Role of two-component systems in the virulence of Free

Abstract

Understanding of how the human pathogen perceives and responds to its environment in the host offers insight into the pathogenesis of disease caused by this important bacterium and the potential for improved interventions. A central role in this environmental response is played by two-component systems (TCSs), which both sense the environment and drive the cellular response. Molecular advances in the form of genome sequencing, signature-tagged mutagenesis, differential fluorescence induction and microarray analysis have yielded considerable progress in the study of these systems in . These recent advances are discussed here, focusing in particular on the role of TCSs in the virulence of .

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2006-04-01
2024-03-29
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References

  1. Barrett J. F., Hoch J. A. 1998; Two-component signal transduction as a target for microbial anti-infective therapy. Antimicrob Agents Chemother 42:1529–1536
    [Google Scholar]
  2. Bartilson M., Marra A., Christine J., Asundi J. S., Schneider W. P., Hromockyj A. E. 2001; Differential fluorescence induction reveals Streptococcus pneumoniae loci regulated by competence stimulatory peptide. Mol Microbiol 39:126–135 [CrossRef]
    [Google Scholar]
  3. Bent C. J., Isaacs N. W., Mitchell T. J., Riboldi-Tunnicliffe A. 2003; Cloning, overexpression, purification, crystallization and preliminary diffraction analysis of the receiver domain of MicA. Acta Crystallogr D Biol Crystallogr 59:758–760 [CrossRef]
    [Google Scholar]
  4. Bent C. J., Isaacs N. W., Mitchell T. J., Riboldi-Tunnicliffe A. 2004; Crystal structure of the response regulator 02 receiver domain, the essential YycF two-component system of Streptococcus pneumoniae in both complexed and native states. J Bacteriol 186:2872–2879 [CrossRef]
    [Google Scholar]
  5. Blue C. E., Mitchell T. J. 2003; Contribution of a response regulator to the virulence of Streptococcus pneumoniae is strain dependent. Infect Immun 71:4405–4413 [CrossRef]
    [Google Scholar]
  6. Bogaert D., Hermans P. W., Adrian P. V., Rumke H. C., de Groot R. 2004; Pneumococcal vaccines: an update on current strategies. Vaccine 22:2209–2220 [CrossRef]
    [Google Scholar]
  7. Chapuy-Regaud S., Ogunniyi A. D., Diallo N., Huet Y., Desnottes J. F., Paton J. C., Escaich S., Trombe M. C. 2003; RegR, a global LacI/GalR family regulator, modulates virulence and competence in Streptococcus pneumoniae . Infect Immun 71:2615–2625 [CrossRef]
    [Google Scholar]
  8. Clausen V. A., Bae W., Throup J., Burnham M. K., Rosenberg M., Wallis N. G. 2003; Biochemical characterization of the first essential two-component signal transduction system from Staphylococcus aureus and Streptococcus pneumoniae . J Mol Microbiol Biotechnol 5:252–260 [CrossRef]
    [Google Scholar]
  9. Claverys J. P., Havarstein L. S. 2002; Extracellular-peptide control of competence for genetic transformation in Streptococcus pneumoniae . Front Biosci 7:d1798–1814 [CrossRef]
    [Google Scholar]
  10. Dagkessamanskaia A., Moscoso M., Henard V., Guiral S., Overweg K., Reuter M., Martin B., Wells J., Claverys J. P. 2004; Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae : competence triggers stationary phase autolysis of ciaR mutant cells. Mol Microbiol 51:1071–1086 [CrossRef]
    [Google Scholar]
  11. de Saizieu A., Gardes C., Flint N., Wagner C., Kamber M., Mitchell T. J., Keck W., Amrein K. E., Lange R. 2000; Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide. J Bacteriol 182:4696–4703 [CrossRef]
    [Google Scholar]
  12. Dutta R., Qin L., Inouye M. 1999; Histidine kinases: diversity of domain organization. Mol Microbiol 34:633–640 [CrossRef]
    [Google Scholar]
  13. Echenique J. R., Trombe M. C. 2001; Competence repression under oxygen limitation through the two-component MicAB signal-transducing system in Streptococcus pneumoniae and involvement of the PAS domain of MicB. J Bacteriol 183:4599–4608 [CrossRef]
    [Google Scholar]
  14. Echenique J. R., Chapuy-Regaud S., Trombe M. C. 2000; Competence regulation by oxygen in Streptococcus pneumoniae : involvement of ciaRH and comCDE . Mol Microbiol 36:688–696
    [Google Scholar]
  15. Fabret C., Hoch J. A. 1998; A two-component signal transduction system essential for growth of Bacillus subtilis : implications for anti-infective therapy. J Bacteriol 180:6375–6383
    [Google Scholar]
  16. Giammarinaro P., Sicard M., Gasc A. M. 1999; Genetic and physiological studies of the CiaH-CiaR two-component signal-transducing system involved in cefotaxime resistance and competence of Streptococcus pneumoniae . Microbiology 145:1859–1869 [CrossRef]
    [Google Scholar]
  17. Guenzi E., Hakenbeck R. 1995; Genetic competence and susceptibility to beta-lactam antibiotics in Streptococcus pneumoniae R6 are linked via a two-component signal-transducing system cia. Dev Biol Stand 85:125–128
    [Google Scholar]
  18. Guenzi E., Gasc A. M., Sicard M. A., Hakenbeck R. 1994; A two-component signal-transducing system is involved in competence and penicillin susceptibility in laboratory mutants of Streptococcus pneumoniae . Mol Microbiol 12:505–515 [CrossRef]
    [Google Scholar]
  19. Guidi-Rontani C. 2002; The alveolar macrophage: the Trojan horse of Bacillus anthracis . Trends Microbiol 10:405–409 [CrossRef]
    [Google Scholar]
  20. Haas W., Sublett J., Kaushal D., Tuomanen E. I. 2004; Revising the role of the pneumococcal vex - vncRS locus in vancomycin tolerance. J Bacteriol 186:8463–8471 [CrossRef]
    [Google Scholar]
  21. Haas W., Kaushal D., Sublett J., Obert C., Tuomanen E. I. 2005; Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae . J Bacteriol 187:8205–8210 [CrossRef]
    [Google Scholar]
  22. Hakenbeck R., Balmelle N., Weber B., Gardes C., Keck W., de Saizieu A. 2001; Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae . Infect Immun 69:2477–2486 [CrossRef]
    [Google Scholar]
  23. Hava D. L., Camilli A. 2002; Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45:1389–1406
    [Google Scholar]
  24. Hoch J. A. 2000; Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3:165–170 [CrossRef]
    [Google Scholar]
  25. Ibrahim Y. M., Kerr A. R., McCluskey J., Mitchell T. J. 2004a; Control of virulence by the two-component system CiaR/H is mediated via HtrA, a major virulence factor of Streptococcus pneumoniae . J Bacteriol 186:5258–5266 [CrossRef]
    [Google Scholar]
  26. Ibrahim Y. M., Kerr A. R., McCluskey J., Mitchell T. J. 2004b; Role of HtrA in the virulence and competence of Streptococcus pneumoniae . Infect Immun 72:3584–3591 [CrossRef]
    [Google Scholar]
  27. Kadioglu A., Echenique J., Manco S., Trombe M.-C., Andrew P. W. 2003; The MicAB two-component signaling system is involved in virulence of Streptococcus pneumoniae . Infect Immun 71:6676–6679 [CrossRef]
    [Google Scholar]
  28. Lange R., Wagner C., de Saizieu A. & 7 other authors; 1999; Domain organization and molecular characterization of 13 two-component systems identified by genome sequencing of Streptococcus pneumoniae . Gene 237:223–234 [CrossRef]
    [Google Scholar]
  29. Lau G. W., Haataja S., Lonetto M., Kensit S. E., Marra A., Bryant A. P., McDevitt D., Morrison D. A., Holden D. W. 2001; A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol Microbiol 40:555–571 [CrossRef]
    [Google Scholar]
  30. Luo P., Morrison D. A. 2003; Transient association of an alternative sigma factor, ComX, with RNA polymerase during the period of competence for genetic transformation in Streptococcus pneumoniae . J Bacteriol 185:349–358 [CrossRef]
    [Google Scholar]
  31. Luo P., Li H., Morrison D. A. 2003; ComX is a unique link between multiple quorum sensing outputs and competence in Streptococcus pneumoniae . Mol Microbiol 50:623–633 [CrossRef]
    [Google Scholar]
  32. Luo P., Li H., Morrison D. A. 2004; Identification of ComW as a new component in the regulation of genetic transformation in Streptococcus pneumoniae . Mol Microbiol 54:172–183 [CrossRef]
    [Google Scholar]
  33. Marra A., Asundi J., Bartilson M. & 7 other authors; 2002; Differential fluorescence induction analysis of Streptococcus pneumoniae identifies genes involved in pathogenesis. Infect Immun 70:1422–1433 [CrossRef]
    [Google Scholar]
  34. Martin P. K., Li T., Sun D., Biek D. P., Schmid M. B. 1999; Role in cell permeability of an essential two-component system in Staphylococcus aureus . J Bacteriol 181:3666–3673
    [Google Scholar]
  35. Mascher T., Zahner D., Merai M., Balmelle N., de Saizieu A. B., Hakenbeck R. 2003; The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis. J Bacteriol 185:60–70 [CrossRef]
    [Google Scholar]
  36. McAllister L. J., Tseng H. J., Ogunniyi A. D., Jennings M. P., McEwan A. G., Paton J. C. 2004; Molecular analysis of the psa permease complex of Streptococcus pneumoniae . Mol Microbiol 53:889–901 [CrossRef]
    [Google Scholar]
  37. McCluskey J., Hinds J., Husain S., Witney A., Mitchell T. J. 2004; A two-component system that controls the expression of pneumococcal surface antigen A (PsaA) and regulates virulence and resistance to oxidative stress in Streptococcus pneumoniae . Mol Microbiol 51:1661–1675 [CrossRef]
    [Google Scholar]
  38. Mindich L. 1966; Bacteriocins of Diplococcus pneumoniae . I. Antagonistic relationships and genetic transformations. J Bacteriol 92:1090–1098
    [Google Scholar]
  39. Mohedano M. L., Overweg K., de la Fuente A., Reuter M., Altabe S., Mulholland F., de Mendoza D., Lopez P., Wells J. M. 2005; Evidence that the essential response regulator YycF in Streptococcus pneumoniae modulates expression of fatty acid biosynthesis genes and alters membrane composition. J Bacteriol 187:2357–2367 [CrossRef]
    [Google Scholar]
  40. Mulholland K. A. 1997; A Report Prepared for the Scientific Advisory Group of Experts, Global Programme for Vaccines and Immunization. World Health Organization, 1997 .
    [Google Scholar]
  41. Ng W. L., Robertson G. T., Kazmierczak K. M., Zhao J., Gilmour R., Winkler M. E. 2003; Constitutive expression of PcsB suppresses the requirement for the essential VicR (YycF) response regulator in Streptococcus pneumoniae R6. Mol Microbiol 50:1647–1663 [CrossRef]
    [Google Scholar]
  42. Ng W. L., Kazmierczak K. M., Winkler M. E. 2004; Defective cell wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator. Mol Microbiol 53:1161–1175 [CrossRef]
    [Google Scholar]
  43. Ng W. L., Tsui H. C., Winkler M. E. 2005; Regulation of the pspA virulence factor and essential pcsB murein biosynthetic genes by the phosphorylated VicR (YycF) response regulator in Streptococcus pneumoniae . J Bacteriol 187:7444–7459 [CrossRef]
    [Google Scholar]
  44. Novak R., Cauwels A., Charpentier E., Tuomanen E. 1999a; Identification of a Streptococcus pneumoniae gene locus encoding proteins of an ABC phosphate transporter and a two-component regulatory system. J Bacteriol 181:1126–1133
    [Google Scholar]
  45. Novak R., Henriques B., Charpentier E., Normark S., Tuomanen E. 1999b; Emergence of vancomycin tolerance in Streptococcus pneumoniae . Nature 399:590–593 [CrossRef]
    [Google Scholar]
  46. Obaro S. K. 2000; Confronting the pneumococcus: a target shift or bullet change?. Vaccine 19:1211–1217 [CrossRef]
    [Google Scholar]
  47. Ogunniyi A. D., Giammarinaro P., Paton J. C. 2002; The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo . Microbiology 148:2045–2053
    [Google Scholar]
  48. Orihuela C. J., Janssen R., Robb C. W., Watson D. A., Niesel D. W. 2000; Peritoneal culture alters Streptococcus pneumoniae protein profiles and virulence properties. Infect Immun 68:6082–6086 [CrossRef]
    [Google Scholar]
  49. Orihuela C. J., Mills J., Robb C. W., Wilson C. J., Watson D. A., Niesel D. W. 2001; Streptococcus pneumoniae PstS production is phosphate responsive and enhanced during growth in the murine peritoneal cavity. Infect Immun 69:7565–7571 [CrossRef]
    [Google Scholar]
  50. Orihuela C. J., Radin J. N., Sublett J. E., Gao G., Kaushal D., Tuomanen E. I. 2004; Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun 72:5582–5596 [CrossRef]
    [Google Scholar]
  51. Paterson G. K., Mitchell T. J. 2006; The role of Streptococcus pneumoniae sortase A in colonisation and pathogenesis. Microbes Infect 8:145–153 [CrossRef]
    [Google Scholar]
  52. Pestova E. V., Havarstein L. S., Morrison D. A. 1996; Regulation of competence for genetic transformation in Streptococcus pneumoniae by an auto-induced peptide pheromone and a two-component regulatory system. Mol Microbiol 21:853–862 [CrossRef]
    [Google Scholar]
  53. Peterson S. N., Sung C. K., Cline R. & 13 other authors; 2004; Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. Mol Microbiol 51:1051–1070 [CrossRef]
    [Google Scholar]
  54. Quin L. R., Carmicle S., Dave S., Pangburn M. K., Evenhuis J. P., McDaniel L. S. 2005; In vivo binding of complement regulator factor H by Streptococcus pneumoniae . J Infect Dis 192:1996–2003 [CrossRef]
    [Google Scholar]
  55. Riboldi-Tunnicliffe A., Trombe M. C., Bent C. J., Isaacs N. W., Mitchell T. J. 2004; Crystallization and preliminary crystallographic studies of the D59A mutant of MicA, a YycF response-regulator homologue from Streptococcus pneumoniae . Acta Crystallogr D Biol Crystallogr 60:950–951 [CrossRef]
    [Google Scholar]
  56. Robertson G. T., Zhao J., Desai B. V., Coleman W. H., Nicas T. I., Gilmour R., Grinius L., Morrison D. A., Winkler M. E. 2002; Vancomycin tolerance induced by erythromycin but not by loss of vncRS , vex3 , or pep27 function in Streptococcus pneumoniae . J Bacteriol 184:6987–7000 [CrossRef]
    [Google Scholar]
  57. Sebert M. E., Palmer L. M., Rosenberg M., Weiser J. N. 2002; Microarray-based identification of htrA , a Streptococcus pneumoniae gene that is regulated by the CiaRH two-component system and contributes to nasopharyngeal colonization. Infect Immun 70:4059–4067 [CrossRef]
    [Google Scholar]
  58. Standish A. J., Stroeher U. H., Paton J. C. 2005; The two-component signal transduction system RR06/HK06 regulates expression of cbpA in Streptococcus pneumoniae . Proc Natl Acad Sci U S A 102:7701–7706 [CrossRef]
    [Google Scholar]
  59. Stock A. M., Robinson V. L., Goudreau P. N. 2000; Two-component signal transduction. Annu Rev Biochem 69:183–215 [CrossRef]
    [Google Scholar]
  60. Sung C. K., Morrison D. A. 2005; Two distinct functions of ComW in stabilization and activation of the alternative sigma factor ComX in Streptococcus pneumoniae . J Bacteriol 187:3052–3061 [CrossRef]
    [Google Scholar]
  61. Tan T. Q. 2003; Antibiotic resistant infections due to Streptococcus pneumoniae : impact on therapeutic options and clinical outcome. Curr Opin Infect Dis 16:271–277 [CrossRef]
    [Google Scholar]
  62. Throup J. P., Koretke K. K., Bryant A. P. & 9 other authors; 2000; A genomic analysis of two-component signal transduction in Streptococcus pneumoniae . Mol Microbiol 35:566–576
    [Google Scholar]
  63. Ulijasz A. T., Andes D. R., Glasner J. D., Weisblum B. 2004; Regulation of iron transport in Streptococcus pneumoniae by RitR, an orphan response regulator. J Bacteriol 186:8123–8136 [CrossRef]
    [Google Scholar]
  64. Valdivia R. H., Falkow S. 1996; Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22:367–378 [CrossRef]
    [Google Scholar]
  65. Wagner C., Saizieu Ad A., Schonfeld H. J., Kamber M., Lange R., Thompson C. J., Page M. G. 2002; Genetic analysis and functional characterization of the Streptococcus pneumoniae vic operon. Infect Immun 70:6121–6128 [CrossRef]
    [Google Scholar]
  66. Whatmore A. M., King S. J., Doherty N. C., Sturgeon D., Chanter N., Dowson C. G. 1999; Molecular characterization of equine isolates of Streptococcus pneumoniae : natural disruption of genes encoding the virulence factors pneumolysin and autolysin. Infect Immun 67:2776–2782
    [Google Scholar]
  67. Zahner D., Kaminski K., van der Linden M., Mascher T., Meral M., Hakenbeck R. 2002; The ciaR / ciaH regulatory network of Streptococcus pneumoniae . J Mol Microbiol Biotechnol 4:211–216
    [Google Scholar]
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