Skip to main content
SpringerLink
Log in

Up-Regulation of Bradykinin B2 Receptor by Pseudomonas aeruginosa via the NF-κB Pathway

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

As the first line of host defense, inflammatory responses in response to bacterial infection are initiated by the production of a range of mediators. Infection of Pseudomonas aeruginosa has been shown to stimulate the production of bradykinin (BK), which is known as a universal mediator for the induction of inflammatory reaction via the predominant interaction with the bradykinin B2 receptor (B2R). Thus, the interaction between BK and B2R represents an important host innate response against invading P. aeruginosa. However, the contribution of P. aeruginosa to the up-regulation of B2R expression remains unclear. Here, we report that P. aeruginosa is potent in inducing the expression of B2R at the mRNA and protein levels in a dose- and time-dependent manner. Components produced and secreted from P. aeruginosa could play an essential role in inducing B2R expression, and the secreted components are not under the control of Type III secretion system or quorum sensing. B2R expression in response to P. aeruginosa is mediated by the induction of cellular signaling that leads to the activation of transcription factor NF-κB. Thus, this study demonstrates that P. aeruginosa is able to up-regulate the expression of B2R during infection via the NF-κB signaling pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Austin CE, Faussner A, Robinson HE, Chakravarty S, Kyle DJ, Bathon JM, Proud D (1997) Stable expression of the human kinin B1 receptor in Chinese hamster ovary cells. Characterization of ligand binding and effector pathways. J Biol Chem 272:11420–11425

    Article  PubMed  CAS  Google Scholar 

  2. Bachar O, Adner M, Uddman R, Cardell LO (2004) Toll-like receptor stimulation induces airway hyper-responsiveness to bradykinin, an effect mediated by JNK and NF-kappaB signaling pathways. Eur J Immunol 34:1196–1207

    Article  PubMed  CAS  Google Scholar 

  3. Bengtson SH, Phagoo SB, Norrby-Teglund A, Pahlman L, Morgelin M, Zuraw BL, Leeb-Lundberg LM, Herwald H (2006) Kinin receptor expression during Staphylococcus aureus infection. Blood 108:2055–2063

    Article  PubMed  CAS  Google Scholar 

  4. Brint JM, Ohman DE (1995) Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of rhlR-rhlI, another set of regulators in strain pao1 with homology to the autoinducer-responsive luxR-luxI family. J Bacteriol 177:7155–7163

    PubMed  CAS  Google Scholar 

  5. Coin D, Louis D, Bernillon J, Guinand M, Wallach J (1997) LasA, alkaline protease and elastase in clinical strains of Pseudomonas aeruginosa: quantification by immunochemical methods. FEMS Immunol Med Microbiol 18:175–184

    Article  PubMed  CAS  Google Scholar 

  6. Forteza R, Lauredo IT, Burch R, Abraham WM (1994) Extracellular metabolites of Pseudomonas aeruginosa produce bronchoconstriction by different mechanisms. Am J Respir Crit Care Med 149:687–693

    PubMed  CAS  Google Scholar 

  7. Fridlianskaia II, Polianskaia GG, Blomquist G, Tatulian SA, Pinaev GP (1983) Expression of the traits characterizing the cell surface in hybrids of malignant and nonmalignant cells. Tsitologiia 25:593–600

    PubMed  CAS  Google Scholar 

  8. Ha U, Jin S (2001) Growth phase-dependent invasion of Pseudomonas aeruginosa and its survival within hela cells. Infect Immun 69:4398–4406

    Article  PubMed  CAS  Google Scholar 

  9. Ha U, Lim JH, Jono H, Koga T, Srivastava A, Malley R, Pages G, Pouyssegur J, Li JD (2007) A novel role for IkappaB kinase (IKK) alpha and IKKbeta in ERK-dependent up-regulation of MUC5AC mucin transcription by Streptococcus pneumoniae. J Immunol 178:1736–1747

    PubMed  CAS  Google Scholar 

  10. Haddad EB, Fox AJ, Rousell J, Burgess G, McIntyre P, Barnes PJ, Chung KF (2000) Post-transcriptional regulation of bradykinin B1 and B2 receptor gene expression in human lung fibroblasts by tumor necrosis factor-alpha: modulation by dexamethasone. Mol Pharmacol 57:1123–1131

    PubMed  CAS  Google Scholar 

  11. Hall JM (1992) Bradykinin receptors: pharmacological properties and biological roles. Pharmacol Ther 56:131–190

    Article  PubMed  CAS  Google Scholar 

  12. Hall JM (1997) Bradykinin receptors. Gen Pharmacol 28:1–6

    PubMed  CAS  Google Scholar 

  13. Hatada EN, Krappmann D, Scheidereit C (2000) NF-kappaB and the innate immune response. Curr Opin Immunol 12:52–58

    Article  PubMed  CAS  Google Scholar 

  14. Holder IA, Neely AN (1989) Pseudomonas elastase acts as a virulence factor in burned hosts by Hageman factor-dependent activation of the host kinin cascade. Infect Immun 57:3345–3348

    PubMed  CAS  Google Scholar 

  15. Huang TJ, Haddad EB, Fox AJ, Salmon M, Jones C, Burgess G, Chung KF (1999) Contribution of bradykinin B1 and B2 receptors in allergen-induced bronchial hyperresponsiveness. Am J Respir Crit Care Med 160:1717–1723

    PubMed  CAS  Google Scholar 

  16. Kaman WE, Wolterink AF, Bader M, Boele LC, van der Kleij D (2009) The bradykinin B2 receptor in the early immune response against listeria infection. Med Microbiol Immunol 198:39–46

    Article  PubMed  CAS  Google Scholar 

  17. Kaufman MR, Jia J, Zeng L, Ha U, Chow M, Jin S (2000) Pseudomonas aeruginosa mediated apoptosis requires the ADP-ribosylating activity of ExoS. Microbiology 146:2531–2541

    PubMed  CAS  Google Scholar 

  18. Khan MM, Yamamoto T, Araki H, Shibuya Y, Kambara T (1993) Role of Hageman factor/kallikrein-kinin system in pseudomonal elastase-induced shock model. Biochim Biophys Acta 1157:119–126

    PubMed  CAS  Google Scholar 

  19. Machen TE (2006) Innate immune response in CF airway epithelia: hyperinflammatory? Am J Physiol Cell Physiol 291:C218–C230

    Article  PubMed  CAS  Google Scholar 

  20. Mattsson E, Herwald H, Cramer H, Persson K, Sjobring U, Bjorck L (2001) Staphylococcus aureus induces release of bradykinin in human plasma. Infect Immun 69:3877–3882

    Article  PubMed  CAS  Google Scholar 

  21. Molla A, Yamamoto T, Akaike T, Miyoshi S, Maeda H (1989) Activation of Hageman factor and prekallikrein and generation of kinin by various microbial proteinases. J Biol Chem 264:10589–10594

    PubMed  CAS  Google Scholar 

  22. Pearson JP, Pesci EC, Iglewski BH (1997) Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767

    PubMed  CAS  Google Scholar 

  23. Prado GN, Taylor L, Zhou X, Ricupero D, Mierke DF, Polgar P (2002) Mechanisms regulating the expression, self-maintenance, and signaling-function of the bradykinin B2 and B1 receptors. J Cell Physiol 193:275–286

    Article  PubMed  CAS  Google Scholar 

  24. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, Ausubel FM (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268:1899–1902

    Article  PubMed  CAS  Google Scholar 

  25. Regoli D, Barabe J (1980) Pharmacology of bradykinin and related kinins. Pharmacol Rev 32:1–46

    PubMed  CAS  Google Scholar 

  26. Rumbaugh KP, Griswold JA, Hamood AN (2000) The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect 2:1721–1731

    Article  PubMed  CAS  Google Scholar 

  27. Sawa T, Ohara M, Kurahashi K, Twining SS, Frank DW, Doroques DB, Long T, Gropper MA, Wiener-Kronish JP (1998) In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect Immun 66:3242–3249

    PubMed  CAS  Google Scholar 

  28. Stewart JM (1995) Bradykinin antagonists: development and applications. Biopolymers 37:143–155

    Article  PubMed  CAS  Google Scholar 

  29. Tuomanen EI, Austrian R, Masure HR (1995) Pathogenesis of pneumococcal infection. N Engl J Med 332:1280–1284

    Article  PubMed  CAS  Google Scholar 

  30. Whiteley M, Parsek MR, Greenberg EP (2000) Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J Bacteriol 182:4356–4360

    Article  PubMed  CAS  Google Scholar 

  31. Wilson R, Pitt T, Taylor G, Watson D, MacDermot J, Sykes D, Roberts D, Cole P (1987) Pyocyanin and 1-hydroxyphenazine produced by Pseudomonas aeruginosa inhibit the beating of human respiratory cilia in vitro. J Clin Invest 79:221–229

    Article  PubMed  CAS  Google Scholar 

  32. Yahr TL, Wolfgang MC (2006) Transcriptional regulation of the Pseudomonas aeruginosa typeIII secretion system. Mol Microbiol 62:631–640

    Article  PubMed  CAS  Google Scholar 

  33. Yayama K, Hiyoshi H, Sugiyama K, Okamoto H (2006) The lipopolysaccharide-induced up-regulation of bradykinin B2-receptor in the mouse heart is mediated by tumor necrosis factor-alpha and angiotensin II. Biol Pharm Bull 29:1143–1147

    Article  PubMed  CAS  Google Scholar 

  34. Zhu H, Thuruthyil SJ, Willcox MD (2002) Determination of quorum-sensing signal molecules and virulence factors of Pseudomonas aeruginosa isolates from contact lens-induced microbial keratitis. J Med Microbiol 51:1063–1070

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Converging Research Center Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (no. 20090083290).

Author information

Authors and Affiliations

  1. Department of Biotechnology and Bioinformatics, Korea University, Jochiwon, Yeongi, Chungnam, 339-700, Republic of Korea

    Hee-Sung Shin & Un-Hwan Ha

Authors
  1. Hee-Sung Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Un-Hwan Ha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Un-Hwan Ha.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shin, HS., Ha, UH. Up-Regulation of Bradykinin B2 Receptor by Pseudomonas aeruginosa via the NF-κB Pathway. Curr Microbiol 63, 138–144 (2011). https://doi.org/10.1007/s00284-011-9959-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-011-9959-4

Keywords

Search

Navigation