Analysis of the in vivo decay of the Escherichia coli dicistronic pyrF-orfF transcript: Evidence for multiple degradation pathways

Journal of Molecular Biology

Volumn 268, Issue 2, 1997, Pages 261-272

  Arraiano, Cecilia M ^a   Cruz, Ana A ^a   Kushner, Sidney R ^b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b University of Georgia ^*  (United States)

Author keywords

Endonucleolytic cleavages; Gene regulation; mRNA decay; RNases

Indexed keywords

GENE PRODUCT; MESSENGER RNA;

ARTICLE; ESCHERICHIA COLI; GENE CONTROL; NONHUMAN; NORTHERN BLOTTING; POLYADENYLATION; PRIORITY JOURNAL; RNA DEGRADATION;

ESCHERICHIA COLI;

EID: 0031547957     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.0962     Document Type: Article

References (54)

1. 35S]DNA probes, trichloroacetate solvent and dideoxy sequencing ladders: a rapid method for identification of transcriptional startpoints. Gene. 65:1988;101-110.
2. Alifano P., Rivellini F., Piscitelli C., Arraiano C. M., Bruni C. B., Carlomagno M. S. Ribonuclease E provides substrates for ribonuclease P-dependent processing of a polycistronic mRNA. Genes Dev. 8:1994;3021-3031.
3. Apirion D. Degradation of RNA in Escherichia coli: an hypothesis. Mol. Gen. Genet. 122:1973;313-322.
4. Apirion D. Isolation, genetic mapping and some characterization of a mutation in Escherichia coli that affects the processing of ribonucleic acid. Genetics. 90:1978;659-671.
5. 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.
6. Arraiano C. M., Yancey S. D., Kushner S. R. Identification of endonucleolytic cleavage sites involved in decay of Escherichia coli trxA mRNA. J. Bacteriol. 175:1993;1043-1052.
7. Babitzke P., Kushner S. R. The Ams (altered mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc. Natl Acad. Sci. USA. 88:1991;1-5.
8. Babitzke P., Granger L., Kushner S. R. Analysis of mRNA decay and rRNA processing in Escherichia coli multiple mutants carrying a deletion in RNase III. J. Bacteriol. 175:1993;229-239.
9. Belasco J. G. mRNA degradation in prokaryotic cells: an overview. Control of Messenger RNA Stability. 1993;Academic Press, Inc. New York.
10. Bouvet P., Belasco J. G. Control of RNase E-mediated RNA degradation by 5′ terminal base pairing in E. coli. Nature. 360:1992;488-491.
11. Cannistraro V. J., Kennell D. The 5′ ends of RNA oligonucleotides in Escherichia coli and mRNA degradation. Eur. J. Biochem. 213:1993;285-293.
12. Cannistraro V. J., Subbarao M. N., Kennell D. Specific endonucleolytic cleavage sites for decay of Escherichia coli mRNA. J. Mol. Biol. 192:1986;257-274.
13. Carpousis A. J., Van Houwe G., Ehretsmann C., Krisch H. M. Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell. 76:1994;889-900.
14. Casarégola S., Jacq A., Laoudj D., McGurk G., Margarson S., Tempête M., Norris V., Holland I. B. Cloning and analysis of the entire Escherichia coli ams gene. ams is identical to hmp-1 and encodes a 114 kDa protein that migrates as a 180 kDa protein. J. Mol. Biol. 228:1992;30-40.
15. Deutscher M. P. Promiscuous exoribonucleases of Escherichia coli. J. Bacteriol. 175:1993a;4577-4583.
16. Deutscher M. P. Ribonuclease multiplicity, diversity and complexity. J. Biol. Chem. 268:1993b;13011-13014.
17. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucl. Acids Res. 12:1984;387-395.
18. Donovan W. P., Kushner S. R. Cloning and physical analysis of the pyrF gene (coding for orotidine-5′-phosphate decarboxylase) fromEscherichia coli K-12. Gene. 25:1983;39-48.
19. 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.
20. 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.
21. Emory S. A., Bouvet P., Belasco J. G. A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev. 6:1992;135-148.
22. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:1983;6-13.
23. Fitzwater T., Zhang X.-Y., Elble R., Polisky B. Conditional high copy number ColE1 mutants; resistance to RNA1 inhibition in vivo and in vitro. EMBO J. 7:1988;3289-3297.
24. Grandbastien M. A., Berry-Lowe S., Shirley B. W., Meagher R. B. Two soybean ribulose-1,5-biphosphate carboxylase small subunit genes share extensive homology even in distant flanking sequences. Plant Mol. Biol. 7:1986;451-465.
25. Hajnsdorf E., Steier O., Coscoy L., Teysset L., Regnier P. Roles of RNase E, RNase II and PNPase in the degradation of the rpsO transcripts of Escherichia coli: stabilizing function of RNase II and evidence for efficient degradation in an ams pnp rnb mutant. EMBO J. 13:1994;3368-3377.
26. Hajnsdorf E., Braun F., Haugel-Nielsen J., Régnier P. Polyadenylylation destabilizes the rpsO mRNA of Escherichia coli. Proc. Natl Acad. Sci. USA. 92:1995;3973-3977.
27. Haugel-Nielsen J., Hajnsdorf E., Régnier P. The rpsO mRNA of Escherichia coli is polyadenylated at multiple sites resulting from endonucleolytic processing and exonucleolytic degradation. EMBO J. 15:1996;3144-3152.
28. Henry M., Yancey S. D., Kushner S. R. The role of the heat-shock response in the stability of mRNA in Escherichia coli K-12. J. Bacteriol. 174:1992;743-748.
29. Jensen K. F., J. N., L., Schack L., Sivertsen A. Studies on the structure and expression of the Escherichia coli pyrC, pyrD and pyrF using the cloned genes. Eur. J. Biochem. 140:1984;343-352.
30. Krzyzek R., Rogers P. Arginine control of transcription of argECBH messenger ribonucleic acid in Escherichia coli. J. Bacteriol. 110:1972;945-954.
31. Kushner S. R. In vivo studies of temperature sensitive recB and recC mutants. J. Bacteriol. 120:1974;1213-1218.
32. Kushner S. R. An improved method for transformation of Escherichia coli with ColE1-derived plasmids. Boyer H. W., Nicosia S. Genetic Engineering. 1978;Elsevier/North-Holland Biomedical Press, Amsterdam.
33. Kushner S. R. mRNA decay. Neidhardt F. C., Curtiss R.,III, Ingraham J. L., Lin E. C. C., Low J., K.B., Magasanik B., Reznikoff W. S., Riley M., Schaechter M., Umbarger H. E. Escherichia coli and Salmonella: Cellular and Molecular Biology. 1996;ASM Press, Washington, DC.
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. Mackie G. A. Specific endonucleolytic cleavage of the mRNA for ribosomal protein S20 of Escherichia coli requires the products of the ams gene in vivo and in vitro. J. Bacteriol. 173:1991;2488-2497.
36. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65:1980;499-560.
37. 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.
38. McDowall K. J., Kaberdin V. R., Wu S.-W., Cohen S. N., Lin-Chao S. Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature. 374:1995;287-290.
39. Melefors Ö., A. von Gabain A. Genetic studies of cleavage-initiated mRNA decay and processing of ribosomal 9S RNA show that the Escherichia coli ams and rne loci are the same. Mol. Microbiol. 5:1991;857-864.
40. Meyer B. J., Schottel J. L. Characterization of cat messenger RNA decay suggests that turnover occurs by endonucleolytic cleavage in a 3′ to 5′ direction. Mol. Microbiol. 6:1992;1095-1104.
41. Miczak A., Kaberdin V. R., Wei C.-L., Lin-Chao S. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl Acad. Sci. USA. 93:1996;3865-3869.
42. Mudd E. A., Krisch H. M., Higgins C. F. RNase E, an endoribonuclease, has a general role in the chemical decay of Escherichia coli mRNA: evidence thatrne and ams are the same genetic locus. Mol. Microbiol. 4:1990;2127-2135.
43. Murray M. G. Use of trichloroacetate and mung bean nuclease to increase sensitivity and precision during transcript mapping. Anal. Biochem. 158:1986;165-170.
44. O'Hara E. B., Chekanova J. A., Ingle C. A., Kushner Z. R., Peters E., Kushner S. R. Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proc. Natl Acad. Sci. USA. 92:1995;1807-1811.
45. Ono M., Kuwano M. A conditional lethal mutation in an Escherichia coli strain with a longer chemical lifetime of mRNA. J. Mol. Biol. 129:1979;343-357.
46. Portier C., Dondon L., Grunberg-Manago M., Regnier P. The first step in the functional inactivation of the Escherichia coli polynucleotide phosphorylase messenger is ribonuclease III processing at the 5′ end. EMBO J. 6:1987;2165-2170.
47. Py B., Causton H., Mudd E. A., Higgins C. F. A protein complex mediating mRNA degradation in Escherichia coli. Mol. Microbiol. 14:1994;717-729.
48. Py B., Higgins C. F., Krisch H. M., Carpousis A. J. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature. 381:1996;169-172.
49. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
50. Subbarao M. N., Kennell D. Evidence for endonucleolytic cleavages in decay of lacZ and lacI mRNAs. J. Bacteriol. 170:1988;2860-2865.
51. Taraseviciene L., Miczak A., Apirion D. The gene specifying RNase E (rne) and a gene affecting mRNA stability (ams) are the same gene. Mol. Microbiol. 5:1991;851-855.
52. Thomas P. Hybridization of denatured RNAs transferred or dotted to nitrocellulose paper. Methods Enzymol. 100:1983;255-266.
53. Turnbough C. L., Kerr K. H., Funderburg W. R., Donahue J. P., Powell F. E. Nucleotide sequence and characterization of the pyrF operon of Escherichia coli K-12. J. Biol. Chem. 262:1987;10239-10245.
54. Williams M. G., Rogers P. Expression of arg genes in Escherichia coli during arginine limitation dependent upon stringent control of translation. J. Bacteriol. 169:1987;1644-1650.