Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1990 Apr;9(4):1259–1266. doi: 10.1002/j.1460-2075.1990.tb08234.x

The IS10 transposase mRNA is destabilized during antisense RNA control.

C C Case 1, E L Simons 1, R W Simons 1
PMCID: PMC551803  PMID: 1691096

Abstract

RNA stability is an important component of gene expression, and antisense RNAs have been proposed to alter target RNA stability. We show here that the IS10 transposase mRNA, RNA-IN, is rendered unstable during control by the IS10 antisense RNA, RNA-OUT. Destabilization requires RNA-OUT/RNA-IN pairing and ribonuclease III cleavage. Independent of such cleavage, RNA-OUT is rendered unstable through disruption of its secondary structure. Pairing has no other obvious effects on RNA-IN transcription or stability. Nevertheless, RNA-IN destabilization is not required for antisense control in vivo. In the accompanying paper [Ma,C. and Simons, R.W. (1990) EMBO J., 9, 1267-1274 we show that pairing blocks ribosome binding to RNA-IN. Were it not for control at this level, destabilization would play a more prominent role.

Full text

PDF
1259

Images in this article

1260Fig. 2.
on p.1260
1261Fig. 3.
on p.1261
1262Fig. 4.
on p.1262
1262Fig. 5.
on p.1262
1263Fig. 6.
on p.1263
1264Fig. 7.
on p.1264

Selected References

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

  1. Belasco J. G., Higgins C. F. Mechanisms of mRNA decay in bacteria: a perspective. Gene. 1988 Dec 10;72(1-2):15–23. doi: 10.1016/0378-1119(88)90123-0. [DOI] [PubMed] [Google Scholar]
  2. Case C. C., Roels S. M., González J. E., Simons E. L., Simons R. W. Analysis of the promoters and transcripts involved in IS10 anti-sense RNA control. Gene. 1988 Dec 10;72(1-2):219–236. doi: 10.1016/0378-1119(88)90147-3. [DOI] [PubMed] [Google Scholar]
  3. Case C. C., Roels S. M., Jensen P. D., Lee J., Kleckner N., Simons R. W. The unusual stability of the IS10 anti-sense RNA is critical for its function and is determined by the structure of its stem-domain. EMBO J. 1989 Dec 20;8(13):4297–4305. doi: 10.1002/j.1460-2075.1989.tb08616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Daniels D. L., Subbarao M. N., Blattner F. R., Lozeron H. A. Q-mediated late gene transcription of bacteriophage lambda: RNA start point and RNase III processing sites in vivo. Virology. 1988 Dec;167(2):568–577. [PubMed] [Google Scholar]
  5. Dempsey W. B. Transcript analysis of the plasmid R100 traJ and finP genes. Mol Gen Genet. 1987 Oct;209(3):533–544. doi: 10.1007/BF00331160. [DOI] [PubMed] [Google Scholar]
  6. Finlay B. B., Frost L. S., Paranchych W., Willetts N. S. Nucleotide sequences of five IncF plasmid finP alleles. J Bacteriol. 1986 Aug;167(2):754–757. doi: 10.1128/jb.167.2.754-757.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Foster T. J., Lundblad V., Hanley-Way S., Halling S. M., Kleckner N. Three Tn10-associated excision events: relationship to transposition and role of direct and inverted repeats. Cell. 1981 Jan;23(1):215–227. doi: 10.1016/0092-8674(81)90286-5. [DOI] [PubMed] [Google Scholar]
  8. Guarneros G. Retroregulation of bacteriophage lambda int gene expression. Curr Top Microbiol Immunol. 1988;136:1–19. doi: 10.1007/978-3-642-73115-0_1. [DOI] [PubMed] [Google Scholar]
  9. Halling S. M., Simons R. W., Way J. C., Walsh R. B., Kleckner N. DNA sequence organization of IS10-right of Tn10 and comparison with IS10-left. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2608–2612. doi: 10.1073/pnas.79.8.2608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kim K., Meyer R. J. Copy-number of broad host-range plasmid R1162 is regulated by a small RNA. Nucleic Acids Res. 1986 Oct 24;14(20):8027–8046. doi: 10.1093/nar/14.20.8027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. King T. C., Sirdeskmukh R., Schlessinger D. Nucleolytic processing of ribonucleic acid transcripts in procaryotes. Microbiol Rev. 1986 Dec;50(4):428–451. doi: 10.1128/mr.50.4.428-451.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kittle J. D., Simons R. W., Lee J., Kleckner N. Insertion sequence IS10 anti-sense pairing initiates by an interaction between the 5' end of the target RNA and a loop in the anti-sense RNA. J Mol Biol. 1989 Dec 5;210(3):561–572. doi: 10.1016/0022-2836(89)90132-0. [DOI] [PubMed] [Google Scholar]
  13. Krinke L., Wulff D. L. OOP RNA, produced from multicopy plasmids, inhibits lambda cII gene expression through an RNase III-dependent mechanism. Genes Dev. 1987 Nov;1(9):1005–1013. doi: 10.1101/gad.1.9.1005. [DOI] [PubMed] [Google Scholar]
  14. Liao S. M., Wu T. H., Chiang C. H., Susskind M. M., McClure W. R. Control of gene expression in bacteriophage P22 by a small antisense RNA. I. Characterization in vitro of the Psar promoter and the sar RNA transcript. Genes Dev. 1987 Apr;1(2):197–203. doi: 10.1101/gad.1.2.197. [DOI] [PubMed] [Google Scholar]
  15. Ma C., Simons R. W. The IS10 antisense RNA blocks ribosome binding at the transposase translation initiation site. EMBO J. 1990 Apr;9(4):1267–1274. doi: 10.1002/j.1460-2075.1990.tb08235.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mizuno T., Chou M. Y., Inouye M. A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci U S A. 1984 Apr;81(7):1966–1970. doi: 10.1073/pnas.81.7.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Novick R. P., Iordanescu S., Projan S. J., Kornblum J., Edelman I. pT181 plasmid replication is regulated by a countertranscript-driven transcriptional attenuator. Cell. 1989 Oct 20;59(2):395–404. doi: 10.1016/0092-8674(89)90300-0. [DOI] [PubMed] [Google Scholar]
  18. Roberts D., Hoopes B. C., McClure W. R., Kleckner N. IS10 transposition is regulated by DNA adenine methylation. Cell. 1985 Nov;43(1):117–130. doi: 10.1016/0092-8674(85)90017-0. [DOI] [PubMed] [Google Scholar]
  19. Robertson H. D. Escherichia coli ribonuclease III cleavage sites. Cell. 1982 Oct;30(3):669–672. doi: 10.1016/0092-8674(82)90270-7. [DOI] [PubMed] [Google Scholar]
  20. Schollmeier K., Hillen W. Transposon Tn10 contains two structural genes with opposite polarity between tetA and IS10R. J Bacteriol. 1984 Nov;160(2):499–503. doi: 10.1128/jb.160.2.499-503.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shapiro D. J., Blume J. E., Nielsen D. A. Regulation of messenger RNA stability in eukaryotic cells. Bioessays. 1987 May;6(5):221–226. doi: 10.1002/bies.950060507. [DOI] [PubMed] [Google Scholar]
  22. Simons R. W., Hoopes B. C., McClure W. R., Kleckner N. Three promoters near the termini of IS10: pIN, pOUT, and pIII. Cell. 1983 Sep;34(2):673–682. doi: 10.1016/0092-8674(83)90400-2. [DOI] [PubMed] [Google Scholar]
  23. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  24. Simons R. W., Kleckner N. Biological regulation by antisense RNA in prokaryotes. Annu Rev Genet. 1988;22:567–600. doi: 10.1146/annurev.ge.22.120188.003031. [DOI] [PubMed] [Google Scholar]
  25. Simons R. W., Kleckner N. Translational control of IS10 transposition. Cell. 1983 Sep;34(2):683–691. doi: 10.1016/0092-8674(83)90401-4. [DOI] [PubMed] [Google Scholar]
  26. Simons R. W. Naturally occurring antisense RNA control--a brief review. Gene. 1988 Dec 10;72(1-2):35–44. doi: 10.1016/0378-1119(88)90125-4. [DOI] [PubMed] [Google Scholar]
  27. Takiff H. E., Chen S. M., Court D. L. Genetic analysis of the rnc operon of Escherichia coli. J Bacteriol. 1989 May;171(5):2581–2590. doi: 10.1128/jb.171.5.2581-2590.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wu T. H., Liao S. M., McClure W. R., Susskind M. M. Control of gene expression in bacteriophage P22 by a small antisense RNA. II. Characterization of mutants defective in repression. Genes Dev. 1987 Apr;1(2):204–212. doi: 10.1101/gad.1.2.204. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES