Degradation of FinP antisense RNA from F-like plasmids: The RNA-binding protein, FinO, protects FinP from ribonuclease E

Journal of Molecular Biology

Volumn 285, Issue 4, 1999, Pages 1457-1473

  Jerome, Lori J ^a   Van Biesen, Tim ^a   Frost, Laura S ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Antisense RNA; F like plasmids; Fertility inhibition; RNA decay; RNase E

Indexed keywords

COMPLEMENTARY RNA; HYBRID PROTEIN; RIBONUCLEASE; RNA BINDING PROTEIN;

ARTICLE; CONTROLLED STUDY; NONHUMAN; NORTHERN BLOTTING; PLASMID; POINT MUTATION; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA DEGRADATION;

EID: 0033613914     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2404     Document Type: Article

References (64)

1. Arraiano C. M., Yancey S. D., Kushner S. R. Stabilization of discrete mRNA breakdown products in ams pnp rnb multiple mutants of Escherichia coli K-12. J. Bacteriol. 170:1988;4625-4633.
2. Bessarab D. A., Kaberdin V. R., Wei C.-L., Liou G.-G., Lin-Chao S. RNA components of Escherichia coli degradasome: evidence for rRNA decay. Proc. Natl Acad. Sci. USA. 95:1998;3157-3161.
3. Blomberg P., Wagner E. G. H., Nordström K. Control of replication of plasmid R1: the duplex between the antisense RNA, CopA and its target, CopT, is processed specifically in vivo and in vitro by RNase III. EMBO J. 9:1990;2331-2340.
4. Cam K., Rome G., Krisch H. M., Bouché J.-P. RNase E processing of essential cell division genes mRNA in Escherichia coli. Nucl. Acids Res. 24:1996;3065-3070.
5. Case C. C., Simons E. L., Simons R. W. The 1S 10 transposase mRNA is destabilized during antisense RNA control. EMBO J. 9:1990;1259-1266.
6. Chandler M., Galas D. Cointegrate formation mediated by Tn 9. II. Activity of IS 1 is modulated by external DNA sequences. J. Mol. Biol. 170:1983;61-91.
7. Cheah K.-C., Skurray R. The F plasmid contains an IS 3 insertion within finO. J. Gen. Microbiol. 132:1986;3269-3275.
8. Coburn G. A., Mackie G. A. Overexpression, purification, and properties of Escherichia coli ribonuclease II. J. Biol. Chem. 271:1996;1048-1053.
9. Cormack R. S., Genereaux J. L., Mackie G. A. RNase E activity is conferred by a single polypeptide: overexpression, purification, and properties of theams/rne/hmpl gene product. Proc. Natl Acad. Sci. USA. 90:1993;9006-9010.
10. Dempsey W. B. Transcript analysis of the plasmid R100 traJ and finP genes. Mol. Gen. Genet. 209:1987;533-544.
11. Dempsey W. B. traJ sense RNA initiates at two different promoters in R100-1 and forms two stable hybrids with antisensefinP RNA. Mol. Microbiol. 13:1994;313-326.
12. Donovan W. P., Kushner S. R. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc. Natl Acad. Sci. USA. 83:1986;120-124.
13. Dunn J. J., Studier F. W. T7 early RNA's and Escherichia coli ribosomal RNA's are cut from large precursor RNA's in vivo by ribonuclease III. Proc. Natl Acad. Sci. USA. 70:1973;3296-3300.
14. Ehretsmann C. P., Carpousis A. J., Krisch H. M. Specificity of Escherichia coli endoribonuclease RNase E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes Dev. 6:1992;149-159.
15. Faubladier M., Cam K., Bouche J.-P. Escherichia coli cell division inhibitor DicF-RNA of the dicB operon. Evidence for its generationin vivo and in vitro by transcription termination and by RNase III- and RNase E-dependent processing. J. Mol. Biol. 212:1990;461-471.
16. Finlay B. B., Frost L. S., Paranchych W., Willetts N. S. Nucleotide sequences of five IncF plasmid finP allelles. J. Bacteriol. 167:1986;754-757.
17. Finnegan D. J., Willetts N. S. Two classes of F lac mutants insensitive to transfer inhibition by an F-like R factor. Mol. Gen. Genet. 111:1971;256-264.
18. Finnegan D. J., Willetts N. S. The site of action of the F transfer inhibitor. Mol. Gen. Genet. 127:1973;307-316.
19. Frost L. S., Lee S., Yanchar N., Paranchych W. finP and fisO mutations in FinP antisense RNA suggest a model for FinOP action in the repression of bacterial conjugation by the F lac plasmid JCFLO. Mol. Gen. Genet. 218:1989;152-160.
20. Frost L. S., Ippen-Ihler K., Skurray R. A. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev. 58:1994;162-210.
21. Gerdes K., Nielsen A., Thorsted P., Wagner E. G. H. Mechanism of killer gene activation. Antisense RNA-dependent RNase III cleavage ensures rapid turn-over of the stable Hok, SrnB and PndA effector messenger RNAs. J. Mol. Biol. 226:1992;637-649.
22. Hanahan D. Studies on the transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:1983;557-580.
23. Hjalt T. A., Wagner E. G. H. The effect of loop size in antisense and target RNAs on the efficiency of antisense RNA control. Nucl. Acids Res. 20:1992;6723-6732.
24. Hjalt T. A., Wagner E. G. H. Bulged-out-nucleotides protect an antisense RNA from RNase III cleavage. Nucl. Acids Res. 23:1995;571-579.
25. Huang H., Liao J., Cohen S. N. Poly(A)- and poly(U)-specific RNA 3′ tail shortening by E. coli ribonuclease E. Nature. 391:1998;99-102.
26. Jain C., Kleckner N. IS 10 mRNA stability and steady-state levels in Escherichia coli: indirect effects of translation and role of rne function. Mol. Microbiol. 9:1993;233-247.
27. Kaberdin V. R., Chao Y.-H., Lin-Chao S. RNase E cleaves at multiple sites in bubble regions of RNA I stem loops yielding products that dissociate differentially from the enzyme. J. Biol. Chem. 271:1996;13103-13109.
28. Koraimann G., Koraimann C., Koronakis V., Schlager S., Högenauer G. Repression and derepression of conjugation of plasmid R1 by wild-type and mutated finP antisense RNA. Mol. Microbiol. 5:1991;77-87.
29. Koraimann G., Teferle K., Markolin G., Woger W., Högenauer G. The FinOP repressor system of plasmid RI: analysis of the antisense RNA control of traJ expression and conjugative DNA transfer. Mol. Microbiol. 21:1996;811-821.
30. Krinke L., Wulff D. L. OOP RNA, produced from multicopy plasmids, inhibits λc II gene expression through an RNase III-dependent mechanism. Genes Dev. 1:1987;1005-1013.
31. Krinke L., Wulff D. L. The cleavage specificity of RNase III. Nucl. Acids Res. 18:1990a;4809-4815.
32. Krinke L., Wulff D. L. RNase III-dependent hydrolysis of λc II- O gene mRNA mediated by λ OOP antisense RNA. Genes Dev. 4:1990b;2223-2233.
33. Lee S. H., Frost L. S., Paranchych W. FinOP repression of the F plasmid involves extension of the half-life of FinP antisense RNA by FinO. Mol. Gen. Genet. 235:1992;131-139.
34. Lin-Chao S., Wong T. T., McDowall K. J., Cohen S. N. Effects of nucleotide sequence on the specificity of rne -dependent and RNase E-mediated cleavages of RNA I encoded by the pBR322 plasmid. J. Biol. Chem. 269:1994;10797-10803.
35. Littauer U. Z., Soreq H. Polynucleotide phosphorylase. Boyer D. The Enzymes. 1982;518-553 Academic Press, New York.
36. Mackie G. A. Specific endonucleolytic cleavage of the mRNA for ribosomal protein S20 of Escherichia coli requires the product of the ams gene in vivo and in vitro. J. Bacteriol. 173:1991;2488-2497.
37. Mackie G. A. Secondary structure of the mRNA for ribosomal protein S20: implications for cleavage by ribonuclease E. J. Biol. Chem. 267:1992;1054-1061.
38. McDowall K. J., Lin-Chao S., Cohen S. N. A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J. Biol. Chem. 269:1994;10790-10796.
39. McLaren R. S., Newbury S. F., Dance G. S. C., Causton H. C., Higgins C. F. mRNA degradation by processive 3′-5′ exoribonucleases in vitro and the implications for prokaryotic mRNA decay in vivo. J. Mol. Biol. 221:1991;81-95.
40. Mikkelsen N. D., Gerdes K. Sok antisense RNA from plasmid R1 is functionally inactivated by RNase E and polyadenylated by poly(A) polymerase I. Mol. Microbiol. 26:1997;311-320.
41. Misra T. K., Apirion D. RNase E an RNA processing enzyme from Escherichia coli. J. Biol. Chem. 254:1979;11154-11159.
42. Mudd E. A., Carpousis A. J., Krisch H. M. Escherichia coli RNase E has a role in the decay of bacteriophage T4 mRNA. Genes Dev. 4:1990;873-881.
43. Mullineaux P., Willetts N. S. Promoters in the transfer region of plasmid F. Helinski D. R., Cohen S. N., Clewell D. B., Jackson D. A., Hollaender A. Plasmids in Bacteria. 1985;605-614 Plenum Publishing Corp. New York.
44. Pansegrau W., Lanka E., Barth P. T., Figurski D. H., Guiney D. G., Haas D., Helinski D. R., Schwab H., Stanisch V. A., Thomas C. M. Complete nucleotide sequence of the Birmingham IncP alpha plasmids. Compilation and comparative analysis. J. Mol. Biol. 239:1994;623-663.
45. Patel A. M., Dunn S. D. RNase E-dependent cleavages in the 5′ and 3′ regions of the Escherichia coli unc mRNA. J. Bacteriol. 174:1992;3541-3548.
46. Plumbridge J. A., Dondon J., Nakamura Y., Grunberg-Manago M. Effect of NusA protein on expression of the nusA, infB operon in E. coli. Nucl. Acids Res. 13:1985;3371-3388.
47. Régnier P., Hajnsdorf E. The decay of mRNA encoding protein S15 of Escherichia coli is initiated by a RNase E-dependent endonucleolytic cleavage which removes the 3′ stabilizing stem and loop structures. J. Mol. Biol. 217:1991;283-292.
48. Robertson H. D., Webster R. E., Zinder N. D. Purification and properties of ribonuclease III from Escherichia coli. J. Biol. Chem. 243:1968;82-91.
49. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning. A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
50. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA. 74:1977;5463-5467.
51. Schmidt M., Delihas N. mic F RNA is a substrate for RNase E. FEMS Microbiol. Letters. 133:1995;209-213.
52. Shen V., Schlessinger D. RNases I, II, and IV of Escherichia coli. Boyer P. E. The Enzymes. 1982;501-515 Academic Press, New York.
53. Söderbom F., Binnie U., Masters M., Wagner E. G. H. Regulation of plasmid R1 replication: PcnB and RNase E expedite the decay of the antisense CopA. Mol. Microbiol. 26:1997;495-504.
54. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad. Sci. USA. 82:1985;1074-1078.
55. Tomcsanyi T., Apirion D. Processing enzyme ribonuclease E specifically cleaves RNA I, an inhibitor of primer formation in plasmid DNA synthesis. J. Mol. Biol. 185:1985;713-720.
56. van Biesen T. PhD thesis. 1994;University of Alberta. Edmonton, Alberta.
57. van Biesen T., Frost L. S. Differential levels of fertility inhibition among F-like plasmids are related to the cellular concentration offinO mRNA. Mol. Microbiol. 6:1992;771-780.
58. van Biesen T., Frost L. S. The FinO protein of IncF plasmids binds FinP antisense RNA and its target, traJ mRNA, and promotes duplex formation. Mol. Microbiol. 14:1994;427-436.
59. van Biesen T., Söderbom F., Wagner E. G. H., Frost L. S. Structural and functional analyses of the FinP antisense RNA regulatory system of the F conjugative plasmid. Mol. Microbiol. 10:1993;35-43.
60. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 19:1982;259-268.
61. Wagner E. G. H., Simons R. W. Antisense RNA control in bacteria, phages, and plasmids. Annu. Rev. Microbiol. 48:1994;713-742.
62. Willetts N. S., Maule J. Specificities of IncF plasmid conjugation genes. Genet. Res. 47:1986;1-11.
63. Yoshioka Y., Ohtsubo H., Ohtsubo E. Repressor gene finO in plasmid R100 and F: constitutive transfer of plasmid F is caused by insertion of IS3 in F finO. J. Bacteriol. 169:1987;619-623.
64. Zuker M. On finding all suboptimal foldings of an RNA molecule. Science. 244:1989;48-52.