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Volume 157, Issue 1

Multiple layers of control govern expression of the heat-shock operon Free

Abstract

The operon encodes two small heat-shock proteins, the inclusion-body-binding proteins IbpA and IbpB. Here, we report that expression of is a complex process involving at least four different layers of control, namely transcriptional control, RNA processing, translation control and protein stability. As a typical member of the heat-shock regulon, transcription of the operon is controlled by the alternative sigma factor (RpoH). Heat-induced transcription of the bicistronic operon is followed by RNase E-mediated processing events, resulting in monocistronic and transcripts and short 3′-terminal fragments. Translation of is controlled by an RNA thermometer in its 5′ untranslated region, forming a secondary structure that blocks entry of the ribosome at low temperatures. A similar structure upstream of is functional but not , suggesting downregulation of expression in the presence of IbpA. The recently reported degradation of IbpA and IbpB by the Lon protease and differential regulation of IbpA and IbpB levels in are discussed.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): RACE, rapid amplification of cDNA ends , ROSE, repression of heat-shock gene expression , SD, Shine–Dalgarno , UTR, untranslated region and WT, wild-type
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2011-01-01
2024-04-16
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References

  1. Allen S. P., Polazzi J. O., Gierse J. K., Easton A. M. 1992; Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli . J Bacteriol 174:6938–6947
     [Google Scholar]
  2. Bissonnette S. A., Rivera-Rivera I., Sauer R. T., Baker T. A. 2010; The IbpA and IbpB small heat-shock proteins are substrates of the AAA+ Lon protease. Mol Microbiol 75:1539–1549
     [Google Scholar]
  3. Brantl S., Wagner E. G. 1994; Antisense RNA-mediated transcriptional attenuation occurs faster than stable antisense/target RNA pairing: an in vitro study of plasmid pIP501. EMBO J 13:3599–3607
     [Google Scholar]
  4. Butland G., Peregrin-Alvarez J. M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D. other authors 2005; Interaction network containing conserved and essential protein complexes in Escherichia coli . Nature 433:531–537
     [Google Scholar]
  5. Campbell E. A., Westblade L. F., Darst S. A. 2008; Regulation of bacterial RNA polymerase σ factor activity: a structural perspective. Curr Opin Microbiol 11:121–127
     [Google Scholar]
  6. Carpousis A. J. 2007; The RNA degradosome of Escherichia coli : an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61:71–87
     [Google Scholar]
  7. Chuang S. E., Burland V., Plunkett G. III, Daniels D. L., Blattner F. R. 1993; Sequence analysis of four new heat-shock genes constituting the hslTS / ibpAB and hslVU operons in Escherichia coli . Gene 134:1–6
     [Google Scholar]
  8. Ehretsmann C. P., Carpousis A. J., Krisch H. M. 1992; Specificity of Escherichia coli endoribonuclease RNase E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site. Genes Dev 6:149–159
     [Google Scholar]
  9. Goldblum K., Apririon D. 1981; Inactivation of the ribonucleic acid-processing enzyme ribonuclease E blocks cell division. J Bacteriol 146:128–132
     [Google Scholar]
  10. Gross C. A., Chan C., Dombroski A., Gruber T., Sharp M., Tupy J., Young B. 1998; The functional and regulatory roles of sigma factors in transcription. Cold Spring Harb Symp Quant Biol 63:141–155
     [Google Scholar]
  11. Guisbert E., Yura T., Rhodius V. A., Gross C. A. 2008; Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol Mol Biol Rev 72:545–554
     [Google Scholar]
  12. Han M. J., Park S. J., Park T. J., Lee S. Y. 2004; Roles and applications of small heat shock proteins in the production of recombinant proteins in Escherichia coli . Biotechnol Bioeng 88:426–436
     [Google Scholar]
  13. Hartz D., McPheeters D. S., Traut R., Gold L. 1988; Extension inhibition analysis of translation initiation complexes. Methods Enzymol 164:419–425
     [Google Scholar]
  14. Hengge-Aronis R. 2002; Signal transduction and regulatory mechanisms involved in control of the σ S (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66:373–395
     [Google Scholar]
  15. Jain C. 2002; Degradation of mRNA in Escherichia coli . IUBMB Life 54:315–321
     [Google Scholar]
  16. Kitagawa M., Matsumura Y., Tsuchido T. 2000; Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stresses in Escherichia coli . FEMS Microbiol Lett 184:165–171
     [Google Scholar]
  17. Kitagawa M., Miyakawa M., Matsumura Y., Tsuchido T. 2002; Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. Eur J Biochem 269:2907–2917
     [Google Scholar]
  18. Klinkert B., Narberhaus F. 2009; Microbial thermosensors. Cell Mol Life Sci 66:2661–2676
     [Google Scholar]
  19. Kuczyńska-Wisńik D., Laskowska E., Taylor A. 2001; Transcription of the ibpB heat-shock gene is under control of σ 32- and σ 54-promoters, a third regulon of heat-shock response. Biochem Biophys Res Commun 284:57–64
     [Google Scholar]
  20. Laskowska E., Wawrzynow A., Taylor A. 1996; IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78:117–122
     [Google Scholar]
  21. Lethanh H., Neubauer P., Hoffmann F. 2005; The small heat-shock proteins IbpA and IbpB reduce the stress load of recombinant Escherichia coli and delay degradation of inclusion bodies. Microb Cell Fact 4:6
     [Google Scholar]
  22. Loayza D., Carpousis A. J., Krisch H. M. 1991; Gene 32 transcription and mRNA processing in T4-related bacteriophages. Mol Microbiol 5:715–725
     [Google Scholar]
  23. Matuszewska M., Kuczyńska-Wisńik D., Laskowska E., Liberek K. 2005; The small heat shock protein IbpA of Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J Biol Chem 280:12292–12298
     [Google Scholar]
  24. Matuszewska E., Kwiatkowska J., , Kuczyńska-Wisńik D., Laskowska E. 2008; Escherichia coli heat-shock proteins IbpA/B are involved in resistance to oxidative stress induced by copper. Microbiology 154:1739–1747
     [Google Scholar]
  25. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  26. Narberhaus F. 2010; Translational control of bacterial heat shock and virulence genes by temperature-sensing mRNAs. RNA Biol 7:84–89
     [Google Scholar]
  27. Narberhaus F., Vogel J. 2009; Regulatory RNAs in prokaryotes: here, there and everywhere. Mol Microbiol 74:261–269
     [Google Scholar]
  28. Narberhaus F., Waldminghaus T., Chowdhury S. 2006; RNA thermometers. FEMS Microbiol Rev 30:3–16
     [Google Scholar]
  29. Newbury S. F., Smith N. H., Higgins C. F. 1987; Differential mRNA stability controls relative gene expression within a polycistronic operon. Cell 51:1131–1143
     [Google Scholar]
  30. Nonaka G., Blankschien M., Herman C., Gross C. A., Rhodius V. A. 2006; Regulon and promoter analysis of the E. coli heat-shock factor, σ 32, reveals a multifaceted cellular response to heat stress. Genes Dev 20:1776–1789
     [Google Scholar]
  31. Norrander J., Kempe T., Messing J. 1983; Construction of improved M13-vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101–106
     [Google Scholar]
  32. Nover L., Scharf K. D., Neumann D. 1989; Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol Cell Biol 9:1298–1308
     [Google Scholar]
  33. Pridmore R. D. 1987; New and versatile cloning vectors with kanamycin-resistance marker. Gene 56:309–312
     [Google Scholar]
  34. Rasouly A., Schonbrun M., Shenhar Y., Ron E. Z. 2009; YbeY, a heat shock protein involved in translation in Escherichia coli . J Bacteriol 191:2649–2655
     [Google Scholar]
  35. Ratajczak E., Zietkiewicz S., Liberek K. 2009; Distinct activities of Escherichia coli small heat shock proteins IbpA and IbpB promote efficient protein disaggregation. J Mol Biol 386:178–189
     [Google Scholar]
  36. Rauhut R., Klug G. 1999; mRNA degradation in bacteria. FEMS Microbiol Rev 23:353–370
     [Google Scholar]
  37. Richmond C. S., Glasner J. D., Mau R., Jin H., Blattner F. R. 1999; Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res 27:3821–3835
     [Google Scholar]
  38. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  39. Schumann W. 2009; Temperature sensors of eubacteria. Adv Appl Microbiol 67:213–256
     [Google Scholar]
  40. Shearstone J. R., Baneyx F. 1999; Biochemical characterization of the small heat shock protein IbpB from Escherichia coli . J Biol Chem 274:9937–9945
     [Google Scholar]
  41. Singh K., Groth-Vasselli B., Farnsworth P. N. 1998; Interaction of DNA with bovine lens alpha-crystallin: its functional implications. Int J Biol Macromol 22:315–320
     [Google Scholar]
  42. Studier F. W. 1975; Genetic mapping of a mutation that causes ribonucleases III deficiency in Escherichia coli . J Bacteriol 124:307–316
     [Google Scholar]
  43. Vaillancourt P. E. 2003 E. coli Gene Expression Protocols Totowa, NJ: Humana Press;
     [Google Scholar]
  44. Veinger L., Diamant S., Buchner J., Goloubinoff P. 1998; The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273:11032–11037
     [Google Scholar]
  45. Wade J. T., Roa D. C., Grainger D. C., Hurd D., Busby S. J., Struhl K., Nudler E. 2006; Extensive functional overlap between sigma factors in Escherichia coli . Nat Struct Mol Biol 13:806–814
     [Google Scholar]
  46. Waldminghaus T., Fippinger A., Alfsmann J., Narberhaus F. 2005; RNA thermometers are common in α - and γ -proteobacteria. Biol Chem 386:1279–1286
     [Google Scholar]
  47. Waldminghaus T., Gaubig L. C., Narberhaus F. 2007; Genome-wide bioinformatic prediction and experimental evaluation of potential RNA thermometers. Mol Genet Genomics 278:555–564
     [Google Scholar]
  48. Waldminghaus T., Gaubig L. C., Klinkert B., Narberhaus F. 2009; The Escherichia coli ibpA thermometer is comprised of stable and unstable structural elements. RNA Biol 6:455–463
     [Google Scholar]
  49. Waters L. S., Storz G. 2009; Regulatory RNAs in bacteria. Cell 136:615–628
     [Google Scholar]
  50. Willkomm D. K., Minnerup J., Huttenhofer A., Hartmann R. K. 2005; Experimental RNomics in Aquifex aeolicus : identification of small non-coding RNAs and the putative 6S RNA homolog. Nucleic Acids Res 33:1949–1960
     [Google Scholar]
  51. Winkler W. C., Breaker R. R. 2005; Regulation of bacterial gene expression by riboswitches. Annu Rev Microbiol 59:487–517
     [Google Scholar]
  52. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
     [Google Scholar]
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Multiple layers of control govern expression of the EscherichiacoliibpAB heat-shock operon
Microbiology 157, 66 (2011); https://doi.org/10.1099/mic.0.043802-0
/content/journal/micro/10.1099/mic.0.043802-0
/content/journal/micro/10.1099/mic.0.043802-0
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