Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1981 Oct 10;9(19):4863–4878. doi: 10.1093/nar/9.19.4863

Control of promoter utilization by bacteriophage T4-induced modification of RNA polymerase alpha subunit.

A Goldfarb, P Palm
PMCID: PMC327485  PMID: 7031602

Abstract

After infection of Escherichia coli cells, bacteriophage T4 induces several changes in the host DNA-dependent RNA polymerase. A well-characterized chemical change is a two-step ADP-ribosylation of the enzyme's alpha subunit (1). In order to investigate the effect of this change on RNA polymerase transcriptional properties in an in vitro system, we have reconstituted the enzyme from separated individual subunits which were obtained from normal or T4-modified RNA polymerases. It is demonstrated that the enzymes containing T4-modified alpha differ from the enzymes with normal alpha in two respects: (i) their overall activity on T4 DNA is reduced and (ii) they fail to utilize certain T4 promotors while efficiently utilizing other promoters. Among the promoters which are switched off by alpha modification are the two promoters of the D region and one of the two promoters of the T4 tRNA gene cluster. The differential effect of alpha modification on the expression of the tRNA and the D regions in vitro correlates with the previously established pattern of their transcription in vivo. It is suggested that the T4-induced ADP-ribosylation of RNA polymerase alpha subunit is involved in the shutoff of the early bacteriophage genes at the late stage of phage development.

Full text

PDF
4863

Images in this article

4866Image
on p.4866
4870Image
on p.4870
4871Image
on p.4871
4873Image
on p.4873

Selected References

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

  1. Chamberlin M. J. The selectivity of transcription. Annu Rev Biochem. 1974;43(0):721–775. doi: 10.1146/annurev.bi.43.070174.003445. [DOI] [PubMed] [Google Scholar]
  2. Depew R. E., Snopek T. J., Cozzarelli N. R. Characterization of a new class of deletions of the D region of the bacteriophage T4 genome. Virology. 1975 Mar;64(1):144–145. doi: 10.1016/0042-6822(75)90086-0. [DOI] [PubMed] [Google Scholar]
  3. Fukada K., Gossens L., Abelson J. The cloning of a T4 transfer RNA gene cluster. J Mol Biol. 1980 Feb 25;137(2):213–234. doi: 10.1016/0022-2836(80)90326-5. [DOI] [PubMed] [Google Scholar]
  4. Fukada K., Otsuka A., Abelson J. A restriction map of the T4 transfer RNA gene cluster. J Mol Biol. 1980 Feb 25;137(2):191–211. doi: 10.1016/0022-2836(80)90325-3. [DOI] [PubMed] [Google Scholar]
  5. Geiduschek E. P., Snyder L., Colvill A. J., Sarnat M. Selective synthesis of T-even bacteriophage early messenger in vitro. J Mol Biol. 1966 Aug;19(2):541–547. doi: 10.1016/s0022-2836(66)80021-9. [DOI] [PubMed] [Google Scholar]
  6. Goff C. G. Chemical structure of a modification of the Escherichia coli ribonucleic acid polymerase alpha polypeptides induced by bacteriophage T4 infection. J Biol Chem. 1974 Oct 10;249(19):6181–6190. [PubMed] [Google Scholar]
  7. Goff C. G., Setzer J. ADP ribosylation of Escherichia coli RNA polymerase is nonessential for bacteriophage T4 development. J Virol. 1980 Jan;33(1):547–549. doi: 10.1128/jvi.33.1.547-549.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goldfarb A., Burger H. J. Mapping of in vitro transcription units and identification of primary transcripts of the D region of bacteriophage T4. Nucleic Acids Res. 1981 Jun 25;9(12):2791–2800. doi: 10.1093/nar/9.12.2791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goldfarb A. Changes in the promoter range of RNA polymerase resulting from bacteriophage T4-induced modification of core enzyme. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3454–3458. doi: 10.1073/pnas.78.6.3454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Goldfarb A., Daniel V. Mapping of transcription units in the bacteriophage T4 tRNA gene cluster. J Mol Biol. 1981 Mar 15;146(4):393–412. doi: 10.1016/0022-2836(81)90039-5. [DOI] [PubMed] [Google Scholar]
  11. Goldfarb A., Daniel V. Transcriptional control of two gene subclusters in the tRNA operon of bacteriophage T4. Nature. 1980 Jul 24;286(5771):418–420. doi: 10.1038/286418a0. [DOI] [PubMed] [Google Scholar]
  12. Goldfarb A. IN vitro transcription of bacteriophage T4 tRNA gene cluster from two different promoters. Nucleic Acids Res. 1981 Feb 11;9(3):519–527. doi: 10.1093/nar/9.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horvitz H. R. Bacteriophage T4 mutants deficient in alteration and modification of the Escherichia coli RNA polymerase. J Mol Biol. 1974 Dec 25;90(4):739–750. doi: 10.1016/0022-2836(74)90537-3. [DOI] [PubMed] [Google Scholar]
  14. Horvitz H. R. Control by bacteriophage T4 of two sequential phosphorylations of the alpha subunit of Escherichia coli RNA polymerase. J Mol Biol. 1974 Dec 25;90(4):727–738. doi: 10.1016/0022-2836(74)90536-1. [DOI] [PubMed] [Google Scholar]
  15. Horvitz H. R. Polypeptide bound to the host RNA polymerase is specified by T4 control gene 33. Nat New Biol. 1973 Aug 1;244(135):137–140. doi: 10.1038/newbio244137a0. [DOI] [PubMed] [Google Scholar]
  16. KHESIN R. B., SHEMIAKIN M. F., GORLENKO Zh M., BOGDANOVA S. L., AFANAS'EVA T. P. [RNA polymerase in E. coli cells infected with T2 phage]. Biokhimiia. 1962 Nov-Dec;27:1092–1105. [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Mailhammer R., Yang H. L., Reiness G., Zubay G. Effects of bacteriophage T4-induced modification of Escherichia coli RNA polymerase on gene expression in vitro. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4928–4932. doi: 10.1073/pnas.72.12.4928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mattson T., Van Houwe G., Epstein R. H. Isolation and characterization of conditional lethal mutations in the mot gene of bacteriophage T4. J Mol Biol. 1978 Dec 15;126(3):551–570. doi: 10.1016/0022-2836(78)90058-x. [DOI] [PubMed] [Google Scholar]
  20. Minkley E. G., Pribnow D. Transcription of the early region of bacteriophage T7: selective initiation with dinucleotides. J Mol Biol. 1973 Jun 25;77(2):255–277. doi: 10.1016/0022-2836(73)90335-5. [DOI] [PubMed] [Google Scholar]
  21. Ovchinnikov Y. A., Lipkin V. M., Modyanov N. N., Chertov O. Y., Smirnov Y. V. Primary structure of alpha-subunit of DNA-dependent RNA polymerase from Escherichia coli. FEBS Lett. 1977 Apr 1;76(1):108–111. doi: 10.1016/0014-5793(77)80131-2. [DOI] [PubMed] [Google Scholar]
  22. Pulitzer J. F., Coppo A., Caruso M. Host--virus interactions in the control of T4 prereplicative transcription. II. Interaction between tabC (rho) mutants and T4 mot mutants. J Mol Biol. 1979 Dec 25;135(4):979–997. doi: 10.1016/0022-2836(79)90523-0. [DOI] [PubMed] [Google Scholar]
  23. Rabussay D., Geiduschek E. P. Construction and properties of a cell-free system for bacteriophage T4 late RNA synthesis. J Biol Chem. 1979 Jan 25;254(2):339–349. [PubMed] [Google Scholar]
  24. Rabussay D., Geiduschek E. P. Phage T4-modified RNA polymerase transcribes T4 late genes in vitro. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5305–5309. doi: 10.1073/pnas.74.12.5305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ratner D. Letter to the editor: Bacteriophage T4 transcriptional control gene 55 codes for a protein bound to Escherichia coli RNA polymerase. J Mol Biol. 1974 Nov 15;89(4):803–807. doi: 10.1016/0022-2836(74)90054-0. [DOI] [PubMed] [Google Scholar]
  26. Rohrer H., Zillig W., Mailhammer R. ADP-ribosylation of DNA-dependent RNA polymerase of Escherichia coli by an NAD+: protein ADP-ribosyltransferase from bacteriophage T4. Eur J Biochem. 1975 Dec 1;60(1):227–238. doi: 10.1111/j.1432-1033.1975.tb20995.x. [DOI] [PubMed] [Google Scholar]
  27. Schachner M., Zillig W. Fingerprint maps of tryptic peptides from subunits of Escherichia coli and T 4 -modified DNA-dependent RNA polymerases. Eur J Biochem. 1971 Oct 26;22(4):513–519. doi: 10.1111/j.1432-1033.1971.tb01571.x. [DOI] [PubMed] [Google Scholar]
  28. Seifert W., Qasba P., Walter G., Palm P., Schachner M., Zillig W. Kinetics of the alteration and modification of DNA-dependent RNA-polymerase in T4-infected E. coli cells. Eur J Biochem. 1969 Jun;9(3):319–324. doi: 10.1111/j.1432-1033.1969.tb00611.x. [DOI] [PubMed] [Google Scholar]
  29. Seifert W., Rabussay D., Zillig W. On the chemical nature of alteration and modification of DNA dependent RNA polymerase of E. coli after T4 infection. FEBS Lett. 1971 Aug 15;16(3):175–179. doi: 10.1016/0014-5793(71)80125-4. [DOI] [PubMed] [Google Scholar]
  30. Skórko R., Zillig W., Rohrer H., Fujiki H., Mailhammer R. Purification and properties of the NAD+: protein ADP-ribosyltransferase responsible for the T4-phage-induced modification of the alpha subunit of DNA-dependent RNA polymerase of Escherichia coli. Eur J Biochem. 1977 Sep 15;79(1):55–66. doi: 10.1111/j.1432-1033.1977.tb11783.x. [DOI] [PubMed] [Google Scholar]
  31. Stevens A. Deoxyribonucleic acid dependent ribonucleic acid polymerases from two T4 phage-infected systems. Biochemistry. 1974 Jan 29;13(3):493–503. doi: 10.1021/bi00700a015. [DOI] [PubMed] [Google Scholar]
  32. Stevens A. New small polypeptides associated with DNA-dependent RNA polymerase of Escherichia coli after infection with bacteriophage T4. Proc Natl Acad Sci U S A. 1972 Mar;69(3):603–607. doi: 10.1073/pnas.69.3.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stevens A., Rhoton J. C. Characterization of an inhibitor causing potassium chloride sensitivity of an RNA polymerase from T4 phage-infected Escherichia coli. Biochemistry. 1975 Nov 18;14(23):5074–5079. doi: 10.1021/bi00694a007. [DOI] [PubMed] [Google Scholar]
  34. Walter G., Seifert W., Zillig W. Modified DNA-dependent RNA polymerase from E. coli infected with bacteriophage T4. Biochem Biophys Res Commun. 1968 Feb 15;30(3):240–247. doi: 10.1016/0006-291x(68)90441-5. [DOI] [PubMed] [Google Scholar]
  35. Wilson J. H., Kim J. S., Abelson J. N. Bacteriophage T4 transfer RNA. 3. Clustering of the genes for the T4 transfer RNA's. J Mol Biol. 1972 Nov 28;71(3):547–556. doi: 10.1016/s0022-2836(72)80022-6. [DOI] [PubMed] [Google Scholar]
  36. Young E. T., Mattson T., Selzer G., Van Houwe G., Bolle A., Epstein R. Bacteriophage T4 gene transcription studied by hybridization to cloned restriction fragments. J Mol Biol. 1980 Apr 15;138(3):423–445. doi: 10.1016/s0022-2836(80)80011-8. [DOI] [PubMed] [Google Scholar]
  37. Zillig W., Mailhammer R., Skorko R., Rohrer H. Covalent structural modification of DNA-dependent RNA polymerase as a means for transcriptional control. Curr Top Cell Regul. 1977;12:263–271. doi: 10.1016/b978-0-12-152812-6.50012-3. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES