Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1989 Feb 11;17(3):1139–1157. doi: 10.1093/nar/17.3.1139

Terminal sequences do not contain the rate-limiting decay determinants of E. coli cat mRNA.

C DeFranco 1, J L Schottel 1
PMCID: PMC331727  PMID: 2466234

Abstract

The mechanism of E. coli chloramphenicol acetyltransferase (cat) mRNA decay was investigated. Alteration of the 5' untranslated terminus does not appear to have an effect on the turnover rate of the mRNA. Similarly, changes at the 3' terminus of the message, including the addition of a stable stem and loop structure, do not affect the half-life of the message. The data suggest that 5' and 3' terminal untranslated sequences do not contain the rate-limiting determinants for cat message decay. Decay rates for various segments of the cat mRNA were measured and indicate that all regions of the message have similar stabilities. The current model of cat mRNA degradation involves a rate-limiting endonucleolytic decay event that occurs internal to the message followed by degradation of the cleavage products.

Full text

PDF
1139

Images in this article

1146Image
on p.1146
1147Image
on p.1147
1148Image
on p.1148
1150Image
on p.1150
1152Image
on p.1152
1153Image
on p.1153

Selected References

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

  1. Achord D., Kennell D. Metabolism of messenger RNA from the gal operon of Escherichia coli. J Mol Biol. 1974 Dec 15;90(3):581–599. doi: 10.1016/0022-2836(74)90236-8. [DOI] [PubMed] [Google Scholar]
  2. Alton N. K., Vapnek D. Nucleotide sequence analysis of the chloramphenicol resistance transposon Tn9. Nature. 1979 Dec 20;282(5741):864–869. doi: 10.1038/282864a0. [DOI] [PubMed] [Google Scholar]
  3. Ambulos N. P., Jr, Duvall E. J., Lovett P. S. The mRNA for an inducible chloramphenicol acetyltransferase gene is cleaved into discrete fragments in Bacillus subtilis. J Bacteriol. 1987 Mar;169(3):967–972. doi: 10.1128/jb.169.3.967-972.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bechhofer D. H., Dubnau D. Induced mRNA stability in Bacillus subtilis. Proc Natl Acad Sci U S A. 1987 Jan;84(2):498–502. doi: 10.1073/pnas.84.2.498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belasco J. G., Beatty J. T., Adams C. W., von Gabain A., Cohen S. N. Differential expression of photosynthesis genes in R. capsulata results from segmental differences in stability within the polycistronic rxcA transcript. Cell. 1985 Jan;40(1):171–181. doi: 10.1016/0092-8674(85)90320-4. [DOI] [PubMed] [Google Scholar]
  6. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  7. Brawerman G. Determinants of messenger RNA stability. Cell. 1987 Jan 16;48(1):5–6. doi: 10.1016/0092-8674(87)90346-1. [DOI] [PubMed] [Google Scholar]
  8. Brosius J., Ullrich A., Raker M. A., Gray A., Dull T. J., Gutell R. R., Noller H. F. Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal RNA operon of E. coli. Plasmid. 1981 Jul;6(1):112–118. doi: 10.1016/0147-619x(81)90058-5. [DOI] [PubMed] [Google Scholar]
  9. Båga M., Göransson M., Normark S., Uhlin B. E. Processed mRNA with differential stability in the regulation of E. coli pilin gene expression. Cell. 1988 Jan 29;52(2):197–206. doi: 10.1016/0092-8674(88)90508-9. [DOI] [PubMed] [Google Scholar]
  10. Cannistraro V. J., Kennell D. Escherichia coli lac operator mRNA affects translation initiation of beta-galactosidase mRNA. Nature. 1979 Feb 1;277(5695):407–409. doi: 10.1038/277407a0. [DOI] [PubMed] [Google Scholar]
  11. Cannistraro V. J., Subbarao M. N., Kennell D. Specific endonucleolytic cleavage sites for decay of Escherichia coli mRNA. J Mol Biol. 1986 Nov 20;192(2):257–274. doi: 10.1016/0022-2836(86)90363-3. [DOI] [PubMed] [Google Scholar]
  12. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  13. Chang A. C., Cohen S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978 Jun;134(3):1141–1156. doi: 10.1128/jb.134.3.1141-1156.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chen C. Y., Beatty J. T., Cohen S. N., Belasco J. G. An intercistronic stem-loop structure functions as an mRNA decay terminator necessary but insufficient for puf mRNA stability. Cell. 1988 Feb 26;52(4):609–619. doi: 10.1016/0092-8674(88)90473-4. [DOI] [PubMed] [Google Scholar]
  15. 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 U S A. 1986 Jan;83(1):120–124. doi: 10.1073/pnas.83.1.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  17. Guarneros G., Montañez C., Hernandez T., Court D. Posttranscriptional control of bacteriophage lambda gene expression from a site distal to the gene. Proc Natl Acad Sci U S A. 1982 Jan;79(2):238–242. doi: 10.1073/pnas.79.2.238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gupta R. S., Schlessinger D. Coupling of rates of transcription, translation, and messenger ribonucleic acid degradation in streptomycin-dependent mutants of Escherichia coli. J Bacteriol. 1976 Jan;125(1):84–93. doi: 10.1128/jb.125.1.84-93.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hu N., Messing J. The making of strand-specific M13 probes. Gene. 1982 Mar;17(3):271–277. doi: 10.1016/0378-1119(82)90143-3. [DOI] [PubMed] [Google Scholar]
  20. Kano Y., Imamoto F. Evidence for endonucleolytic cleavage at the 5'-proximal segment of the trp messenger RNA in Escherichia coli. Mol Gen Genet. 1979 Apr 17;172(1):25–30. doi: 10.1007/BF00276211. [DOI] [PubMed] [Google Scholar]
  21. Kinscherf T. G., Apirion D. Polynucleotide phosphorylase can participate in decay of mRNA in Escherichia coli in the absence of ribonuclease II. Mol Gen Genet. 1975 Sep 8;139(4):357–362. doi: 10.1007/BF00267975. [DOI] [PubMed] [Google Scholar]
  22. Klug G., Adams C. W., Belasco J., Doerge B., Cohen S. N. Biological consequences of segmental alterations in mRNA stability: effects of deletion of the intercistronic hairpin loop region of the Rhodobacter capsulatus puf operon. EMBO J. 1987 Nov;6(11):3515–3520. doi: 10.1002/j.1460-2075.1987.tb02677.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Le Grice S. F., Matzura H. Localisation of the transcription initiation site of the chloramphenicol resistance gene on plasmid pAC184. FEBS Lett. 1980 Apr 21;113(1):42–46. doi: 10.1016/0014-5793(80)80490-x. [DOI] [PubMed] [Google Scholar]
  24. Lim L. W., Kennell D. Evidence for random endonucleolytic cleavages between messages in decay of Escherichia coli trp mRNA. J Mol Biol. 1980 Aug 5;141(2):227–233. doi: 10.1016/0022-2836(80)90388-5. [DOI] [PubMed] [Google Scholar]
  25. Lim L. W., Kennell D. Models for decay of Escherichia coli lac messenger RNA and evidence for inactivating cleavages between its messages. J Mol Biol. 1979 Dec 5;135(2):369–390. doi: 10.1016/0022-2836(79)90442-x. [DOI] [PubMed] [Google Scholar]
  26. Mackie G. A. Posttranscriptional regulation of ribosomal protein S20 and stability of the S20 mRNA species. J Bacteriol. 1987 Jun;169(6):2697–2701. doi: 10.1128/jb.169.6.2697-2701.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Melefors O., von Gabain A. Site-specific endonucleolytic cleavages and the regulation of stability of E. coli ompA mRNA. Cell. 1988 Mar 25;52(6):893–901. doi: 10.1016/0092-8674(88)90431-x. [DOI] [PubMed] [Google Scholar]
  28. Mott J. E., Galloway J. L., Platt T. Maturation of Escherichia coli tryptophan operon mRNA: evidence for 3' exonucleolytic processing after rho-dependent termination. EMBO J. 1985 Jul;4(7):1887–1891. doi: 10.1002/j.1460-2075.1985.tb03865.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Newbury S. F., Smith N. H., Higgins C. F. Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell. 1987 Dec 24;51(6):1131–1143. doi: 10.1016/0092-8674(87)90599-x. [DOI] [PubMed] [Google Scholar]
  30. Newbury S. F., Smith N. H., Robinson E. C., Hiles I. D., Higgins C. F. Stabilization of translationally active mRNA by prokaryotic REP sequences. Cell. 1987 Jan 30;48(2):297–310. doi: 10.1016/0092-8674(87)90433-8. [DOI] [PubMed] [Google Scholar]
  31. Nilsson G., Belasco J. G., Cohen S. N., von Gabain A. Growth-rate dependent regulation of mRNA stability in Escherichia coli. Nature. 1984 Nov 1;312(5989):75–77. doi: 10.1038/312075a0. [DOI] [PubMed] [Google Scholar]
  32. Portier C., Dondon L., Grunberg-Manago M., Régnier P. The first step in the functional inactivation of the Escherichia coli polynucleotide phosphorylase messenger is a ribonuclease III processing at the 5' end. EMBO J. 1987 Jul;6(7):2165–2170. doi: 10.1002/j.1460-2075.1987.tb02484.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Roberts T. M., Kacich R., Ptashne M. A general method for maximizing the expression of a cloned gene. Proc Natl Acad Sci U S A. 1979 Feb;76(2):760–764. doi: 10.1073/pnas.76.2.760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rose R. E. The nucleotide sequence of pACYC184. Nucleic Acids Res. 1988 Jan 11;16(1):355–355. doi: 10.1093/nar/16.1.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Santiago T. C., Purvis I. J., Bettany A. J., Brown A. J. The relationship between mRNA stability and length in Saccharomyces cerevisiae. Nucleic Acids Res. 1986 Nov 11;14(21):8347–8360. doi: 10.1093/nar/14.21.8347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schindler D., Echols H. Retroregulation of the int gene of bacteriophage lambda: control of translation completion. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4475–4479. doi: 10.1073/pnas.78.7.4475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schlessinger D., Jacobs K. A., Gupta R. S., Kano Y., Imamoto F. Decay of individual Escherichia coli trp messenger RNA molecules is sequentially ordered. J Mol Biol. 1977 Mar 5;110(3):421–439. doi: 10.1016/s0022-2836(77)80107-1. [DOI] [PubMed] [Google Scholar]
  39. Schmeissner U., McKenney K., Rosenberg M., Court D. Removal of a terminator structure by RNA processing regulates int gene expression. J Mol Biol. 1984 Jun 15;176(1):39–53. doi: 10.1016/0022-2836(84)90381-4. [DOI] [PubMed] [Google Scholar]
  40. Schneider E., Blundell M., Kennell D. Translation and mRNA decay. Mol Gen Genet. 1978 Apr 6;160(2):121–129. doi: 10.1007/BF00267473. [DOI] [PubMed] [Google Scholar]
  41. Schottel J. L., Sninsky J. J., Cohen S. N. Effects of alterations in the translation control region on bacterial gene expression: use of cat gene constructs transcribed from the lac promoter as a model system. Gene. 1984 May;28(2):177–193. doi: 10.1016/0378-1119(84)90255-5. [DOI] [PubMed] [Google Scholar]
  42. Squires C., Krainer A., Barry G., Shen W. F., Squires C. L. Nucleotide sequence at the end of the gene for the RNA polymerase beta' subunit (rpoC). Nucleic Acids Res. 1981 Dec 21;9(24):6827–6840. doi: 10.1093/nar/9.24.6827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stüber D., Bujard H. Organization of transcriptional signals in plasmids pBR322 and pACYC184. Proc Natl Acad Sci U S A. 1981 Jan;78(1):167–171. doi: 10.1073/pnas.78.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Summers W. C. A simple method for extraction of RNA from E. coli utilizing diethyl pyrocarbonate. Anal Biochem. 1970 Feb;33(2):459–463. doi: 10.1016/0003-2697(70)90316-7. [DOI] [PubMed] [Google Scholar]
  45. Sutcliffe J. G. Complete nucleotide sequence of the Escherichia coli plasmid pBR322. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):77–90. doi: 10.1101/sqb.1979.043.01.013. [DOI] [PubMed] [Google Scholar]
  46. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [PubMed] [Google Scholar]
  47. Wong H. C., Chang S. Identification of a positive retroregulator that stabilizes mRNAs in bacteria. Proc Natl Acad Sci U S A. 1986 May;83(10):3233–3237. doi: 10.1073/pnas.83.10.3233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. von Gabain A., Belasco J. G., Schottel J. L., Chang A. C., Cohen S. N. Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc Natl Acad Sci U S A. 1983 Feb;80(3):653–657. doi: 10.1073/pnas.80.3.653. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES