1887

Abstract

The expression of genes for cold-shock proteins is proposed to be regulated primarily at the post-transcriptional level by increase of mRNA stability after transition to low temperatures. Destabilization of the cold-induced transcript at 37 °C as well as stabilization upon cold shock is known to depend on the unusually long (159 nt) 5′-untranslated region. Determination of the mRNA 5′-end from revealed a shorter distance between the start of transcription and the start codon for translation. The mRNA of was shown to be stabilized at low temperatures to a greater extent than other investigated transcripts. To address the mechanism of decay of the transcript, it was incubated with purified degradosome of . Endoribonucleolytic cleavage in the 5′-untranslated region as reported for the transcript of was not observed. Instead, the data indicated that the mRNA decay in is mediated by endoribonucleolytic cleavages within the coding region.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26666-0
2004-03-01
2020-08-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/3/mic1500687.html?itemId=/content/journal/micro/10.1099/mic.0.26666-0&mimeType=html&fmt=ahah

References

  1. Bae W., Jones P. G., Inouye M.. 1997; CspA, the major cold shock protein of Escherichia coli, negatively regulates its own gene expression. J Bacteriol179:7081–7088
    [Google Scholar]
  2. Bae W., Phadtare S., Sverinov K., Inouye M.. 1999; Characterization of Escherichia coli cspE, whose product negatively regulates transcription of cspA, the gene for the major cold shock protein. Mol Microbiol31:1429–1441[CrossRef]
    [Google Scholar]
  3. Beran R. K., Simons R. W.. 2001; Cold-temperature induction of Escherichia coli polynucleotide phosphorylase occurs by reversal of its autoregulation. Mol Microbiol39:112–125[CrossRef]
    [Google Scholar]
  4. Brandi A., Pietroni P., Gualerzi C. O., Pon C. L.. 1996; Post-transcriptional regulation of CspA expression in Escherichia coli. Mol Microbiol19:231–240[CrossRef]
    [Google Scholar]
  5. Brandi A., Spurio R., Gualerzi C. O., Pon C. L.. 1999; Massive presence of the Escherichia coli ‘major cold-shock protein’ CspA under non-stress conditions. EMBO J18:1653–1659[CrossRef]
    [Google Scholar]
  6. Carpousis A. J., Van Houwe G., Ehretsmann C., Krisch H. M.. 1994; Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell76:889–900[CrossRef]
    [Google Scholar]
  7. Drews G.. 1983; Mikrobiologisches Praktikum Berlin, Heidelberg & New York: Springer;
  8. Ehretsmann C. P., Carpousis A. J., Krisch H. M.. 1992; Specificity of the Escherichia coli endoribonuclease RNAse E:in vivo and in vitro analysis of mutants in a bacteriophage T4 processing site. Genes Dev6:149–159[CrossRef]
    [Google Scholar]
  9. Emory S. A., Belasco J. G.. 1990; The ompA 5′ untranslated segment functions in E. coli as a growth-rate-regulated mRNA stabilizer whose activity is unrelated to transcriptional efficiency. J Bacteriol172:4472–4481
    [Google Scholar]
  10. Emory S. A., Bouvet P., Belasco J. G.. 1992; A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev6:135–148[CrossRef]
    [Google Scholar]
  11. Fang L., Jiang W., Bae W., Inouye M.. 1997; Promoter-independent cold-shock induction of cspA and its derepression at 37 °C by mRNA stabilization. Mol Microbiol23:355–364[CrossRef]
    [Google Scholar]
  12. Fang L., Xia B., Inouye M.. 1999; Transcription of cspA, the gene for the major cold-shock protein of Escherichia coli, is negatively regulated at 37 °C by the 5′-untranslated region of its mRNA. FEMS Microbiol Lett176:39–43
    [Google Scholar]
  13. Fritsch J., Rothfuchs R., Rauhut R., Klug G.. 1995; Identification of an mRNA element promoting rate-limiting cleavage of the polycistronic puf mRNA in Rhodobacter capsulatus by an enzyme similar to RNase E. Mol Microbiol15:1017–1029[CrossRef]
    [Google Scholar]
  14. Goldenberg D., Azar I., Oppenheim A. B.. 1996; Differential mRNA stability of the cspA gene in the cold-shock response of Escherichia coli. Mol Microbiol19:241–248[CrossRef]
    [Google Scholar]
  15. Graumann P. L., Marahiel M. A.. 1998; A superfamily of proteins that contain the cold-shock domain. Trends Biol Sci23:286–290[CrossRef]
    [Google Scholar]
  16. Graumann P. L., Marahiel M. A.. 1999; Cold shock proteins CspB and CspC are major stationary-phase-induced proteins in Bacillus subtilis. Arch Microbiol171:135–138[CrossRef]
    [Google Scholar]
  17. Gualerzi C. O., Giuliodori A. M., Pon C. L.. 2003; Transcriptional and post-transcriptional control of cold shock genes. J Mol Biol331:527–539[CrossRef]
    [Google Scholar]
  18. Heck C., Klug G., Rothfuchs R., Jäger A., Rauhut R.. 1996; Effect of the pufQ-pufB intercistronic region on puf mRNA stability in Rhodobacter capsulatus. Mol Microbiol20:1165–1178[CrossRef]
    [Google Scholar]
  19. Hübner P., Dame G., Sandmeier U., Vandekerckhove J., Beyer P., Tadros M. H.. 1996; Molecular analysis of the Rhodobacter capsulatus chaperonin (groESL) operon: purification and characterization of Cpn60. Arch Microbiol166:193–203[CrossRef]
    [Google Scholar]
  20. Jaeger J. A., Turner D. H., Zuker M.. 1989; Improved predictions of secondary structures for RNA. Proc Natl Acad Sci U S A86:7706–7710[CrossRef]
    [Google Scholar]
  21. Jäger S., Fuhrmann O., Heck C., Hebermehl M., Schiltz E., Rauhut R., Klug G.. 2001; An mRNA degrading complex in Rhodobacter capsulatus. Nucleic Acids Res29:4581–4588[CrossRef]
    [Google Scholar]
  22. Jiang W., Hou Y., Inouye M.. 1997; CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem272:196–202[CrossRef]
    [Google Scholar]
  23. Jones P. G., VanBogelen R. A., Neidhardt F. C.. 1987; Induction of proteins in response to low temperatures in Escherichia coli. J Bacteriol169:2092–2095
    [Google Scholar]
  24. Kim B. H., Bang I. S., Lee S. Y., Hong S. K., Bang S. H., Lee I. S., Park Y. K.. 2001; Expression of cspH, encoding the cold shock protein in Salmonella enterica serovar typhimurium UK1. J Bacteriol183:5580–5588[CrossRef]
    [Google Scholar]
  25. Klug G.. 1991; Endonucleolytic degradation of puf mRNA in Rhodobacter capsulatus is influenced by oxygen. Proc Natl Acad Sci U S A88:1765–1769[CrossRef]
    [Google Scholar]
  26. Klug G., Jock S., Rothfuchs R.. 1992; The rate of decay of Rhodobacter capsulatus-specific puf mRNA segments is differentially affected by RNase E activity inEscherichia coli. Gene121:95–102[CrossRef]
    [Google Scholar]
  27. Klug G., Jäger A., Heck C., Rauhut R.. 1997; Identification, sequence analysis, and expression of the lepB gene for a leader peptidase in Rhodobacter capsulatus. Mol Gen Genet253:666–673[CrossRef]
    [Google Scholar]
  28. Lee S. J., Xie A., Jiang W., Etchegaray J. P., Jones P. G., Inouye M.. 1994; Family of the major cold-shock protein, CspA (CS7.4), of Escherichia coli, whose members show a high sequence similarity with the eukaryotic Y-box binding proteins. Mol Microbiol11:833–839[CrossRef]
    [Google Scholar]
  29. Mackie G. A.. 1998; Ribonuclease E is a 5′-end dependent endonuclease. Nature395:720–723[CrossRef]
    [Google Scholar]
  30. McDowall K. J., Lin-Chao S., Cohen S. N.. 1994; A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem269:10790–10796
    [Google Scholar]
  31. McDowall K. J., Kaberdin V. R., Wu S. W., Cohen S. N., Lin-Chao S.. 1995; Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature374:287–290[CrossRef]
    [Google Scholar]
  32. Mitta M., Fang L., Inouye M.. 1997; Deletion analysis of cspA of Escherichia coli: requirement of the AT-rich UP element for cspA transcription and the downstream box in the coding region for its cold shock induction. Mol Microbiol26:321–335[CrossRef]
    [Google Scholar]
  33. Neuhaus K., Francis K. P., Rapposch S., Görg A., Scherer S.. 1999; Pathogenic Yersinia species carry a novel, cold-inducible major cold shock protein tandem gene duplication producing both bicistronic and monocistronic mRNA. J Bacteriol181:6449–6455
    [Google Scholar]
  34. Nieuwlandt D. T., Palmer J. R., Armbruster D. T., Kuo Y.-P., Oda W., Daniels C. J.. 1995; A rapid procedure for the isolation of RNA from Haloferax volcanii. In Archaea, a Laboratory Manual, Halophiles pp161–162 Cold Spring Harbor NY: Cold Spring Harbor Laboratory;
  35. Pasternak C., Chen W., Heck C., Klug G.. 1996; Cloning, nucleotide sequence and characterization of the rpoD gene encoding the primary sigma factor ofRhodobacter capsulatus. Gene176:177–184[CrossRef]
    [Google Scholar]
  36. Phadtare S., Yamanaka K., Inouye M.. 2000; The cold shock response. In Bacterial Stress Responses pp33–45 Washington, DC: American Society for Microbiology;
  37. Rauhut R., Jäger A., Conrad C., Klug G.. 1996; Identification and analysis of the rnc gene for RNase III inRhodobacter capsulatus. Nucleic Acids Res24:1246–1251[CrossRef]
    [Google Scholar]
  38. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  39. Sanger F., Nicklen S., Coulson A. R.. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A74:5463–5467[CrossRef]
    [Google Scholar]
  40. Sato N., Nakamura A.. 1998; Involvement of the 5′-untranslated region in cold-regulated expression of the rbpA1 gene in the cyanobacterium Anabaena variabilis M3. Nucleic Acids Res26:2192–2199[CrossRef]
    [Google Scholar]
  41. Schindelin H., Marahiel M. A., Heinemann U.. 1993; Universal nucleic acid-binding domain revealed by crystal structure of the Bacillus subtilis major cold-shock protein. Nature364:164–168[CrossRef]
    [Google Scholar]
  42. Schindelin H., Jiang W., Inouye M., Heinemann U.. 1994; Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc Natl Acad Sci U S A91:5119–5123[CrossRef]
    [Google Scholar]
  43. von Hippel P. H.. 1998; An integrated model of the transcription complex in elongation, termination and editing. Science281:660–665[CrossRef]
    [Google Scholar]
  44. Xia B., Ke H., Jiang W., Inouye M.. 2002; The cold box stem-loop proximal to the 5′-end of the Escherichia coli cspA gene stabilizes its mRNA at low temperature. J Biol Chem277:6005–6011[CrossRef]
    [Google Scholar]
  45. Yamanaka K., Inouye M.. 1997; Growth-phase-dependent expression of cspD, encoding a member of the CspA family inEscherichia coli. J Bacteriol179:5126–5130
    [Google Scholar]
  46. Yanisch-Perron C., Viera J., Messing J.. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene33:103–119[CrossRef]
    [Google Scholar]
  47. Yura T., Nagai N., Mori H.. 1993; Regulation of the heat-shock response in bacteria. Annu Rev Microbiol47:321–350[CrossRef]
    [Google Scholar]
  48. Zuker M.. 1989; On finding all suboptimal foldings of an RNA molecule. Science244:48–52[CrossRef]
    [Google Scholar]
  49. Zuker M.. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res31:3406–3415[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26666-0
Loading
/content/journal/micro/10.1099/mic.0.26666-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error