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. 1994 Apr;176(7):2082–2089. doi: 10.1128/jb.176.7.2082-2089.1994

Role for 10Sa RNA in the growth of lambda-P22 hybrid phage.

D M Retallack 1, L L Johnson 1, D I Friedman 1
PMCID: PMC205314  PMID: 8144474

Abstract

Certain lambda-P22 hybrids, providing that they express the P22 C1 protein, fail to grow in Escherichia coli with the sipB391 mutation. We show that sipB391, previously located to the 57-min region of the E. coli chromosome, is a large deletion that extends into the 3' end of ssrA, a gene encoding the small stable 10Sa RNA. This deletion, apparently created by the excision of a cryptic prophage, CP4-57 (identified by Kirby et al. [J. E. Kirby, J. E. Trempy, and S. Gottesman, J. Bacteriol. 176:2068-2081]), leaves most of ssrA intact but removes the sequence encoding the 3' end of the precursor form of 10Sa RNA. The lack of functional 10Sa RNA, resulting from either the excision of CP4-57 or insertional inactivation of ssrA, appears to be responsible for the inhibition of lambda-P22 growth in E. coli with the sipB391 mutation. We propose that 10Sa RNA acts either directly or indirectly to facilitate removal of C1 protein from its DNA target site.

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Selected References

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

  1. Backhaus H., Petri J. B. Sequence analysis of a region from the early right operon in phage P22 including the replication genes 18 and 12. Gene. 1984 Dec;32(3):289–303. doi: 10.1016/0378-1119(84)90004-0. [DOI] [PubMed] [Google Scholar]
  2. Barondess J. J., Beckwith J. A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature. 1990 Aug 30;346(6287):871–874. doi: 10.1038/346871a0. [DOI] [PubMed] [Google Scholar]
  3. Bear S. E., Court D. L., Friedman D. I. An accessory role for Escherichia coli integration host factor: characterization of a lambda mutant dependent upon integration host factor for DNA packaging. J Virol. 1984 Dec;52(3):966–972. doi: 10.1128/jvi.52.3.966-972.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bolivar F. Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique Eco RI sites for selection of Eco RI generated recombinant DNA molecules. Gene. 1978 Oct;4(2):121–136. doi: 10.1016/0378-1119(78)90025-2. [DOI] [PubMed] [Google Scholar]
  5. Botstein D., Herskowitz I. Properties of hybrids between Salmonella phage P22 and coliphage lambda. Nature. 1974 Oct 18;251(5476):584–589. doi: 10.1038/251584a0. [DOI] [PubMed] [Google Scholar]
  6. Brown J. W., Hunt D. A., Pace N. R. Nucleotide sequence of the 10Sa RNA gene of the beta-purple eubacterium Alcaligenes eutrophus. Nucleic Acids Res. 1990 May 11;18(9):2820–2820. doi: 10.1093/nar/18.9.2820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Calendar R., Ljungquist E., Deho G., Usher D. C., Goldstein R., Youderian P., Sironi G., Six E. W. Lysogenization by satellite phage P4. Virology. 1981 Aug;113(1):20–38. doi: 10.1016/0042-6822(81)90133-1. [DOI] [PubMed] [Google Scholar]
  8. Campbell A. M. Chromosomal insertion sites for phages and plasmids. J Bacteriol. 1992 Dec;174(23):7495–7499. doi: 10.1128/jb.174.23.7495-7499.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chauhan A. K., Apirion D. The gene for a small stable RNA (10Sa RNA) of Escherichia coli. Mol Microbiol. 1989 Nov;3(11):1481–1485. doi: 10.1111/j.1365-2958.1989.tb00133.x. [DOI] [PubMed] [Google Scholar]
  10. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fien K., Turck A., Kang I., Kielty S., Wulff D. L., McKenney K., Rosenberg M. CII-dependent activation of the pRE promoter of coliphage lambda fused to the Escherichia coli galK gene. Gene. 1984 Dec;32(1-2):141–150. doi: 10.1016/0378-1119(84)90042-8. [DOI] [PubMed] [Google Scholar]
  12. Friedman D. I. Interaction between bacteriophage lambda and its Escherichia coli host. Curr Opin Genet Dev. 1992 Oct;2(5):727–738. doi: 10.1016/s0959-437x(05)80133-9. [DOI] [PubMed] [Google Scholar]
  13. Friedman D. I., Olson E. R., Georgopoulos C., Tilly K., Herskowitz I., Banuett F. Interactions of bacteriophage and host macromolecules in the growth of bacteriophage lambda. Microbiol Rev. 1984 Dec;48(4):299–325. doi: 10.1128/mr.48.4.299-325.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Friedman D. I., Olson E. R., Johnson L. L., Alessi D., Craven M. G. Transcription-dependent competition for a host factor: the function and optimal sequence of the phage lambda boxA transcription antitermination signal. Genes Dev. 1990 Dec;4(12A):2210–2222. doi: 10.1101/gad.4.12a.2210. [DOI] [PubMed] [Google Scholar]
  15. Gemski P., Jr, Baron L. S., Yamamoto N. Formation of hybrids between coliphage lambda and Salmonella phage P22 with a Salmonella typhimurium hybrid sensitive to these phages. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3110–3114. doi: 10.1073/pnas.69.11.3110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hilliker S., Botstein D. Specificity of genetic elements controlling regulation of early functions in temperate bacteriophages. J Mol Biol. 1976 Sep 25;106(3):537–566. doi: 10.1016/0022-2836(76)90251-5. [DOI] [PubMed] [Google Scholar]
  17. Ho Y. S., Pfarr D., Strickler J., Rosenberg M. Characterization of the transcription activator protein C1 of bacteriophage P22. J Biol Chem. 1992 Jul 15;267(20):14388–14397. [PubMed] [Google Scholar]
  18. Ho Y. S., Wulff D. L., Rosenberg M. Bacteriophage lambda protein cII binds promoters on the opposite face of the DNA helix from RNA polymerase. Nature. 1983 Aug 25;304(5928):703–708. doi: 10.1038/304703a0. [DOI] [PubMed] [Google Scholar]
  19. Ji H., Moore D. P., Blomberg M. A., Braiterman L. T., Voytas D. F., Natsoulis G., Boeke J. D. Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell. 1993 Jun 4;73(5):1007–1018. doi: 10.1016/0092-8674(93)90278-x. [DOI] [PubMed] [Google Scholar]
  20. KAISER A. D. Mutations in a temperate bacteriophage affecting its ability to lysogenize Escherichia coli. Virology. 1957 Feb;3(1):42–61. doi: 10.1016/0042-6822(57)90022-3. [DOI] [PubMed] [Google Scholar]
  21. Kirby J. E., Trempy J. E., Gottesman S. Excision of a P4-like cryptic prophage leads to Alp protease expression in Escherichia coli. J Bacteriol. 1994 Apr;176(7):2068–2081. doi: 10.1128/jb.176.7.2068-2081.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. LEVINE M. Mutations in the temperate phage P22 and lysogeny in Salmonella. Virology. 1957 Feb;3(1):22–41. doi: 10.1016/0042-6822(57)90021-1. [DOI] [PubMed] [Google Scholar]
  23. Leason K. R., Friedman D. I. Analysis of transcription termination signals in the nin region of bacteriophage lambda: the roc deletion. J Bacteriol. 1988 Nov;170(11):5051–5058. doi: 10.1128/jb.170.11.5051-5058.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lee S. Y., Bailey S. C., Apirion D. Small stable RNAs from Escherichia coli: evidence for the existence of new molecules and for a new ribonucleoprotein particle containing 6S RNA. J Bacteriol. 1978 Feb;133(2):1015–1023. doi: 10.1128/jb.133.2.1015-1023.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Levine M., Truesdell S., Ramakrishnan T., Bronson M. J. Dual control of lysogeny by bacteriophage P22: an antirepressor locus and its controlling elements. J Mol Biol. 1975 Feb 5;91(4):421–438. doi: 10.1016/0022-2836(75)90270-3. [DOI] [PubMed] [Google Scholar]
  26. Lindsey D. F., Mullin D. A., Walker J. R. Characterization of the cryptic lambdoid prophage DLP12 of Escherichia coli and overlap of the DLP12 integrase gene with the tRNA gene argU. J Bacteriol. 1989 Nov;171(11):6197–6205. doi: 10.1128/jb.171.11.6197-6205.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mozola M. A., Friedman D. I., Crawford C. L., Wulff D. L., Shimatake H., Rosenberg M. Mutations reducing the activity of c17, a promoter of phage lambda formed by a tandem duplication. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1122–1125. doi: 10.1073/pnas.76.3.1122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Oh B. K., Apirion D. 10Sa RNA, a small stable RNA of Escherichia coli, is functional. Mol Gen Genet. 1991 Sep;229(1):52–56. doi: 10.1007/BF00264212. [DOI] [PubMed] [Google Scholar]
  29. Oh B. K., Chauhan A. K., Isono K., Apirion D. Location of a gene (ssrA) for a small, stable RNA (10Sa RNA) in the Escherichia coli chromosome. J Bacteriol. 1990 Aug;172(8):4708–4709. doi: 10.1128/jb.172.8.4708-4709.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Poteete A. R., Hehir K., Sauer R. T. Bacteriophage P22 Cro protein: sequence, purification, and properties. Biochemistry. 1986 Jan 14;25(1):251–256. doi: 10.1021/bi00349a035. [DOI] [PubMed] [Google Scholar]
  31. Retallack D. M., Johnson L. L., Ziegler S. F., Strauch M. A., Friedman D. I. A single-base-pair mutation changes the specificities of both a transcription activation protein and its binding site. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9562–9565. doi: 10.1073/pnas.90.20.9562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sternberg N. L., Maurer R. Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol. 1991;204:18–43. doi: 10.1016/0076-6879(91)04004-8. [DOI] [PubMed] [Google Scholar]
  33. Strauch M. A., Baumann M., Friedman D. I., Baron L. S. Identification and characterization of mutations in Escherichia coli that selectively influence the growth of hybrid lambda bacteriophages carrying the immunity region of bacteriophage P22. J Bacteriol. 1986 Jul;167(1):191–200. doi: 10.1128/jb.167.1.191-200.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Subbarao M. N., Apirion D. A precursor for a small stable RNA (10Sa RNA) of Escherichia coli. Mol Gen Genet. 1989 Jun;217(2-3):499–504. doi: 10.1007/BF02464923. [DOI] [PubMed] [Google Scholar]
  35. Sun J., Inouye M., Inouye S. Association of a retroelement with a P4-like cryptic prophage (retronphage phi R73) integrated into the selenocystyl tRNA gene of Escherichia coli. J Bacteriol. 1991 Jul;173(13):4171–4181. doi: 10.1128/jb.173.13.4171-4181.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Susskind M. M., Botstein D. Mechanism of action of Salmonella phage P22 antirepressor. J Mol Biol. 1975 Oct 25;98(2):413–424. doi: 10.1016/s0022-2836(75)80127-6. [DOI] [PubMed] [Google Scholar]
  37. Susskind M. M., Botstein D. Molecular genetics of bacteriophage P22. Microbiol Rev. 1978 Jun;42(2):385–413. doi: 10.1128/mr.42.2.385-413.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Trempy J. E., Kirby J. E., Gottesman S. Alp suppression of Lon: dependence on the slpA gene. J Bacteriol. 1994 Apr;176(7):2061–2067. doi: 10.1128/jb.176.7.2061-2067.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tyagi J. S., Kinger A. K. Identification of the 10Sa RNA structural gene of Mycobacterium tuberculosis. Nucleic Acids Res. 1992 Jan 11;20(1):138–138. doi: 10.1093/nar/20.1.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wulff D. L., Mahoney M. E. Cross-specificities between cII-like proteins and pRE-like promoters of lambdoid bacteriophages. Genetics. 1987 Apr;115(4):597–604. doi: 10.1093/genetics/115.4.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yamamoto N., Wohlhieter J. A., Gemski P., Baron L. S. lambdaimm P22dis: a hybrid of coliphage lambda with both immunity regions of Salmonella phage P22. Mol Gen Genet. 1978 Nov 9;166(3):233–243. [PubMed] [Google Scholar]
  42. 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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