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The bradykinin B2 receptor in the early immune response against Listeria infection

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Abstract

The endogenous danger signal bradykinin was recently found implicated in the development of immunity against parasites via dendritic cells. We here report an essential role of the B2 (B2R) bradykinin receptor in the early immune response against Listeria infection. Mice deficient in B2R (B2R−/− mice) were shown to suffer from increased hepatic bacterial burden and concomitant dramatic weight loss during infection with Listeria monocytogenes. Levels of cytokines known to play a pivotal role in the early phase immune response against L. monocytogenes, IL-12p70 and IFN-γ, were reduced in B2R−/− mice. To extend these findings to the human system, we show that bradykinin potentiates the production of IL-12p70 in human monocyte-derived dendritic cells. Thus, we show that bradykinin and the B2R play a role in early innate immune functions during bacterial infection.

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References

  1. Pamer EG (2004) Immune responses to Listeria monocytogenes. Nat Rev Immunol 4:812–823. doi:10.1038/nri1461

    Article  PubMed  CAS  Google Scholar 

  2. Edelson BT, Unanue ER (2000) Immunity to Listeria infection. Curr Opin Immunol 12:425–431. doi:10.1016/S0952-7915(00)00112-6

    Article  PubMed  CAS  Google Scholar 

  3. Guleria I, Pollard JW (2001) Aberrant macrophage and neutrophil population dynamics and impaired Th1 response to Listeria monocytogenes in colony-stimulating factor 1-deficient mice. Infect Immun 69:1795–1807. doi:10.1128/IAI.69.3.1795-1807.2001

    Article  PubMed  CAS  Google Scholar 

  4. Berg RE, Crossley E, Murray S, Forman J (2005) Relative contributions of NK and CD8 T cells to IFN-gamma mediated innate immune protection against Listeria monocytogenes. J Immunol 175:1751–1757

    PubMed  CAS  Google Scholar 

  5. Harty JT, Bevan MJ (1995) Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 3:109–117. doi:10.1016/1074-7613(95)90163-9

    Article  PubMed  CAS  Google Scholar 

  6. Huang S, Hendriks W, Althage A, Hemmi S, Bluethmann H, Kamijo R et al (1993) Immune response in mice that lack the interferon-gamma receptor. Science 19(259):1742–1745. doi:10.1126/science.8456301

    Article  Google Scholar 

  7. Carrero JA, Calderon B, Unanue ER (2004) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med 200:535–540. doi:10.1084/jem.20040769

    Article  PubMed  CAS  Google Scholar 

  8. Aliberti J, Viola JP, Vieira-de-Abreu A, Bozza PT, Sher A, Scharfstein J (2003) Cutting edge: bradykinin induces IL-12 production by dendritic cells: a danger signal that drives Th1 polarization. J Immunol 170:5349–5353

    PubMed  CAS  Google Scholar 

  9. Scharfstein J, Schmitz V, Svensjo E, Granato A, Monteiro AC (2007) Kininogens coordinate adaptive immunity through the proteolytic release of bradykinin, an endogenous danger signal driving dendritic cell maturation. Scand J Immunol 66:128–136. doi:10.1111/j.1365-3083.2007.01983.x

    Article  PubMed  CAS  Google Scholar 

  10. Bertram C, Misso NL, Fogel-Petrovic M, Figueroa C, Thompson PJ, Bhoola KD (2007) Comparison of kinin B(1) and B(2) receptor expression in neutrophils of asthmatic and non-asthmatic subjects. Int Immunopharmacol 20(7):1862–1868. doi:10.1016/j.intimp.2007.07.012

    Article  Google Scholar 

  11. Monteiro AC, Schmitz V, Svensjo E, Gazzinelli RT, Almeida IC, Todorov A et al (2006) Cooperative activation of TLR2 and bradykinin B2 receptor is required for induction of type 1 immunity in a mouse model of subcutaneous infection by Trypanosoma cruzi. J Immunol 177:6325–6335

    PubMed  CAS  Google Scholar 

  12. Mizuki M, Nakane A, Sekikawa K, Tagawa YI, Iwakura Y (2002) Comparison of host resistance to primary and secondary Listeria monocytogenes infections in mice by intranasal and intravenous routes. Infect Immun 70:4805–4811. doi:10.1128/IAI.70.9.4805-4811.2002

    Article  PubMed  CAS  Google Scholar 

  13. Brombacher F, Dorfmuller A, Magram J, Dai WJ, Kohler G, Wunderlin A et al (1999) IL-12 is dispensable for innate and adaptive immunity against low doses of Listeria monocytogenes. Int Immunol 11:325–332. doi:10.1093/intimm/11.3.325

    Article  PubMed  CAS  Google Scholar 

  14. Torres D, Barrier M, Bihl F, Quesniaux VJ, Maillet I, Akira S et al (2004) Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect Immun 72:2131–2139. doi:10.1128/IAI.72.4.2131-2139.2004

    Article  PubMed  CAS  Google Scholar 

  15. Monteiro AC, Schmitz V, Morrot A, de Arruda LB, Nagajyothi F, Granato A et al (2007) Bradykinin B2 Receptors of dendritic cells, acting as sensors of kinins proteolytically released by Trypanosoma cruzi, are critical for the development of protective type-1 responses. PLoS Pathog 3:185. doi:10.1371/journal.ppat.0030185

    Article  Google Scholar 

  16. Gekara NO, Weiss S (2008) Mast cells initiate early anti-Listeria host defences. Cell Microbiol 10:225–236

    PubMed  CAS  Google Scholar 

  17. Miller HR, Pemberton AD (2002) Tissue-specific expression of mast cell granule serine proteinases and their role in inflammation in the lung and gut. Immunology 105:375–390. doi:10.1046/j.1365-2567.2002.01375.x

    Article  PubMed  CAS  Google Scholar 

  18. Tripp CS, Gately MK, Hakimi J, Ling P, Unanue ER (1994) Neutralization of IL-12 decreases resistance to Listeria in SCID and C·B-17 mice. Reversal by IFN-gamma. J Immunol 152:1883–1887

    PubMed  CAS  Google Scholar 

  19. Shtrichman R, Samuel CE (2001) The role of gamma interferon in antimicrobial immunity. Curr Opin Microbiol 4:251–259. doi:10.1016/S1369-5274(00)00199-5

    Article  PubMed  CAS  Google Scholar 

  20. Bancroft GJ (1993) The role of natural killer cells in innate resistance to infection. Curr Opin Immunol 5:503–510. doi:10.1016/0952-7915(93)90030-V

    Article  PubMed  CAS  Google Scholar 

  21. Emoto Y, Yoshizawa I, Hurwitz R, Brinkmann V, Kaufmann SH, Emoto M (2008) Role of interleukin-12 in determining differential kinetics of invariant natural killer T cells in response to differential burden of Listeria monocytogenes. Microbes Infect 10:224–232. doi:10.1016/j.micinf.2007.11.008

    Article  PubMed  CAS  Google Scholar 

  22. Munder M, Mallo M, Eichmann K, Modolell M (1998) Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: a novel pathway of autocrine macrophage activation. J Exp Med 187:2103–2108. doi:10.1084/jem.187.12.2103

    Article  PubMed  CAS  Google Scholar 

  23. Stober D, Schirmbeck R, Reimann J (2001) IL-12/IL-18-dependent IFN-gamma release by murine dendritic cells. J Immunol 167:957–965

    PubMed  CAS  Google Scholar 

  24. Berg RE, Crossley E, Murray S, Forman J (2003) Memory CD8 + T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J Exp Med 198:1583–1593. doi:10.1084/jem.20031051

    Article  PubMed  CAS  Google Scholar 

  25. Yang J, Murphy TL, Ouyang W, Murphy KM (1999) Induction of interferon-gamma production in Th1 CD4 + T cells: evidence for two distinct pathways for promoter activation. Eur J Immunol 29:548–555. doi :10.1002/(SICI)1521-4141(199902)29:02<548::AID-IMMU548>3.0.CO;2-Z

    Article  PubMed  CAS  Google Scholar 

  26. Dai WJ, Bartens W, Kohler G, Hufnagel M, Kopf M, Brombacher F (1997) Impaired macrophage listericidal and cytokine activities are responsible for the rapid death of Listeria monocytogenes-infected IFN-gamma receptor-deficient mice. J Immunol 158:5297–5304

    PubMed  CAS  Google Scholar 

  27. Portnoy DA, Schreiber RD, Connelly P, Tilney LG (1989) Gamma interferon limits access of Listeria monocytogenes to the macrophage cytoplasm. J Exp Med 170:2141–2146. doi:10.1084/jem.170.6.2141

    Article  PubMed  CAS  Google Scholar 

  28. Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A, Alber G (1996) Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 184:747–752. doi:10.1084/jem.184.2.747

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was funded by the Dutch Ministry of Defence, grant no V502.

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Authors and Affiliations

  1. TNO Defence, Security and Safety, Business Unit Biological and Chemical Protection, PO Box 45, 2280 AA, Rijswijk, The Netherlands

    Wendy E. Kaman, Arthur F. W. M. Wolterink, Linda C. L. Boele & Desiree van der Kleij

  2. Max-Delbrück-Center for Molecular Medicine, Robert-Rössle-Strasse 10, Berlin-Buch, Germany

    Michael Bader

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  1. Wendy E. Kaman
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  2. Arthur F. W. M. Wolterink
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  3. Michael Bader
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  4. Linda C. L. Boele
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Correspondence to Desiree van der Kleij.

Additional information

W. E. Kaman and A. F. W. M. Wolterink contributed equally to this work.

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Kaman, W.E., Wolterink, A.F.W.M., Bader, M. et al. The bradykinin B2 receptor in the early immune response against Listeria infection. Med Microbiol Immunol 198, 39–46 (2009). https://doi.org/10.1007/s00430-008-0103-4

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  • DOI: https://doi.org/10.1007/s00430-008-0103-4

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