Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1978 Aug;23(2):247–256. doi: 10.1016/S0006-3495(78)85446-0

Postreplication repair in mammalian cells after ultraviolet irradiation: a model.

M F Lavin
PMCID: PMC1473511  PMID: 687763

Abstract

A model is presented for bypass of ultraviolet-induced damage in DNA during replication. The overall process is initiated by the introduction of a single-strand break into parental DNA near the point of arrest of synthesis, followed by a transient crossing-over step similar to that envisaged in genetic recombination. The mechanism proposed provides an alternative explanation to existing models and is entirely consistent with available data on postreplication repair in mammalian cells. In addition the model explains the low level of recombination repair observed in mammalian cells.

Full text

PDF
247

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alberts B. M., Frey L. T4 bacteriophage gene 32: a structural protein in the replication and recombination of DNA. Nature. 1970 Sep 26;227(5265):1313–1318. doi: 10.1038/2271313a0. [DOI] [PubMed] [Google Scholar]
  2. Baase W. A., Wang J. C. An omega protein from Drosophila melanogaster. Biochemistry. 1974 Oct 8;13(21):4299–4303. doi: 10.1021/bi00718a009. [DOI] [PubMed] [Google Scholar]
  3. Bridges B. A. Recent advances in basic mutation research. Mutat Res. 1977 Aug;44(2):149–164. doi: 10.1016/0027-5107(77)90073-2. [DOI] [PubMed] [Google Scholar]
  4. Broker T. R., Lehman I. R. Branched DNA molecules: intermediates in T4 recombination. J Mol Biol. 1971 Aug 28;60(1):131–149. doi: 10.1016/0022-2836(71)90453-0. [DOI] [PubMed] [Google Scholar]
  5. Buhl S. N., Regan J. D. Repair endonuclease-sensitive sites in daughter DNA of ultraviolet-irradiated human cells. Nature. 1973 Dec 21;246(5434):484–484. doi: 10.1038/246484a0. [DOI] [PubMed] [Google Scholar]
  6. Buhl S. N., Setlow R. B., Regan J. D. Recovery of the ability to synthesize DNA in segments of normal size at long times after ultraviolet irradiation of human cells. Biophys J. 1973 Dec;13(12):1265–1275. doi: 10.1016/S0006-3495(73)86061-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Buhl S. N., Setlow R. B., Regan J. D. Steps in DNA chain elongation and joining after ultra-violet irradiation of human cells. Int J Radiat Biol Relat Stud Phys Chem Med. 1972 Nov;22(5):417–424. doi: 10.1080/09553007214551301. [DOI] [PubMed] [Google Scholar]
  8. Buhl S. N., Stillman R. M., Setlow R. B., Regan J. D. DNA chain elongation and joining in normal human and xeroderma pigmentosum cells after ultraviolet irradiation. Biophys J. 1972 Sep;12(9):1183–1191. doi: 10.1016/S0006-3495(72)86154-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Champoux J. J., Dulbecco R. An activity from mammalian cells that untwists superhelical DNA--a possible swivel for DNA replication (polyoma-ethidium bromide-mouse-embryo cells-dye binding assay). Proc Natl Acad Sci U S A. 1972 Jan;69(1):143–146. doi: 10.1073/pnas.69.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Champoux J. J. Evidence for an intermediate with a single-strand break in the reaction catalyzed by the DNA untwisting enzyme. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3488–3491. doi: 10.1073/pnas.73.10.3488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Clarkson J. M., Hewitt R. R. Significance of dimers to the size of newly synthesized DNA in UV-irradiated Chinese hamster ovary cells. Biophys J. 1976 Oct;16(10):1155–1164. doi: 10.1016/S0006-3495(76)85764-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cleaver J. E. The relationship between the rate of DNA synthesis and its inhibition by ultraviolet light in mammalian cells. Radiat Res. 1967 Apr;30(4):795–810. [PubMed] [Google Scholar]
  13. Cleaver J. E., Thomas G. H. Single strand interruptions in DNA and the effects of caffeine in Chinese hamster cells irradiated with ultraviolet light. Biochem Biophys Res Commun. 1969 Jul 23;36(2):203–208. doi: 10.1016/0006-291x(69)90315-5. [DOI] [PubMed] [Google Scholar]
  14. Djordjevic B., Tolmach L. J. Responses of synchronous populations of HeLa cells to ultraviolet irradiation at selected stages of the generation cycle. Radiat Res. 1967 Oct;32(2):327–346. [PubMed] [Google Scholar]
  15. Domon M., Rauth A. M. Ultraviolet irradiation of mouse L cells: effects on DNA synthesis and progression through the cell cycle. Radiat Res. 1968 Aug;35(2):350–368. [PubMed] [Google Scholar]
  16. Edenberg H. J., Huberman J. A. Eukaryotic chromosome replication. Annu Rev Genet. 1975;9:245–284. doi: 10.1146/annurev.ge.09.120175.001333. [DOI] [PubMed] [Google Scholar]
  17. Edenberg H. J. Inhibition of DNA replication by ultraviolet light. Biophys J. 1976 Aug;16(8):849–860. doi: 10.1016/S0006-3495(76)85735-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Edenberg H. J. Inhibition of DNA synthesis by ultraviolet light. Basic Life Sci. 1975;5B:631–633. doi: 10.1007/978-1-4684-2898-8_34. [DOI] [PubMed] [Google Scholar]
  19. Friedberg E. C., King J. J. Dark repair of ultraviolet-irradiated deoxyribonucleic acid by bacteriophage T4: purification and characterization of a dimer-specific phage-induced endonuclease. J Bacteriol. 1971 May;106(2):500–507. doi: 10.1128/jb.106.2.500-507.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fujiwara Y., Kondo T. Caffeine-sensitive repair of ultraviolet light-damaged DNA of mouse L cells. Biochem Biophys Res Commun. 1972 May 12;47(3):557–564. doi: 10.1016/0006-291x(72)90915-1. [DOI] [PubMed] [Google Scholar]
  21. Fujiwara Y. Postreplication repair of alkylation damage to DNA of mammalian cells in culture. Cancer Res. 1975 Oct;35(10):2780–2789. [PubMed] [Google Scholar]
  22. Fujiwara Y., Tatsumi M. Low-level DNA exchanges in normal human and xeroderma pigmentosum cells after UV irradiation. Mutat Res. 1977 May;43(2):279–290. doi: 10.1016/0027-5107(77)90011-2. [DOI] [PubMed] [Google Scholar]
  23. Fujiwara Y., Tatsumi M. Replicative bypass repair of ultraviolet damage to DNA of mammalian cells: caffeine sensitive and caffeine resistant mechanisms. Mutat Res. 1976 Oct;37(1):91–110. doi: 10.1016/0027-5107(76)90058-0. [DOI] [PubMed] [Google Scholar]
  24. Ganesan A. K. Persistence of pyrimidine dimers during post-replication repair in ultraviolet light-irradiated Escherichia coli K12. J Mol Biol. 1974 Jul 25;87(1):103–119. doi: 10.1016/0022-2836(74)90563-4. [DOI] [PubMed] [Google Scholar]
  25. Higgins N. P., Kato K., Strauss B. A model for replication repair in mammalian cells. J Mol Biol. 1976 Mar 5;101(3):417–425. doi: 10.1016/0022-2836(76)90156-x. [DOI] [PubMed] [Google Scholar]
  26. Holliday R. Molecular aspects of genetic exchange and gene conversion. Genetics. 1974 Sep;78(1):273–287. doi: 10.1093/genetics/78.1.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Holloman W. K., Holliday R. Studies on a nuclease from Ustilago maydis. I. Purification, properties, and implication in recombination of the enzyme. J Biol Chem. 1973 Dec 10;248(23):8107–8113. [PubMed] [Google Scholar]
  28. Holloman W. K. Studies on a nuclease from Ustilago maydis. II. Substrate specificity and mode of action of the enzyme. J Biol Chem. 1973 Dec 10;248(23):8114–8119. [PubMed] [Google Scholar]
  29. Holloman W. K., Wiegand R., Hoessli C., Radding C. M. Uptake of homologous single-stranded fragments by superhelical DNA: a possible mechanism for initiation of genetic recombination. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2394–2398. doi: 10.1073/pnas.72.6.2394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kaplan J. C., Kushner S. R., Grossman L. Enzymatic repair of DNA. 3. Properties of the UV-endonuclease and UV-exonuclease. Biochemistry. 1971 Aug 31;10(18):3315–3324. doi: 10.1021/bi00794a001. [DOI] [PubMed] [Google Scholar]
  31. Lavin M. F., Kikuchi T., Counsilman C., Jenkins A., Winzor D. J., Kidson C. A mammalian nicking endonuclease. Biochemistry. 1976 Jun 1;15(11):2409–2414. doi: 10.1021/bi00656a025. [DOI] [PubMed] [Google Scholar]
  32. Lavin M. F., McCombie P., Kidson C. DNA replication and post-replication repair in U.V.-sensitive mouse neuroblastoma cells. Int J Radiat Biol Relat Stud Phys Chem Med. 1976 Jul;30(1):31–40. doi: 10.1080/09553007614550781. [DOI] [PubMed] [Google Scholar]
  33. Lavin M. F., Willett G. M., Chalmers A. H., Kidson C. DNA replication and repair in a human melanoma cell-line resistant to ultra-violet-radiation. Int J Radiat Biol Relat Stud Phys Chem Med. 1977 Feb;31(2):101–111. doi: 10.1080/09553007714550121. [DOI] [PubMed] [Google Scholar]
  34. Lehmann A. R., Kirk-Bell S., Arlett C. F., Paterson M. C., Lohman P. H., de Weerd-Kastelein E. A., Bootsma D. Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. Proc Natl Acad Sci U S A. 1975 Jan;72(1):219–223. doi: 10.1073/pnas.72.1.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lehmann A. R. Postreplication repair of DNA in mammalian cells. Life Sci. 1974 Dec 15;15(12):2005–2016. doi: 10.1016/0024-3205(74)90018-6. [DOI] [PubMed] [Google Scholar]
  36. Lehmann A. R. Postreplication repair of DNA in ultraviolet-irradiated mammalian cells. J Mol Biol. 1972 May 28;66(3):319–337. doi: 10.1016/0022-2836(72)90418-4. [DOI] [PubMed] [Google Scholar]
  37. Meneghini R. Gaps in DNA synthesized by ultraviolet light-irradiated WI38 human cells. Biochim Biophys Acta. 1976 Apr 2;425(4):419–427. doi: 10.1016/0005-2787(76)90006-x. [DOI] [PubMed] [Google Scholar]
  38. Meneghini R., Hanawalt P. T4-endonuclease V-sensitive sites in DNA from ultraviolet-irradiated human cells. Biochim Biophys Acta. 1976 Apr 2;425(4):428–437. doi: 10.1016/0005-2787(76)90007-1. [DOI] [PubMed] [Google Scholar]
  39. Meselson M. S., Radding C. M. A general model for genetic recombination. Proc Natl Acad Sci U S A. 1975 Jan;72(1):358–361. doi: 10.1073/pnas.72.1.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Meselson M. Formation of hybrid DNA by rotary diffusion during genetic recombination. J Mol Biol. 1972 Nov 28;71(3):795–798. doi: 10.1016/s0022-2836(72)80040-8. [DOI] [PubMed] [Google Scholar]
  41. Meyn R. E., Hewitt R. R., Thomas L. F., Humphrey R. M. Effects of ultraviolet irradiation on the rate and sequence of DNA replication in synchronized Chinese hamster cells. Biophys J. 1976 May;16(5):517–525. doi: 10.1016/S0006-3495(76)85706-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Meyn R. E., Humphrey R. M. Deoxyribonucleic acid synthesis in ultraviolet-light-irradiated Chinese hamster cells. Biophys J. 1971 Mar;11(3):295–301. doi: 10.1016/S0006-3495(71)86215-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Moore P. D., Holliday R. Evidence for the formation of hybrid DNA during mitotic recombination in Chinese hamster cells. Cell. 1976 Aug;8(4):573–579. doi: 10.1016/0092-8674(76)90225-7. [DOI] [PubMed] [Google Scholar]
  44. Painter R. B. DNA damage and repair in eukaryotic cells. Genetics. 1974 Sep;78(1):139–148. doi: 10.1093/genetics/78.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Pedrini A. M., Ranzani G., Pedrali Noy G. C., Spadari S., Falaschi A. A novel endonuclease of human cells specific for single-stranded DNA. Eur J Biochem. 1976 Nov 1;70(1):275–283. doi: 10.1111/j.1432-1033.1976.tb10979.x. [DOI] [PubMed] [Google Scholar]
  46. Potter H., Dressler D. On the mechanism of genetic recombination: electron microscopic observation of recombination intermediates. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3000–3004. doi: 10.1073/pnas.73.9.3000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. RASMUSSEN R. E., PAINTER R. B. EVIDENCE FOR REPAIR OF ULTRA-VIOLET DAMAGED DEOXYRIBONUCLEIC ACID IN CULTURED MAMMALIAN CELLS. Nature. 1964 Sep 26;203:1360–1362. doi: 10.1038/2031360a0. [DOI] [PubMed] [Google Scholar]
  48. Radding C. M. Molecular mechanisms in genetic recombination. Annu Rev Genet. 1973;7:87–111. doi: 10.1146/annurev.ge.07.120173.000511. [DOI] [PubMed] [Google Scholar]
  49. Rauth A. M., Tammemagi M., Hunter G. Nascent DNA synthesis in ultraviolet light-irradiated mouse, human and Chinese hamster cells. Biophys J. 1974 Mar;14(3):209–220. doi: 10.1016/S0006-3495(74)85908-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Rommelaere J., Miller-Faurès A. Detection by density equilibrium centrifugation of recombinant-like DNA molecules in somatic mammalian cells. J Mol Biol. 1975 Oct 15;98(1):195–218. doi: 10.1016/s0022-2836(75)80109-4. [DOI] [PubMed] [Google Scholar]
  51. Rupp W. D., Wilde C. E., 3rd, Reno D. L., Howard-Flanders P. Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli. J Mol Biol. 1971 Oct 14;61(1):25–44. doi: 10.1016/0022-2836(71)90204-x. [DOI] [PubMed] [Google Scholar]
  52. Sedgwick S. G. Genetic and kinetic evidence for different types of postreplication repair in Escherichia coli B. J Bacteriol. 1975 Jul;123(1):154–161. doi: 10.1128/jb.123.1.154-161.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Sigal N., Alberts B. Genetic recombination: the nature of a crossed strand-exchange between two homologous DNA molecules. J Mol Biol. 1972 Nov 28;71(3):789–793. doi: 10.1016/s0022-2836(72)80039-1. [DOI] [PubMed] [Google Scholar]
  54. Stern H., Hotta Y. DNA metabolism during pachytene in relation to crossing over. Genetics. 1974 Sep;78(1):227–235. doi: 10.1093/genetics/78.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Tait R. C., Harris A. L., Smith D. W. DNA repair in Escherichia coli mutants deficient in DNA polymerases I, II and-or 3. Proc Natl Acad Sci U S A. 1974 Mar;71(3):675–679. doi: 10.1073/pnas.71.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Vosberg H. P., Grossman L. I., Vinograd J. Isolation and partial characterisation of the relaxation protein from nuclei of cultured mouse and human cells. Eur J Biochem. 1975 Jun 16;55(1):79–93. doi: 10.1111/j.1432-1033.1975.tb02140.x. [DOI] [PubMed] [Google Scholar]
  57. Wang E. C., Henner D., Furth J. J. An endonuclease from calf thymus which introduces a limited number of single strand breaks into DNA. Biochem Biophys Res Commun. 1975 Aug 18;65(4):1177–1183. doi: 10.1016/s0006-291x(75)80353-6. [DOI] [PubMed] [Google Scholar]
  58. Wang J. C. Interaction between DNA and an Escherichia coli protein omega. J Mol Biol. 1971 Feb 14;55(3):523–533. doi: 10.1016/0022-2836(71)90334-2. [DOI] [PubMed] [Google Scholar]
  59. Waters R., Regan J. D. Recombination of UV-induced pyrimidine dimers in human fibroblasts. Biochem Biophys Res Commun. 1976 Oct 4;72(3):803–807. doi: 10.1016/s0006-291x(76)80204-5. [DOI] [PubMed] [Google Scholar]
  60. Youngs D. A., Smith K. C. Genetic control of multiple pathways of post-replicational repair in uvrB strains of Escherichia coli K-12. J Bacteriol. 1976 Jan;125(1):102–110. doi: 10.1128/jb.125.1.102-110.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES