1887

Abstract

Intracellular signal transfer in bacteria is dominated by phosphoryl transfer between conserved transmitter and receiver domains in regulatory proteins of so-called two-component systems. contains 30 such systems, which allow it to modulate gene expression, enzyme activity and the direction of flagellar rotation. The authors have investigated whether, and to what extent, these separate systems form (an) interacting network(s) , focussing on interactions between four major systems, involved in the responses to the availability of phosphorylated sugars (Uhp), phosphate (Pho), nitrogen (Ntr) and oxygen (Arc). Significant cross-talk was not detectable in wild-type cells. Decreasing expression levels of succinate dehydrogenase (reporting Arc activation), upon activation of the Pho system, appeared to be independent of signalling through PhoR. Cross-talk towards NtrC did occur, however, in a deletion strain, upon joint activation of Pho, Ntr and Uhp. UhpT expression was demonstrated when cells were grown on pyruvate, through non-cognate phosphorylation of UhpA by acetyl phosphate.

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2002-01-01
2020-09-29
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References

  1. Alexeeva S.. 2000; Molecular physiology of responses to oxygen in Escherichia coli PhD thesis, University of Amsterdam;
    [Google Scholar]
  2. Amemura M., Makino K., Shinagawa H., Nakata A.. 1990; Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoM-open reading frame 2. J Bacteriol172:6300–6307
    [Google Scholar]
  3. Appleby J. L., Parkinson J. S., Bourret R. B.. 1996; Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell86:845–848[CrossRef]
    [Google Scholar]
  4. Arber W.. 1958; Transduction of chromosomal genes and episomes in Escherichia coli . Virology11:273–288
    [Google Scholar]
  5. Backman K. C., Chen Y. M., Ueno-Nishio S., Magasanik B.. 1983; The product of glnL is not essential for regulation of bacterial nitrogen assimilation. J Bacteriol154:516–519
    [Google Scholar]
  6. Beier D., Schwarz B., Fuchs T. M., Gross R.. 1995; In vivo characterization of the unorthodox BvgS two-component sensor protein of Bordetella pertussis . J Mol Biol248:596–610[CrossRef]
    [Google Scholar]
  7. Bouché S., Klauck E., Fischer D., Lucassen M., Jung K., Hengge-Aronis R.. 1998; Regulation of RssB-dependent proteolysis in Escherichia coli : a role for acetyl phosphate in a response regulator-controlled process. Mol Microbiol27:787–795[CrossRef]
    [Google Scholar]
  8. Bueno R., Pahel G., Magasanik B.. 1985; Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli . J Bacteriol164:816–822
    [Google Scholar]
  9. Cotter P. A., Chepuri V., Gennis R. B., Gunsalus R. P.. 1990; Cytochrome o ( cyoABCDE ) and d ( cydAB )oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J Bacteriol172:6333–6338
    [Google Scholar]
  10. Danese P. N., Snyder W. B., Cosma C. L., Davis L. J., Silhavy T. J.. 1995; The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev9:387–398[CrossRef]
    [Google Scholar]
  11. De Wulf P., Lin E. C.. 2000; Cpx two-component signal transduction in Escherichia coli : excessive CpxR-P levels underlie CpxA* phenotypes. J Bacteriol182:1423–1426[CrossRef]
    [Google Scholar]
  12. Dorel C., Vidal O., Prigent-Combaret C., Vallet I., Lejeune P.. 1999; Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol Lett178:169–175[CrossRef]
    [Google Scholar]
  13. Feng J., Atkinson M. R., McCleary W., Stock J. B., Wanner B. L., Ninfa A. J.. 1992; Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli . J Bacteriol174:6061–6070
    [Google Scholar]
  14. Fisher S. L., Jiang W., Wanner B. L., Walsh C. T.. 1995; Cross-talk between the histidine protein kinase VanS and the response regulator PhoB. Characterization and identification of a VanS domain that inhibits activation of PhoB. J Biol Chem270:23143–23149[CrossRef]
    [Google Scholar]
  15. Georgellis D., Kwon O., Lin E. C.. 1999; Amplification of signaling activity of the Arc two-component system of Escherichia coli by anaerobic metabolites. An in vitro study with different protein modules. J Biol Chem274:35950–35954[CrossRef]
    [Google Scholar]
  16. Hellingwerf K. J., Postma P. W., Tommassen J., Westerhoff H. V.. 1995; Signal transduction in bacteria: phospho-neural network(s) in Escherichia coli? FEMS. Microbiol Rev16:309–321[CrossRef]
    [Google Scholar]
  17. Hellingwerf K. J., Crielaard W. C., Hoff W. D., Kort R., Verhamme D. T., Avignone-Rossa C., Joost Teixeira de Mattos M.. 1998; Current topics in signal transduction in bacteria. Antonie Leeuwenhoek74:211–227[CrossRef]
    [Google Scholar]
  18. Hess J. F., Oosawa K., Kaplan N., Simon M. I.. 1988; Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell53:79–87[CrossRef]
    [Google Scholar]
  19. Heyde M., Laloi P., Portalier R.. 2000; Involvement of carbon source and acetyl phosphate in the external-pH-dependent expression of porin genes in Escherichia coli . J Bacteriol182:198–202[CrossRef]
    [Google Scholar]
  20. Holms H.. 1996; Flux analysis and control of the central metabolic pathways in Escherichia coli . FEMS Microbiol Rev19:85–116[CrossRef]
    [Google Scholar]
  21. Igo M. M., Ninfa A. J., Silhavy T. J.. 1989; A bacterial environmental sensor that functions as a protein kinase and stimulates transcriptional activation. Genes Dev3:598–605[CrossRef]
    [Google Scholar]
  22. Kadner R. J.. 1995; Expression of the Uhp sugar-phosphate transport system of Escherichia coli . In Two-Component Signal Transduction pp263–274 Edited by Hoch J. A.. Silhavy T. J.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Kim S. K., Wilmes-Riesenberg M. R., Wanner B. L.. 1996; Involvement of the sensor kinase EnvZ in the in vivo activation of the response-regulator PhoB by acetyl phosphate. Mol Microbiol22:135–147[CrossRef]
    [Google Scholar]
  24. Lynch A. S., Lin E. C. C.. others 1996; Responses to molecular oxygen. In Escherichia coli and Salmonella: Cellular and Molecular Biology . , 2nd edn. pp1526–1538 Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
  25. McCleary W. R., Stock J. B.. 1994; Acetyl phosphate and the activation of two-component response regulators. J Biol Chem269:31567–31572
    [Google Scholar]
  26. McCleary W. R., Stock J. B., Ninfa A. J.. 1993; Is acetyl phosphate a global signal in Escherichia coli? . J Bacteriol175:2793–2798
    [Google Scholar]
  27. McFarland N., McCarter L., Artz S., Kustu S.. 1981; Nitrogen regulatory locus glnR of enteric bacteria is composed of cistrons ntrB and ntrC : identification of their protein products. Proc Natl Acad Sci USA78:2135–2139[CrossRef]
    [Google Scholar]
  28. Magasanik B.. 1996; Regulation of nitrogen utilization. In Escherichia coli and Salmonella: Cellular and Molecular Biology . , 2nd edn. pp1344–1356 Edited by Neidhardt F. C..and others Washington, DC: American Society for Microbiology;
  29. Matsubara M., Mizuno T.. 1999; EnvZ-independent phosphotransfer signaling pathway of the OmpR-mediated osmoregulatory expression of OmpC and OmpF in Escherichia coli . Biosci Biotechnol Biochem63:408–414[CrossRef]
    [Google Scholar]
  30. Matsubara M., Kitaoka S. I., Takeda S. I., Mizuno T.. 2000; Tuning of the porin expression under anaerobic growth conditions by His-to-Asp cross-phosphorelay through both the EnvZ-osmosensor and ArcB-anaerosensor in Escherichia coli . Genes Cells5:555–569[CrossRef]
    [Google Scholar]
  31. Matsushika A., Mizuno T.. 1998; A dual-signaling mechanism mediated by the ArcB hybrid sensor kinase containing the histidine-containing phosphotransfer domain in Escherichia coli . J Bacteriol180:3973–3977
    [Google Scholar]
  32. Michaelis S., Inouye H., Oliver D., Beckwith J.. 1983; Mutations that alter the signal sequence of alkaline phosphatase in Escherichia coli . J Bacteriol154:366–374
    [Google Scholar]
  33. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  34. Mizuno T.. 1997; Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli . DNA Res4:161–168[CrossRef]
    [Google Scholar]
  35. Neidhardt F. C., Bloch P. L., Smith D. F.. 1974; Culture medium for enterobacteria. J Bacteriol119:736–747
    [Google Scholar]
  36. Ninfa A. J., Magasanik B.. 1986; Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli . Proc Natl Acad Sci USA83:5909–5913[CrossRef]
    [Google Scholar]
  37. Ninfa A. J., Ninfa E. G., Lupas A. N., Stock A., Magasanik B., Stock J.. 1988; Crosstalk between bacterial chemotaxis signal transduction proteins and regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. Proc Natl Acad Sci USA85:5492–5496[CrossRef]
    [Google Scholar]
  38. Park S. J., Tseng C. P., Gunsalus R. P.. 1995; Regulation of succinate dehydrogenase ( sdhCDAB ) operon expression in Escherichia coli in response to carbon supply and anaerobiosis: role of ArcA and Fnr. Mol Microbiol15:473–482[CrossRef]
    [Google Scholar]
  39. Park S. J., Chao G., Gunsalus R. P.. 1997; Aerobic regulation of the sucABCD genes of Escherichia coli , which encode alpha-ketoglutarate dehydrogenase and succinyl coenzyme A synthetase: roles of ArcA, Fnr, and the upstream sdhCDAB promoter. J Bacteriol179:4138–4142
    [Google Scholar]
  40. Parkinson J. S., Kofoid E. C.. 1992; Communication modules in bacterial signaling proteins. Annu Rev Genet26:71–112[CrossRef]
    [Google Scholar]
  41. Perraud A. L., Kimmel B., Weiss V., Gross R.. 1998; Specificity of the BvgAS and EvgAS phosphorelay is mediated by the C-terminal HPt domains of the sensor proteins. Mol Microbiol27:875–887[CrossRef]
    [Google Scholar]
  42. Perraud A. L., Weiss V., Gross R.. 1999; Signalling pathways in two-component phosphorelay systems. Trends Microbiol7:115–120[CrossRef]
    [Google Scholar]
  43. Pruss B. M.. 1998; Acetyl phosphate and the phosphorylation of OmpR are involved in the regulation of the cell division rate in Escherichia coli . Arch Microbiol170:141–146[CrossRef]
    [Google Scholar]
  44. Pruss B. M., Wolfe A. J.. 1994; Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli . Mol Microbiol12:973–984[CrossRef]
    [Google Scholar]
  45. Rabin R. S., Stewart V.. 1993; Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J Bacteriol175:3259–3268
    [Google Scholar]
  46. Shattuck-Eidens D. M., Kadner R. J.. 1981; Exogenous induction of the Escherichia coli hexose phosphate transport system defined by uhp–lac operon fusions. J Bacteriol148:203–209
    [Google Scholar]
  47. Shen J., Gunsalus R. P.. 1997; Role of multiple ArcA recognition sites in anaerobic regulation of succinate dehydrogenase ( sdhCDAB ) gene expression in Escherichia coli . Mol Microbiol26:223–236[CrossRef]
    [Google Scholar]
  48. Silva J. C., Haldimann A., Prahalad M. K., Walsh C. T., Wanner B. L.. 1998; In vivo characterization of the type A and B vancomycin-resistant enterococci (VRE) VanRS two-component systems in Escherichia coli : a nonpathogenic model for studying the VRE signal transduction pathways. Proc Natl Acad Sci USA95:11951–11956[CrossRef]
    [Google Scholar]
  49. Singer M., Baker T. A., Schnitzler G.. 7 other authors 1989; A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli . Microbiol Rev53:1–24
    [Google Scholar]
  50. Stock J. B., Ninfa A. J., Stock A. M.. 1989; Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev53:450–490
    [Google Scholar]
  51. Tseng C. P., Albrecht J., Gunsalus R. P.. 1996; Effect of microaerophilic cell growth conditions on expression of the aerobic ( cyoABCDE and cydAB ) and anaerobic ( narGHJI , frdABCD , and dmsABC ) respiratory pathway genes in Escherichia coli . J Bacteriol178:1094–1098
    [Google Scholar]
  52. Verhamme D. T., Arents J. C., Postma P. W., Crielaard W., Hellingwerf K. J.. 2001; Glucose-6-phosphate-dependent phosphoryl flow through the Uhp two-component regulatory system. Microbiology147:3345–3352
    [Google Scholar]
  53. Wanner B. L.. 1995; Signal transduction and cross regulation in the Escherichia coli phosphate regulon by PhoR, CreC and acetyl phosphate. In Two-component Signal Transduction pp203–221 Edited by Hoch J. A.. Silhavy T. J.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  54. Wanner B. L., Wilmes-Riesenberg M. R.. 1992; Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli . J Bacteriol174:2124–2130
    [Google Scholar]
  55. Webber C. A., Kadner R. J.. 1995; Action of receiver and activator modules of UhpA in transcriptional control of the Escherichia coli sugar phosphate transport system. Mol Microbiol15:883–893[CrossRef]
    [Google Scholar]
  56. Yaku H., Kato M., Hakoshima T., Tsuzuki M., Mizuno T.. 1997; Interaction between the CheY response regulator and the histidine-containing phosphotransfer (HPt) domain of the ArcB sensory kinase in Escherichia coli . FEBS Lett408:337–340[CrossRef]
    [Google Scholar]
  57. Yamada M., Makino K., Amemura M., Shinagawa H., Nakata A.. 1989; Regulation of the phosphate regulon of Escherichia coli : analysis of mutant phoB and phoR genes causing different phenotypes. J Bacteriol171:5601–5606
    [Google Scholar]
  58. Wanner B. L.. 1992; Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria?. J Bacteriol174:2053–2058
    [Google Scholar]
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