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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1981 Aug;78(8):4669–4673. doi: 10.1073/pnas.78.8.4669

Translational regulation: identification of the site on bacteriophage T4 rIIB mRNA recognized by the regA gene function.

J Karam, L Gold, B S Singer, M Dawson
PMCID: PMC320220  PMID: 7029523

Abstract

The bacteriophage T4 gene regA encodes a protein that diminishes the expression of many unlinked early T4 genes. Previous work demonstrated that regA-mediated repression occurs after transcription. We report here on the identification of the target site on one regA-sensitive mRNA, the message encoding the phage T4 rIIB protein. The target for regA-mediated action overlaps the translational initiation domain of the rIIB messenger. The regA protein may be a repressor that operates translationally on a significant and interesting set of early phage T4 mRNAs.

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Selected References

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  1. Belin D. Bacteriophage T4 rIIB protein synthesis with a temperature-sensitive mutation in the rIIB initiation codon. Mol Gen Genet. 1979 Mar 9;171(1):35–42. doi: 10.1007/BF00274012. [DOI] [PubMed] [Google Scholar]
  2. Belin D., Hedgpeth J., Selzer G. B., Epstein R. H. Temperature-sensitive mutation in the initiation codon of the rIIB gene of bacteriophage T4. Proc Natl Acad Sci U S A. 1979 Feb;76(2):700–704. doi: 10.1073/pnas.76.2.700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benzer S. ON THE TOPOGRAPHY OF THE GENETIC FINE STRUCTURE. Proc Natl Acad Sci U S A. 1961 Mar;47(3):403–415. doi: 10.1073/pnas.47.3.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernardi A., Spahr P. F. Nucleotide sequence at the binding site for coat protein on RNA of bacteriophage R17. Proc Natl Acad Sci U S A. 1972 Oct;69(10):3033–3037. doi: 10.1073/pnas.69.10.3033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bolle A., Epstein R. H., Salser W., Geiduschek E. P. Transcription during bacteriophage T4 development: requirements for late messenger synthesis. J Mol Biol. 1968 Apr 28;33(2):339–362. doi: 10.1016/0022-2836(68)90193-9. [DOI] [PubMed] [Google Scholar]
  6. Borisova G. P., Volkova T. M., Berzin V., Rosenthal G., Gren E. J. The regulatory region of MS2 phage RNA replicase cistron. IV. Functional activity of specific MS2 RNA fragments in formation of the 70 S initiation complex of protein biosynthesis. Nucleic Acids Res. 1979;6(5):1761–1774. doi: 10.1093/nar/6.5.1761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brot N., Caldwell P., Weissbach H. Autogenous control of Escherichia coli ribosomal protein L10 synthesis in vitro. Proc Natl Acad Sci U S A. 1980 May;77(5):2592–2595. doi: 10.1073/pnas.77.5.2592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cardillo T. S., Landry E. F., Wiberg J. S. regA protein of bacteriophage T4D: identification, schedule of synthesis, and autogenous regulation. J Virol. 1979 Dec;32(3):905–916. doi: 10.1128/jvi.32.3.905-916.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cole M. D., Beer M., Koller T., Strycharz W. A., Nomura M. Electron microscopic determination of the binding sites of ribosomal proteins S4 and S8 on 16S RNA. Proc Natl Acad Sci U S A. 1978 Jan;75(1):270–274. doi: 10.1073/pnas.75.1.270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. David M., Vekstein R., Kaufmann G. RNA ligase reaction products in plasmolyzed Escherichia coli cells infected by T4 bacteriophage. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5430–5434. doi: 10.1073/pnas.76.11.5430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dean D., Nomura M. Feedback regulation of ribosomal protein gene expression in Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3590–3594. doi: 10.1073/pnas.77.6.3590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dennis P. P., Fill N. P. Transcriptional and post-transcriptional control of RNA polymerase and ribosomal protein genes cloned on composite ColE1 plasmids in the bacterium Escherichia coli. J Biol Chem. 1979 Aug 25;254(16):7540–7547. [PubMed] [Google Scholar]
  13. Dunn J. J., Buzash-Pollert E., Studier F. W. Mutations of bacteriophage T7 that affect initiation of synthesis of the gene 0.3 protein. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2741–2745. doi: 10.1073/pnas.75.6.2741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dunn J. J., Studier F. W. Effect of RNAase III, cleavage on translation of bacteriophage T7 messenger RNAs. J Mol Biol. 1975 Dec 15;99(3):487–499. doi: 10.1016/s0022-2836(75)80140-9. [DOI] [PubMed] [Google Scholar]
  15. Fallon A. M., Jinks C. S., Strycharz G. D., Nomura M. Regulation of ribosomal protein synthesis in Escherichia coli by selective mRNA inactivation. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3411–3415. doi: 10.1073/pnas.76.7.3411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gold L., O'Farrell P. Z., Russel M. Regulation of gene 32 expression during bacteriophage T4 infection of Escherichia coli. J Biol Chem. 1976 Nov 25;251(22):7251–7262. [PubMed] [Google Scholar]
  17. Gralla J., Steitz J. A., Crothers D. M. Direct physical evidence for secondary structure in an isolated fragment of R17 bacteriophage mRNA. Nature. 1974 Mar 15;248(445):204–208. doi: 10.1038/248204a0. [DOI] [PubMed] [Google Scholar]
  18. Higgins N. P., Geballe A. P., Snopek T. J., Sugino A., Cozzarelli N. R. Bacteriophage T4 RNA ligase: preparation of a physically homogeneous, nuclease-free enzyme from hyperproducing infected cells. Nucleic Acids Res. 1977 Sep;4(9):3175–3186. doi: 10.1093/nar/4.9.3175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Johnson A., Meyer B. J., Ptashne M. Mechanism of action of the cro protein of bacteriophage lambda. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1783–1787. doi: 10.1073/pnas.75.4.1783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Karam J. D., Bowles M. G. Mutation to overproduction of bacteriophage T4 gene products. J Virol. 1974 Feb;13(2):428–438. doi: 10.1128/jvi.13.2.428-438.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Karam J., McCulley C., Leach M. Genetic control of mRNA decay in T4 phage-infected Escherichia coli. Virology. 1977 Feb;76(2):685–700. doi: 10.1016/0042-6822(77)90251-3. [DOI] [PubMed] [Google Scholar]
  22. Katz E. R., Brenner S. Genetic map of the beginning of the rIIB cistron of bacteriophage T4. Mol Gen Genet. 1975 Dec 30;143(1):101–104. doi: 10.1007/BF00269426. [DOI] [PubMed] [Google Scholar]
  23. Kolakofsky D., Weissmann C. Q replicase as repressor of Q RNA-directed protein synthesis. Biochim Biophys Acta. 1971 Sep 24;246(3):596–599. doi: 10.1016/0005-2787(71)90799-4. [DOI] [PubMed] [Google Scholar]
  24. Krisch H. M., Bolle A., Epstein R. H. Regulation of the synthesis of bacteriophage T4 gene 32 protein. J Mol Biol. 1974 Sep 5;88(1):89–104. doi: 10.1016/0022-2836(74)90296-4. [DOI] [PubMed] [Google Scholar]
  25. Lemaire G., Gold L., Yarus M. Autogenous translational repression of bacteriophage T4 gene 32 expression in vitro. J Mol Biol. 1978 Nov 25;126(1):73–90. doi: 10.1016/0022-2836(78)90280-2. [DOI] [PubMed] [Google Scholar]
  26. Mackie G. A., Zimmermann R. A. Characterization of fragments of 16 S ribonucleic acid protected against pancreatic ribonuclease digestion by ribosomal protein S4. J Biol Chem. 1975 Jun 10;250(11):4100–4112. [PubMed] [Google Scholar]
  27. Miller J. H. Genetic studies of the lac repressor. XI. On aspects of lac repressor structure suggested by genetic experiments. J Mol Biol. 1979 Jun 25;131(2):249–258. doi: 10.1016/0022-2836(79)90075-5. [DOI] [PubMed] [Google Scholar]
  28. Morris C. F., Hama-Inaba H., Mace D., Sinha N. K., Alberts B. Purification of the gene 43, 44, 45, and 62 proteins of the bacteriophage T4 DNA replication apparatus. J Biol Chem. 1979 Jul 25;254(14):6787–6796. [PubMed] [Google Scholar]
  29. Müller R., Garrett R. A., Noller H. F. The structure of the RNA binding site of ribosomal proteins S8 and S15. J Biol Chem. 1979 May 25;254(10):3873–3878. [PubMed] [Google Scholar]
  30. O'Farrell P. Z., Gold L. M. Bacteriophage T4 gene expression. Evidence for two classes of prereplicative cistrons. J Biol Chem. 1973 Aug 10;248(15):5502–5511. [PubMed] [Google Scholar]
  31. Ogata R. T., Gilbert W. An amino-terminal fragment of lac repressor binds specifically to lac operator. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5851–5854. doi: 10.1073/pnas.75.12.5851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pabo C. O., Sauer R. T., Sturtevant J. M., Ptashne M. The lambda repressor contains two domains. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1608–1612. doi: 10.1073/pnas.76.4.1608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ptashne M., Jeffrey A., Johnson A. D., Maurer R., Meyer B. J., Pabo C. O., Roberts T. M., Sauer R. T. How the lambda repressor and cro work. Cell. 1980 Jan;19(1):1–11. doi: 10.1016/0092-8674(80)90383-9. [DOI] [PubMed] [Google Scholar]
  34. Ray P. N., Pearson M. L. Evidence for post-transcriptional control of the morphogenetic genes of bacteriophage lambda. J Mol Biol. 1974 May 5;85(1):163–175. doi: 10.1016/0022-2836(74)90135-1. [DOI] [PubMed] [Google Scholar]
  35. Ray P. N., Pearson M. L. Functional inactivation of bacteriophage lambda morphogenetic gene in RNA. Nature. 1975 Feb 20;253(5493):647–650. doi: 10.1038/253647a0. [DOI] [PubMed] [Google Scholar]
  36. Russel M., Gold L., Morrissett H., O'Farrell P. Z. Translational, autogenous regulation of gene 32 expression during bacteriophage T4 infection. J Biol Chem. 1976 Nov 25;251(22):7263–7270. [PubMed] [Google Scholar]
  37. Sauer R. T., Pabo C. O., Meyer B. J., Ptashne M., Backman K. C. Regulatory functions of the lambda repressor reside in the amino-terminal domain. Nature. 1979 May 31;279(5712):396–400. doi: 10.1038/279396a0. [DOI] [PubMed] [Google Scholar]
  38. Sauerbier W., Hercules K. Control of gene function in bacteriophage T4. IV. Post-transcriptional shutoff of expression of early genes. J Virol. 1973 Sep;12(3):538–547. doi: 10.1128/jvi.12.3.538-547.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Singer B. S., Gold L. A mutation that confers temperature sensitivity on the translation of rIIB in bacteriophage T4. J Mol Biol. 1976 May 25;103(3):627–646. doi: 10.1016/0022-2836(76)90221-7. [DOI] [PubMed] [Google Scholar]
  41. Snopek T. J., Wood W. B., Conley M. P., Chen P., Cozzarelli N. R. Bacteriophage T4 RNA ligase is gene 63 product, the protein that promotes tail fiber attachment to the baseplate. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3355–3359. doi: 10.1073/pnas.74.8.3355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stahl D. A., Meyhack B., Pace N. R. Recognition of local nucleotide conformation in contrast to sequence by a rRNA processing endonuclease. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5644–5648. doi: 10.1073/pnas.77.10.5644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Steitz J. A. Specific recognition of the isolated R17 replicase initiator region by R17 coat protein. Nature. 1974 Mar 15;248(445):223–225. doi: 10.1038/248223a0. [DOI] [PubMed] [Google Scholar]
  44. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  45. Trimble R. B., Maley Level of specific prereplicative mRNA's during bacteriophage T4 regA-, 43- and T4 43- infection of Escherichia coli B. J Virol. 1976 Feb;17(2):538–549. doi: 10.1128/jvi.17.2.538-549.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. WIBERG J. S., DIRKSEN M. L., EPSTEIN R. H., LURIA S. E., BUCHANAN J. M. Early enzyme synthesis and its control in E. coli infected with some amber mutants of bacteriophage T4. Proc Natl Acad Sci U S A. 1962 Feb;48:293–302. doi: 10.1073/pnas.48.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wiberg J. S., Mendelsohn S., Warner V., Hercules K., Aldrich C., Munro J. L. SP62, a viable mutant of bacteriophage T4D defective in regulation of phage enzyme synthesis. J Virol. 1973 Oct;12(4):775–792. doi: 10.1128/jvi.12.4.775-792.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wood W. B., Conley M. P., Lyle H. L., Dickson R. C. Attachment of tail fibers in bacteriophage T4 assembly. Purification, properties, and site of action of the accessory protein coded by gene 63. J Biol Chem. 1978 Apr 10;253(7):2437–2445. [PubMed] [Google Scholar]
  49. Wood W. B., Revel H. R. The genome of bacteriophage T4. Bacteriol Rev. 1976 Dec;40(4):847–868. doi: 10.1128/br.40.4.847-868.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yates J. L., Arfsten A. E., Nomura M. In vitro expression of Escherichia coli ribosomal protein genes: autogenous inhibition of translation. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1837–1841. doi: 10.1073/pnas.77.4.1837. [DOI] [PMC free article] [PubMed] [Google Scholar]

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