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. 1990 May;9(5):1383–1389. doi: 10.1002/j.1460-2075.1990.tb08253.x

The optional E. coli prr locus encodes a latent form of phage T4-induced anticodon nuclease.

R Levitz 1, D Chapman 1, M Amitsur 1, R Green 1, L Snyder 1, G Kaufmann 1
PMCID: PMC551823  PMID: 1691706

Abstract

The optional Escherichia coli prr locus restricts phage T4 mutants lacking polynucleotide kinase or RNA ligase. Underlying this restriction is the specific manifestation of the T4-induced anticodon nuclease, an enzyme which triggers the cleavage-ligation of the host tRNALys. We report here the molecular cloning, nucleotide sequence and mutational analysis of prr-associated DNA. The results indicate that prr encodes a latent form of anticodon nuclease consisting of a core enzyme and cognate masking agents. They suggest that the T4-encoded factors of anticodon nuclease counteract the prr-encoded masking agents, thus activating the latent enzyme. The encoding of a tRNA cleavage-ligation pathway by two separate genetic systems which cohabitate E. coli may provide a clue to the evolution of RNA splicing mechanisms mediated by proteins.

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Selected References

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

  1. Amitsur M., Levitz R., Kaufmann G. Bacteriophage T4 anticodon nuclease, polynucleotide kinase and RNA ligase reprocess the host lysine tRNA. EMBO J. 1987 Aug;6(8):2499–2503. doi: 10.1002/j.1460-2075.1987.tb02532.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amitsur M., Morad I., Kaufmann G. In vitro reconstitution of anticodon nuclease from components encoded by phage T4 and Escherichia coli CTr5X. EMBO J. 1989 Aug;8(8):2411–2415. doi: 10.1002/j.1460-2075.1989.tb08371.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cami B., Kourilsky P. Screening of cloned recombinant DNA in bacteria by in situ colony hybridization. Nucleic Acids Res. 1978 Jul;5(7):2381–2390. doi: 10.1093/nar/5.7.2381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chapman D., Morad I., Kaufmann G., Gait M. J., Jorissen L., Snyder L. Nucleotide and deduced amino acid sequence of stp: the bacteriophage T4 anticodon nuclease gene. J Mol Biol. 1988 Jan 20;199(2):373–377. doi: 10.1016/0022-2836(88)90320-8. [DOI] [PubMed] [Google Scholar]
  5. David M., Borasio G. D., Kaufmann G. Bacteriophage T4-induced anticodon-loop nuclease detected in a host strain restrictive to RNA ligase mutants. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7097–7101. doi: 10.1073/pnas.79.23.7097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Depew R. E., Cozzarelli N. R. Genetics and physiology of bacteriophage T4 3'-phosphatase: evidence for involvement of the enzyme in T4 DNA metabolism. J Virol. 1974 Apr;13(4):888–897. doi: 10.1128/jvi.13.4.888-897.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Greer C. L., Peebles C. L., Gegenheimer P., Abelson J. Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell. 1983 Feb;32(2):537–546. doi: 10.1016/0092-8674(83)90473-7. [DOI] [PubMed] [Google Scholar]
  8. Henikoff S. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol. 1987;155:156–165. doi: 10.1016/0076-6879(87)55014-5. [DOI] [PubMed] [Google Scholar]
  9. Herrero A., Elhai J., Hohn B., Wolk C. P. Infrequent cleavage of cloned Anabaena variabilis DNA by restriction endonucleases from A. variabilis. J Bacteriol. 1984 Nov;160(2):781–784. doi: 10.1128/jb.160.2.781-784.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jabbar M. A., Snyder L. Genetic and physiological studies of an Escherichia coli locus that restricts polynucleotide kinase- and RNA ligase-deficient mutants of bacteriophage T4. J Virol. 1984 Aug;51(2):522–529. doi: 10.1128/jvi.51.2.522-529.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kano-Sueoka T., Sueoka N. Characterization of a modified leucyl-tRNA of Escherichia coli after bacteriophage T2 infection. J Mol Biol. 1968 Nov 14;37(3):475–491. doi: 10.1016/0022-2836(68)90116-2. [DOI] [PubMed] [Google Scholar]
  12. Kaufmann G., David M., Borasio G. D., Teichmann A., Paz A., Amitsur M. Phage and host genetic determinants of the specific anticodon loop cleavages in bacteriophage T4-infected Escherichia coli CTr5X. J Mol Biol. 1986 Mar 5;188(1):15–22. doi: 10.1016/0022-2836(86)90476-6. [DOI] [PubMed] [Google Scholar]
  13. Runnels J. M., Soltis D., Hey T., Snyder L. Genetic and physiological studies of the role of the RNA ligase of bacteriophage T4. J Mol Biol. 1982 Jan 15;154(2):273–286. doi: 10.1016/0022-2836(82)90064-x. [DOI] [PubMed] [Google Scholar]
  14. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sirotkin K., Cooley W., Runnels J., Snyder L. R. A role in true-late gene expression for the T4 bacteriophage 5' polynucleotide kinase 3' phosphatase. J Mol Biol. 1978 Aug 5;123(2):221–233. doi: 10.1016/0022-2836(78)90322-4. [DOI] [PubMed] [Google Scholar]
  16. Snyder L., Gold L., Kutter E. A gene of bacteriophage T4 whose product prevents true late transcription on cytosine-containing T4 DNA. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3098–3102. doi: 10.1073/pnas.73.9.3098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Way J. C., Davis M. A., Morisato D., Roberts D. E., Kleckner N. New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene. 1984 Dec;32(3):369–379. doi: 10.1016/0378-1119(84)90012-x. [DOI] [PubMed] [Google Scholar]
  18. Wood W. B. Host specificity of DNA produced by Escherichia coli: bacterial mutations affecting the restriction and modification of DNA. J Mol Biol. 1966 Mar;16(1):118–133. doi: 10.1016/s0022-2836(66)80267-x. [DOI] [PubMed] [Google Scholar]
  19. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]

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