1887

Abstract

The functional stability of the chloramphenicol acetyltransferase (cat) mRNA, as well as the functional stability of the total mRNA pool, change during the course of culture growth. mRNA half-lives are long during lag phase, decrease during the exponential phase and increase again during the stationary phase of the bacterial growth cycle. The half-lives of mRNA and total mRNA also increase three- to fourfold during amino acid starvation when compared to exponential culture growth. Even though the stability of the message changes about fourfold during culture growth, the amount of mRNA per cell mass does not vary significantly between the culture growth phases, indicating that there are compensating changes in gene transcription. Translation of mRNA also changes during culture growth. In exponential phase, the rate of translation is about 14-fold higher than when the culture is in stationary phase. This is in contrast to the fourfold increase in stability of mRNA in the stationary-phase culture compared to the exponentially growing culture and indicates that active translation is not correlated with increased mRNA stability. When a stationary-phase culture was diluted into fresh medium, there was a five- to sevenfold increase in CAT synthesis and a threefold increase in total protein synthesis in the presence or absence of rifampicin. These results suggest that while mRNA becomes generally more stable and less translated in the stationary-phase culture, the mRNA is available for immediate translation when nutrients are provided to the culture even when transcription is inhibited.

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1998-03-01
2021-09-24
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References

  1. Albertson N.H., Nystrom T. 1994; Effects of starvation for exogenous carbon on functional mRNA stability and rate of peptide chain elongation inEscherichia coli. . FEMS Microbiol Lett 117:181–188
    [Google Scholar]
  2. Albertson N.H., Nystrom T., Kjelleberg S. 1990; Functional mRNA half-lives in the marineVibrio sp. S14 during starvation and recovery. J Gen Microbiol 136:2195–2199
    [Google Scholar]
  3. Alifano P., Bruni C.B., Carlomagno M.S. 1994; Control of mRNA processing and decay in prokaryotes. Genetica 94:157–172
    [Google Scholar]
  4. Arraiano C.M., Yancey S.D., Kushner S.R. 1988; Stabilization of discrete mRNA breakdown products inams pnp rnb multiple mutants ofEscherichia coli K-12. J Bacteriol 170:4625–4633
    [Google Scholar]
  5. Belasco J.G., Brawerman G. 1993; Experimental approaches to the study of mRNA decay.. In Control of mRNA Stability, pp. 475–493 Belasco J. G., Brawerman. G. Edited by San Diego:: Academic Press;
    [Google Scholar]
  6. Belasco J.G., Higgins C.F. 1988; Mechanisms of mRNA decay in bacteria; a perspective. Gene 72:15–23
    [Google Scholar]
  7. Bradford M.M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
    [Google Scholar]
  8. Casadaban M.J., Cohen S.N. 1980; Analysis of gene control signals by DNA fusion and cloning inEscherichia coli. . J Mol Biol 138:179–207
    [Google Scholar]
  9. Chang A.C.Y., Cohen S.N. 1978; Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134:1141–1156
    [Google Scholar]
  10. Chuang S.-E., Daniels D.L., Blattner F.R. 1993; Global regulation of gene expression inEscherichia coli. . J Bacteriol 175:2026–2036
    [Google Scholar]
  11. Cohen S.N., McDowall K.J. 1995; Surprises at the 3' end of prokaryotic RNA. Cell 80:829–832
    [Google Scholar]
  12. Cohen S.N., McDowall K.J. 1997; RNase E: still a wonderfully mysterious enzyme. Mol Microbiol 23:1099–1106
    [Google Scholar]
  13. Davis B.D., Mingioli E.S. 1950; Mutants ofEscherichia colirequiring methionine or vitamin B12 . J Bacteriol 60:17–28
    [Google Scholar]
  14. Deutscher M.P. 1993a; Promiscuous exoribonucleases ofEscherichia coli. . J Bacteriol 175:4577–4583
    [Google Scholar]
  15. Deutscher M.P. 1993b; Ribonuclease multiplicity, diversity, and complexity.. J Biol Chem 268:13011–13014
    [Google Scholar]
  16. Donovan W.P., Kushner S.R. 1986; Polynucleotide phos- phorylase and ribonuclease II are required for cell viability and mRNA turnover inEscherichia coli K-12. Proc Natl Acad Set USA 83120–124
    [Google Scholar]
  17. Ehretsmann C.P., Carpousis A.J., Krisch H.M. 1992; mRNA degradation in procaryotes. FASEB J 6:3186–3192
    [Google Scholar]
  18. Emory S.A., Belasco J.G. 1990; TheompA 5' untranslated RNA segment functions inEscherichia coli as a growth-rate- regulated mRNA stabilizer whose activity is unrelated to translational efficiency. J Bacterial 172:4472–4481
    [Google Scholar]
  19. Feinberg A.P., Vogelstein B. 1983; A technique for radiolabelling DNA restriction fragments to high specific activity. Anal Biochem 132:6–13
    [Google Scholar]
  20. Georgellis D., Arvidson S., van Gabain A. 1992; Decay ofompA mRNA and processing of 9S RNA are immediately affected by shifts in growth rate, but in opposite manners. J Bacterial 174:5382–5390
    [Google Scholar]
  21. Georgellis D., Barlow T., Arvidson S., von Gabain A. 1993; Retarded RNA turnover inEscherichia coli: a means of maintaining gene expression during anaerobiosis. Mol Microbiol 9:375–381
    [Google Scholar]
  22. Goldbium K., Apirion D. 1981; Inactivation of the ribonucleic acid processing enzyme ribonuclease E blocks cell division. J Bacterial 146:128–132
    [Google Scholar]
  23. Gorski K., Roch J.-M., Prentki P., Krisch H.M. 1985; The stability of bacteriophage T4 Gene 32 mRNA: a5' leader sequence that can stabilize mRNA transcripts. Cell 43:461–469
    [Google Scholar]
  24. Gray W.J.H., Midgiey J.E.M. 1970; The control of ribonucleic acid synthesis in bacteria. Steady-state content of messenger ribonucleic acid inEscherichia coli M.R.E.600. Biochem J 120:279–288
    [Google Scholar]
  25. Groat R.G., Schultz J.E., Zynchlinsky E., Bockman A., Matin A. 1986; Starvation proteins inEscherichia coli : kinetics of synthesis and role in starvation survival. J Bacterial 168:486–493
    [Google Scholar]
  26. Gupta R.S., Schlessinger D. 1975; Differential modes of chemical decay for early and late lambda messenger RNA. J Mol Biol 92:311–318
    [Google Scholar]
  27. Hengge-Aronis R. 1996; Regulation of gene expression during entry into stationary phase.. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology,, 2. pp. 1497–1512 Neidhard F. C. Edited by Washington, DC:: American Society for Microbiology.;
    [Google Scholar]
  28. Ingram J.L, Maaloe O., Neidhardt F.C. 1983; Growth of cells and cultures. Growth rate as a variable.. In Growth of the Bacterial Cell, pp. 227–315 Sunderland, MA:: Sinaur Associates.;
    [Google Scholar]
  29. Isaksson LA., Fodor K., Kirsebom L.A., Bouadloun F., Muren E. 1980; Effects of growth conditions and mutations in RNA polymerase on translational activityin vitro inEscherichia coli. . Mol Gen Genet 180:27–33
    [Google Scholar]
  30. Jackson R.J., Standart N. 1990; Do the poly (A) tail and 3' untranslated region control mRNA translation ?. Cell 62:15–24
    [Google Scholar]
  31. Kenneli D., Simmons C. 1972; Synthesis and decay of messenger ribonucleic acid from the lactose operon ofEscherichia coli during amino-acid starvation. J Mol Biol 70:451–464
    [Google Scholar]
  32. Kessler S.W. 1976; Cell membrane antigen isolation with the staphylococcal protein A-antibody adsorbent. J Immunol 117:1482–1490
    [Google Scholar]
  33. Krinke L., Wulff D. 1990; The cleavage specificity of RNase III. Nucleic Acids Res 18:4809–4815
    [Google Scholar]
  34. Laemmli U.K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  35. Laskey R.A., Mills A.D. 1975; Quantitative film detection of 3Hand 14C in polyacrylamide gels by fluorography. Eur J Biochem 56:335–341
    [Google Scholar]
  36. Lundberg U., Nilsson G., von Gabain A. 1988; The differential stability of theEscherichia coli ompA andbla mRNA at various growth rates is not correlated to the efficiency of translation. Gene 72:141–149
    [Google Scholar]
  37. Matin A. 1991; The molecular basis of carbon-starvation- induced general resistance inEscherichia coli. . Mol Microbiol 5:3–10
    [Google Scholar]
  38. Meiefors O., Lundberg U., von Gabain A. 1993; RNA processing and degradation by RNase K and RNase E.. In Control of Messenger RNA Stability, pp. 53–70 Belasco J., Brawerman. G. Edited by San Diego:: Academic Press.;
    [Google Scholar]
  39. Melin L., Rutberg L., von Gabain A. 1989; Transcriptional and posttranscriptional control of theBacillus subtilis succinate dehydrogenase operon. J Bacterial 171:2110–2115
    [Google Scholar]
  40. Meyer B.J., Schottel J.L. 1991; A novel transcriptional response by thecat gene during slow growth ofEscherichia coli. . J Bacterial 173:3523–3530
    [Google Scholar]
  41. Meyer B.J., Schottel J.L. 1992; Characterization ofcatmessenger RNA decay suggests that turnover occurs by endonucleolytic cleavage in a 3' to5' direction. Mol Microbiol 6:1095–1104
    [Google Scholar]
  42. Minks M.A., Suryanarayana T., Subramanian A.R. 1978; Metabolic stability of the two forms of initiation factor IF-3 inEscherichia coli during the growth cycle. Eur J Biochem 82:271–277
    [Google Scholar]
  43. Morse D.E., Guertin M. 1971; Regulation of mRNA utilization and degradation by amino acid starvation. Nature New Biol 232:165–169
    [Google Scholar]
  44. Neidhardt F.C., Savageau M.A. 1996; Regulation beyond the operon.. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology,, 2. pp. 1310–1324 Neidhardt F. C. et al. Edited by Washington, DC:: American Society for Microbiology.;
    [Google Scholar]
  45. Neidhardt F.C., Bloch P.L., Smith D.F. 1974; Culture medium for enterobacteria. J Bacterial 119:736–747
    [Google Scholar]
  46. Nilsson G., Belasco J.G., Cohen S.N., von Gabain A. 1984; Growth-rate dependent regulation of mRNA stability inEscherichia coli. . Nature 312:75–77
    [Google Scholar]
  47. O'Hara E.B., Chekanova J.A., Ingle C.A., Kushner Z.R., Peters E., Kushner S.R. 1995; Polyadenylation helps regulate mRNA decay inEscherichia coli. . Proc Natl Acad Sci USA 921807–1811
    [Google Scholar]
  48. Pato M.L., von Meyenburg K. 1970; Residual RNA synthesis inEscherichia coli after inhibition of initiation of transcription by rifampicin. Cold Spring Harbor Symp Quant Biol 35:497–504
    [Google Scholar]
  49. Pedersen S., Bloch P.L., Reeh S., Neidhardt F.C. 1978a; Patterns of protein synthesis inE. coli : a catalog of the amount of 140 individual proteins at different growth rates. Cell 14:179–190
    [Google Scholar]
  50. Pedersen S., Reeh S., Friesen J. D. 1978b; Functional mRNA half lives inE. coli. . Mol Gen Genet 166:329–336
    [Google Scholar]
  51. Pelham H.R.B., Jackson R.J. 1976; An efficient mRNA- dependent translation system from reticulocyte lysates. Eur J Biochem 67:247–256
    [Google Scholar]
  52. Petersen C. 1992; Control of functional mRNA stability in bacteria: multiple mechanisms of nucleolytic and non-nucleolytic inactivation. Mol Microbiol 6:277–282
    [Google Scholar]
  53. Petersen C. 1993; Translation and mRNA stability in bacteria: a complex relationship.. In Control of mRNA Stability, pp. 117–145 Belasco J. G., Brawerman. G. Edited by San Diego:: Academic Press.;
    [Google Scholar]
  54. Raynal L.C, Krisch H.M, Carpousis A.J. 1996; Bacterial poly(A) polymerase: An enzyme that modulates RNA stability. Biochimie 78:390–398
    [Google Scholar]
  55. Reeh S., Pedersen S., Friesen J.D. 1976; Biosynthetic regulation of individual proteins inrelA + andrelA + strains ofEscherichia coli during amino acid starvation. Mol Gen Genet 149:279–289
    [Google Scholar]
  56. Reeve C.A., Amy P.S, Matin A. 1984; Role of protein synthesis in the survival of carbon-starvedEscherichia coli K-12. J Bacterial 160:1041–1046
    [Google Scholar]
  57. Sambrook J., Fritsch E.F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual,, 2nd. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory.;
    [Google Scholar]
  58. Schneider E., Blundell M., Kenneli D. 1978; Translation and mRNA decay. Mol Gen Genet 160:121–129
    [Google Scholar]
  59. Xu F., Cohen S.N. 1995; RNA degradation inEscherichia coli regulated by 3' adenylation and 5' phosphorylation. Nature 374:180–183
    [Google Scholar]
  60. Yamagishi M., Matsushima H., Wada A., Sakagami M., Fujita N., Ishihama A. 1993; Regulation of theEscherichia coli rmf gene encoding the ribosome modulation factor: growth-phase- and growth-rate-dependent control. EMBO J 12:625–630
    [Google Scholar]
  61. Zaidenzaig Y., Shaw W.V. 1976; Affinity and hydrophobic chromatography of three variants of chloramphenicol acetyltransferases specified by R factors in Escherichia coli. . FEBS Lett 62:266–271
    [Google Scholar]
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