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DNA Repair Enzymes in Mammalian Cells

  • Errol C. Friedberg
  • Kern H. Cook
  • James Duncan
  • Kristien Mortelmans

Abstract

In the past two decades, considerable strides have been made in understanding the phenomenon of DNA damage and its repair at all levels of biological organization. Studies on living cells using prokaryote models have been extensively reviewed by a number of authors (Town et al., 1973; Setlow and Setlow, 1972; Smith, 1971; Witkin, 1969; Hanawalt, 1968; Howard-Flanders, 1968; Strauss, 1968). In recent years, considerable emphasis has been placed on DNA repair in mammalian systems, and this area of investigation too has been the subject of a number of review articles (Cleaver and Bootsma, 1975; Cleaver, 1974a; Strauss, 1974; Painter, 1970). Closely paralleling these biological studies, there have been significant efforts made to identify, purify, and characterize the numerous enzymatic and nonenzymatic components involved in the molecular mechanisms of DNA repair. These efforts have enjoyed particular success in prokaryote models such as Micrococcus luteus, Escherichia coli, and phage T4-infected E. coli (for recent reviews, see Grossman et al., 1975; Grossman, 1974). The present chapter addresses itself to a review of mammalian cell enzymes that may be significant in DNA repair. Where appropriate, we have discussed aspects of prokaryote enzymology that have not received much attention in the literature, and that are, or may be, directly relevant to mammalian repair systems.

Keywords

Excision Repair Ataxia Telangiectasia Xeroderma Pigmentosum Endonuclease Activity Pyrimidine Dimer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Bacchetti, S., and Benne, R., 1975, Purification and characterization of an endonuclease from calf thymus acting on irradiated DNA, Biochim. Biophys. Acta 390:285–297.Google Scholar
  2. Bacchetti, S., Van der Plas, A., and Veldhuisen, G., 1972, A UV-specific endonucleolytic activity present in human cell extracts, Biochem. Biophys. Res. Commun. 48:662–669.Google Scholar
  3. Beard, P., 1972, Polynucleotide ligase in mouse cells infected by polyoma virus, Biochim. Biophys. Acta 269:385–396.Google Scholar
  4. Bertazzoni, U., Mathelet, M., and Campagnari, F., 1972, Purification and properties of a polynucleotide ligase from calf thymus glands, Biochim. Biophys. Acta 287:404–414.Google Scholar
  5. Bertazzoni, U., Stefanini, M., Pedrali Noy, E. G., Nuzzo, F., Falaschi, A., and Spadari, S., 1976, Variations of DNA polymerases α and β during prolonged stimulation of human lymphocytes, Proc. Natl. Acad. Sci. USA 73:785–789.Google Scholar
  6. Bloom, G. E., Warner, S., Gerald, P. S., and Diamond, L. K., 1966, Chromosome abnormalities in constitutional aplastic anemia, N. Engl. J. Med. 274:8–14.Google Scholar
  7. Boyce, R. P., and Howard-Flanders, P., 1964, Release of ultraviolet light-induced thymine dimers from DNA in E. coli, Proc. Natl. Acad. Sci. USA 51:293–300.Google Scholar
  8. Brent, T. P., 1972, Repair enzyme suggested by mammalian endonuclease activity specific for ultraviolet-irradiated DNA, Nature (London) New Biol. 239:172–173.Google Scholar
  9. Brent, T. P., 1973, A human endonuclease activity for gamma-irradiated DNA, Biophys. J. 13:399–401.Google Scholar
  10. Brent, T. P., 1975, Partial purification of endonuclease activity from human lymphoblasts. Separation of activities for depurinated DNA and DNA irradiated with ultraviolet light, Biochim. Biophys. Acta 407:191–199.Google Scholar
  11. Burt, D. H., and Brent, T. P., 1971, A deoxyribonuclease activity of HeLa cells specific for UV-irradiated DNA, Biochem. Biophys. Res. Commun. 43:1382–1387.Google Scholar
  12. Byrnes, J. J., Downey, K. M., and So, A. G., 1973, Bone marrow cytoplasmic deoxyribonucleic acid polymerase. Variation of pH and ionic environment as a possible control mechanism, Biochemistry 12:4378–4384.Google Scholar
  13. Capps, M. J., O’Connor, P. J., and Craig, A. W., 1973, The influence of liver regeneration on the stability of 7-methylguanine in rat liver DNA after treatment with N,N-dimethyl-nitrosamine, Biochim. Biophys. Acta 331:33–40.Google Scholar
  14. Cerutti, P., 1975, Repairable damage in DNA: Overview, in: Molecular Mechanisms for Repair of DNA (P. C. Hanawalt and R. B. Setlow, eds.), pp. 3–12, Plenum Press, New York.Google Scholar
  15. Chang, L. M. S., and Bollum, F. J., 1972, Low molecular weight deoxyribonucleic acid polymerase from rabbit bone marrow, Biochemistry 11:1264–1272.Google Scholar
  16. Chang, L. M. S., and Bollum, F. J., 1973, A comparison of associated enzyme activities in various deoxyribonucleic acid polymerases, J. Biol. Chem. 248:3398–3404.Google Scholar
  17. Cleaver, J. E., 1968, Defective repair replication of DNA in xeroderma pigmentosum, Nature (London) 218:652–656.Google Scholar
  18. Cleaver, J. E., 1969, Xeroderma pigmentosum: A human disease in which an initial stage of DNA repair is defective, Proc. Natl. Acad. Sci. USA 63:428–435.Google Scholar
  19. Cleaver, J. E., 1971, Repair of alkylation damage in ultraviolet-sensitive (xeroderma pigmentosum) human cells, Mutat. Res. 12:453–462.Google Scholar
  20. Cleaver, J. E., 1973, DNA repair with purines and pyrimidines in radiation-and carcinogen-damaged normal and xeroderma pigmentosum cells, Cancer Res. 33:362–369.Google Scholar
  21. Cleaver, J. E., 1914a, Repair processes for photochemical damage in mammalian cells, Adv. Radiat. Biol. 4:1–76.Google Scholar
  22. Cleaver, J. E., 1914b, Sedimentation of DNA from human fibroblasts irradiated with ultraviolet light: Possible detection of excision breaks in normal and repair-deficient xeroderma pigmentosum cells, Radiat. Res. 57:207–227.Google Scholar
  23. Cleaver, J. E., and Bootsma, D., 1975, Xeroderma pigmentosum—biochemical and genetic characteristics, Annu. Rev. Genet. 9:19–38.Google Scholar
  24. Cleaver, J. E., and Trosko, J. E., 1970, Absence of excision of ultraviolet-induced cyclobutane dimers in xeroderma pigmentosum, Photochem. Photobiol. 11:547–550.Google Scholar
  25. Cleaver, J. E., Bootsma, D., and Friedberg, E. C., 1975, Human diseases with genetically altered DNA repair processes, Genetics 79:215–225.Google Scholar
  26. Cleaver, J. E., Paterson, M., and Friedberg, E. C., 1976, Absence of photoenzymatic monomerisation of pyrimidine dimers in normal and xeroderma pigmentosum cells, Biophys. J. 16:185a.Google Scholar
  27. Cook, J. S., 1970, Photoreactivation in animal cells, Photophysiology 5:191–233.Google Scholar
  28. Cook, J. S., and McGrath, J. R., 1967, Photoreactivating enzyme activity in metazoa, Proc. Natl. Acad. Sci. USA 58:1359–1365.Google Scholar
  29. Cook, K. H., and Friedberg, E. C., 1976, Measurement of thymine dimers in DNA by thin-layer chromatography. II. The use of one-dimensional systems. Anal. Biochem. 73:411–418.Google Scholar
  30. Cook, K., Friedberg, E. C., Cleaver, J. E., and Slor, H., 1975, Excision of thymine dimers from specifically incised DNA by extracts of xeroderma pigmentosum cells, Nature (London) 256:235–236.Google Scholar
  31. Cunliffe, P. N., Mann, J. R., Cameron, A. H., Roberts, K. D., and Ward, H. W. C., 1975, Radiosensitivity in ataxia-telengiectasia, Br. J. Radiol. 48:374–376.Google Scholar
  32. Cunningham, L., and Laskowski, M., 1953, Presence of two different desoxyribonucleodepolymerases in veal kidney, Biochim. Biophys. Acta 11:590–591.Google Scholar
  33. Daniels, M., Scholes, G., and Weiss, J. J., 1956, Chemical action of ionizing radiations in solutions. Part XVI. Formation of labile phosphate esters from purine and pyrimidine ribonucleotides by irradiation with X-rays in aqueous solution, J. Chem. Soc. (London), 3771-3779.Google Scholar
  34. Day, R., III, 1975, The use of human adenovirus 2 in the study of the xeroderma DNA-repair defect, Molecular Mechanisms for the Repair of DNA (P. C. Hanawalt and R. B. Setlow, ed.), pp. 747–752, Plenum, New York.Google Scholar
  35. Doniger, J., and Grossman, L., 1975, The characterization of an exonuclease purified from human placenta capable of pyrimidine dimer excision, Biophys. J. 15:297a.Google Scholar
  36. Ducolomb, R., Cadet, J., and Teoule, R., 1974, Irradiation γ de l’acide uridylique-rupture de la liaison N-glycosidique, Int. J. Radiat. Biol. 25:139–149.Google Scholar
  37. Duker, N. J., and Tabor, G. W., 1975, Different ultraviolet DNA endonuclease activity in human cells, Nature 255:82–84.Google Scholar
  38. Duncan, J., Slor, H., Cook, K., and Friedberg, E. C., 1975, Thymine dimer excision by extracts of human cells, in: Molecular Mechanisms for Repair of DNA (P. C. Hanawalt and R. B. Setlow, ed.), pp. 643–649, Plenum, New York.Google Scholar
  39. Duncan, J. A., Hamilton, L. D., and Friedberg, E. C., 1976, The enzymatic degradation of uracil-containing DNA. II. Evidence for N-glycosidase and nuclease activities in unfractionated extracts of B. subtilis, J. Virology (in press).Google Scholar
  40. Epstein, W. L., Fukuyama, K., and Epstein, J., 1971, Ultraviolet light, DNA repair and skin carcinogenesis in man, Fed. Proc. 30:1766–1771.Google Scholar
  41. Eron, L. J., and McAuslan, B. R., 1966, The nature of pox-virus induced deoxyribonucleases, Biochem. Biophys. Res. Commun. 22:518–523.Google Scholar
  42. Fanconi, G., 1927, Familiarer infantile perniziosaartige anämie (perniziöses blutbild und konstitution), Jahrb. Kinderheilkd. 117:257–280.Google Scholar
  43. Fanconi, G., 1967, Familial constitutional panmyelocytopathy, Fanconi’s anemia (FA). I. Clinical Aspects, Semin. Hematol. 4:233–240.Google Scholar
  44. Fansler, B. S., 1974, Eukaryotic DNA polymerases: Their association with the nucleus and relationship to DNA replication, Int. Rev. Cytol. Supp. 4:363–415.Google Scholar
  45. Frei, J. V., and Lawley, P. D., 1975, Methylation of DNA in various organs of C57B1 mice by a carcinogenic dose of N-methyl-N-nitrosourea and stability of some methylation products up to 18 hours, Chem. Biol. Interact. 10:413–427.Google Scholar
  46. Fridlender, B., Fry, M., Bolden, A., and Weissbach, A., 1972, A new synthetic RNA-dependent DNA polymerase from human tissue culture cells, Proc. Natl. Acad. Sci. USA 69:452–455.Google Scholar
  47. Friedberg, E. C., 1975, DNA repair of ultraviolet-irradiated bacteriophage T4, Photochem. Photobiol. 21:271–289.Google Scholar
  48. Friedberg, E. C., and Clayton, D. A., 1972, Electron microscopic studies on substrate specificity of T4 excision repair endonuclease, Nature (London) 237:99–103.Google Scholar
  49. Friedberg, E. C., and Goldthwait, D. A., 1969, Endonuclease II of E. coli. I. Isolation and purification, Proc. Natl. Acad. Sci. USA 62:934–940.Google Scholar
  50. Friedberg, E. C., and Lehman, I. R., 1974, Excision of thymine dimers by proteolytic and amber fragments of E. coli DNA polymerase I, Biochem. Biophys. Res. Commun. 58:132–139.Google Scholar
  51. Friedberg, E. C., Hadi, S., and Goldthwait, D. A., 1969, Endonuclease II of E. coli. II. Enzyme properties and studies on the degradation of alkylated and native deoxyribonucleic acid, J. Biol. Chem. 244:5879–5889.Google Scholar
  52. Friedberg, E. C., Duncan, J., and Cleaver, J. E., 1974, Thymine dimer excision nuclease in extracts of human cells, Radiat. Res. 59:98.Google Scholar
  53. Friedberg, E. C., Ganesan, A. K., and Minton, K., 1975, N-Glycosidase activity in extracts of Bacillus subtilis and its inhibition after infection with bacteriophage PBS2, J. Virol. 16:315–321.Google Scholar
  54. Geliert, M., 1967, Formation of covalent circles of lambda DNA by E. coli extracts, Proc. Natl. Acad. Sci. USA 57:148–155.Google Scholar
  55. Georgatsos, J. G., and Symeonidis, A., 1965, A deoxyribonuclease from mammary tumors of C3H mice preferentially hydrolyzing heat-denatured DNA, Nature (London) 206:1362–1363.Google Scholar
  56. German, J., 1972, Genes which increase chromosomal instability in somatic cells and predispose to cancer, Prog. Med. Genet. 8:61–101.Google Scholar
  57. Gotoff, S. P., Amirmokri, E., and Liebner, E. J., 1967, Ataxia telangiectasia: Neoplasia, untoward response to X-irradiation, and tuberous sclerosis, Am. J. Dis. Child. 114:617–625.Google Scholar
  58. Greer, S., and Zamenhof, S., 1962, Studies on depurination of DNA by heat, J. Mol. Biol. 4:123–141.Google Scholar
  59. Grossman, L., 1974, Enzymes involved in the repair of DNA, Adv. Radiat. Biol. 4:77–129.Google Scholar
  60. Grossman, L., 1975, Excision repair of DNA, in: DNA Synthesis and Its Regulation (M. Goulian and P. C. Hanawalt, eds.), pp. 791–814, W. A. Benjamin, San Francisco.Google Scholar
  61. Grossman, L., Kaplan, J. C., Kushner, S. R., and Mahler, I., 1968, Enzymes involved in the early stages of repair of ultraviolet-irradiated DNA, Cold Spring Harbor Symp. Quant. Biol. 33:229–234.Google Scholar
  62. Grossman, L., Braun, A., Feldberg, R., and Mahler, I., 1975, Enzymatic repair of DNA, Annu. Rev. Biochem. 44:19–43.Google Scholar
  63. Hadi, S., and Goldthwait, D. A., 1971, Endonuclease II of Escherichia coli: Degradation of partially depurinated deoxyribonucleic acid, Biochemistry 10:4986–4994.Google Scholar
  64. Hadi, S., Kirtikar, D. M., and Goldthwait, D. A., 1973, Endonuclease II of Escherichia coli: degradation of double and single-stranded deoxyribonucleic acid, Biochemistry 12:2747–2754.Google Scholar
  65. Hanawalt, P. C., 1968, Cellular recovery from photochemical damage, Photophysiology 4:203–251.Google Scholar
  66. Hariharan, P., and Cerutti, P., 1971, Repair of γ-ray-induced thymine damage in Micrococcus radiodurans, Nature (London) New Biol. 229:247–249.Google Scholar
  67. Hariharan, P., and Cerutti, P., 1972, Formation and repair of γ-ray-induced thymine damage in Micrococcus radiodurans, J. Mol. Biol. 66:65–81.Google Scholar
  68. Hariharan, P. V., and Cerutti, P. A., 1974a, Excision of damaged thymine residues from gamma-irradiated poly(dA-dT) by crude extracts of Escherichia coli, Proc. Natl. Acad. Sci. USA 71:3532–3536.Google Scholar
  69. Hariharan, P. V., and Cerutti, P. A., 1974b, The incision and strand rejoining step in the excision repair of 5,6-dihydroxy-dihydrothymine by crude E. coli extracts, Biochem. Biophys. Res. Commun. 61:375–379.Google Scholar
  70. Harm, H., 1974, Biological action of DNA photoreactivating enzyme from mammalian cells, Abst. Am. Soc. Photobiol., p. 137.Google Scholar
  71. Harnden, D. G., 1974, Ataxia telangiectasia syndrome: Cytogenetic and cancer aspects, Chromosomes and Cancer (J. German, ed.), pp. 619–636, Wiley, New York.Google Scholar
  72. Hart, R. W., and Setlow, R. B., 1973, Evidence for a role of UV-induced pyrimidine dimers in malignant transformation, Abst. Am. Soc. Photobiol., p. 120.Google Scholar
  73. Hart, R. W., and Setlow, R. B., 1975, Direct evidence that pyrimidine dimers in DNA result in neoplastic transformation, in: Molecular Mechanisms for Repair in DNA (P. C. Hanawalt and R. B. Setlow, eds.), pp. 719–728, Plenum Press, New York.Google Scholar
  74. Haynes, R. H., 1966, The interpretation of microbial inactivation and recovery phenomena, Radiat. Res. Suppl. 6:1–29.Google Scholar
  75. Higurashi, M., and Conen, P. E., 1973, In vitro chromosomal radiosensitivity in “chromosomal breakage syndromes,” Cancer 32:380–383.Google Scholar
  76. Howard-Flanders, P., 1968, DNA repair, Annu. Rev. Biochem. 37:175–200.Google Scholar
  77. Howard-Flanders, P., and Boyce, R. P., 1966, DNA repair and genetic recombination: Studies on mutants of Escherichia coli defective in these processes, Radiat. Res. Suppl. 6:156–184.Google Scholar
  78. Huang, P. C., and Vincent, R., Jr., 1975, Repair deficiency and genetic complementarity of fibroblast cells in culture from six xeroderma pigmentosum patients, in: Molecular Mechanisms for the Repair of DNA (eds., P. C. Hanawalt and R. B. Setlow, eds.), pp. 729–733, Plenum Press, New York.Google Scholar
  79. Jacobs, A. J., O’Brien, R. L., Parker, J. W., and Paolilli, P., 1972, Abnormal DNA repair of 4-nitroquinidine-l-oxide damage by lymphocytes in xeroderma pigmentosum, Mutat. Res. 16:420–424.Google Scholar
  80. Keir, H. M., and Smellie, R. M. S., 1962, Intracellular location of DNA nucleotidyl transferase, Nature (London) 196:752–754.Google Scholar
  81. Kirtikar, D. M., and Goldthwait, D. A., 1974, The enzymatic release of O 6-methylguanine and 3-methyladenine from DNA reacted with the carcinogen N-methyl-N-nitrosourea, Proc. Natl. Acad. Sci. USA 71:2022–2026.Google Scholar
  82. Kirtikar, D. M., Dipple, A., and Goldthwait, D. A., 1975a, Endonuclease II of Escherichia coli: DNA reacted with 7-bromomethyl-12-methylbenz[a]anthracene as a substrate, Biochemistry 14:5548–5553.Google Scholar
  83. Kirtikar, D. M., Slaughter, J., and Goldthwait, D. A., 1975b, Endonuclease II of Escherichia coli: Degradation of 7-irradiated DNA, Biochemistry 14:1235–1244.Google Scholar
  84. Kirtikar, D. M., Kuebler, J. P., Dipple, A., and Goldthwait, D. A., 1976, Enzymes involved in repair of DNA damaged by chemical carcinogens and γ-irradiation, in: Cancer Enzymology—8th Miami Winter Symposium (J. Schultz and F. Ahmad, eds.), Academic Press, New York.Google Scholar
  85. Kleijer, W. J., Lehman, P. H. M., Mulder, M. P., and Bootsma, D., 1970, Repair of X-ray damage in DNA of cultivated cells from patients having xeroderma pigmentosum, Mutat. Res. 9:517–523.Google Scholar
  86. Kondo, S., and Jagger, J., 1966, Action spectra for photoreactivation of mutation to prototrophy in strains of Escherichia coli possessing and lacking photoreactivating-enzyme activity, Photochem. Photobiol. 5:189–200.Google Scholar
  87. Kornberg, A., 1974, DNA Synthesis, W. H. Freeman, San Francisco.Google Scholar
  88. Kuhnlein, U., Penhoet, E. E., and Linn, S., 1976, An altered apurinic DNA endonuclease activity in xeroderma pigmentosum fibroblasts, Proc. Natl. Acad. Sci. USA 73: 1169–1173.Google Scholar
  89. Lawley, P. D., 1966, Effects of some chemical mutagens and carcinogens on nucleic acids, Prog. Nucleic Acid Res. Mol. Biol. 5:89–131.Google Scholar
  90. Lawley, P. D., and Brookes, P., 1963, Further studies on the alkylation of nucleic acids and their constituent nucleotides, Biochem. J. 89:127–138.Google Scholar
  91. Lindahl, T., 1970, An exonuclease specific for double-stranded DNA: Deoxyribonuclease IV from rabbit tissues, in: Methods in Enzymology, Vol. 21 (L. Grossman and K. Moldave, eds.), pp. 148–153, Academic Press, New York.Google Scholar
  92. Lindahl, T., 1971, Excision of pyrimidine dimers from ultraviolet-irradiated DNA by exonucleases from mammalian cells, Eur. J. Biochem. 18:407–414.Google Scholar
  93. Lindahl, T., 1972, Mammalian deoxyribonucleases acting on damaged DNA, in: Molecular and Cellular Repair Processes (R. F. Beers, R. M. Herriott, and R. C. Tilghman, eds.), pp. 3–13, Johns Hopkins University Press, Baltimore, Maryland.Google Scholar
  94. Lindahl, T., 1974, An N-glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues, Proc. Natl. Acad. Sci. USA 71:3649–3653.Google Scholar
  95. Lindahl, T., 1976, New class of enzymes acting on damaged DNA, Nature (London) 259:64–66.Google Scholar
  96. Lindahl, T., and Andersson, A., 1972, Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid, Biochemistry 11:3618–3623.Google Scholar
  97. Lindahl, T., and Edelman, G. M., 1968, Polynucleotide ligase from myeloid and lymphoid tissues, Proc. Natl. Acad. Sci. USA 61:680–687.Google Scholar
  98. Lindahl, T., and Karlström, O., 1973, Heat-induced depyrimidination of deoxyribonucleic acid in neutral solution, Biochemistry 12:5151–5154.Google Scholar
  99. Lindahl, T., and Ljungquist, S., 1975, Apurinic and apyrimidinic sites in DNA, in: Molecular Mechanisms for Repair of DNA (P. C. Hanawalt and R. B. Setlow, eds.), pp. 31–38, Plenum Press, New York.Google Scholar
  100. Lindahl, T., and Nyberg, B., 1972, Rate of depurination of native deoxyribonucleic acid, Biochemistry 11:3610–3618.Google Scholar
  101. Lindahl, T., and Nyberg, B., 1974, Heat-induced deamination of cytosine residues in deoxyribonucleic acid, Biochemistry 13:3405–3410.Google Scholar
  102. Lindahl, T., Gaily, J. A., and Edelman, G. M., 1969a, Deoxyribonuclease IV: A new exonuclease from mammalian tissues, Proc. Natl. Acad. Sci. USA 62:597–603.Google Scholar
  103. Lindahl, T., Gaily, J. A., and Edelman, G. M., 1969b, Properties of deoxyribonuclease III from mammalian tissue, J. Biol. Chem. 244:5014–5019.Google Scholar
  104. Ljungquist, S., and Lindahl, T., 1974, A mammalian endonuclease specific for apurinic sites in double-stranded deoxyribonucleic acid. I. Purification and general properties, J. Biol. Chem. 249:1530–1535.Google Scholar
  105. Ljungquist, S., Andersson, A., and Lindahl, T., 1974, A mammalian endonuclease specific for apurinic sites in double-stranded deoxyribonucleic acid. II. Further studies on the substrate specificity, J. Biol. Chem. 249:1536–1540.Google Scholar
  106. Loeb, L. A., 1974, Eucaryotic DNA polymerases, in: The Enzymes, Vol. 10 (P. D. Boyer, ed.), pp. 173–209, Academic Press, New York.Google Scholar
  107. Maher, V. M., Douville, D., Tomura, T., and Van Lancker, J. L., 1974, Mutagenecity of reactive derivatives of carcinogenic hydrocarbons: Evidence of DNA repair, Mutat. Res. 23:113–123.Google Scholar
  108. Maitra, S. C., and Frei, J. V., 1975, Organ-specific effects of DNA methylation by alkylating agents in the inbred Swiss mouse, Chem. Biol. Interact. 10:285–293.Google Scholar
  109. Margison, G. P., and O’Connor, P. J., 1973, Biological implications of the instability of the N-glycosidic bond of 3-methyldeoxyadenosine in DNA, Biochim. Biophys. Acta. 331:349–356.Google Scholar
  110. Mattern, M., Hariharan, P., Dunlop, B., and Cerutti, P., 1973, DNA degradation and excision repair in 7-irradiated Chinese hamster ovary cells, Nature (London) New Biol. 245:230–232.Google Scholar
  111. McFarlin, D. E., Strober, W., and Walmann, T. A., 1972, Ataxia telangiectasia, Medicine 51:281–314.Google Scholar
  112. Morgan, J. L., Holcomb, T. M., and Morrissey, R. W., 1968, Radiation reaction in ataxia telangectasia, Am. J. Dis. Child. 116:557–558.Google Scholar
  113. Morrison, J. M., and Keir, H. M., 1966, Heat sensitive deoxyribonuclease activity in cells infected with herpes simplex virus, Biochim. J. 98:37c–39c.Google Scholar
  114. Morse, L. S., and Pauling, C., 1975, Induction of error-prone repair as a consequence of DNA ligase deficiency in Escherichia coli, Proc. Natl. Acad. Sci. USA 72:4645–4649.Google Scholar
  115. Mortelmans, K., Friedberg, E. C., Slor, H., Thomas, G., and Cleaver, J. E., 1976, Evidence for a defect in thymine dimer excision in extracts of xeroderma pigmentosum cells, Proc. Natl. Acad. Sci. USA 73:2757–2761.Google Scholar
  116. Morton, H., 1970, A survey of commercially available tissue culture media, In Vitro 6:89–108.Google Scholar
  117. Nishioka, H., and Harm, W., 1972, Analysis of photoenzymatic repair of UV lesions in DNA by single light flashes. IX. Excess production of photoreactivating enzyme in E. coli Bs-i 160 under different growth conditions, and its suppression by adenine, Mutat. Res. 16:121–131.Google Scholar
  118. O’Connor, P. J., Capps, M. J., and Craig, A. W., 1973, Comparative studies of the hepatocarcinogen N,N-dimethyl nitrosamine in vivo: Reaction sites in rat liver DNA and the significance of their relative stabilities, Br. J. Cancer 27:153.Google Scholar
  119. Olivera, B. M., and Lehman, I. R., 1967, Linkage of polynucleotides through phosphodiester bonds by an enzyme from Escherichia coli, Proc. Natl. Acad. Sci. USA 57:1426–1433.Google Scholar
  120. Painter, R. B., 1970, The action of ultraviolet light on mammalian cells, Photophysiology 5:169–189.Google Scholar
  121. Paquette, Y., Crine, P., and Verly, W. G., 1972, Properties of the endonuclease for depurinated DNA from Escherichia coli, Can. J. Biochem. 50:1199–1209.Google Scholar
  122. Paterson, M. C., and Setlow, R. B., 1972, Endonucleolytic activity from Micrococcus luteus that acts on γ-ray-induced damage in plasmid DNA of Escherichia coli minicells, Proc. Natl. Acad. Sci. USA 69:2927–2931.Google Scholar
  123. Paterson, M. C., and Smith, B. P., 1976, Defective excision repair of γ-ray-damaged DNA in human (ataxia telangiectasia) fibroblasts, Biophys. J. 16:183a.Google Scholar
  124. Paterson, M. C., Lohman, P. H. M., and Sluyter, M. L., 1973, Use of a UV endonuclease from Micrococcus luteus to monitor the progress of DNA repair in UV-irradiated human cells, Mutat. Res. 19:235–256.Google Scholar
  125. Paterson, M. C., Lohman, P. H. M., De Weerd-Kastelein, E. A., and Westerveld, A., 1974, Photoreactivation and excision repair of ultraviolet radiation-injured DNA in primary embryonic chick cells, Biophys. J. 14:454–466.Google Scholar
  126. Pedrali Noy, G. C. F., Spadari, S., Ciarrocchi, G., Pedrini, A. M., and Falaschi, A., 1973, Two forms of the DNA ligase of human cells, Eur. J. Biochem. 39:343–351.Google Scholar
  127. Pettijohn, D., and Hanawalt, P. C., 1964, Evidence for repair-replication of ultraviolet damaged DNA in bacteria, J. Mol. Biol. 9:395–410.Google Scholar
  128. Poon, P. K., O’Brien, R. L., and Parker, J. W., 1974, Defective DNA repair in Fanconi’s anemia, Nature (London) 250:223–225.Google Scholar
  129. Rary, J. M., Bender, M. A., and Kelly, T. E., 1974, Cytogenetic studies of ataxia telangiectasia, Am. J. Hum. Genet. 26:70a.Google Scholar
  130. Rasmussen, R. E., and Painter, R. B., 1964, Evidence for repair of ultraviolet damaged deoxyribonucleic acid in cultured mammalian cells, Nature (London) 203:1360–1362.Google Scholar
  131. Rasmussen, R. E., and Painter, R. B., 1966, Radiation-stimulated DNA synthesis in cultured mammalian cells, J. Cell Biol. 29:11–19.Google Scholar
  132. Regan, J. D., and Setlow, R. B., 1974, Two forms of repair in the DNA of human cells damaged by chemical carcinogens and mutagens, Cancer Res. 34:3318–3325.Google Scholar
  133. Regan, J. D., Setlow, R. B., Carrier, W. L., and Lee, W. H., 1970, Molecular events following the ultraviolet irradiation of human cells from ultraviolet-sensitive individuals, Adv. Radiat. Res. Biol. Med. 1:119.Google Scholar
  134. Riklis, E., 1965, Studies on mechanism of repair of ultraviolet-irradiated viral and bacterial DNA in vivo and in vitro, Can. J. Biochem. 43:1207–1219.Google Scholar
  135. Robbins, J. H., and Burk, P. G., 1973, Relationship of DNA repair to carcinogenesis in xeroderma pigmentosum, Cancer Res. 33:929–935.Google Scholar
  136. Robbins, J. H., Kraemer, K. H., Lutzner, M. A., Festoff, B. W., and Coon, H. G., 1974, Xeroderma pigmentosum, Ann. Intern. Med. 80:221–248.Google Scholar
  137. Rupert, C. S., 1975, Enzymatic photoreactivation: Overview, in: Molecular Mechanisms for Repair of DNA (P. C. Hanawalt and R. B. Setlow, eds.), pp. 73–87, Plenum Press, New York.Google Scholar
  138. Sambrook, J., and Shatkin, A. S., 1969, Polynucleotide ligase activity in cells infected with simian virus 40, polyoma virus, or vaccinia virus, J. Virol. 4:719–726.Google Scholar
  139. Sasaki, M. S., and Tonomura, A., 1973, A high susceptibility of Fanconi’s anemia to chromosome breakage by DNA cross-linking agents, Cancer Res. 33:1829–1836.Google Scholar
  140. Scholes, G., Ward, J. F., and Weiss, J. J., 1960, Mechanism of the radiation-induced degradation of nucleic acids, J. Mol. Biol. 2:379–391.Google Scholar
  141. Schroeder, T. M., Anshütz, F., and Knopp, A., 1964, Spontane Chromosomenaberrationen bei familiäer Panmyelopathie, Humangenetik 1:194–196.Google Scholar
  142. Schuler, D., Kiss, A., and Fabian, F., 1969, Chromosomal peculiarities and “in vitro” exami-nations in Fanconi’s anemia, Humangenetik 7:314–322.Google Scholar
  143. Schuster, H., 1960, Die Reaktionsweise der Desoxyribonucleinaure mit salpetriger Säure, Z. Naturforsch. 15b:298–304.Google Scholar
  144. Setlow, R. B., and Carrier, W. L., 1964, The disappearance of thymine dimers from DNA: An error-correcting mechanism, Proc. Natl. Acad. Sci. USA 51:226–231.Google Scholar
  145. Setlow, R. B., and Regan, J. D., 1972, Defective repair of N-acetoxy-2-acetyl-aminofluorene-induced lesions in the DNA of xeroderma pigmentosum cells, Biochem. Biophys. Res. Commun. 46:1019–1024.Google Scholar
  146. Setlow, R. B., and Setlow, J. R., 1972, Effects of radiation on polynucleotides, Annu. Rev. Biophys. Bioeng. 1:293–346.Google Scholar
  147. Setlow, R. B., Regan, J. D., German, J., and Carrier, W. L., 1969, Evidence that xeroderma pigmentosum cells do not perform the first step in the repair of ultraviolet damage to their DNA, Proc. Natl. Acad. Sci. USA 64:1035–1041.Google Scholar
  148. Shapiro, R., and Klein, R. S., 1966, The deamination of cytidine and cytosine by acidic buffer solutions: Mutagenic implications, Biochemistry 5:2358–2362.Google Scholar
  149. Shapiro, R., and Yamaguchi, H., 1972, Nucleic acid reactivity and conformation. I. Deamination of cytosine by nitrous acid, Biochim. Biophys. Acta 281:501–506.Google Scholar
  150. Shapiro, R., Braverman, B., Louis, J. B., and Servis, R. E., 1973, Nucleic acid reactivity and conformation. II. Reaction of cytosine and uracil with sodium bisulfite, J. Biol. Chem. 248:4060–4064.Google Scholar
  151. Slor, H., 1973, Induction of unscheduled DNA synthesis by the carcinogen 7-bromomethylbenz (A) anthracene and its removal from the DNA of normal and xeroderma pigmentosum lymphocytes, Mutat. Res. 19:231–235.Google Scholar
  152. Slor, H., and Lev, T., 1973, Ultraviolet-induced changes in DNA: Possible confusion of repair and degradation enzymes, Biochim. Biophys. Acta 312:637–644.Google Scholar
  153. Smith, K. C., 1971, The roles of genetic recombination and DNA polymerase in the repair of damaged DNA, Photophysiology 6:209–278.Google Scholar
  154. Söderhäll, S., and Lindahl, T., 1973a, Mammalian deoxyribonucleic acid ligase, J. Biol. Chem. 248:672–675.Google Scholar
  155. Söderhäll, S., and Lindahl, T., 1973b, Two DNA ligase activities from calf thymus, Biochem. Biophys. Res. Commun. 53:910–916.Google Scholar
  156. Söderhäll, S., and Lindahl, T., 1975, Mammalian DNA ligases, J. Biol. Chem. 250:8438–8444.Google Scholar
  157. Spadari, S., and Weissbach, A., 1974, HeLa cell R-deoxyribonucleic acid polymerases, J. Biol. Chem. 249:5809–5815.Google Scholar
  158. Spadari, S., Ciarrocchi, G., and Falaschi, A., 1971, Purification and properties of a polynucleotide ligase from human cell cultures, Eur. J. Biochem. 22:75–78.Google Scholar
  159. Stich, J. F., 1975, Response of homozygous and heterozygous xeroderma pigmentosum cells to several chemical and viral carcinogens, in: Molecular Mechanisms for Repair of DNA (P. C. Hanawalt and R. B. Setlow, eds.), pp. 773–784, Plenum Press, New York.Google Scholar
  160. Strauss, B. S., 1968, DNA repair mechanisms and their relation to mutation and recombination, Curr. Top. Microbiol. Immunol. 44:1–85.Google Scholar
  161. Strauss, B. S., 1974, Repair of DNA in mammalian cells, Life Sci. 15:1685–1693.Google Scholar
  162. Strauss, B. S., and Hill, T., 1970, The intermediate in the degradation of DNA alkylated with a monofunctional alkylating agent, Biochim. Biophys. Acta 213:14–25.Google Scholar
  163. Strauss, B., Scudiero, D., and Henderson, E., 1975, The nature of the alkylation lesion in mammalian cells, in: Molecular Mechanisms for Repair of DNA (P. C. Hanawalt and R. B. Setlow, eds.), pp. 13–24, Plenum Press, New York.Google Scholar
  164. Striniste, G. F., and Wallace, S. S., 1975, An Escherichia coli endonuclease which acts on X-irradiated DNA, in: Molecular Mechanisms for Repair of DNA (P. C. Hanawalt and R. B. Setlow, eds.), pp. 201–204, Plenum Press, New York.Google Scholar
  165. Sugimoto, K., Okazaki, T., and Okazaki, R., 1968, Mechanism of DNA chain growth. II. Accumulation of newly synthesized short chains in E. coli infected with ligase-defective T4 phages, Proc. Natl. Acad. Sci. USA 60:1356–1362.Google Scholar
  166. Sutherland, B. M., 1974, Photoreactivating enzyme from human leukocytes, Nature (London) 248:109–112.Google Scholar
  167. Sutherland, B. M., and Oliver, R., 1975, Low levels of photoreactivating enzyme in xeroderma pigmentosum variants, Nature (London) 257:132–134.Google Scholar
  168. Sutherland, B. M., and Oliver, R., 1976, Culture conditions affect photoreactivating enzyme levels in human fibroblasts, Biochim. Biophys. Acta 442:358–367.Google Scholar
  169. Sutherland, B. M., Runge, P., and Sutherland, J. C., 1974, DNA photoreactivating enzyme from placental mammals. Origin and characteristics, Biochemistry 13:4710–4715.Google Scholar
  170. Sutherland, B. M., Rice, M., and Wagner, E. K., 1975, Xeroderma pigmentosum cells contain low levels of photoreactivating enzyme, Proc. Natl. Acad. Sci. USA 72:103–107.Google Scholar
  171. Sutherland, B. M., Oliver, R., Fuselier, C. O., and Sutherland, J. C., 1976, Photoreactivation of pyrimidine dimers in the DNA of normal and xeroderma pigmentosum cells, Biochemistry 15:402–406.Google Scholar
  172. Sutherland, J. C., and Sutherland, B. M., 1975, Human photoreactivating enzyme. Action spectrum and safelight conditions, Biophys. J. 15:435–440.Google Scholar
  173. Tanaka, K., Sekiguchi, M., and Okada, Y., 1975, Restoration of ultraviolet-induced unscheduled DNA synthesis of xeroderma pigmentosum cells by the concomitant treatment with T4 endonuclease V and HVJ (Sendai virus), Proc. Natl. Acad. Sci. USA 72:4071–4075.Google Scholar
  174. Taylor, A. M. R., Harnden, D. G., Arlett, C. F., Harcourt, S. A., Lehmann, A. R., Stevens, S., and Bridges, B., 1975, Ataxia telangiectasia: A human mutation with abnormal radiation sensitivity. Nature (London) 258:427–429.Google Scholar
  175. Todaro, G. J., Green, H., and Swift, M. R., 1966, Susceptibility of human diploid fibroblast strains to transformation by SV40 virus, Science 153:1252–1254.Google Scholar
  176. Tomura, T., and Van Lancker, J. L., 1975, The effect of a mammalian repair endonuclease on X-irradiated DNA, Biochim. Biophys. Acta 402:343–350.Google Scholar
  177. Town, E. D., Smith, K. C., and Kaplan, H. S., 1973, Repair of X-ray damage to bacterial DNA, Curr. Top. Radiat. Res. Q. 8:351–399.Google Scholar
  178. Tsukada, K., and Ichimura, M., 1971, Polynucleotide ligase from rat liver after partial hepatectomy, Biochem. Biophys. Res. Commun. 42:1156–1161.Google Scholar
  179. Van Lancker, J. L., and Tomura, T., 1974, Purification and some properties of a mammalian repair endonuclease, Biochim. Biophys. Acta 353:99–114.Google Scholar
  180. Verly, W. G., and Paquette, Y., 1972, An endonuclease for depurinated DNA in Escherichia coli B, Can. J. Biochem. 50:217–224.Google Scholar
  181. Verly, W. G., and Paquette, Y., 1973, An endonuclease for depurinated DNA in rat liver, Can. J. Biochem. 51:1003–1009.Google Scholar
  182. Verly, W. G., and Rassart, E., 1975, Purification of Escherichia coli endonuclease specific for apurinic sites in DNA, J. Biol. Chem. 250:8214–8219.Google Scholar
  183. Verly, W. G., Gossard, F., and Crine, P., 1974, In vitro repair of apurinic sites in DNA, Proc. Natl. Acad. Sci. USA 71:2273–2275.Google Scholar
  184. Wagner, E. K., Rice, M., and Sutherand, B. M., 1975, Photoreactivation of herpes simplex virus in human fibroblasts, Nature (London) 254:627–628.Google Scholar
  185. Wang, T. Y., 1967, The isolation and purification of mammalian cell nuclei, in: Methods in Enzymology, Vol. 22A (L. Grossman and K. Moldave, eds.), pp. 417–421, Academic Press, New York.Google Scholar
  186. Wang, T. S. F., Sedwick, W. D., and Korn, D., 1975, Nuclear deoxyribonucleic acid polymerase, J. Biol. Chem. 250:7040–7044.Google Scholar
  187. Ward, J. F., 1971, Deoxynucleotides models for studying mechanisms of strand breakage in DNA. I. Protection by sulfhydryl compounds, Int. J. Radiat. Phys. Chem. 3:239–249.Google Scholar
  188. Ward, J. F., 1975, Molecular mechanisms of radiation-induced damage to nucleic acids, Adv. Radiat. Biol. 5:181–239.Google Scholar
  189. Weiss, B., and Richardson, C. C., 1967, Enzymatic breakage and joining of deoxyribonucleic acid. I. Repair of single strand breaks in DNA by an enzyme system from Escherichia coli infected with T4 bacteriophage, Proc. Natl. Acad. Sci. USA 57:1021–1028.Google Scholar
  190. Weissbach, A., 1975, Vertebrate DNA polymerases, Cell 5:101–108.Google Scholar
  191. Wilkins, R. J., 1973, DNA repair: A simple enzymatic assay for human cells, Int. J. Radiat. Biol. 24:609–613.Google Scholar
  192. Witkin, E. M., 1964, Photoreversal and “dark repair” of mutations to prototrophy induced by ultraviolet light in photoreactivable and non-photoreactivable strains of Escherichia coli, Mutat. Res. 1:22–64.Google Scholar
  193. Witkin, E. M., 1969, Ultraviolet-induced mutation and DNA repair, Annu. Rev. Microbiol. 23:487–514.Google Scholar
  194. Yajko, D. M., and Weiss, B., 1975, Mutations simultaneously affecting endonuclease II and exonuclease III in Escherichia coli, Proc. Natl. Acad. Sci. USA 72:688–692.Google Scholar

Copyright information

© Plenum Press, New York 1977

Authors and Affiliations

  • Errol C. Friedberg
    • 1
  • Kern H. Cook
    • 1
  • James Duncan
    • 1
  • Kristien Mortelmans
    • 1
  1. 1.Laboratory of Experimental Oncology, Department of PathologyStanford University School of MedicineStanfordUSA

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