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The genetics of the Luria–Latarjet effect in bacteriophage T4: evidence for the involvement of multiple DNA repair pathways

Published online by Cambridge University Press:  14 April 2009

Paul Hyman
Affiliation:
Department of Microbiology and Immunology, The University of Arizona, Tucson, Arizona 85724, USA

Summary

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The Luria-Latarjet effect is an increase in resistance of a virus to DNA damage during infection of a host. It has often been assumed to involve recombinational repair, but this has never been demonstrated experimentally. Using nine bacteriophage (phage) T4 mutants, I present evidence indicating that, for phage T4, the Luria-Latarjet effect is due to three repair pathways-excision repair, post-replication-recombinational-repair (PRRR) and multiplicity reactivation (MR) (a second form of recombinational repair). The results also show that the Luria-Latarjet effect develops in two stages. The first stage starts soon after infection. Damage which occurs during the first stage can be repaired by excision repair or PRRR. The second stage appears to start after the first round of DNA replication is complete. DNA damage which occurs during this stage can apparently be repaired by MR as well as the other two repair pathways. The results of this study support the hypothesis that recombinational repair has been selected to ensure that the progeny phage genomes which are packaged have minimum DNA damage. Since other viruses which infect bacterial, animal and plant cells show a Luria-Latarjet effect similar to that in phage T4, the conclusions from this study may have wide applicability.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

References

Adams, M. H. (1959). Bacteriophages. New York: Interscience Publishers, Inc.CrossRefGoogle Scholar
Amla, D. V. (1979). Photoreactivation of ultraviolet irradiated blue-green alga Anacystis nidulans and cyanophage AS-1. Archives of Virology 59, 173179.CrossRefGoogle ScholarPubMed
Benzer, S. (1952). Resistance to ultraviolet light as an index to the reproduction of bacteriophage. Journal of Bacteriology 63, 5972.CrossRefGoogle Scholar
Berger, H., Warren, A. J. & Fry, K. E. (1969). Variations in genetic recombination due to amber mutations in T4D bacteriophage. Journal of Virology 3, 171175.CrossRefGoogle ScholarPubMed
Bernstein, C. (1981). Deoxyribonucleic acid repair in bacteriophage. Microbiological Reviews 45, 7298.CrossRefGoogle ScholarPubMed
Bernstein, C. & Wallace, S. S. (1983). DNA Repair. In Bacteriophage T4. (ed. Mathews, C. K.Kutter, E. M.Mosig, G. and Berget, P. B.), pp. 103109. Washington D.C.: American Society of Microbiology.Google Scholar
Bernstein, H., Hopf, F. A. & Michod, R. E. (1987). The molecular basis of the evolution of sex. Advances in Genetics 24, 323370.CrossRefGoogle ScholarPubMed
Cheah, P. Y. (1990). Hypothesis for the etiology of colorectal cancer -an overview. Nutrition and Cancer 14, 513.CrossRefGoogle Scholar
Derr, L. K. & Kreuzer, K. N. (1990). Expression and function of the uvsW gene, of bacteriophage T4. Journal of Molecular Biology 214, 643656.CrossRefGoogle ScholarPubMed
Epstein, R. H., Bolle, A., Steinberg, C. M., Kellenberger, E., Boy de la Tour, E., Chevalley, R., Edgar, R. S., Susman, M., Denhardt, G. H. & Lielausis, A. (1963). Physiological studies of conditional lethal mutants of bacteriophage T4D. Cold Spring Harbor Symposium on Quantitative Biology 28, 375394.CrossRefGoogle Scholar
Fenner, F., McAuslan, B. R., Mims, C. A., Sambrook, J. & White, D. O. (1974). The Biology of Animal Viruses, 2nd edn. New York: Academic Press, Inc.Google Scholar
Friedberg, E. C. (1985). DNA Repair. New York: W. H. Freeman and Company.Google Scholar
Garen, A. (1968). Sense and nonsense in the genetic code. Science 160, 149159.CrossRefGoogle ScholarPubMed
Hamlett, N. V. & Berger, H. (1975). Mutations altering genetic recombination and repair of DNA in bacteriophage T4. Virology 63, 539567.CrossRefGoogle ScholarPubMed
Harm, W. (1963). Mutants of phage T4 with increased sensitivity to ultraviolet. Virology 19, 6671.CrossRefGoogle ScholarPubMed
Harm, W. (1980). Biological Effects of Ultraviolet Radiation. Cambridge: Cambridge University Press.Google Scholar
Kodadek, T. (1990). The role of the bacteriophage T4 gene 32 protein in homologous pairing. Journal of Biological Chemistry 265, 2096620969.CrossRefGoogle ScholarPubMed
Kodadek, T., Gan, D. C. & Stemke-Hale, K. (1989). The phage T4 uvsY recombination protein stabilizes presynaptic filaments. Journal of Biological Chemistry 264, 1654116547.CrossRefGoogle ScholarPubMed
Kornberg, A. (1980). DNA Replication. San Francisco: W. H. Freeman and Company.Google Scholar
Latarjet, R. (1948). Intracellular growth of bacteriophage studied by Roentgen irradiation. Journal of General Physiology 31, 529546.CrossRefGoogle ScholarPubMed
Luria, S. E. & Latarjet, R. (1947). Ultraviolet irradiation of bacteriophage during intracellular growth. Journal of Bacteriology 53, 149163.CrossRefGoogle ScholarPubMed
Luria, S. E. & Steiner, D. L. (1954). The role of calcium in the penetration of bacteriophage T5 into its host. Journal of Bacteriology 67, 635639.CrossRefGoogle ScholarPubMed
Lytle, C. D. & Hester, L. D. (1976). Photodynamic treatment of Herpes simplex virus infection in vitro. Photochemistry and Photobiology 1A, 443448.CrossRefGoogle ScholarPubMed
McCarthy, D. (1979). Gyrase-dependent initiation of bacteriophage T4 DNA replication: interactions of Escherichia coli gyrase with novobiocin, coumermycin and phage DNA-delay gene products. Journal of Molecular Biology 127, 265283.CrossRefGoogle ScholarPubMed
McCarthy, D., Minner, C., Bernstein, H. & Bernstein, C. (1976). DNA elongation rates and growing point distributions of wild-type phage T4 and a DNA-delay amber mutant. Journal of Molecular Biology 106, 963981.CrossRefGoogle Scholar
Miller, I. & Freund, J. E. (1985). Probability and Statistics for Engineers. Englewood Cliffs: Prentice-Hall, Inc.Google Scholar
Minagawa, T., Fujisawa, H., Yonesaki, T. & Ryo, Y. (1988). Function of cloned T4 recombination genes, uvsX and uvsY in cells of Escherichia coli. Molecular and General Genetics 211, 350356.CrossRefGoogle ScholarPubMed
Minner, C. A. & Bernstein, H. (1976). Genes 46 and 47 of phage T4; possible compensation for loss of their function. Journal of General Virology 31, 277280.CrossRefGoogle ScholarPubMed
Miskimins, R., Schneider, S., Johns, V. & Bernstein, H. (1982). Topoisomerase involvement in multiplicity reactivation of phage T4. Genetics 101, 157177.Google ScholarPubMed
Mosig, G. & Eiserling, F. (1988). Phage T4 structure and metabolism. In The Bacteriophages (ed. Calendar, R.), pp. 521606, New York: Plenum Press.CrossRefGoogle Scholar
Mufti, S. & Bernstein, H. (1974). The DNA-delay mutants of bacteriophage T4. Journal of Virology 14, 860871.CrossRefGoogle ScholarPubMed
Prashad, N. & Hosoda, J. (1972). Roles of genes 46 and 47 in bacteriophage T4 reproduction. II. Formation of gaps on parental DNA of polynucleotide ligase defective mutants. Journal of Molecular Biology 70, 617635.CrossRefGoogle ScholarPubMed
Pratt, D., Stent, G. S. & Harriman, P. D. (1961). Stabilization to 32P decay and onset of DNA replication of T4 bacteriophage. Journal of Molecular Biology 3, 409424.CrossRefGoogle ScholarPubMed
Ritchie, D. A. & Symonds, N. (1970). The relation between radiation stability and DNA replication of phage T4. Journal of General Virology 8, 121131.CrossRefGoogle ScholarPubMed
Savage, D. C. (1977). Microbial ecology of the gastrointestinal tract. Annual Reviews of Microbiology 31, 107133.CrossRefGoogle ScholarPubMed
Selick, H. E., Barry, J., Cha, T.-A., Munn, M., Nakanishi, M., Wong, M. L. & Alberts, B. M. (1987). Studies on the T4 bacteriophage DNA replication system. In DNA Replication and Recombination (ed. McMacken, R. and Kelly, T. J.), pp. 183214. New York: Alan Liss, R., Inc.Google Scholar
Steinberg, C. M. & Edgar, R. S. (1962). A critical test of a current theory of recombination in bacteriophage. Genetics 47, 187208.CrossRefGoogle ScholarPubMed
Stent, G. S. (1955). Decay of incorporated radioactive phosphorus during reproduction of bacteriophage T2. Journal of General Physiology 38, 853865.CrossRefGoogle ScholarPubMed
Symonds, N. (1957). Effects of ultraviolet light during the second half of the latent period on bacteria infected with phage T2. Virology 3, 485495.CrossRefGoogle ScholarPubMed
Symonds, N., Heindl, H. & White, P. (1973). Radiation sensitive mutants of phage T4: A comparative study. Molecular and General Genetics 120, 253259.CrossRefGoogle ScholarPubMed
Symonds, N. & McCloy, E. W. (1958). The irradiation of phage-infected bacteria: its bearing on the relationship between functional and genetic radiation damage. Virology 6, 649668.CrossRefGoogle ScholarPubMed
Wachsman, J. T. & Drake, J. W. (1987). A new epistasis group for the repair of DNA damage in bacteriophage T4: replication repair. Genetics 115, 405417.CrossRefGoogle Scholar
Warner, H. R. & Snustad, D. P. (1983). T4 DNA nucleases. In Bacteriophage T4 (ed. Mathews, C.K, Kutter, E. M., Mosig, G. and Berget, P. B.), pp. 103109. Washington D.C.: American Society of Microbiology.Google Scholar
Yonesaki, T. & Minagawa, T. (1985). T4 phage gene uvsX product catalyses homologous DNA pairing. EMBO Journal 4, 33213327.CrossRefGoogle Scholar