Infection of mast cells with live streptococci causes a toll-like receptor 2- and cell-cell contact-dependent cytokine and chemokine response

Infection and Immunity

Volumn 78, Issue 2, 2010, Pages 854-864

  Rönnberg, Elin ^a   Guss, Bengt ^a   Pejler, Gunnar ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHEMOKINE; CXCL2 CHEMOKINE; CYTOKINE; HISTAMINE; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PROTEINASE; RANTES; TOLL LIKE RECEPTOR 2; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ATTENUATION; BONE MARROW CELL; CELL CONTACT; CELL ULTRASTRUCTURE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HEAT; HISTAMINE RELEASE; MAST CELL; MAST CELL DEGRANULATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; ROUGH ENDOPLASMIC RETICULUM; STREPTOCOCCUS EQUI; STREPTOCOCCUS INFECTION; UPREGULATION;

ANIMALS; BONE MARROW CELLS; CELL COMMUNICATION; CELLS, CULTURED; CHEMOKINES; COCULTURE TECHNIQUES; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; MAST CELLS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS EQUI; TOLL-LIKE RECEPTOR 2;

EID: 76749127155     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01004-09     Document Type: Article

References (66)

1. Abbott, Y., E. Acke, S. Khan, E. Muldoon, B. Markey, M. Pinilla, F. Leonard, K. Steward, and A. S. Waller. 2009. Zoonotic transmission of Streptococcus equi subsp. zooepidemicus from a dog to a handler. J. Med. Microbiol. 59:120-123.
2. Abrink, M., M. Grujic, and G. Pejler. 2004. Serglycin is essential for maturation of mast cell secretory granule. J. Biol. Chem. 279:40897-40905.
3. Arock, M., E. Ross, R. Lai-Kuen, G. Averlant, Z. Gao, and S. N. Abraham. 1998. Phagocytic and tumor necrosis factor alpha response of human mast cells following exposure to gram-negative and gram-positive bacteria. Infect. Immun. 66:6030-6034.
4. Barbuti, G., M. Moschioni, S. Censini, A. Covacci, C. Montecucco, and P. Montemurro. 2006. Streptococcus pneumoniae induces mast cell degranulation. Int. J. Med. Microbiol. 296:325-329.
5. Barton, G. M., and J. C. Kagan. 2009. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. 9:535-542.
6. Billington, S. J., B. H. Jost, and J. G. Songer. 2000. Thiol-activated cytolysins: structure, function and role in pathogenesis. FEMS Microbiol. Lett. 182:197-205.
7. Boyce, J. A. 2007. Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol. Rev. 217:168-185.
8. Braga, T., M. Grujic, A. Lukinius, L. Hellman, M. Abrink, and G. Pejler. 2007. Serglycin proteoglycan is required for secretory granule integrity in mucosal mast cells. Biochem. J. 403:49-57.
9. Dawicki, W., and J. S. Marshall. 2007. New and emerging roles for mast cells in host defense. Curr. Opin. Immunol. 19:31-38.
10. Di Nardo, A., K. Yamasaki, R. A. Dorschner, Y. Lai, and R. L. Gallo. 2008. Mast cell cathelicidin antimicrobial peptide prevents invasive group A Streptococcus infection of the skin. J. Immunol. 180:7565-7573.
11. Echtenacher, B., D. N. Mannel, and L. Hultner. 1996. Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381:75-77.
12. Elson, G., I. Dunn-Siegrist, B. Daubeuf, and J. Pugin. 2007. Contribution of Toll-like receptors to the innate immune response to Gram-negative and Gram-positive bacteria. Blood 109:1574-1583.
13. Feger, F., S. Varadaradjalou, Z. Gao, S. N. Abraham, and M. Arock. 2002. The role of mast cells in host defense and their subversion by bacterial pathogens. Trends Immunol. 23:151-158.
14. Feng, B. S., S. H. He, P. Y. Zheng, L. Wu, and P. C. Yang. 2007. Mast cells play a crucial role in Staphylococcus aureus peptidoglycan-induced diarrhea. Am. J. Pathol. 171:537-547.
15. Flock, M., K. Jacobsson, L. Frykberg, T. R. Hirst, A. Franklin, B. Guss, and J. I. Flock. 2004. Recombinant Streptococcus equi proteins protect mice in challenge experiments and induce immune response in horses. Infect. Immun. 72:3228-3236.
16. Galli, S. J., S. Nakae, and M. Tsai. 2005. Mast cells in the development of adaptive immune responses. Nat. Immunol. 6:135-142.
17. Gekara, N. O., and S. Weiss. 2008. Mast cells initiate early anti-Listeria host defenses. Cell. Microbiol. 10:225-236.
18. Grimbaldeston, M. A., S. Nakae, J. Kalesnikoff, M. Tsai, and S. J. Galli. 2007. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat. Immunol. 8:1095-1104.
19. Guo, Y., P. A. Singleton, A. Rowshan, M. Gucek, R. N. Cole, D. R. Graham, J. E. Van Eyk, and J. G. Garcia. 2007. Quantitative proteomics analysis of human endothelial cell membrane rafts: evidence of MARCKS and MRP regulation in the sphingosine 1-phosphate-induced barrier enhancement. Mol. Cell Proteomics 6:689-696.
20. Hochberg, Y., and Y. Benjamini. 1990. More powerful procedures for multiple significance testing. Stat. Med. 9:811-818.
21. Ikeda, T., and M. Funaba. 2003. Altered function of murine mast cells in response to lipopolysaccharide and peptidoglycan. Immunol. Lett. 88:21-26.
22. Irizarry, R. A., B. Hobbs, F. Collin, Y. D. Beazer-Barclay, K. J. Antonellis, U. Scherf, and T. P. Speed. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
23. Jones, K. L., D. M. de Kretser, S. Patella, and D. J. Phillips. 2004. Activin A and follistatin in systemic inflammation. Mol. Cell. Endocrinol. 225:119-125.
24. Kulka, M., N. Fukuishi, M. Rottem, Y. A. Mekori, and D. D. Metcalfe. 2006. Mast cells, which interact with Escherichia coli, up-regulate genes associated with innate immunity and become less responsive to Fc(epsilon)RI-mediated activation. J. Leukoc. Biol. 79:339-350.
25. Lantz, C. S., J. Boesiger, C. H. Song, N. Mach, T. Kobayashi, R. C. Mulligan, Y. Nawa, G. Dranoff, and S. J. Galli. 1998. Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites. Nature 392:90-93.
26. Lee, D. M., D. S. Friend, M. F. Gurish, C. Benoist, D. Mathis, and M. B. Brenner. 2002. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 297:1689-1692.
27. Lindmark, H., and B. Guss. 1999. SFS, a novel fibronectin-binding protein from Streptococcus equi, inhibits the binding between fibronectin and collagen. Infect. Immun. 67:2383-2388.
28. Lindmark, H., M. Nilsson, and B. Guss. 2001. Comparison of the fibronectin-binding protein FNE from Streptococcus equi subspecies equi with FNZ from S. equi subspecies zooepidemicus reveals a major and conserved difference. Infect. Immun. 69:3159-3163.
29. Lu, L. F., E. F. Lind, D. C. Gondek, K. A. Bennett, M. W. Gleeson, K. Pino-Lagos, Z. A. Scott, A. J. Coyle, J. L. Reed, J. Van Snick, T. B. Strom, X. X. Zheng, and R. J. Noelle. 2006. Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442:997-1002.
30. Malaviya, R., T. Ikeda, E. Ross, and S. N. Abraham. 1996. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 381:77-80.
31. Malaviya, R., E. A. Ross, J. I. MacGregor, T. Ikeda, J. R. Little, B. A. Jakschik, and S. N. Abraham. 1994. Mast cell phagocytosis of FimH-expressing enterobacteria. J. Immunol. 152:1907-1914.
32. Malley, R., P. Henneke, S. C. Morse, M. J. Cieslewicz, M. Lipsitch, C. M. Thompson, E. Kurt-Jones, J. C. Paton, M. R. Wessels, and D. T. Golenbock. 2003. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc. Natl. Acad. Sci. U. S. A. 100:1966-1971.
33. Marshall, J. S. 2004. Mast-cell responses to pathogens. Nat. Rev. 4:787-799.
34. Maurer, M., B. Echtenacher, L. Hultner, G. Kollias, D. N. Mannel, K. E. Langley, and S. J. Galli. 1998. The c-kit ligand, stem cell factor, can enhance innate immunity through effects on mast cells. J. Exp. Med. 188:2343-2348.
35. Maurer, M., J. Wedemeyer, M. Metz, A. M. Piliponsky, K. Weller, D. Chatterjea, D. E. Clouthier, M. M. Yanagisawa, M. Tsai, and S. J. Galli. 2004. Mast cells promote homeostasis by limiting endothelin-1-induced toxicity. Nature 432:512-516.
36. McCurdy, J. D., T. J. Lin, and J. S. Marshall. 2001. Toll-like receptor 4-mediated activation of murine mast cells. J. Leukoc. Biol. 70:977-984.
37. Metcalfe, D. D., D. Baram, and Y. A. Mekori. 1997. Mast cells. Physiol. Rev. 77:1033-1079.
38. Mrabet-Dahbi, S., M. Metz, A. Dudeck, T. Zuberbier, and M. Maurer. 2009. Murine mast cells secrete a unique profile of cytokines and prostaglandins in response to distinct TLR2 ligands. Exp. Dermatol. 18:437-444.
39. Okumura, S., K. Yuki, R. Kobayashi, S. Okamura, K. Ohmori, H. Saito, C. Ra, and Y. Okayama. 2009. Hyperexpression of NOD2 in intestinal mast cells of Crohn's disease patients: preferential expression of inflammatory cell-recruiting molecules via NOD2 in mast cells. Clin. Immunol. 130:175-185.
40. Olivera, A., K. Mizugishi, A. Tikhonova, L. Ciaccia, S. Odom, R. L. Proia, and J. Rivera. 2007. The sphingosine kinase-sphingosine-1-phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26:287-297.
41. Oskeritzian, C. A., S. E. Alvarez, N. C. Hait, M. M. Price, S. Milstien, and S. Spiegel. 2008. Distinct roles of sphingosine kinases 1 and 2 in human mast-cell functions. Blood 111:4193-4200.
42. Park, J. M., V. H. Ng, S. Maeda, R. F. Rest, and M. Karin. 2004. Anthrolysin O and other gram-positive cytolysins are Toll-like receptor 4 agonists. J. Exp. Med. 200:1647-1655.
43. Park, S. K., H. Qiao, and M. A. Beaven. 2009. Src-like adaptor protein (SLAP) is upregulated in antigen-stimulated mast cells and acts as a negative regulator. Mol. Immunol. 46:2133-2139.
44. Pei, L., A. Castrillo, and P. Tontonoz. 2006. Regulation of macrophage inflammatory gene expression by the orphan nuclear receptor Nur77. Mol. Endocrinol. 20:786-794.
45. Pejler, G., M. Åbrink, M. Ringvall, and S. Wernersson. 2007. Mast cell proteases. Adv. Immunol. 95:167-255.
46. Qiao, H., M. V. Andrade, F. A. Lisboa, K. Morgan, and M. A. Beaven. 2006. FcepsilonR1 and Toll-like receptors mediate synergistic signals to markedly augment production of inflammatory cytokines in murine mast cells. Blood 107:610-618.
47. Razin, E., C. Cordon-Cardo, and R. A. Good. 1981. Growth of a pure population of mouse mast cells in vitro with conditioned medium derived from concanavalin A-stimulated splenocytes. Proc. Natl. Acad. Sci. U. S. A. 78:2559-2561.
48. Secor, V. H., W. E. Secor, C. A. Gutekunst, and M. A. Brown. 2000. Mast cells are essential for early onset and severe disease in a murine model of multiple sclerosis. J. Exp. Med. 191:813-822.
49. Sher, A., A. Hein, G. Moser, and J. P. Caulfield. 1979. Complement receptors promote the phagocytosis of bacteria by rat peritoneal mast cells. Lab. Invest. 41:490-499.
50. Siebenhaar, F., W. Syska, K. Weller, M. Magerl, T. Zuberbier, M. Metz, and M. Maurer. 2007. Control of Pseudomonas aeruginosa skin infections in mice is mast cell-dependent. Am. J. Pathol. 170:1910-1916.
51. Smyth, G. K. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:Article3.
52. Soucek, L., E. R. Lawlor, D. Soto, K. Shchors, L. B. Swigart, and G. I. Evan. 2007. Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat. Med. 13:1211-1218.
53. Sun, J., G. K. Sukhova, P. J. Wolters, M. Yang, S. Kitamoto, P. Libby, L. A. MacFarlane, J. Mallen-St Clair, and G. P. Shi. 2007. Mast cells promote atherosclerosis by releasing proinflammatory cytokines. Nat. Med. 13:719-724.
54. Sun, J., G. K. Sukhova, M. Yang, P. J. Wolters, L. A. MacFarlane, P. Libby, C. Sun, Y. Zhang, J. Liu, T. L. Ennis, R. Knispel, W. Xiong, R. W. Thompson, B. T. Baxter, and G. P. Shi. 2007. Mast cells modulate the pathogenesis of elastase-induced abdominal aortic aneurysms in mice. J. Clin. Invest. 117:3359-3368.
55. Supajatura, V., H. Ushio, A. Nakao, S. Akira, K. Okumura, C. Ra, and H. Ogawa. 2002. Differential responses of mast cell Toll-like receptors 2 and 4 in allergy and innate immunity. J. Clin. Invest. 109:1351-1359.
56. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21:335-376.
57. Tam, S. Y., M. Tsai, J. N. Snouwaert, J. Kalesnikoff, D. Scherrer, S. Nakae, D. Chatterjea, D. M. Bouley, and S. J. Galli. 2004. RabGEF1 is a negative regulator of mast cell activation and skin inflammation. Nat. Immunol. 5:844-852.
58. Thakurdas, S. M., E. Melicoff, L. Sansores-Garcia, D. C. Moreira, Y. Petrova, R. L. Stevens, and R. Adachi. 2007. The mast cell-restricted tryptase mMCP-6 has a critical immunoprotective role in bacterial infections. J. Biol. Chem. 82:20809-20815.
59. Timoney, J. F. 2004. The pathogenic equine streptococci. Vet. Res. 35:397-409.
60. Tsai, M., T. Takeishi, H. Thompson, K. E. Langley, K. M. Zsebo, D. D. Metcalfe, E. N. Geissler, and S. J. Galli. 1991. Induction of mast cell proliferation, maturation, and heparin synthesis by the rat c-kit ligand, stem cell factor. Proc. Natl. Acad. Sci. U. S. A. 88:6382-6386.
61. Varadaradjalou, S., F. Feger, N. Thieblemont, N. B. Hamouda, J. M. Pleau, M. Dy, and M. Arock. 2003. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human mast cells. Eur. J. Immunol. 33:899-906.
62. Wei, O. L., A. Hilliard, D. Kalman, and M. Sherman. 2005. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infect. Immun. 73:1978-1985.
63. Velin, D., D. Bachmann, H. Bouzourene, and P. Michetti. 2005. Mast cells are critical mediators of vaccine-induced Helicobacter clearance in the mouse model. Gastroenterology 129:142-155.
64. Wetzler, L. M. 2003. The role of Toll-like receptor 2 in microbial disease and immunity. Vaccine 21(Suppl. 2):S55-S60.
65. von Kockritz-Blickwede, M., O. Goldmann, P. Thulin, K. Heinemann, A. Norrby-Teglund, M. Rohde, and E. Medina. 2008. Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111:3070-3080.
66. Yang, Y. J., W. Chen, A. Edgar, B. Li, J. D. Molkentin, J. N. Berman, and T. J. Lin. 2009. Rcan1 negatively regulates FcεRI-mediated signaling and mast cell function. J. Exp. Med. 206:195-207.