Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1989 May;171(5):2542–2546. doi: 10.1128/jb.171.5.2542-2546.1989

Role of exonuclease III and endonuclease IV in repair of pyrimidine dimers initiated by bacteriophage T4 pyrimidine dimer-DNA glycosylase.

S M Saporito 1, M Gedenk 1, R P Cunningham 1
PMCID: PMC209932  PMID: 2468648

Abstract

The role of exonuclease III and endonuclease IV in the repair of pyrimidine dimers in bacteriophage T4-infected Escherichia coli was examined. UV-irradiated T4 showed reduced survival when plated on an xth nfo double mutant but showed wild-type survival on either single mutant. T4 denV phage were equally sensitive when plated on wild-type E. coli or an xth nfo double mutant, suggesting that these endonucleases function in the same repair pathway as T4 pyrimidine dimer-DNA glycosylase. A uvrA mutant of E. coli in which the repair of pyrimidine dimers was dependent on the T4 denV gene carried on a plasmid was constructed. Neither an xth nor an nfo derivative of this strain was more sensitive than the parental strain to UV irradiation. We were unable to construct a uvrA xth nfo triple mutant. In addition, T4, which turns off the host UvrABC excision nuclease, showed reduced plating efficiency on an xth nfo double mutant.

Full text

PDF

Selected References

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

  1. Bachmann B. J. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev. 1972 Dec;36(4):525–557. doi: 10.1128/br.36.4.525-557.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bailly V., Verly W. G. Escherichia coli endonuclease III is not an endonuclease but a beta-elimination catalyst. Biochem J. 1987 Mar 1;242(2):565–572. doi: 10.1042/bj2420565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bonura T., Radany E. H., McMillan S., Love J. D., Schultz R. A., Edenberg H. J., Friedberg E. C. Pyrimidine dimer-DNA glycosylases: studies on bacteriophage T4-infected and on uninfected Escherichia coli. Biochimie. 1982 Aug-Sep;64(8-9):643–654. doi: 10.1016/s0300-9084(82)80104-1. [DOI] [PubMed] [Google Scholar]
  4. Chase M, Doermann A H. High Negative Interference over Short Segments of the Genetic Structure of Bacteriophage T4. Genetics. 1958 May;43(3):332–353. doi: 10.1093/genetics/43.3.332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Clyman J., Cunningham R. P. Escherichia coli K-12 mutants in which viability is dependent on recA function. J Bacteriol. 1987 Sep;169(9):4203–4210. doi: 10.1128/jb.169.9.4203-4210.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cunningham R. P., Saporito S. M., Spitzer S. G., Weiss B. Endonuclease IV (nfo) mutant of Escherichia coli. J Bacteriol. 1986 Dec;168(3):1120–1127. doi: 10.1128/jb.168.3.1120-1127.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Demple B., Linn S. DNA N-glycosylases and UV repair. Nature. 1980 Sep 18;287(5779):203–208. doi: 10.1038/287203a0. [DOI] [PubMed] [Google Scholar]
  8. Demple B., Linn S. On the recognition and cleavage mechanism of Escherichia coli endodeoxyribonuclease V, a possible DNA repair enzyme. J Biol Chem. 1982 Mar 25;257(6):2848–2855. [PubMed] [Google Scholar]
  9. Gates F. T., 3rd, Linn S. Endonuclease V of Escherichia coli. J Biol Chem. 1977 Mar 10;252(5):1647–1653. [PubMed] [Google Scholar]
  10. Gordon L. K., Haseltine W. A. Comparison of the cleavage of pyrimidine dimers by the bacteriophage T4 and Micrococcus luteus UV-specific endonucleases. J Biol Chem. 1980 Dec 25;255(24):12047–12050. [PubMed] [Google Scholar]
  11. HARM W. Mutants of phage T4 with increased sensitivity to ultraviolet. Virology. 1963 Jan;19:66–71. doi: 10.1016/0042-6822(63)90025-4. [DOI] [PubMed] [Google Scholar]
  12. Howard-Flanders P., Boyce R. P., Theriot L. Three loci in Escherichia coli K-12 that control the excision of pyrimidine dimers and certain other mutagen products from DNA. Genetics. 1966 Jun;53(6):1119–1136. doi: 10.1093/genetics/53.6.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kow Y. W., Wallace S. S. Mechanism of action of Escherichia coli endonuclease III. Biochemistry. 1987 Dec 15;26(25):8200–8206. doi: 10.1021/bi00399a027. [DOI] [PubMed] [Google Scholar]
  14. Krisch H. M., Hamlett N. V., Berger H. Polynucleotide ligase in bacteriophage T4D recombination. Genetics. 1972 Oct;72(2):187–203. doi: 10.1093/genetics/72.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Laspia M. F., Wallace S. S. Excision repair of thymine glycols, urea residues, and apurinic sites in Escherichia coli. J Bacteriol. 1988 Aug;170(8):3359–3366. doi: 10.1128/jb.170.8.3359-3366.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lindahl T., Andersson A. Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid. Biochemistry. 1972 Sep 12;11(19):3618–3623. doi: 10.1021/bi00769a019. [DOI] [PubMed] [Google Scholar]
  17. Male R., Fosse V. M., Kleppe K. Polyamine-induced hydrolysis of apurinic sites in DNA and nucleosomes. Nucleic Acids Res. 1982 Oct 25;10(20):6305–6318. doi: 10.1093/nar/10.20.6305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mosbaugh D. W., Linn S. Characterization of the action of Escherichia coli DNA polymerase I at incisions produced by repair endodeoxyribonucleases. J Biol Chem. 1982 Jan 10;257(1):575–583. [PubMed] [Google Scholar]
  19. Nakabeppu Y., Yamashita K., Sekiguchi M. Purification and characterization of normal and mutant forms of T4 endonuclease V. J Biol Chem. 1982 Mar 10;257(5):2556–2562. [PubMed] [Google Scholar]
  20. Povirk L. F., Goldberg I. H. Endonuclease-resistant apyrimidinic sites formed by neocarzinostatin at cytosine residues in DNA: evidence for a possible role in mutagenesis. Proc Natl Acad Sci U S A. 1985 May;82(10):3182–3186. doi: 10.1073/pnas.82.10.3182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Povirk L. F., Houlgrave C. W. Effect of apurinic/apyrimidinic endonucleases and polyamines on DNA treated with bleomycin and neocarzinostatin: specific formation and cleavage of closely opposed lesions in complementary strands. Biochemistry. 1988 May 17;27(10):3850–3857. doi: 10.1021/bi00410a049. [DOI] [PubMed] [Google Scholar]
  22. Radany E. H., Friedberg E. C. A pyrimidine dimer-DNA glycosylase activity associated with the v gene product of bacterophage T4. Nature. 1980 Jul 10;286(5769):182–185. doi: 10.1038/286182a0. [DOI] [PubMed] [Google Scholar]
  23. Radany E. H., Nguyen H. T., Minton K. W. Activities involved in base excision repair of bacteriophage T4 and lambda DNA in vivo. Mol Gen Genet. 1987 Aug;209(1):83–89. doi: 10.1007/BF00329840. [DOI] [PubMed] [Google Scholar]
  24. Sancar A., Sancar G. B. DNA repair enzymes. Annu Rev Biochem. 1988;57:29–67. doi: 10.1146/annurev.bi.57.070188.000333. [DOI] [PubMed] [Google Scholar]
  25. Saporito S. M., Cunningham R. P. Nucleotide sequence of the nfo gene of Escherichia coli K-12. J Bacteriol. 1988 Nov;170(11):5141–5145. doi: 10.1128/jb.170.11.5141-5145.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Saporito S. M., Smith-White B. J., Cunningham R. P. Nucleotide sequence of the xth gene of Escherichia coli K-12. J Bacteriol. 1988 Oct;170(10):4542–4547. doi: 10.1128/jb.170.10.4542-4547.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Smithsm, Ymonds N., White P. The Kornberg polymerase and the repair of irradiated T4 bacteriophage. J Mol Biol. 1970 Dec 14;54(2):391–393. doi: 10.1016/0022-2836(70)90438-9. [DOI] [PubMed] [Google Scholar]
  28. Taylor A. F., Weiss B. Role of exonuclease III in the base excision repair of uracil-containing DNA. J Bacteriol. 1982 Jul;151(1):351–357. doi: 10.1128/jb.151.1.351-357.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wallace S. S., Melamede R. J. Host- and phage-mediated repair of radiation damage in bacteriophage T4. J Virol. 1972 Dec;10(6):1159–1169. doi: 10.1128/jvi.10.6.1159-1169.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Warner H. R., Demple B. F., Deutsch W. A., Kane C. M., Linn S. Apurinic/apyrimidinic endonucleases in repair of pyrimidine dimers and other lesions in DNA. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4602–4606. doi: 10.1073/pnas.77.8.4602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Weiss B., Cunningham R. P. Genetic mapping of nth, a gene affecting endonuclease III (thymine glycol-DNA glycosylase) in Escherichia coli K-12. J Bacteriol. 1985 May;162(2):607–610. doi: 10.1128/jb.162.2.607-610.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. White B. J., Hochhauser S. J., Cintron N. M., Weiss B. Genetic mapping of xthA, the structural gene for exonuclease III in Escherichia coli K-12. J Bacteriol. 1976 Jun;126(3):1082–1088. doi: 10.1128/jb.126.3.1082-1088.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES