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01-05-2009 | Original Investigation

Influence of Pseudomonas aeruginosa quorum sensing signal molecule N-(3-oxododecanoyl) homoserine lactone on mast cells

Authors: Hongtao Li, Lili Wang, Lu Ye, Yan Mao, Xuhua Xie, Chao Xia, Jia Chen, Zimin Lu, Jianxin Song

Published in: Medical Microbiology and Immunology | Issue 2/2009

Abstract

Quorum sensing system is a cell-to-cell communication system that plays a pivotal role in virulence expression in bacteria. Recent advances have demonstrated that the Pseudomonas aeruginosa quorum sensing molecule, N-3-oxododecanoyl homoserine lactone (3OC₁₂-HSL), exerts effects on mammalian cells and modulates host immune response. Mast cells (MCs) are strategically located in the tissues that are constantly exposed to external stimulus. Therefore, it is very much possible that 3OC₁₂-HSL may interact with MCs. Little is known, however, about specific effects of 3OC₁₂-HSL on MCs. To address this, we investigated the influence of 3OC₁₂-HSL on cell viability, apoptosis, intracellular calcium and cytokine release in MCs. We found that at high concentrations (100 μM), 3OC₁₂-HSL inhibited proliferation and induced apoptosis in P815. The 3OC₁₂-HSL treatment significantly increased intracellular calcium release in both P815 and HMC-1. We also observed that 3OC₁₂-HSL-induced histamine release and degranulation in HMC-1 cells. Furthermore, 3OC₁₂-HSL-induced IL-6 production at lower concentrations (6.25–12.5 μM) but steadily reduced IL-6 production at high concentration (50–100 μM). These data demonstrate that P. aeruginosa 3OC₁₂-HSL affects MCs function.

de Kievit TR, Iglewski BH (2000) Bacterial quorum sensing in pathogenic relationships. Infect Immun 68:4839–4849. doi:10.1128/IAI.68.9.4839-4849.2000 PubMedCrossRef

Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468. doi:10.1146/annurev.genet.35.102401.090913 PubMedCrossRef

Smith RS, Harris SG, Phipps R et al (2002) The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl) homoserine lactone contributes to virulence and induces inflammation in vivo. J Bacteriol 184:1132–1139. doi:10.1128/jb.184.4.1132-1139.2002 PubMedCrossRef

Davies DG, Parsek MR, Pearson JP et al (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298. doi:10.1126/science.280.5361.295 PubMedCrossRef

Hentzer M, Wu H, Andersen JB et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815. doi:10.1093/emboj/cdg366 PubMedCrossRef

Shiner EK, Rumbaugh KP, Williams SC (2005) Inter-kingdom signaling: deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 29:935–947. doi:10.1016/j.femsre.2005.03.001 PubMedCrossRef

Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111–120. doi:10.1038/nrmicro1836 PubMedCrossRef

Kravchenko VV, Kaufmann GF, Mathison JC et al (2008) Modulation of gene expression via disruption of NF-kappaB signaling by a bacterial small molecule. Science 321:259–263. doi:10.1126/science.1156499 PubMedCrossRef

Bradding P, Walls AF, Holgate ST (2006) The role of the mast cell in the pathophysiology of asthma. J Allergy Clin Immunol 117:1277–1284. doi:10.1016/j.jaci.2006.02.039 PubMedCrossRef

10.

Bischoff SC (2007) Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat Rev Immunol 7:93–104. doi:10.1038/nri2018 PubMedCrossRef

11.

Metz M, Maurer M (2007) Mast cells—key effector cells in immune responses. Trends Immunol 28:234–241. doi:10.1016/j.it.2007.03.003 PubMedCrossRef

12.

Siebenhaar F, Syska W, Weller K et al (2007) Control of Pseudomonas aeruginosa skin infections in mice is mast cell-dependent. Am J Pathol 170:1910–1916. doi:10.2353/ajpath.2007.060770 PubMedCrossRef

13.

Song Z, Johansen HK, Faber V et al (1997) Ginseng treatment reduces bacterial load and lung pathology in chronic Pseudomonas aeruginosa pneumonia in rats. Antimicrob Agents Chemother 41:961–964PubMed

14.

Henderson WR Jr, Chi EY (1992) Degranulation of cystic fibrosis nasal polyp mast cells. J Pathol 166:395–404. doi:10.1002/path.1711660412 PubMedCrossRef

15.

Wu H, Song Z, Givskov M et al (2001) Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology 147:1105–1113PubMed

16.

Metz M, Grimbaldeston MA, Nakae S et al (2007) Mast cells in the promotion and limitation of chronic inflammation. Immunol Rev 217:304–328. doi:10.1111/j.1600-065X.2007.00520.x PubMedCrossRef

17.

Erickson DL, Endersby R, Kirkham A et al (2002) Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect Immun 70:1783–1790. doi:10.1128/IAI.70.4.1783-1790.2002 PubMedCrossRef

18.

Singh PK, Schaefer AL, Parsek MR et al (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764. doi:10.1038/35037627 PubMedCrossRef

19.

Charlton TS, de Nys R, Netting A et al (2000) A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol 2:530–541. doi:10.1046/j.1462-2920.2000.00136.x PubMedCrossRef

20.

Rumbaugh KP (2007) Convergence of hormones and autoinducers at the host/pathogen interface. Anal Bioanal Chem 387:425–435. doi:10.1007/s00216-006-0694-9 PubMedCrossRef

21.

Chhabra SR, Harty C, Hooi DS et al (2003) Synthetic analogues of the bacterial signal (quorum sensing) molecule N-(3-oxododecanoyl)-l-homoserine lactone as immune modulators. J Med Chem 46:97–104. doi:10.1021/jm020909n PubMedCrossRef

22.

Chun CK, Ozer EA, Welsh MJ et al (2004) Inactivation of a Pseudomonas aeruginosa quorum-sensing signal by human airway epithelia. Proc Natl Acad Sci USA 101:3587–3590. doi:10.1073/pnas.0308750101 PubMedCrossRef

23.

Shiner EK, Terentyev D, Bryan A et al (2006) Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell Microbiol 8:1601–1610. doi:10.1111/j.1462-5822.2006.00734.x PubMedCrossRef

24.

Horikawa M, Tateda K, Tuzuki E et al (2006) Synthesis of Pseudomonas quorum-sensing autoinducer analogs and structural entities required for induction of apoptosis in macrophages. Bioorg Med Chem Lett 16:2130–2133. doi:10.1016/j.bmcl.2006.01.054 PubMedCrossRef

25.

Tateda K, Ishii Y, Horikawa M et al (2003) The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun 71:5785–5793. doi:10.1128/IAI.71.10.5785-5793.2003 PubMedCrossRef

26.

Li L, Hooi D, Chhabra SR et al (2004) Bacterial N-acylhomoserine lactone-induced apoptosis in breast carcinoma cells correlated with down-modulation of STAT3. Oncogene 23:4894–4902PubMedCrossRef

27.

Pearce FL (1985) Calcium and mast cell activation. Br J Clin Pharmacol 20(Suppl 2):267S–274SPubMed

28.

Giorgi C, Romagnoli A, Pinton P et al (2008) Ca²⁺ signaling, mitochondria and cell death. Curr Mol Med 8:119–130. doi:10.2174/156652408783769571 PubMedCrossRef

29.

Butterfield JH, Weiler D, Dewald G et al (1988) Establishment of an immature mast cell line from a patient with mast cell leukemia. Leuk Res 12:345–355. doi:10.1016/0145-2126(88)90050-1 PubMedCrossRef

30.

Brown JM, Wilson TM, Metcalfe DD (2008) The mast cell and allergic diseases: role in pathogenesis and implications for therapy. Clin Exp Allergy 38:4–18PubMed

31.

Cole N, Bao S, Stapleton F et al (2003) Pseudomonas aeruginosa keratitis in IL-6-deficient mice. Int Arch Allergy Immunol 130:165–172. doi:10.1159/000069006 PubMedCrossRef

32.

Sadikot RT, Blackwell TS, Christman JW et al (2005) Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 171:1209–1223. doi:10.1164/rccm.200408-1044SO PubMedCrossRef

33.

Koch C, Hoiby N (1993) Pathogenesis of cystic fibrosis. Lancet 341:1065–1069. doi:10.1016/0140-6736(93)92422-P PubMedCrossRef

34.

Malaviya R, Ikeda T, Ross E et al (1996) Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 381:77–80PubMedCrossRef

35.

Echtenacher B, Mannel DN, Hultner L (1996) Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381:75–77. doi:10.1038/381075a0 PubMedCrossRef

36.

Jenkins CE, Swiatoniowski A, Power MR et al (2006) Pseudomonas aeruginosa-induced human mast cell apoptosis is associated with up-regulation of endogenous Bcl-xS and down-regulation of Bcl-xL. J Immunol 177:8000–8007PubMed

37.

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. doi:10.1111/j.1365-2249.2005.02909.x PubMedCrossRef

38.

Lin TJ, Maher LH, Gomi K et al (2003) Selective early production of CCL20, or macrophage inflammatory protein 3alpha, by human mast cells in response to Pseudomonas aeruginosa. Infect Immun 71:365–373. doi:10.1128/IAI.71.1.365-373.2003 PubMedCrossRef

39.

Lin TJ, Garduno R, Boudreau RT et al (2002) Pseudomonas aeruginosa activates human mast cells to induce neutrophil transendothelial migration via mast cell-derived IL-1 alpha and beta. J Immunol 169:4522–4530PubMed

40.

Pearson JP, Feldman M, Iglewski BH et al (2000) Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect Immun 68:4331–4334. doi:10.1128/IAI.68.7.4331-4334.2000 PubMedCrossRef

41.

Telford G, Wheeler D, Williams P et al (1998) The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun 66:36–42PubMed

42.

Saleh A, Figarella C, Kammouni W et al (1999) Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-l-homoserine lactone inhibits expression of P2Y receptors in cystic fibrosis tracheal gland cells. Infect Immun 67:5076–5082PubMed

43.

Smith RS, Kelly R, Iglewski BH et al (2002) The Pseudomonas autoinducer N-(3-oxododecanoyl) homoserine lactone induces cyclooxygenase-2 and prostaglandin E2 production in human lung fibroblasts: implications for inflammation. J Immunol 169:2636–2642PubMed

44.

Ritchie AJ, Jansson A, Stallberg J et al (2005) The Pseudomonas aeruginosa quorum-sensing molecule N-3-(oxododecanoyl)-l-homoserine lactone inhibits T-cell differentiation and cytokine production by a mechanism involving an early step in T-cell activation. Infect Immun 73:1648–1655. doi:10.1128/IAI.73.3.1648-1655.2005 PubMedCrossRef

45.

Wagner C, Zimmermann S, Brenner-Weiss G et al (2006) The quorum-sensing molecule N-3-oxododecanoyl homoserine lactone (3OC12-HSL) enhances the host defence by activating human polymorphonuclear neutrophils (PMN) Anal Bioanal Chem

46.

Zimmermann S, Wagner C, Muller W et al (2006) Induction of neutrophil chemotaxis by the quorum-sensing molecule N-(3-oxododecanoyl)-l-homoserine lactone. Infect Immun 74:5687–5692. doi:10.1128/IAI.01940-05 PubMedCrossRef

47.

Wagner C, Zimmermann S, Brenner-Weiss G et al (2007) The quorum-sensing molecule N-3-oxododecanoyl homoserine lactone (3OC12-HSL) enhances the host defence by activating human polymorphonuclear neutrophils (PMN). Anal Bioanal Chem 387:481–487. doi:10.1007/s00216-006-0698-5 PubMedCrossRef

48.

Kravchenko VV, Kaufmann GF, Mathison JC et al (2006) N-(3-oxo-acyl) homoserine lactones signal cell activation through a mechanism distinct from the canonical pathogen-associated molecular pattern recognition receptor pathways. J Biol Chem 281:28822–28830. doi:10.1074/jbc.M606613200 PubMedCrossRef

49.

Hotchkiss RS, Dunne WM, Swanson PE et al (2001) Role of apoptosis in Pseudomonas aeruginosa pneumonia. Science 294:1783. doi:10.1126/science.294.5548.1783a PubMedCrossRef

50.

Lunderius C, Xiang Z, Nilsson G et al (2000) Murine mast cell lines as indicators of early events in mast cell and basophil development. Eur J Immunol 30:3396–3402. doi:10.1002/1521-4141(2000012)30:12<3396::AID-IMMU3396>3.0.CO;2-O PubMedCrossRef

51.

Ohtsu H, Kuramasu A, Suzuki S et al (1996) Histidine decarboxylase expression in mouse mast cell line P815 is induced by mouse peritoneal cavity incubation. J Biol Chem 271:28439–28444. doi:10.1074/jbc.271.45.28439 PubMedCrossRef

52.

Moser C, Jensen PO, Kobayashi O et al (2002) Improved outcome of chronic Pseudomonas aeruginosa lung infection is associated with induction of a Th1-dominated cytokine response. Clin Exp Immunol 127:206–213. doi:10.1046/j.1365-2249.2002.01731.x PubMedCrossRef

53.

Hooi DS, Bycroft BW, Chhabra SR et al (2004) Differential immune modulatory activity of Pseudomonas aeruginosa quorum-sensing signal molecules. Infect Immun 72:6463–6470. doi:10.1128/IAI.72.11.6463-6470.2004 PubMedCrossRef

Title: Influence of Pseudomonas aeruginosa quorum sensing signal molecule N-(3-oxododecanoyl) homoserine lactone on mast cells
Authors: Hongtao Li
Lili Wang
Lu Ye
Yan Mao
Xuhua Xie
Chao Xia
Jia Chen
Zimin Lu
Jianxin Song
Publication date: 01-05-2009
Publisher: Springer-Verlag
Published in: Medical Microbiology and Immunology / Issue 2/2009
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI: https://doi.org/10.1007/s00430-009-0111-z

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Influence of Pseudomonas aeruginosa quorum sensing signal molecule N-(3-oxododecanoyl) homoserine lactone on mast cells

Abstract

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