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Inducible Cellular Responses to DNA Damage in Mammalian Cells

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Antimutagenesis and Anticarcinogenesis Mechanisms

Part of the book series: Basic Life Sciences ((BLSC,volume 39))

Abstract

The mechanisms by which chemical carcinogens induce cellular transformation are unknown. Polycyclic aromatic hydrocarbons, such as benzo(α)pyrene (BP), have been extensively studied, and their chemical properties, metabolic activation, and DNA-binding properties have been elucidated in great detail (34). There is also evidence that covalent binding of metabolites of these and of other carcinogens to cellular DNA is a critical event in their action as carcinogens (77). The subsequent series of biochemical and genetic events, however, that lead to the conversion of a normal cell to a cancer cell are not known.

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References

  1. Ames, B.N., W.E. Durston, E. Yamasaki, and F.D. Lee (1973) Carcipogens are mutagens: A simple test system combining liver homogenates for activation and bacteria for detection. Proc. Natl. Acad. Sci., USA 70:2281–2285.

    Article  CAS  Google Scholar 

  2. Ashburner, M., and J.J. Bonner (1979) The induction of gene activity in Drosophila by heat shock. Cell 17:241–254.

    Article  CAS  Google Scholar 

  3. Baltimore, D. (1985) Retroviruses and retrotransposons: The role of reverse transcription in shaping the eukaryotic genome. Cell 40:481- 482.

    Article  CAS  Google Scholar 

  4. Basilico, C., D. Zouzias, G. Delia Valle, S. Gattoni, V. Colantuoni, R. Fenton, and L. Dailey (1980) Integration and excision of polyoma virus genomes. Cold Spring Harbor Symp. Quant. Biol. 44:611–620.

    Article  CAS  Google Scholar 

  5. Bensaude, O., C. Babinet, M. Morange, and F. Jacob (1983) Heat shock proteins, first major products of zygotic gene activity in mouse exnbryo. Nature 305:331–332.

    Article  CAS  Google Scholar 

  6. Berenblum, I. (1982) Sequential aspects of chemical carcinogenesis: Skin. In Cancer: A Comprehensive Treatise, Vol. 1, F.F. Becker, ed. I Plenum Press, New York.

    Google Scholar 

  7. Boehm, L.J., and D. Drahovsky (1983) Alteration of enzymatic methyla- tion of DNA cytosines by chemical carcinogens: A mechanism involved in the initiation of carcinogenesis. J. Natl. Cancer Inst. 71:429–434.

    CAS  Google Scholar 

  8. Boeke, J.D., D.J. Garfinkel, C.A. Styles, and G.R. Fink (1985) Ty elements transpose through an RNA intermediate. Cell 40:491–500.

    Article  CAS  Google Scholar 

  9. Botchan, M., W. Topp, and J. Sambrook (1978) Studies on SV40 excision from cellular chromosomes. Cold Spring Harbor Symp. Quant. Biol. 43: 709–719.

    Article  Google Scholar 

  10. Capon, D.J., E.Y. Chen, A.D. Levinson, P.H. Seeburg, and D.V. Goeddel (1983) Complete nucleotide sequences of the T24 human bladder carcinoma oncogene and its normal homologue. Nature 302:33–37.

    Article  CAS  Google Scholar 

  11. Collins, A. (1983) DNA repair in ultraviolet-irradiated HeLa cells is disrupted by aphidicolin. Biochim. Biophys. Acta 741:341–347.

    CAS  Google Scholar 

  12. Coohill, T.P., and S.P. Moore (1983) An SV40 mammalian inductest for putative carcinogens. Mutat. Res. Lett. 113:431–440.

    CAS  Google Scholar 

  13. Cornells, J.J., Z.Z. Su, and J. Rommelaire (1982) Direct and indirect effects of ultraviolet light on the mutagenesis of parvovirus H-1 in human cells. EMBO J. 1:693–699.

    Google Scholar 

  14. Criessen, D., and S. Shall (1982) Regulation of DNA ligase activity by poly (ADP) ribose. Nature 296:271–272.

    Article  Google Scholar 

  15. DasGupta, U.B., and W.C. Summers (1978) Ultraviolet re-activation of herpes simplex virus is mutagenic and inducible in mammalian cells. Proc. Natl. Acad. Sci., USA 75:2378–2381.

    Article  CAS  Google Scholar 

  16. Di Nocera, P.P., and I.B. Dawid (1983) Transient expression of genes introduced into cultured cells of Drosophila. Proc. Natl. Acad. Sci., USA 80:7095–7098.

    Article  Google Scholar 

  17. Doll, R., and R. Peto (1978) Cigarette smoking and bronchial carcinoma: Dose and time relationships among regular and lifelong non-smok- ers. J. Epidem. Comm. Health 32:303–313.

    Article  CAS  Google Scholar 

  18. Farzaneh, F., R. Zalin, D. Brill, and S. Shall (1982) DNA strand breaks and ADP-ribosyl transferase activation during cell differentiation. Nature 300:362–366.

    Article  CAS  Google Scholar 

  19. Fisher, P.B., and I.B. Weinstein (1980) Chemical-viral interactions and multistep aspects of cell transformation. In Molecular and Cellular Aspects of Carcinogen Screening Test, R. Montesanto, L. Bartsch, and L. Tomatis, eds. lARC Scient. Publ., 37, Lyon, France.

    Google Scholar 

  20. Fogel, M. (1972) Induction of viral synthesis in polyoma transformed cells by DNA anti-metabolites and by irradiation after pre-treatment by 5-bromodeoxyuridine. Virology 49:12–22.

    Article  CAS  Google Scholar 

  21. Franza, B.R., and J.I. Garrels (1984) Transformation-sensitive proteins of REF52 cells detected by computer-analyzed two-dimensional gel electrophoresis. In Cancer Cells I The Transformed Phenotype, A. Levine, G.F. Vande Woude, W.C. Topp, and J.D. Watson, eds. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp. 137–145.

    Google Scholar 

  22. Garrels, J.I. (1979) Two dimensional gel electrophoresis and computer analysis of proteins synthesized by clonal cell lines. J. Biol. Chem. 254:7961.

    CAS  Google Scholar 

  23. Garrels, J.I. (1983) Quantitative two-dimensional gel electrophoresis of proteins. Methods Enzymol. 100:411–417.

    Article  CAS  Google Scholar 

  24. Garrels, J.I., J.T. Farrar, and C.B. Burwell (1984) The QUEST system for computer analyzed two-dimensional gel electrophoresis of proteins. In Two-dimensional Gel Electrophoresis of Proteins; Methods and Applications, J.E. Gelis and R. Bravo, eds. Academic Press, New York, pp. 37–91.

    Google Scholar 

  25. Gattoni, S., V. Colantuoni, and C. Basilico (1980) Relationship between integrated and non-integrated viral DNA in rat cells transformed by polyoma virus. J. Virol. 34:615–626.

    CAS  Google Scholar 

  26. Gattoni-Celli, S., W.L. Hsiao, and I.B. Weinstein (1983) Re-arranged c-mos locus in a MOPC-21 murine myeloma cell line and its persistence in hybridomas. Nature 306:795–796.

    Article  CAS  Google Scholar 

  27. Goldschmidt, R., and L.K. Peternick (1947) The genetic background of chemically induced phenocopies in Drosophila. J. Exp. Zool. 135:127- 202.

    Google Scholar 

  28. Gorman, C.M., L.F. Moffat, and B.H. Howard (1982) Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044–1051.

    CAS  Google Scholar 

  29. Groudine, M., and S. Collins (1982) Amplification of endogenous myc- related DNA sequences in a human myeloid leukemia cell line. Nature 298:679–681.

    Article  Google Scholar 

  30. Grunberger, D., and R.M. Santella (1983) Conformational changes in DNA induced by chemical carcinogens. In Genes and Proteins in Oncogenesis, I.B. Weinstein and H. Vogel, eds. Academic Press, New York, pp. 13–40.

    Google Scholar 

  31. Guerrero, I., A. Villasante, V. Corces, and A. Pellicer (1984) Activation of a c-K-ras oncogene by somatic mutation in mouse Ijnnphomas induced by gamma radiation. Nature 304:1159–1162.

    Google Scholar 

  32. Ivanovic, V., and I.B. Weinstein (1980) Genetic factors in Escherichia coli that affect cell killing and mutagenesis induced by benzo(a)py- rene 7,8-dihydrodiol,9,10-oxide. Cancer Res. 40:3508–3511.

    CAS  Google Scholar 

  33. Ivarie, R.D., and J.A. Morris (1982) Induction of prolactin-deficient variants of G3 rat pituitary tumor cells by ethyl methanesulfonate: Reversion by 5-azacytidine, a DNA methylation inhibitor. Proc. Natl. Acad. Sci., USA 79:2967–2970.

    Article  CAS  Google Scholar 

  34. Jeffrey, A.M., T. Kinoshita, R.M. Santella, D. Grunberger, L. Katz, and I.B. Weinstein (1980) The chemistry of polycyclic aromatic hydrocarbon DNA adducts. In Carcinogenesis; Fundamental Mechanisms and Environmental Effects, B. Pullman, P.O.P. Ts’O, and H. Gelboin, eds. Reidel Publishing Co., Amsterdam, pp. 565–579.

    Chapter  Google Scholar 

  35. Jones, C., and R.T. Su (1982) DNA polymerase alpha from the nuclear matrix of cells infected with simian virus 40. Nucl. Acids Res. 10: 5517–5532.

    Article  CAS  Google Scholar 

  36. Kelley, P.M., and M.J. Schlesinger (1982) Antibodies to two major chicken heat shock proteins cross-react with similar proteins in widely divergent species. Mol. Cell. Biol. 2:267–274.

    CAS  Google Scholar 

  37. Kennedy, A.R. (1985) Evidence that the first step leading to carcinogen induced malignant transformation is a high frequency, coiranon event. In Cell Transformation Assays: Application to Studies of Mechanisms of Carcinogenesis and to Carcinogen Testing, J.C. Barrett, ed. Raven Press, New York (in press).

    Google Scholar 

  38. Kirschmeier, P., S. Gattoni-Celli, D. Dina, and I.B. Weinstein (1982) Carcinogen and radiation transformed C3H lOTl/2 cells contain RNA’s homologous to the long terminal repeat sequences of a murine leukemia virus. Proc. Natl. Acad. Sci., USA 79:2773–2777.

    Article  CAS  Google Scholar 

  39. Kohl, N.E., N. Kanda, R.R. Schreck, G. Bruns, S. Latt, F. Gilbert, and F.W. Alt (1983) Transposition and amplification of oncogene related sequences in human neuroblastomas. Cell 35:359–367.

    Article  CAS  Google Scholar 

  40. Kunz, B.A. (1982) Genetic effects of deoxyribonucleotide pool imbalances. Environ. Mutag. 4:695–725.

    CAS  Google Scholar 

  41. Lambert, M.E., S. Gattoni-Celli, P. Kirschmeier, and I.B. Weinstein (1983) Benzo(a)pyrene induction of extrachromosomal viral DNA synthesis in rat cells transformed by polyoma virus. Carcinogenesis 4:587–593.

    Article  CAS  Google Scholar 

  42. Lavi, S. (1981) Carcinogen-mediated amplification of viral DNA se quences in simian virus 40 transformed Chinese hamster embryo cells. Proc. Natl. Acad. Sci., USA 78:6144–6148.

    Article  CAS  Google Scholar 

  43. Lavi, S., N. Kohn, T. Kleinberger, Y. Berko, and S. Etkin (1983) Am plification of SV40 and cellular genes in SV40 transformed Chinese hamster embryo cells treated with chemical carcinogens. In Cellular Responses to DNA Damage, E. Friedberg and B. Bridges, eds. Alan R. Liss, Inc., New York, pp. 659–670.

    Google Scholar 

  44. Li, G.C., N.S. Petersen, and H.K. Mitchell (1982) Induced thermal tolerance and heat shock protein synthesis in CHO cells. Int. J. Rad. Oncol. Biol. Phys. 8:63–67.

    Article  CAS  Google Scholar 

  45. Lieberman, M.W., L.R. Beach, and R.D. Palmiter (1983) Ultraviolet radiation-induced metallothionein-I gene activation is associated with extensive DNA demethylation. Cell 35:207–214.

    Article  CAS  Google Scholar 

  46. Lowe, D.G., W.D. Fulford, and L.A. Moran (1983) Mouse and Drosophila genes encoding the major heat shock protein (hsp70) are highly conserved. Mol. Cell. Biol. 3:1540–1543.

    CAS  Google Scholar 

  47. Lowy, D.R., W.P. Rowe, N. Teich, and J. Hartley (1971) Murine leukemia virus: High frequency activation in vitro by 5-iododeoxyuridine and 5-bromodeoxyuridine. Science 174:155–156.

    Article  CAS  Google Scholar 

  48. Matz, B., J.R. Schlehofer, and H. zurHausen (1984) Identification of a gene function of Herpes Simplex Virus Type 1 essential for amplification of simian virus 40 DNA sequences in transformed hamster cells. Virology 134:328–337.

    Article  CAS  Google Scholar 

  49. McClanahan, T., and K. McEntee (1984) Specific transcripts are elevated in Saccharomyces cerevisiae in response to DNA damage. Mol. Cell. Biol. 4:2356–2363.

    CAS  Google Scholar 

  50. McDonald, J. (1983) The molecular basis of adaptation: A critical review of relevant ideas and observations. Ann. Rev. Ecol. Systm. 14: 77–102.

    Article  Google Scholar 

  51. Miskin, R., and E. Reich (1980) Plasminogen activator: Induction of synthesis by DNA damage. Cell 19:217–224.

    Article  CAS  Google Scholar 

  52. Mitchell, R.E.J., and D.P. Morrison (1982) Heat shock induction of ionizing radiation resistance in Saccharomyces cerevisiae and correlation with stationary growth phase. Radiat. Res. 90:284–291.

    Article  Google Scholar 

  53. Mulligan, R.C., and P. Berg (1981) Selection for animal cells that express the Escherichia coli gene coding for xanthine-guanine phosphori- bosyltransferase. Proc. Natl. Acad. Sci., USA 7:2072–2076.

    Article  Google Scholar 

  54. Nomura, S., and M. Gisha (1984) ÜV irradiation induces an activity which stimulates simian virus 40 rescue upon cell fusion. Mol. Cell. Biol. 4:1159–1162.

    CAS  Google Scholar 

  55. Notario, V., S. Sukumar, E. Santos, and M. Barbacid (1984) A common mechanism for the malignant activation of ras oncogenes in human neoplasia and in chemically induced animal tumors. In Cancer Cells, Vol. II, G. Vande Woude and A.J. Levine, eds. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp. 425–432.

    Google Scholar 

  56. Paquin, C.E., and V.M. Williamson (1984) Temperature effects on the rate of Ty transposition. Science 226:53–55.

    Article  CAS  Google Scholar 

  57. Parker, C.S., and J. Topol (1984) A Drosophila RNA polymerase II transcription factor binds to the regulatory site of an hsp 70 gene. Cell 37:273–283.

    Article  CAS  Google Scholar 

  58. Pearson, M.N., J.J. Karchesy, A. Deeney, M.L. Dwinzer, and G.S. Beaudreau (1984) Induction of endogenous avian tumor virus gene expression by pyrrolizidine alkaloids. Chem. Biol. Interact. 49:341–350.

    Article  CAS  Google Scholar 

  59. Pelham, H.R.B. (1982) A regulatory upstream promoter element in the Drosophila hsp70 heat shock gene. Cell 3:517–528.

    Article  Google Scholar 

  60. Pellegrini, S., L. Dailey, and C. Basilico (1984) Amplification and excision of integrated polyoma DNA sequences require a functional origin of replication. Cell 36:943–949.

    Article  CAS  Google Scholar 

  61. Peterson, A.R., and V. Klement (1985) Oncogenic transformation of C3H/10T1/2 cells: Methods and mechanisms. In Cell Transformation Assays, J.C. Barrett and R. Tennant, eds. Raven Press, New York (in press).

    Google Scholar 

  62. Pfister, H., A. Gassenmaier, F. Nurnbergen, and G. Stuggen (1983) HPV-5 DNA in a carcinoma of an epidermodysplasia verruciformis patient infected with various human papillomavirus types. Cancer Res. 43:1436–1441.

    CAS  Google Scholar 

  63. Potter, S.S., W.J. Brorein, Jr., P. Dunsmuir, and G.M. Rubin (1979) Transposition of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell 17:415–427.

    Article  CAS  Google Scholar 

  64. Prasad, I., D. Zouzias, and C. Basilico (1976) State of the viral DNA in rat cells transformed by polyoma virus I. Virus rescue and the presence of non-integrated viral DNA molecules. J. Virol. 18:436–444.

    CAS  Google Scholar 

  65. Prieto-Soto, A., B. Gourlie, M. Miwa, V. Pigiet, T. Sugimura, N. Malik, and M. Smulson (1983) Polyoma virus minichromosomes: Poly ADP- ribosylation of associated chromatin proteins. J. Virol. 45:600–606.

    CAS  Google Scholar 

  66. Rahmsdorf, H.J., U. Mallick, H. Ponta, and P. Herrlich (1982) A B-lym- phocyte specific high turnover protein: Constitutive expression in resting B cells and induction of synthesis in proliferating cells. Cell 29:459–468.

    Article  CAS  Google Scholar 

  67. Rechavi, G., A. Givol, and L. Canaani (1982) Activation of a cellular oncogene by DNA re-arrangement: Possible involvement of an IS-like element. Nature 300:607–611.

    Article  CAS  Google Scholar 

  68. Rubin, J.S., V.R. Prideaux, H.F. Willard, A.M. Dulhanty, G.F. Whitmore, and A. Bernstein (1985) Molecular cloning and chromosomal localization of DNA sequences associated with a human DNA repair gene. Mol. Cell. Biol. 5:398–405.

    CAS  Google Scholar 

  69. Ryo, H., M.A. Yoo, K. Fujikawa, and S. Kondo (1985) Comparison of somatic reversions between the ivory allele and transposon-caused mutant alleles at the white locus of Drosophlla melanogaster after larval treatment with X-rays and ethyl methanesulfonate. Genetics 110:441–451.

    CAS  Google Scholar 

  70. Sarasin, A., F. Bourre, and A. Benoit (1982) Error prone replication of ultraviolet-irradiated simian virus 40 in carcinogen treated monkey kidney cells. Biochemie 64:815–821.

    Article  CAS  Google Scholar 

  71. Schimke, R.T. (1984) Gene amplification in cultured animal cells. Cell 37:705–713.

    Article  CAS  Google Scholar 

  72. Schorpp, M., U. Mallick, H.J. Rahmsdorf, and J. Herrlich (1984) UV-in- duced extracellular factor from human-fibroblasts communicates the UV response to non-irradiated cells. Cell 37:861–868.

    Article  CAS  Google Scholar 

  73. Strand, D.J., and J.F. McDonald (1985) Copia is transcriptionally responsive to environmental stress. Nucl. Acids Res. 13:4401–4410.

    Article  CAS  Google Scholar 

  74. Tlsty, T.D., P.C. Brown, and R.T. Schimke (1984) UV radiation facilitates methotrexate resistance and amplification of the dihydrofolate reductase gene in cultured 3T6 mouse cells, Mol. Cell. Biol. 4:1050–1056.

    CAS  Google Scholar 

  75. Van der Ploeg, L.H.T., S.H. Giannini, and C.R. Cantor (1985) Heat shock genes: Regulatory role for differentiation in parasitic protozoa. Science 228:1443–1446.

    Article  Google Scholar 

  76. Velazquez, J.M., and S. Lindquist (1984) Hsp70: Nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 36:655–662.

    Article  CAS  Google Scholar 

  77. Weinstein, I.B. (1981) Current concepts and controversies in chemical carcinogenesis. J. Supramol. Struct. Cell. Biochem. 17:99–120.

    Article  CAS  Google Scholar 

  78. Weinstein, I.B., J. Arcoleo, M. Lambert, W. Hsiao, S. Gattoni-Celli, A. Jeffrey, and P. Kirschmeier (1985) Molecular mechanisms of multistage chemical carcinogenesis. In Molecular Biology of Tumor Cells, B. Wahren et al., eds. Raven Press, New York, pp. 55–70.

    Google Scholar 

  79. Weinstein, I.B., S. Gattoni-Celli, P. Kirschmeier, M. Lambert, W. L.-W. Hsiao, J. Backer, and A. Jeffrey (1984) Multistage carcinogenesis involves multiple genes and multiple mechanisms. In Cancer Cells I/The Transformed Phenotype, A. Levine, G.F. Vande Woude, W.C. Topp, and J.D. Watson, eds. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp. 229–237.

    Google Scholar 

  80. Wilson, V.L., and P.A. Jones (1983) Inhibition of DNA methylation by chemical carcinogens in vitro. Cell 32:329–346.

    Article  Google Scholar 

  81. Witkin, E. (1985) The SOS response: Implications for cancer. In Genes and Cancer, J.M. Bishop, J. Rowley, and M. Greaves, eds. Alan R. Liss, Inc., New York, pp. 99–115.

    Google Scholar 

  82. Yavelow, J., M. Collins, Y. Birk, W. Troll, and A.R. Kennedy (1985) Nanomolar concentrations of Bowman-Birk soybean protease inhibitor suppress X-ray induced transformation in vitro. Proc. Natl. Acad. Sci., USA (in press).

    Google Scholar 

  83. Yu, L.Z., J.J. Cornells, J.M. Vos, and J. Rommelaire (1982) U.V.-enhanced reactivation of capsid protein synthesis and infectious centre formation in mouse cells infected with U.V.-irradiated minute-virus- of-mice. Int. J. Radiat. Biol. 41:119–126.

    Article  CAS  Google Scholar 

  84. Zimmerman, W., and A. Weissbach (1981) Participation of deoxyribonucleic acid polymerase-alpha in amplifications of ribosomal deoxyribonucleic acid in Xenopus laevis. Mol. Cell. Biol. 1:680–686.

    Google Scholar 

  85. Zuker, C., J. Capello, R.L. Chisholm, and H. Lodish (1983) A repetitive Dictyostelium gene family that is induced during differentiation and by heat shock. Cell 34:997–1005.

    Article  CAS  Google Scholar 

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Lambert, M.E., Garrels, J.I., McDonald, J., Weinstein, I.B. (1986). Inducible Cellular Responses to DNA Damage in Mammalian Cells. In: Shankel, D.M., Hartman, P.E., Kada, T., Hollaender, A., Wilson, C.M., Kuny, G. (eds) Antimutagenesis and Anticarcinogenesis Mechanisms. Basic Life Sciences, vol 39. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5182-5_25

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