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Volume 63, Issue 3

Methyl-accepting chemotaxis proteins 3 and 4 are responsible for chemotaxis and jejuna colonization in mice in response to sodium deoxycholate Free

Abstract

Methyl-accepting chemotaxis proteins (MCPs), also termed transducer-like proteins (Tlps), serve as sensors in bacterial chemotactic signalling, and detect attractants and promote bacterial movement towards suitable sites for colonization. is a leading cause of human enteritis, but the mechanisms responsible for bacterial chemotaxis and early colonization in the jejunum of hosts are poorly understood. In the present study, we identified several types of bile and sodium deoxycholate (SDC) acting as chemotactic attractants of strain NCTC 11168-O , in which SDC was the most efficient chemoattractant. In mice with bile duct ligation, the wild-type strain displayed a markedly attenuated ability for colonization. Blockage of Tlp3 or Tlp4 protein with antibody or disruption of the or gene (Δ or Δ) caused a significant inhibition of SDC-induced chemotaxis and attenuation for colonization on jejunal mucosa in mice of the bacterium. Disruption of both the genes (ΔΔ) resulted in the absence of bacterial chemotaxis and colonization, while the -gene-complemented mutants (CΔ and CΔ) reacquired these abilities. The results indicate that SDC is an effective chemoattractant for , and Tlp3 and Tlp4 are the SDC-specific sensor proteins responsible for the bacterial chemoattraction.

  • Received:
  • Accepted:
  • Published Online:
© 2014 SGM
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2014-03-01
2024-04-19
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References

  1. Alexander R. P., Zhulin I. B. 2007; Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc Natl Acad Sci U S A 104:2885–2890 [View Article][PubMed]
     [Google Scholar]
  2. Allos B. M. 2001; Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis 32:1201–1206 [View Article][PubMed]
     [Google Scholar]
  3. Bachtiar B. M., Coloe P. J., Fry B. N. 2007; Knockout mutagenesis of the kpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium-host interactions. FEMS Immunol Med Microbiol 49:149–154 [View Article][PubMed]
     [Google Scholar]
  4. Baker M. D., Wolanin P. M., Stock J. B. 2006; Signal transduction in bacterial chemotaxis. BioEssays 28:9–22 [View Article][PubMed]
     [Google Scholar]
  5. Baqar S., Applebee L. A., Bourgeois A. L. 1995; Immunogenicity and protective efficacy of a prototype Campylobacter killed whole-cell vaccine in mice. Infect Immun 63:3731–3735[PubMed]
     [Google Scholar]
  6. Bingham-Ramos L. K., Hendrixson D. R. 2008; Characterization of two putative cytochrome c peroxidases of Campylobacter jejuni involved in promoting commensal colonization of poultry. Infect Immun 76:1105–1114 [View Article][PubMed]
     [Google Scholar]
  7. Boushaba R., Kumpalume P., Slater N. K. 2003; Kinetics of whole serum and prepurified IgG digestion by pepsin for F(ab’)2 manufacture. Biotechnol Prog 19:1176–1182 [View Article][PubMed]
     [Google Scholar]
  8. Brøndsted L., Andersen M. T., Parker M., Jørgensen K., Ingmer H. 2005; The HtrA protease of Campylobacter jejuni is required for heat and oxygen tolerance and for optimal interaction with human epithelial cells. Appl Environ Microbiol 71:3205–3212 [View Article][PubMed]
     [Google Scholar]
  9. Cerda O., Rivas A., Toledo H. 2003; Helicobacter pylori strain ATCC700392 encodes a methyl-accepting chemotaxis receptor protein (MCP) for arginine and sodium bicarbonate. FEMS Microbiol Lett 224:175–181 [View Article][PubMed]
     [Google Scholar]
  10. Chang C., Miller J. F. 2006; Campylobacter jejuni colonization of mice with limited enteric flora. Infect Immun 74:5261–5271 [View Article][PubMed]
     [Google Scholar]
  11. Croxen M. A., Sisson G., Melano R., Hoffman P. S. 2006; The Helicobacter pylori chemotaxis receptor TlpB (HP0103) is required for pH taxis and for colonization of the gastric mucosa. J Bacteriol 188:2656–2665 [View Article][PubMed]
     [Google Scholar]
  12. Fernando U., Biswas D., Allan B., Willson P., Potter A. A. 2007; Influence of Campylobacter jejuni fliA, rpoN and flgK genes on colonization of the chicken gut. Int J Food Microbiol 118:194–200 [View Article][PubMed]
     [Google Scholar]
  13. Hanning I., Donoghue D. J., Jarquin R., Kumar G. S., Aguiar V. F., Metcalf J. H., Reyes-Herrera I., Slavik M. 2009; Campylobacter biofilm phenotype exhibits reduced colonization potential in young chickens and altered in vitro virulence. Poult Sci 88:1102–1107 [View Article][PubMed]
     [Google Scholar]
  14. Hansen C. H., Endres R. G., Wingreen N. S. 2008; Chemotaxis in Escherichia coli: a molecular model for robust precise adaptation. PLOS Comput Biol 4:e1 [View Article][PubMed]
     [Google Scholar]
  15. Hazelbauer G. L., Falke J. J., Parkinson J. S. 2008; Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33:9–19 [View Article][PubMed]
     [Google Scholar]
  16. Hendrixson D. R., DiRita V. J. 2004; Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52:471–484 [View Article][PubMed]
     [Google Scholar]
  17. Hinds J., Mahenthiralingam E., Kempsell K. E., Duncan K., Stokes R. W., Parish T., Stoker N. G. 1999; Enhanced gene replacement in mycobacteria. Microbiology 145:519–527 [View Article][PubMed]
     [Google Scholar]
  18. Hugdahl M. B., Beery J. T., Doyle M. P. 1988; Chemotactic behavior of Campylobacter jejuni. Infect Immun 56:1560–1566[PubMed]
     [Google Scholar]
  19. Jørgensen F., Bailey R., Williams S., Henderson P., Wareing D. R., Bolton F. J., Frost J. A., Ward L., Humphrey T. J. 2002; Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. Int J Food Microbiol 76:151–164 [View Article][PubMed]
     [Google Scholar]
  20. Khanna M. R., Bhavsar S. P., Kapadnis B. P. 2006; Effect of temperature on growth and chemotactic behaviour of Campylobacter jejuni.. Lett Appl Microbiol 43:84–90 [View Article][PubMed]
     [Google Scholar]
  21. Kirby J. R. 2009; Chemotaxis-like regulatory systems: unique roles in diverse bacteria. Annu Rev Microbiol 63:45–59 [View Article][PubMed]
     [Google Scholar]
  22. Kramer J. M., Frost J. A., Bolton F. J., Wareing D. R. 2000; Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. J Food Prot 63:1654–1659[PubMed]
     [Google Scholar]
  23. Laub M. T., Goulian M. 2007; Specificity in two-component signal transduction pathways. Annu Rev Genet 41:121–145 [View Article][PubMed]
     [Google Scholar]
  24. Liu X., Parales R. E. 2008; Chemotaxis of Escherichia coli to pyrimidines: a new role for the signal transducer tap. J Bacteriol 190:972–979 [View Article][PubMed]
     [Google Scholar]
  25. Marchant J., Wren B., Ketley J. 2002; Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. Trends Microbiol 10:155–159 [View Article][PubMed]
     [Google Scholar]
  26. Moisi M., Jenul C., Butler S. M., New A., Tutz S., Reidl J., Klose K. E., Camilli A., Schild S. 2009; A novel regulatory protein involved in motility of Vibrio cholerae.. J Bacteriol 191:7027–7038 [View Article][PubMed]
     [Google Scholar]
  27. Nadeau E., Messier S., Quessy S. 2002; Prevalence and comparison of genetic profiles of Campylobacter strains isolated from poultry and sporadic cases of campylobacteriosis in humans. J Food Prot 65:73–78[PubMed]
     [Google Scholar]
  28. Nielsen L. N., Sheppard S. K., McCarthy N. D., Maiden M. C. J., Ingmer H., Krogfelt K. A. 2010; MLST clustering of Campylobacter jejuni isolates from patients with gastroenteritis, reactive arthritis and Guillain–Barré syndrome. J Appl Microbiol 108:591–599 [View Article][PubMed]
     [Google Scholar]
  29. Parkhill J., Wren B. W., Mungall K., Ketley J. M., Churcher C., Basham D., Chillingworth T., Davies R. M., Feltwell T.& other authors ( 2000; The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [View Article][PubMed]
     [Google Scholar]
  30. Pfaffl M. W., Horgan G. W., Dempfle L. 2002; Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36 [View Article][PubMed]
     [Google Scholar]
  31. Rodríguez-Garay E. A. 2003; Cholestasis: human disease and experimental animal models. Ann Hepatol 2:150–158[PubMed]
     [Google Scholar]
  32. Stecher B., Hapfelmeier S., Müller C., Kremer M., Stallmach T., Hardt W. D. 2004; Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72:4138–4150 [View Article][PubMed]
     [Google Scholar]
  33. Stock A. M., Robinson V. L., Goudreau P. N. 2000; Two-component signal transduction. Annu Rev Biochem 69:183–215 [View Article][PubMed]
     [Google Scholar]
  34. Takata T., Fujimoto S., Amako K. 1992; Isolation of nonchemotactic mutants of Campylobacter jejuni and their colonization of the mouse intestinal tract. Infect Immun 60:3596–3600[PubMed]
     [Google Scholar]
  35. Terry K., Williams S. M., Connolly L., Ottemann K. M. 2005; Chemotaxis plays multiple roles during Helicobacter pylori animal infection. Infect Immun 73:803–811 [View Article][PubMed]
     [Google Scholar]
  36. Thompson-Chagoyán O. C., Maldonado J., Gil A. 2007; Colonization and impact of disease and other factors on intestinal microbiota. Dig Dis Sci 52:2069–2077 [View Article][PubMed]
     [Google Scholar]
  37. van Doorn P. A., Ruts L., Jacobs B. C. 2008; Clinical features, pathogenesis, and treatment of Guillain–Barré syndrome. Lancet Neurol 7:939–950 [View Article][PubMed]
     [Google Scholar]
  38. Vegge C. S., Brøndsted L., Li Y. P., Bang D. D., Ingmer H. 2009; Energy taxis drives Campylobacter jejuni toward the most favorable conditions for growth. Appl Environ Microbiol 75:5308–5314 [View Article][PubMed]
     [Google Scholar]
  39. Velayudhan J., Jones M. A., Barrow P. A., Kelly D. J. 2004; l-Serine catabolism via an oxygen-labile l-serine dehydratase is essential for colonization of the avian gut by Campylobacter jejuni.. Infect Immun 72:260–268 [View Article][PubMed]
     [Google Scholar]
  40. Wallis M. R. 1994; The pathogenesis of Campylobacter jejuni.. Br J Biomed Sci 51:57–64[PubMed]
     [Google Scholar]
  41. Wassenaar T. M., Fry B. N., van der Zeijst B. A. 1993; Genetic manipulation of Campylobacter: evaluation of natural transformation and electro-transformation. Gene 132:131–135 [View Article][PubMed]
     [Google Scholar]
  42. Williams S. M., Chen Y. T., Andermann T. M., Carter J. E., McGee D. J., Ottemann K. M. 2007; Helicobacter pylori chemotaxis modulates inflammation and bacterium-gastric epithelium interactions in infected mice. Infect Immun 75:3747–3757 [View Article][PubMed]
     [Google Scholar]
  43. Yao R., Burr D. H., Guerry P. 1997; CheY-mediated modulation of Campylobacter jejuni virulence. Mol Microbiol 23:1021–1031 [View Article][PubMed]
     [Google Scholar]
  44. Young K. T., Davis L. M., Dirita V. J. 2007; Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5:665–679 [View Article][PubMed]
     [Google Scholar]
  45. Zhao J. F., Sun A. H., Ruan P., Zhao X. H., Lu M. Q., Yan J. 2009; Vibrio vulnificus cytolysin induces apoptosis in HUVEC, SGC-7901 and SMMC-7721 cells via caspase-9/3-dependent pathway. Microb Pathog 46:194–200 [View Article][PubMed]
     [Google Scholar]
  46. Zhulin I. B. 2001; The superfamily of chemotaxis transducers: from physiology to genomics and back. Adv Microb Physiol 45:157–198 [View Article][PubMed]
     [Google Scholar]
  47. Zilbauer M., Dorrell N., Wren B. W., Bajaj-Elliott M. 2008; Campylobacter jejuni-mediated disease pathogenesis: an update. Trans R Soc Trop Med Hyg 102:123–129 [View Article][PubMed]
     [Google Scholar]
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Methyl-accepting chemotaxis proteins 3 and 4 are responsible for Campylobacter jejuni chemotaxis and jejuna colonization in mice in response to sodium deoxycholate
J. Med. Microbiol. 63, 343 (2014); https://doi.org/10.1099/jmm.0.068023-0
/content/journal/jmm/10.1099/jmm.0.068023-0
/content/journal/jmm/10.1099/jmm.0.068023-0
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