Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1976 Feb;17(2):326–334. doi: 10.1128/jvi.17.2.326-334.1976

Bacteriophage T4-induced shut-off of host-specific translation.

S B Svenson, O H Karlström
PMCID: PMC515424  PMID: 768517

Abstract

To study the mechanism by which bacteriophage T4 inhibits the synthesis of inducible host enzymes we measured the formation of beta-galactosidase from preformed lac mRNA. Beta-Galactosidase was induced with isopropyl-beta-D-thiogalactopyranoside in the presence of 7-azatryptophan, a tryptophan analogue that is incorporated into proteins and renders the beta-galactosidase formed inactive. The accumulated las mRNA was measured by capacity to form active beta-galactosidase after a chase of the analogue with excess tryptophan. After T4 infection the ability to form beta-galactosidase from the preformed lac mRNA was rapidly lost even when T4 infection took place in the presence of rifampin. This restriction was dependent on the multiplicity of infection. At a multiplicity of infection of 8.6, 90% of the ability to express preformed lac mRNA was lost within 30 s. The kinetics of cessation of beta-galactosidase synthesis after T4 infection indicate that infection blocks initiation of lac mRNA translation.

Full text

PDF
326

Selected References

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

  1. ASTRACHAN L., VOLKIN E. Properties of ribonucleic acid turnover in T2-infected Escherichia coli. Biochim Biophys Acta. 1958 Sep;29(3):536–544. doi: 10.1016/0006-3002(58)90010-6. [DOI] [PubMed] [Google Scholar]
  2. COHEN G., JACOB F. Sur la répression de la synthèse des enzymes intervenant dans la formation du tryptophane chez Escherichia coll. C R Hebd Seances Acad Sci. 1959 Jun 15;248(24):3490–3492. [PubMed] [Google Scholar]
  3. Doolittle W. F., Yanofsky C. Mutants of Escherichia coli with an altered tryptophanyl-transfer ribonucleic acid synthetase. J Bacteriol. 1968 Apr;95(4):1283–1294. doi: 10.1128/jb.95.4.1283-1294.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Duckworth D. H. Biological activity of bacteriophage ghosts and "take-over" of host functions by bacteriophage. Bacteriol Rev. 1970 Sep;34(3):344–363. doi: 10.1128/br.34.3.344-363.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Duckworth D. H. Inhibition of T4 bacteriophage multiplication by superinfecting ghosts and the development of tolerance after bacteriophage infection. J Virol. 1971 Jan;7(1):8–14. doi: 10.1128/jvi.7.1.8-14.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. EDLIN G. GENE REGULATION DURING BACTERIOPHAGE T4 DEVLOPMENT. I. PHENOTYPIC REVERSION OF T4 AMBER MUTANTS BY 5-FLUOROURACIL. J Mol Biol. 1965 Jun;12:363–374. doi: 10.1016/s0022-2836(65)80260-1. [DOI] [PubMed] [Google Scholar]
  7. FRASER D., JERREL E. A. The amino acid composition of T3 bacteriophage. J Biol Chem. 1953 Nov;205(1):291–295. [PubMed] [Google Scholar]
  8. Goldman E., Lodish H. F. T4 phage and T4 ghosts inhibit f2 phage replication by different mechanisms. J Mol Biol. 1973 Feb 25;74(2):151–161. doi: 10.1016/0022-2836(73)90104-6. [DOI] [PubMed] [Google Scholar]
  9. Haselkorn R., Vogel M., Brown R. D. Conservation of the rifamycin sensitivity of transcription during T4 development. Nature. 1969 Mar 1;221(5183):836–838. doi: 10.1038/221836a0. [DOI] [PubMed] [Google Scholar]
  10. Kaempfer R. O., Magasanik B. Effect of infection with T-even phage on the inducible synthesis of beta-glactosidase in Escherichia coli. J Mol Biol. 1967 Aug 14;27(3):453–468. doi: 10.1016/0022-2836(67)90051-4. [DOI] [PubMed] [Google Scholar]
  11. Kaempfer R. O., Magasanik B. Mechanism of beta-galactosidase induction in Escherichia coli. J Mol Biol. 1967 Aug 14;27(3):475–494. doi: 10.1016/0022-2836(67)90053-8. [DOI] [PubMed] [Google Scholar]
  12. Kennell D. Inhibition of host protein synthesis during infection of Escherichia coli by bacteriophage T4. I. Continued synthesis of host ribonucleic acid. J Virol. 1968 Nov;2(11):1262–1271. doi: 10.1128/jvi.2.11.1262-1271.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kennell D. Inhibition of host protein synthesis during infection of Escherichia coli by bacteriophage T4. II. Induction of host messenger ribonucleic acid and its exclusion from polysomes. J Virol. 1970 Aug;6(2):208–217. doi: 10.1128/jvi.6.2.208-217.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kepes A. Sequential transcription and translation in the lactose operon of Escherichia coli. Biochim Biophys Acta. 1967 Mar 29;138(1):107–123. doi: 10.1016/0005-2787(67)90591-6. [DOI] [PubMed] [Google Scholar]
  15. MOYED H. S. False feedback inhibition: inhibition of tryptophan biosynthesis by 5-methyltryptophan. J Biol Chem. 1960 Apr;235:1098–1102. [PubMed] [Google Scholar]
  16. Mosteller R. D., Yanofsky C. Evidence that tryptophanyl transfer ribonucleic acid is not the corepressor of the tryptophan operon of Escherichia coli. J Bacteriol. 1971 Jan;105(1):268–275. doi: 10.1128/jb.105.1.268-275.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. NOMURA M., OKAMOTO K., ASANO K. RNA metabolism in Escherichia coli infected with bacteriophage T4. Inhibition of host ribosomal and soluble RNA synthesis by phage and effect of chloromycetin. J Mol Biol. 1962 May;4:376–387. doi: 10.1016/s0022-2836(62)80018-7. [DOI] [PubMed] [Google Scholar]
  18. Nomura M., Witten C., Mantei N., Echols H. Inhibition of host nucleic acid synthesis by bacteriophage T4: effect of chloramphenicol at various multiplicities of infection. J Mol Biol. 1966 May;17(1):273–278. doi: 10.1016/s0022-2836(66)80107-9. [DOI] [PubMed] [Google Scholar]
  19. PARDEE A. B., PRESTIDGE L. S. Effects of azatryptophan on bacterial enzymes and bacteriophage. Biochim Biophys Acta. 1958 Feb;27(2):330–344. doi: 10.1016/0006-3002(58)90340-8. [DOI] [PubMed] [Google Scholar]
  20. PARDEE A. B., PRESTIDGE L. S., SHORE V. G. Incorporation of azatryptophan into proteins of bacteria and bacteriophage. Biochim Biophys Acta. 1956 Aug;21(2):406–407. doi: 10.1016/0006-3002(56)90044-0. [DOI] [PubMed] [Google Scholar]
  21. Pato M. L., Bennett P. M., von Meyenburg K. Messenger ribonucleic acid synthesis and degradation in Escherichia coli during inhibition of translation. J Bacteriol. 1973 Nov;116(2):710–718. doi: 10.1128/jb.116.2.710-718.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Quintero-Ruiz A., Brody E. N. Effect of T4 ghosts on T4 development. Virology. 1975 Jul;66(1):241–252. doi: 10.1016/0042-6822(75)90194-4. [DOI] [PubMed] [Google Scholar]
  23. Rouvière J., Wyngaarden J., Cantoni J., Gros F., Kepes A. Effect of T4 infection on messenger RNA synthesis in Escherichia coli. Biochim Biophys Acta. 1968 Aug 23;166(1):94–114. doi: 10.1016/0005-2787(68)90494-2. [DOI] [PubMed] [Google Scholar]
  24. Schlesinger S. The effect of amino acid analogues on alkaline phosphatase. Formation in Escherichia coli K-12. II. Replacement of tryptophan by azatryptophan and by tryptazan. J Biol Chem. 1968 Jul 25;243(14):3877–3883. [PubMed] [Google Scholar]
  25. Squires C. L., Rose J. K., Yanofsky C., Yang H. L., Zubay G. Tryptophanyl-tRNA and tryptophanyl-tRNA synthetase are not required for in vitro repression of the tryptophan operon. Nat New Biol. 1973 Oct 3;245(144):131–133. doi: 10.1038/newbio245131a0. [DOI] [PubMed] [Google Scholar]
  26. Terzi M. Studies on the mechanism of bacteriophage T4 interference with host metabolism. J Mol Biol. 1967 Aug 28;28(1):37–44. doi: 10.1016/s0022-2836(67)80075-5. [DOI] [PubMed] [Google Scholar]
  27. VOLKIN E., ASTRACHAN L. Phosphorus incorporation in Escherichia coli ribo-nucleic acid after infection with bacteriophage T2. Virology. 1956 Apr;2(2):149–161. doi: 10.1016/0042-6822(56)90016-2. [DOI] [PubMed] [Google Scholar]
  28. Wehrli W., Staehelin M. Actions of the rifamycins. Bacteriol Rev. 1971 Sep;35(3):290–309. doi: 10.1128/br.35.3.290-309.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES