Selective activation of human intestinal mast cells by Escherichia coli hemolysin

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 1438-1445

  Krämer, Sigrid ^a   Sellge, Gernot ^b   Lorentz, Axel ^a   Krueger, Dagmar ^c   Schemann, Michael ^c   Feilhauer, Katharina ^d   Gunzer, Florian ^e   Bischoff, Stephan C ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b INSTITUT PASTEUR   (France)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d KATHARINENHOSPITAL   (Germany)

^e DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; CALCINEURIN; CALCIUM ION; CALMODULIN; CYCLOSPORIN A; HISTAMINE; LEUKOTRIENE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; AUTACOID; CALCIUM; CYTOKINE; ESCHERICHIA COLI PROTEIN; HEMOLYSIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ARTICLE; BACTERIAL STRAIN; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL INTERACTION; CELL ISOLATION; CELL SELECTION; CONTROLLED STUDY; ENZYME INHIBITION; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; EX VIVO STUDY; EXTRACELLULAR CALCIUM; HISTAMINE RELEASE; HUMAN; HUMAN CELL; INTESTINE CELL; LAMINA PROPRIA; MAST CELL; MUTANT; PRIORITY JOURNAL; PURIFICATION; SHIGELLA FLEXNERI; CELL CULTURE; CYTOLOGY; IMMUNOLOGY; INTESTINE MUCOSA; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY;

CALCIUM; CELLS, CULTURED; CYTOKINES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEMOLYSIN PROTEINS; HISTAMINE RELEASE; HUMANS; INFLAMMATION MEDIATORS; INTESTINAL MUCOSA; LEUKOTRIENES; LYMPHOCYTE ACTIVATION; MAST CELLS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES;

EID: 49049118311     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.1438     Document Type: Article

References (45)

1. Marshall, J. S. 2004. Mast-cell responses to pathogens. Nat. Rev. Immunol. 4: 787-799.
2. Bischoff, S. C. 2007. Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat. Rev. Immunol. 7: 93-104.
3. 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-α. Nature 381: 77-80. (Pubitemid 26130006)
4. Malaviya, R., and S. N. Abraham. 2000. Role of mast cell leukotrienes in neutrophil recruitment and bacterial clearance in infectious peritonitis. J. Leukocyte Biol. 67: 841-846. (Pubitemid 30677893)
5. 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. (Pubitemid 26130005)
6. McLachlan, J. B., J. P. Hart, S. V. Pizzo, C. P. Shelburne, H. F. Staats, M. D. Gunn, and S. N. Abraham. 2003. Mast cell-derived tumor necrosis factor induces hypertrophy of draining lymph nodes during infection. Nat. Immunol. 4: 1199-1205.
7. Galli, S. J., S. Nakae, and M. Tsai. 2005. Mast cells in the development of adaptive immune responses. Nat. Immunol. 6: 135-142. (Pubitemid 40268194)
8. Malaviya, R., Z. Gao, K. Thankavel, P. A. van der Merwe, and S. N. Abraham. 1999. The mast cell tumor necrosis factor α response to FimH-expressing Escherichia coli is mediated by the glycosylphosphatidylinositol-anchored molecule CD48. Proc. Natl. Acad. Sci. USA 96: 8110-8115. (Pubitemid 29328416)
9. Matsushima, H., N. Yamada, H. Matsue, and S. Shimada. 2004. TLR3-, TLR7-, and TLR9-mediated production of proinflammatory cytokines and chemokines from murine connective tissue type skin-derived mast cells but not from bone marrow-derived mast cells. J. Immunol. 173: 531-541. (Pubitemid 38797381)
10. McCurdy, J. D., T. J. Olynych, L. H. Maher, and J. S. Marshall. 2003. Cutting edge: distinct Toll-like receptor 2 activators selectively induce different classes of mediator production from human mast cells. J. Immunol. 170: 1625-1629.
11. Kulka, M., L. Alexopoulou, R. A. Flavell, and D. D. Metcalfe. 2004. Activation of mast cells by double-stranded RNA: evidence for activation through Toll-like receptor 3. J. Allergy Clin. Immunol. 114: 174-182. (Pubitemid 39005135)
12. 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. (Pubitemid 36546677)
13. Arock, M., E. Ross, R. Lai-Kuen, G. Averlant, Z. Gao, and S. N. Abraham. 1998. Phagocytic and tumor necrosis factor α response of human mast cells following exposure to Gram-negative and gram-positive bacteria. Infect. Immun. 66: 6030-6034. (Pubitemid 28531872)
14. Sansonetti, P. J. 2004. War and peace at mucosal surfaces. Nat. Rev. Immunol. 4: 953-964.
15. Malaviya, R., E. Ross, B. A. Jakschik, and S. N. Abraham. 1994. Mast cell degranulation induced by type 1 fimbriated Escherichia coli in mice. J. Clin. Invest. 93: 1645-1653. (Pubitemid 24116404)
16. Renesto, P., J. Mounier, and P. J. Sansonetti. 1996. Induction of adherence and degranulation of polymorphonuclear leukocytes: a new expression of the invasive phenotype of Shigella flexneri. Infect. Immun. 64: 719-723. (Pubitemid 26065539)
17. Chang, A. C., and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134: 1141-1156.
18. Gunzer, F., U. Bohn, S. Fuchs, I. Muhldorfer, J. Hacker, S. Tzipori, and A. Donohue-Rolfe. 1998. Construction and characterization of an isogenic slt-ii deletion mutant of enterohemorrhagic Escherichia coli. Infect. Immun. 66: 2337-2341. (Pubitemid 28194139)
19. Sellge, G., and S. C. Bischoff. 2006. Isolation, culture, and characterization of intestinal mast cells. Methods Mol. Biol. 315: 123-138.
20. Lorentz, A., S. Schwengberg, G. Sellge, M. P. Manns, and S. C. Bischoff. 2000. Human intestinal mast cells are capable of producing different cytokine profiles: role of IgE receptor cross-linking and IL-4. J. Immunol. 164: 43-48. (Pubitemid 30012970)
21. Barbara, G., V. Stanghellini, R. De Giorgio, C. Cremon, G. S. Cottrell, D. Santini, G. Pasquinelli, A. M. Morselli-Labate, E. F. Grady, N. W. Bunnett, et al. 2004. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126: 693-702. (Pubitemid 38298317)
22. Valeva, A., I. Walev, H. Kemmer, S. Weis, I. Siegel, F. Boukhallouk, T. M. Wassenaar, T. Chavakis, and S. Bhakdi. 2005. Binding of Escherichia coli hemolysin and activation of the target cells is not receptor-dependent. J. Biol. Chem. 280: 36657-36663. (Pubitemid 41587743)
23. Gilfillan, A. M., and C. Tkaczyk. 2006. Integrated signalling pathways for mastcell activation. Nat. Rev. Immunol. 6: 218-230.
24. Lorentz, A., M. Wilke, G. Sellge, H. Worthmann, J. Klempnauer, M. P. Manns, and S. C. Bischoff. 2005. IL-4-induced priming of human intestinal mast cells for enhanced survival and Th2 cytokine generation is reversible and associated with increased activity of ERK1/2 and c-fos. J. Immunol. 174: 6751-6756. (Pubitemid 40705637)
25. Lorentz, A., I. Klopp, T. Gebhardt, M. P. Manns, and S. C. Bischoff. 2003. Role of activator protein 1, nuclear factor-κB, and nuclear factor of activated T cells in IgE receptor-mediated cytokine expression in mature human mast cells. J. Allergy Clin. Immunol. 111: 1062-1068. (Pubitemid 36570867)
26. Giambartolomei, G. H., A. Zwerdling, J. Cassataro, L. Bruno, C. A. Fossati, and M. T. Philipp. 2004. Lipoproteins, not lipopolysaccharide, are the key mediators of the proinflammatory response elicited by heat-killed Brucella abortus. J. Immunol. 173: 4635-4642.
27. Cuschieri, J., J. Billgren, and R. V. Maier. 2006. Phosphatidylcholine- specific phospholipase C (PC-PLC) is required for LPS-mediated macrophage activation through CD14. J. Leukocyte Biol. 80: 407-414. (Pubitemid 44835514)
28. Aroian, R., and F. G. van der Goot. 2007. Pore-forming toxins and cellular nonimmune defenses (CNIDs). Curr. Opin. Microbiol. 10: 57-61. (Pubitemid 46216878)
29. May, A. K., T. G. Gleason, R. G. Sawyer, and T. L. Pruett. 2000. Contribution of Escherichia coli α-hemolysin to bacterial virulence and to intraperitoneal alterations in peritonitis. Infect. Immun. 68: 176-183.
30. Kaper, J. B., J. P. Nataro, and H. L. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140.
31. Schultsz, C., M. Moussa, R. van Ketel, G. N. Tytgat, and J. Dankert. 1997. Frequency of pathogenic and enteroadherent Escherichia coli in patients with inflammatory bowel disease and controls. J. Clin. Pathol. 50: 573-579. (Pubitemid 27359515)
32. Darfeuille-Michaud, A., C. Neut, N. Barnich, E. Lederman, P. Di Martino, P. Desreumaux, L. Gambiez, B. Joly, A. Cortot, and J. F. Colombel. 1998. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115: 1405-1413. (Pubitemid 28545991)
33. Friman, V., F. Nowrouzian, I. Adlerberth, and A. E. Wold. 2002. In creased frequency of intestinal Escherichia coli carrying genes for S. fimbriae and haemolysin in IgA-deficient individuals. Microb. Pathog. 32: 35-42. (Pubitemid 34112363)
34. Kleessen, B., A. J. Kroesen, H. J. Buhr, and M. Blaut. 2002. Mucosal and invading bacteria in patients with inflammatory bowel disease compared with controls. Scand. J. Gastroenterol. 37: 1034-1041.
35. Schultsz, C., F. M. Van Den Berg, F. W. Ten Kate, G. N. Tytgat, and J. Dankert. 1999. The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 117: 1089-1097. (Pubitemid 29512667)
36. Swidsinski, A., V. Loening-Baucke, F. Theissig, H. Engelhardt, S. Bengmark, S. Koch, H. Lochs, and Y. Dorffel. 2007. Comparative study of the intestinal mucus barrier in normal and inflamed colon. Gut 56: 343-350. (Pubitemid 46579762)
37. Rose, F., L. Kiss, F. Grimminger, K. Mayer, U. Grandel, W. Seeger, E. Bieniek, and U. Sibelius. 2000. E. coli hemolysin-induced lipid mediator metabolism in alveolar macrophages: impact of eicosapentaenoic acid. Am. J. Physiol. 279: L100-LL109. (Pubitemid 30619529)
38. Gross-Weege, W., W. Konig, J. Scheffer, and W. Nimmich. 1988. Induction of histamine release from rat mast cells and human basophilic granulocytes by clinical Escherichia coli isolates and relation to hemolysin production and adhesin expression. J. Clin. Microbiol. 26: 1831-1837. (Pubitemid 18208319)
39. Scheffer, J., W. Konig, J. Hacker, and W. Goebel. 1985. Bacterial adherence and hemolysin production from Escherichia coli induces histamine and leukotriene release from various cells. Infect. Immun. 50: 271-278. (Pubitemid 15239220)
40. Grimminger, F., F. Rose, U. Sibelius, M. Meinhardt, B. Potzsch, R. Spriestersbach, S. Bhakdi, N. Suttorp, and W. Seeger. 1997. Human endothelial cell activation and mediator release in response to the bacterial exotoxins Escherichia coli hemolysin and staphylococcal α-toxin. J. Immunol. 159: 1909-1916. (Pubitemid 127484180)
41. Grimminger, F., C. Scholz, S. Bhakdi, and W. Seeger. 1991. Subhemolytic doses of Escherichia coli hemolysin evoke large quantities of lipoxygenase products in human neutrophils. J. Biol. Chem. 266: 14262-14269. (Pubitemid 21907494)
42. 2+ oscillations in renal epithelial cells. Nature 405: 694-697.
43. Koschinski, A., H. Repp, B. Unver, F. Dreyer, D. Brockmeier, A. Valeva, S. Bhakdi, and I. Walev. 2006. Why Escherichia coli α-hemolysin induces calcium oscillations in mammalian cells: the pore is on its own. FASEB J. 20: 973-975. (Pubitemid 44943921)
44. Ratner, A. J., K. R. Hippe, J. L. Aguilar, M. H. Bender, A. L. Nelson, and J. N. Weiser. 2006. Epithelial cells are sensitive detectors of bacterial pore-forming toxins. J. Biol. Chem. 281: 12994-12998. (Pubitemid 43855393)
45. Stassen, M., C. Mueller, C. Richter, C. Neudoerfl, L. Hultner, S. Bhadki, I. Walev, and E. Schmitt. 2003. The streptococcal exotoxin streptolysin O activates mast cells to produce tumor necrosis factor α by p38 mitogen-activated protein kinase- and protein kinase C-dependent pathways. Infect. Immun. 71: 6171-6177. (Pubitemid 37337671)