Skip to main content

Advertisement

Log in

Stenotrophomonas maltophilia fimbrin stimulates mouse bladder innate immune response

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

The role of Stenotrophomonas maltophilia fimbrin (SMF) to stimulate the bladder innate immune response was evaluated in this study. SMF was isolated and purified from clinical isolates of S .maltophilia. Different amounts of SMF (1, 5 and 15 μg) was instilled transurethrally. The innate immune response was evaluated in terms of IL-1β, TNF-α, IL-8 and NO concentrations, and mRNA expressions of IL-1β, TNF-α, IL-8 and iNOS in mouse bladder tissue. Moreover, neutrophil infiltration in urine, myeloperoxidase (MPO) activity in bladder tissue and bladder epithelial cells (BECs) activity to engulf and kill bacteria in vitro was studied. The maximum pro-inflammatory cytokines (IL-1β and TNF-α) and chemokine (IL-8) concentrations and their mRNA expressions were found in bladder homogenates of mice that were instilled with 15 μg of SMF transurethrally. The high levels of these mediators was concomitant with the high level of neutrophil infiltration in bladder tissue (MPO) and in collected urine (neutrophil count). The administration of SMF transurethrally activated the BECs in terms of bacterial uptake and intracellular bacterial killing in vitro. This study showed that the SMF administration increased the level of nitric oxide (NO) in bladder tissue. The present study proved for the first time that the administration of mice with SMF transurethrally induced cellular and molecular elements of innate immune response in mouse bladder.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Looney WJ, Narita M, Mühlemann K (2009) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9:312–323

    Article  PubMed  CAS  Google Scholar 

  2. Safdar A, Rolston KV (2007) Stenotrophomonas maltophilia: changing spectrum of a serious bacterial pathogen in patients with cancer. Clin Infect Dis 45:1602–1609

    Article  PubMed  Google Scholar 

  3. Sattler CA, Mason EO Jr, Kaplan SL (2000) Nonrespiratory Stenotrophomonas maltophilia infection at a children’s hospital. Clin Infect Dis 31:1321–1330

    Article  PubMed  CAS  Google Scholar 

  4. Weber DJ, Rutala WA, Sickbert-Bennett EE, Samsa GP, Brown V, Niederman MS (2007) Microbiology of ventilator-associated pneumonia compared with that of hospital-acquired pneumonia. Infect Control Hosp Epidemiol 28:825–831

    Article  PubMed  Google Scholar 

  5. De Vidipó LA, De Marques EA, Puchelle E, Plotkowski MC (2001) Stenotrophomonas maltophilia interaction with human epithelial respiratory cells in vitro. Microbiol Immunol 45:563–569

    PubMed  Google Scholar 

  6. de Oliveira-Garcia D, Dall’Agnol M, Rosales M, Azzuz ACGS, Martinez MB, Girón JA (2002) Characterization of flagella produced by clinical strains of Stenotrophomonas maltophilia. Emerg Infect Dis 8:918–923

    Article  PubMed  Google Scholar 

  7. Chhibber S, Zgair AK (2009) Involvement of Stenotrophomonas maltophilia flagellin in bacterial adhesion to airway biotic surfaces: an in vitro study. Am J Biomed Sci 1:188–195

    CAS  Google Scholar 

  8. Zgair AK, Chhibber S (2011) Adhesion of Stenotrophomonas maltophilia to mouse tracheal mucus is mediated through flagella. J Med Microbiol 60:1032–1037

    Article  PubMed  Google Scholar 

  9. Zgair AK, Chhibber S (2011) Immunoassay method to check the flagellin mediated binding of Stenotrophomonas maltophilia to polystyrene. Mikrobiologiia 80:136–138

    PubMed  Google Scholar 

  10. de Oliveira-Garcia D, Dall’Agnol M, Rosales M, Azzuz ACGS, Alcántara N, Martinez MB, Girón JA (2003) Fimbriae and adherence of Stenotrophomonas maltophilia to epithelial cells and to abiotic surfaces. Cell Microbiol 5:625–636

    Article  PubMed  Google Scholar 

  11. Takahashi K, Ip WE, Michelow IC, Ezekowitz RA (2006) The mannose-binding lectin: a prototypic pattern recognition molecule. Curr Opin Immunol 18:16–23

    Article  PubMed  CAS  Google Scholar 

  12. Diamond G, Beckloff N, Ryan LK (2008) Host defense peptides in the oral cavity and the lung: similarities and differences. J Dent Res 87:915–927

    Article  PubMed  CAS  Google Scholar 

  13. Zgair AK, Chhibber S (2010) Stenotrophomonas maltophilia flagellin induces a compartmentalized innate immune response in mouse lung. J Med Microbiol 59:913–919

    Article  PubMed  CAS  Google Scholar 

  14. Yin X, Chen L, Liu Y, Yang J, Ma C, Yao Z, Yang L, Wei L, Li M (2010) Enhancement of the innate immune response of bladder epithelial cells by Astragalus polysaccharides through upregulation of TLR4 expression. Biochem Biophys Res Commun 397:232–238

    Article  PubMed  CAS  Google Scholar 

  15. Mossman KL, Mian MF, Lauzon NM, Gyles CL, Lichty B, Mackenzie R, Gill N, Ashkar AA (2008) Cutting edge: FimH adhesin of type 1 fimbriae is a novel TLR4 ligand. J Immunol 181:6702–6706

    PubMed  CAS  Google Scholar 

  16. Mian MF, Lauzon NM, Andrews DW, Lichty BD, Ashkar AA (2010) FimH can directly activate human and murine natural killer cells via TLR4. Mol Ther 18:1379–1388

    Article  PubMed  CAS  Google Scholar 

  17. Andersen-Nissen E, Smith KD, Bonneau R, Strong RK, Aderem A (2007) A conserved surface on Toll-like receptor 5 recognizes bacterial flagellin. J Exp Med 204:393–403

    Article  PubMed  CAS  Google Scholar 

  18. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  19. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  20. Jang CH, Choi JH, Byun MS, Jue DM (2006) Chloroquine inhibits production of TNF-α, IL-1β and IL-6 from lipopolysaccharide-stimulated human monocytes/macrophages by different modes. Rheumatology (Oxford) 45:703–710

    Article  CAS  Google Scholar 

  21. Hwang JH, Chen JC, Yang SY, Wang MF, Chan YC (2011) Expression of tumor necrosis factor-α and interleukin-1β genes in the cochlea and inferior colliculus in salicylate-induced tinnitus. J Neuroinflammation 8:30

    Article  PubMed  CAS  Google Scholar 

  22. Zimová-Herknerová M, Mysliveček J, Potměšil P (2008) Retinoic acid attenuates the mild hyperoxic lung injury in newborn mice. Physiol Res 57:33–40

    PubMed  Google Scholar 

  23. Tanioka T, Tamura Y, Fukaya M, Shinozaki S, Mao J, Kim M, Shimizu N, Kitamura T, Kaneki M (2011) Inducible nitric-oxide synthase and nitric oxide donor decrease insulin receptor substrate-2 protein expression by promoting proteasome-dependent degradation in pancreatic β-cells: involvement of glycogen synthase kinase-3β. J Biol Chem 286:29388–29396

    Article  PubMed  CAS  Google Scholar 

  24. Riederer M, Lechleitner M, Hrzenjak A, Koefeler H, Desoye G, Heinemann A, Frank S (2011) Endothelial lipase (EL) and EL-generated lysophosphatidylcholines promote IL-8 expression in endothelial cells. Atherosclerosis 214:338–344

    Article  PubMed  CAS  Google Scholar 

  25. Hirano S (1996) Migratory responses of PMN after intraperitoneal and intratracheal administration of lipopolysaccharide. Am J Physiol 270:L836–L845

    PubMed  CAS  Google Scholar 

  26. Tsai WC, Strieter RM, Zisman DA, Wilkowski JM, Bucknell KA, Chen GH, Standiford TJ (1997) Nitric oxide is required for effective innate immunity against Klebsiella pneumoniae. Infect Immun 65:1870–1875

    PubMed  CAS  Google Scholar 

  27. Agace WW, Hedges SR, Ceska M, Svanborg C (1993) Interleukin-8 and the neutrophil response to mucosal gram-negative infection. J Clin Invest 92:780–785

    Article  PubMed  CAS  Google Scholar 

  28. Zgair AK (2012) The effect of high temperature on the kinetics of lipopolysaccharide (LPS)-induced human monocytes activity in vitro. Cell Immunol 275:55–60

    Article  PubMed  CAS  Google Scholar 

  29. El-Achkar TM, Huang X, Plotkin Z, Sandoval RM, Rhodes GJ, Dagher PC (2006) Sepsis induces changes in the expression and distribution of Toll-like receptor 4 in the rat kidney. Am J Physiol Renal Physiol 290:F1034–F1043

    Article  PubMed  CAS  Google Scholar 

  30. Chassin C, Tourneur E, Bens M, Vandewalle A (2011) A role for collecting duct epithelial cells in renal antibacterial defences. Cell Microbiol 13:1107–1113

    Article  PubMed  CAS  Google Scholar 

  31. Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A (2002) Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 195:559–570

    Article  PubMed  CAS  Google Scholar 

  32. Chassin C, Vimont S, Cluzeaud F, Bens M, Goujon JM, Fernandez B, Hertig A, Rondeau E, Arlet G, Hornef MW, Vandewalle A (2008) TLR4 facilitates translocation of bacteria across renal collecting duct cells. J Am Soc Nephrol 19:2364–2374

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. K. Zgair.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zgair, A.K., Al-Adressi, A.M.H. Stenotrophomonas maltophilia fimbrin stimulates mouse bladder innate immune response. Eur J Clin Microbiol Infect Dis 32, 139–146 (2013). https://doi.org/10.1007/s10096-012-1729-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-012-1729-0

Keywords

Navigation