert, and M. A. Oettinger. 1995. Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell 83:387–395.
   PubMed Web of Science ®Google Scholar
• Miller-Faures, A., A. Slave, M. Caudron, C. Sene, and A. O. A. Miller. 1985. Flow cytometric analysis of hepatoma tissue and HeLa cells grown on various types of microbeads using hydroxyurea, nocodazole and aphidicolin in succession. Dev. Biol. Stand. 60:209–218.
   PubMedGoogle Scholar
• Milne, G. T., S. Jin, K. B. Shannon, and D. T. Weaver. 1996. Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:4189–4198.
   PubMedGoogle Scholar
• Mimori, T., J. A. Hardin, and J. A. Steitz. 1986. Characterization of the DNA-binding protein antigen Ku recognized by autoantibodies from patients with rheumatic disorders. J. Biol. Chem. 261:2274–2278.
   PubMedGoogle Scholar
• Modrich, P. 1994. Mismatch repair, genetic stability, and cancer. Science 266:1959–1960.
   PubMed Web of Science ®Google Scholar
• Moore, J. K., and J. E. Haber. 1996. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2164–2173.
   PubMed Web of Science ®Google Scholar
• Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131–134.
   PubMed Web of Science ®Google Scholar
• Nagasawa, H., P. Keng, R. Harley, W. Dahlberg, and J. B. Little. 1994. Relationship between 7-ray-induced G2/M delay and cellular radiosensitiv-ity. Int. J. Radiat. Biol. 66:373–379.
   PubMed Web of Science ®Google Scholar
• Nussenzweig, A., C. Chen, V. da Costa Soares, M. Sanchez, K. Sokol, M. C. Nussenzweig, and G. C. Li. 1996. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382:551–555.
   PubMed Web of Science ®Google Scholar
• Pan, Z.-Q., A. A. Amin, E. Gibbs, H. Niu, and J. Hurwitz. 1994. Phosphorylation of the p34 subunit of human single-stranded DNA-binding protein in cyclin A-activated G1 extracts is catalyzed by CDK-cyclin A complex and DNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA 91:8343–8347.
   PubMedGoogle Scholar
• Petersen, L. N., D. K. Orren, and V. A. Bohr. 1995. Gene-specific and strand-specific DNA repair in the G1 and G2 phases of the cell cycle. Mol. Cell. Biol. 15:3731–3737.
   PubMed Web of Science ®Google Scholar
• Rathmell, W. K., and G. Chu. 1994. Involvement of the Ku autoantigen in the cellular response to DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 91:7623–7627.
   PubMed Web of Science ®Google Scholar
• Sancar, A. 1994. Mechanisms of DNA excision repair. Science 266:1954–1956.
   PubMed Web of Science ®Google Scholar
• Sandell, L. L., and V. A. Zakian. 1993. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75:729–739.
   PubMed Web of Science ®Google Scholar
• Schlissel, M., A. Constantinescu, T. Morrow, M. Baxter, and A. Peng. 1993. Double-strand signal sequence breaks in V(D)J recombination are blunt, 5′-phosphorylated, RAG-dependent, and cell-cycle regulated. Genes Dev. 7:2520–2532.
   PubMedGoogle Scholar
• Seide, W., A. A. Friedl, I. Dianova, F. Eckardt-Schupp, and E. C. Friedberg. 1996. The Saccharomyces cerevisiae Ku autoantigen homologue affects ra-diosensitivity only in the absence of homologous recombination. Genetics 142:91–102.
   PubMedGoogle Scholar
• Shenoy, S., J.-K. Choi, S. Bagrodia, T. D. Copeland, J. L. Mailer, and D. Shalloway. 1989. Purified maturation promoting factor phosphorylates pp60c-src at the sites phosphorylated during fibroblast mitosis. Cell 57:763–774.
   PubMedGoogle Scholar
• Stamato, T. D., and N. Denko. 1990. Asymmetric field inversion gel electrophoresis: a new method for detecting DNA double-strand breaks in mammalian cells. Radiat. Res. 121:196–205.
   PubMed Web of Science ®Google Scholar
• Stamato, T. D., R. Weinstein, A. Giaccia, and L. Mackenzie. 1983. Isolation of cell cycle-dependent gamma ray-sensitive Chinese hamster ovary cell. Somatic Cell Genet. 9:165–173.
   PubMedGoogle Scholar
• Sun, S., and T. H. Carter. DNA-dependent protein kinase (DNA-PK) in HeLa cells is regulated during the cell cycle by phosphorylation. Submitted for publication.
   Google Scholar
• Szostak, J. W., T. L. Orr-Weaver, R. J. Rothstein, and F. W. Stahl. 1983. The double-strand-break repair model for recombination. Cell 33:25–35.
   PubMed Web of Science ®Google Scholar
• Taccioli, G. E., H.-L. Cheng, A. J. Varghese, G. Whitmore, and F. W. Alt. 1994. A DNA repair defect in Chinese hamster ovary cells affects V(D)J recombination similarly to the murine scid mutation. J. Biol. Chem. 269:7439–7442.
   PubMedGoogle Scholar
• Taccioli, G. E., G. Rathbun, E. Oltz, T. Stamato, P. A. Jeggo, and F. W. Alt. 1993. Impairment of V(D)J recombination in double-strand break repair mutants. Science 260:207–210.
   PubMed Web of Science ®Google Scholar
• Walworth, N. C., and R. Bernards. 1996. rad-dependent response of the chkl-encoded protein kinase at the DNA damage checkpoint. Science 271:353–356.
   PubMed Web of Science ®Google Scholar
• Weibezahn, K. F., H. Lohrer, and P. Herrlich. 1985. Double-strand break repair and G2 block in Chinese hamster ovary cells and their radiosensitive mutants. Mutat. Res. 145:177–183.
   PubMed Web of Science ®Google Scholar
• Weinert, T. A., and L. H. Hartwell. 1988. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241:317–322.
   PubMed Web of Science ®Google Scholar
• Whitmore, G. F., A. J. Varghese, and S. Gulyas. 1989. Cell cycle responses of two X-ray sensitive mutants defective in DNA repair. Int. J. Radiat. Biol. 56:657–665.
   PubMed Web of Science ®Google Scholar
• Yaneva, M., and S. Jhiang. 1991. Expression of the Ku protein during cell proliferation. Biochim. Biophys. Acta 1090:181–187.
   PubMedGoogle Scholar
• Zdzienicka, M. Z. 1995. Mammalian mutants defective in the response to ionizing radiation-induced DNA damage. Mutat. Res. 336:203–213.
   PubMedGoogle Scholar
• Zdzienicka, M. Z., Q. Tran, G. P. van der Schans, and J. W. I. M. Simons. 1988. Characterization of an X-ray-hypersensitive mutant of V79 Chinese hamster cells. Mutat. Res. 194:239–249.
   PubMed Web of Science ®Google Scholar