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Mast cells mediate Pseudomonas aeruginosa lipopolysaccharide-induced lung inflammation in rat

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Abstract

Activated mast cells have been demonstrated to play a pivotal role in Pseudomonas aeruginosa lung infections. However, there is no report about the involvement of mast cells in P. aeruginosa lipopolysaccharide (LPS)-induced lung inflammation. This study aimed at evaluating the role of mast cells in P. aeruginosa LPS-induced lung inflammation in rats. Mast cells stabilization was carried out by intraperitoneal injections of cromolyn. Lung inflammation was induced by the intratracheal instillation of P. aeruginosa LPS (5 μg/kg bw) and inflammatory status was evaluated 4 h post-LPS instillation. We found that activated mast cells could constitute a pivotal source of several inflammatory cytokines, including TNF-α, IL-1β, and IL-6. These cells might regulate polymorphonuclear neutrophil (PMN) recruitment and be implicated in the alteration of alveolar–capillary permeability via the release of TNF-α and IL-1β. We also detected that activated mast cells could be involved in the alteration of the expression of two epithelial tight junction proteins (claudin-1 and occludin) during the acute phase of inflammation. Our results suggest that activated mast cells might play a critical role in P. aeruginosa LPS-induced lung inflammation. Therefore, mast cell stabilization may be a potential novel approach for the prevention and treatment of P. aeruginosa-induced lung infections.

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References

  1. Siebenhaar F, Syska W, Weller K, Magerl M, Zuberbier T, Metz M, Maurer M (2007) Control of Pseudomonas aeruginosa skin infections in mice is mast cell-dependent. Am J Pathol 170:1910–1916

    Article  PubMed  CAS  Google Scholar 

  2. Boudreau RT, Garduno R, Lin TJ (2002) Protein phosphatase 2A and protein kinase Cα are physically associated and are involved in Pseudomonas aeruginosa-induced interleukin 6 production by mast cells. J Biol Chem 277:5322–5329

    Article  PubMed  CAS  Google Scholar 

  3. Lin TJ, Garduno R, Boudreau RTM, Issekutz AC (2002) Pseudomonas aeruginosa activates human mast cells to induce neutrophil transendothelial migration via mast cell-derived IL-1 α and β. J Immunol 169:4522–4530

    PubMed  CAS  Google Scholar 

  4. Lin TJ, Maher LH, Gomi K, McCurdy JD, Garduno R, Marshall JS (2003) Selective early production of CCL20, or macrophage inflammatory protein 3α, by human mast cells in response to Pseudomonas aeruginosa. Infect Immun 71:365–373

    Article  PubMed  CAS  Google Scholar 

  5. Sun G, Liu F, Lin TJ (2005) Identification of Pseudomonas aeruginosa-induced genes in human mast cells using suppression subtractive hybridization: up-regulation of IL-8 and CCL4 production. Clin Exp Immunol 142:199–205

    Article  PubMed  CAS  Google Scholar 

  6. Hirsch EB, Tam VH (2010) Impact of multidrug-resistant Pseudomonas aeruginosa infection on patient outcomes. Expert Rev Pharmacoecon Outcomes Res 10:441–451

    Article  PubMed  Google Scholar 

  7. Veesenmeyer JL, Hauser AR, Lisboa T, Rello J (2009) Pseudomonas aeruginosa virulence and therapy: evolving translational strategies. Crit Care Med 37:1777–1786

    Article  PubMed  Google Scholar 

  8. Ramphal R, Balloy V, Jyot J, Verma A, Si-Tahar M, Chignard M (2008) Control of Pseudomonas aeruginosa in the lung requires the recognition of either lipopolysaccharide or flagellin. J Immunol 181:586–592

    PubMed  CAS  Google Scholar 

  9. Azghani AO, Miller EJ, Peterson BT (2000) Virulence factors from Pseudomonas aeruginosa increase lung epithelial permeability. Lung 178:261–269

    Article  PubMed  CAS  Google Scholar 

  10. Boncoeur E, Tardif V, Tessier MC, Morneau F, Lavoie J, Gendreau-Berthiaume E, Grygorczyk R, Dagenais A, Berthiaume Y (2010) Modulation of epithelial sodium channel activity by lipopolysaccharide in alveolar type II cells: involvement of purinergic signaling. Am J Physiol Lung Cell Mol Physiol 298:L417–L426

    Article  PubMed  CAS  Google Scholar 

  11. Eutamène H, Theodorou V, Schmidlin F, Tondereau V, Garcia-Villar R, Salvador-Cartier C, Chovet M, Bertrand C, Bueno L (2005) LPS-induced lung inflammation is linked to increased epithelial permeability: role of MLCK. Eur Respir J 25:789–796

    Article  PubMed  Google Scholar 

  12. Wang Y, Thorlacius H (2005) Mast cell-derived tumour necrosis factor-α mediates macrophage inflammatory protein-2-induced recruitment of neutrophils in mice. Br J Pharmacol 145:1062–1068

    Article  PubMed  CAS  Google Scholar 

  13. Biedermann T, Kneilling M, Mailhammer R, Maier K, Sander CA, Kollias G, Kunkel SL, Hültner L, Röcken M (2000) Mast cells control neutrophil recruitment during T cell-mediated delayed-type hypersensitivity reactions through tumor necrosis factor and macrophage inflammatory protein 2. J Exp Med 192:1441–1452

    Article  PubMed  CAS  Google Scholar 

  14. Theoharides TC, Alysandratos KD, Angelidou A, Delivanis DA, Sismanopoulos N, Zhang B, Asadi S, Vasiadi M, Weng Z, Miniati A, Kalogeromitros D (2011) Mast cells and inflammation. Biochim Biophys Acta 1822:21–33

    Google Scholar 

  15. Supajatura V, Ushio H, Nakao A, Akira S, Okumura K, Ra C, Ogawa H (2002) Differential responses of mast cell Toll-like receptors 2 and 4 in allergy and innate immunity. J Clin Invest 109:1351–1359

    PubMed  CAS  Google Scholar 

  16. Lê BV, Khorsi-Cauet H, Bach V, Gay-Quéheillard J (2011) Modulation of Pseudomonas aeruginosa lipopolysaccharide-induced lung inflammation by chronic iron overload in rat. FEMS Immunol Med Microbiol (in press)

  17. Shishibori T, Oyama Y, Matsushita O, Yamashita K, Furuichi H, Okabe A, Maeta H, Hata Y, Kobayashi R (1999) Three distinct anti-allergic drugs, amlexanox, cromolyn and tranilast, bind to S100A12 and S100A13 of the S100 protein family. Biochem J 338:583–589

    Article  PubMed  CAS  Google Scholar 

  18. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  19. Gay J, Fioramonti J, Garcia-Villar R, Bueno L (2000) Development and sequels of intestinal inflammation in nematode-infected rats: role of mast cells and capsaicin-sensitive afferents. Neuroimmunomodulation 8:171–178

    Article  PubMed  CAS  Google Scholar 

  20. Nava F, Caputi AP (1999) Central effects of cromoglycate sodium salt in rats treated with lipopolysaccharide. Eur J Pharmacol 367:351–359

    Article  PubMed  CAS  Google Scholar 

  21. Tigani B, Hannon JP, Rondeau C, Mazzoni L, Fozard JR (2002) Airway hyperresponsiveness to adenosine induced by lipopolysaccharide in Brown Norway rats. Br J Pharmacol 136:111–119

    Article  PubMed  CAS  Google Scholar 

  22. Dentener MA, Vreugdenhil AC, Hoet PH, Vernooy JH, Nieman FH, Heumann D, Janssen YM, Buurman WA, Wouters EF (2000) Production of the acute-phase protein lipopolysaccharide-binding protein by respiratory type II epithelial cells: implications for local defense to bacterial endotoxins. Am J Respir Cell Mol Biol 23:146–153

    PubMed  CAS  Google Scholar 

  23. Hansen GH, Rasmussen K, Niels-Christiansen LL, Danielsen E (2009) Lipopolysaccharide-binding protein: localization in secretory granules of Paneth cells in the mouse small intestine. Histochem Cell Biol 131:727–32

    Article  PubMed  CAS  Google Scholar 

  24. Yi ES, Ulich TR (1992) Endotoxin, interleukin-1, and tumor necrosis factor cause neutrophil-dependent microvascular leakage in postcapillary venules. Am J Pathol 140:659–663

    PubMed  CAS  Google Scholar 

  25. Nelson S, Bagby GJ, Bainton BG, Wilson LA, Thompson JJ, Summer WR (1989) Compartmentalization of intraalveolar and systemic lipopolysaccharide-induced tumor necrosis factor and the pulmonary inflammatory response. J Infect Dis 159:189–194

    Article  PubMed  CAS  Google Scholar 

  26. Lukacs NW, Hogaboam CM, Kunkel SL, Chensue SW, Burdick MD, Evanoff HL, Strieter RM (1998) Mast cells produce ENA-78, which can function as a potent neutrophil chemoattractant during allergic airway inflammation. J Leukoc Biol 63:746–751

    PubMed  CAS  Google Scholar 

  27. Lino dos Santos Franco A, Damazo AS, Beraldo de Souza HR, Domingos HV, Oliveira-Filho RM, Oliani SM, Costa SKP, Tavares de Lima W (2006) Pulmonary neutrophil recruitment and bronchial reactivity in formaldehyde-exposed rats are modulated by mast cells and differentially by neuropeptides and nitric oxide. Toxicol Appl Pharmacol 214:35–42

    Article  PubMed  CAS  Google Scholar 

  28. Faith M, Sukumaran A, Pulimood AB, Jacob M (2008) How reliable an indicator of inflammation is myeloperoxidase activity? Clin Chim Acta 396:23–25

    Article  PubMed  CAS  Google Scholar 

  29. Kuo HP, Hwang KH, Lin HC, Wang CH, Lu LC (1997) Effect of endogenous nitric oxide on tumour necrosis factor-α-induced leukosequestration and IL-8 release in guinea-pigs airways in vivo. Br J Pharmacol 122:103–111

    Article  PubMed  CAS  Google Scholar 

  30. Nakamura Y, Kambe N, Saito M, Nishikomori R, Kim YG, Murakami M, Núñez G, Matsue H (2009) Mast cells mediate neutrophil recruitment and vascular leakage through the NLRP3 inflammasome in histamine-independent urticaria. J Exp Med 206:1037–1046

    Article  PubMed  CAS  Google Scholar 

  31. Gougerot-Pocidalo M-A (2002) Polynucléaires neutrophiles humains. Rev Fr Lab 2002:43–51

    Google Scholar 

  32. Suarez-Cuervo C, Harris KW, Kallman L, Kalervo Väänänen H, Selander KS (2003) Tumor necrosis factor-α induces interleukin-6 production via extracellular-regulated kinase 1 activation in breast cancer cells. Breast Cancer Res Treat 80:71–78

    Article  PubMed  CAS  Google Scholar 

  33. Santen S, Wang Y, Menger MD, Jeppsson B, Thorlacius H (2008) Mast-cell-dependent secretion of CXC chemokines regulates ischemia-reperfusion-induced leukocyte recruitment in the colon. Int J Colorectal Dis 23:527–534

    Article  PubMed  Google Scholar 

  34. Lacherade JC, Van De Louw A, Planus E, Escudier E, D’Ortho MP, Lafuma C, Harf A, Delclaux C (2001) Evaluation of basement membrane degradation during TNF-α-induced increase in epithelial permeability. Am J Physiol Lung Cell Mol Physiol 281:L134–L143

    PubMed  CAS  Google Scholar 

  35. Ganter MT, Roux J, Miyazawa B, Howard M, Frank JA, Su G, Sheppard D, Violette SM, Weinreb PH, Horan GS, Matthay MA, Pittet JF (2008) Interleukin-1β causes acute lung injury via αvβ5 and αvβ6 integrin-dependent mechanisms. Circ Res 102:804–812

    Article  PubMed  CAS  Google Scholar 

  36. Wray C, Mao Y, Pan J, Chandrasena A, Piasta F, Frank JA (2009) Claudin-4 augments alveolar epithelial barrier function and is induced in acute lung injury. Am J Physiol Lung Cell Mol Physiol 297:L219–L227

    Article  PubMed  CAS  Google Scholar 

  37. Coyne CB, Gambling TM, Boucher RC, Carson JL, Johnson LG (2003) Role of claudin interactions in airway tight junctional permeability. Am J Physiol Lung Cell Mol Physiol 285:L1166–L1178

    PubMed  CAS  Google Scholar 

  38. Jacob C, Yang PC, Darmoul D, Amadesi S, Saito T, Cottrell GS, Coelho AM, Singh P, Grady EF, Perdue M, Bunnett NW (2005) Mast cell tryptase controls paracellular permeability of the intestine. Role of protease-activated receptor 2 and β-arrestins. J Biol Chem 280:31936–31948

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

The authors thank Picardy Regional Council (France) for the financial support in this work and for a doctoral award to B.V.L.

Conflict of interest

The authors declare that they have no competing or financial interests.

Authors’ contributions

B.V.L. participated in the design of the study, collected the study material, carried out the ELISA, spectrophotometric, histological, and statistical analyses, and drafted the manuscript. H.K.-C. helped to draft the manuscript. V.B. helped to perform the statistical analysis and draft the manuscript. J.G.-Q. is the head of the project, participated in the design of the study, collected the study material, carried out RT-PCR analyses, and helped to draft the manuscript. All authors have read and approved the final manuscript.

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  1. Peritox Laboratory, EA4285-UMI 01, Faculty of Medicine, Picardy Jules Verne University, 3 rue des Louvels, 80036, Amiens, France

    B. V. Lê, H. Khorsi-Cauet, V. Bach & J. Gay-Quéheillard

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  1. B. V. Lê
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  2. H. Khorsi-Cauet
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  4. J. Gay-Quéheillard
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Correspondence to J. Gay-Quéheillard.

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Lê, B.V., Khorsi-Cauet, H., Bach, V. et al. Mast cells mediate Pseudomonas aeruginosa lipopolysaccharide-induced lung inflammation in rat. Eur J Clin Microbiol Infect Dis 31, 1983–1990 (2012). https://doi.org/10.1007/s10096-011-1530-5

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  • DOI: https://doi.org/10.1007/s10096-011-1530-5

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