The multiple mechanisms of Ca2+ signalling by listeriolysin O, the cholesterol-dependent cytolysin of Listeria monocytogenes

Cellular Microbiology

Volumn 9, Issue 8, 2007, Pages 2008-2021

  Gekara, Nelson O ^a   Westphal, Kathrin ^a   Ma, Bin ^a   Rohde, Manfred ^a   Groebe, Lothar ^a   Weiss, Siegfried ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CALCIUM CHANNEL; CALCIUM ION; CYTOLYSIN; GUANINE NUCLEOTIDE BINDING PROTEIN; LISTERIOLYSIN O; PHOSPHOLIPASE C; PROTEIN TYROSINE KINASE; CALCIUM; CHOLESTEROL; CYTOKINE; HEAT SHOCK PROTEIN; HEMOLYSIN; HLYA PROTEIN, LISTERIA MONOCYTOGENES; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACILLUS ANTHRACIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DAMAGE; CELL ORGANELLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOPLASMIC RETICULUM; GRAM POSITIVE BACTERIUM; LISTERIA MONOCYTOGENES; MAST CELL DEGRANULATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; STREPTOCOCCUS PYOGENES; ANIMAL; CELL LINE; CELL SURVIVAL; CHANNEL GATING; CYTOPLASM; INTRACELLULAR SPACE; MAST CELL; METABOLISM; MICROBIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RAT; SECRETION;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; POSIBACTERIA; STREPTOCOCCUS PYOGENES;

ANIMALS; BACTERIAL TOXINS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL LINE; CELL SURVIVAL; CHOLESTEROL; CYTOKINES; CYTOPLASM; ENDOPLASMIC RETICULUM; GTP-BINDING PROTEINS; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INTRACELLULAR SPACE; ION CHANNEL GATING; LISTERIA MONOCYTOGENES; MAST CELLS; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RATS; TYPE C PHOSPHOLIPASES;

EID: 34447619164     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00932.x     Document Type: Article

References (45)

1. de Bernard, M., Cappon, A., Pancotto, L., Ruggiero, P., Rivera, J., Del Giudice, G., and Montecucco, C. (2005) The Helicobacter pylori VacA cytotoxin activates RBL-2H3 cells by inducing cytosolic calcium oscillations. Cell Microbiol 7: 191-198.
2. Berridge, M.J., Bootman, M.D., and Roderick, H.L. (2003) Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4: 517-529.
3. Berry, A.M., Yother, J., Briles, D.E., Hansman, D., and Paton, J.C. (1989) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect Immun 57: 2037-2042.
4. Billington, S.J., Jost, B.H., and Songer, J.G., (2000) Thiol-activated cytolysins: Structure, function and role in pathogenesis. FEMS Microbiol Lett 182: 197-205.
5. Boulnois, G.J., Paton, J.C., Mitchell, T.J., and Andrew, P.W. (1991) Structure and function of pneumolysin, the multifunctional, thiol-activated toxin of Streptococcus pneumoniae. Mol Microbiol 5: 2611-2616.
6. Carrero, J.A., Calderon, B., and Unanue, E.R., (2004a) Listeriolysin O from Listeria monocytogenes is a lymphocyte apoptogenic molecule. J Immunol 172: 4866-4874.
7. Carrero, J.A., Calderon, B., and Unanue, E.R., (2004b) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med 200: 535-540.
8. Chakravortty, D., Rohde, M., Jager, L., Deiwick, J., and Hensel, M., (2005) Formation of a novel surface structure encoded by Salmonella Pathogenicity Island 2. EMBO J 24: 2043-2052.
9. Cybulsky, A.V., Salant, D.J., Quigg, R.J., Badalamenti, J., and Bonventre, J.V. (1989) Complement C5b-9 complex activates phospholipases in glomerular epithelial cells. Am J Physiol 257: F826-F836.
10. Cywes-Bentley, C., Hakansson, A., Christianson, J., and Wessels, M.R. (2005) Extracellular group A Streptococcus induces keratinocyte apoptosis by dysregulating calcium signalling. Cell Microbiol 7: 945-955.
11. Darji, A., Chakraborty, T., Wehland, J., and Weiss, S. (1995a) Listeriolysin generates a route for the presentation of exogenous antigens by major histocompatibility complex class I. Eur J Immunol 25: 2967-2971.
12. Darji, A., Chakraborty, T., Niebuhr, K., Tsonis, N., Wehland, J., and Weiss, S., (1995b) Hyperexpression of listeriolysin in the nonpathogenic species Listeria innocua and high yield purification. J Biotechnol 43: 205-212.
13. Dramsi, S., and Cossart, P. (2003) Listeriolysin O-mediated calcium influx potentiates entry of Listeria monocytogenes into the human Hep-2 epithelial cell line. Infect Immun 71: 3614-3618.
14. Edelson, B.T., Li, Z., Pappan, L.K., and Zutter, M.M. (2004) Mast cell-mediated inflammatory responses require the alpha 2 beta 1 integrin. Blood 103: 2214-2220.
15. Edelson, B.T., Stricker, T.P., Li, Z., Dickeson, S.K., Shepherd, V.L., Santoro, S.A., and Zutter, M.M. (2006) Novel collectin/C1q receptor mediates mast cell activation and innate immunity. Blood 107: 143-150.
16. Gaillard, J.L., Berche, P., and Sansonetti, P. (1986) Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun 52: 50-55.
17. Gekara, N.O., and Weiss, S. (2004) Lipid rafts clustering and signalling by listeriolysin O. Biochem Soc Trans 32: 712-714.
18. Gekara, N.O., Jacobs, T., Chakraborty, T., and Weiss, S. (2005) The cholesterol-dependent cytolysin listeriolysin O aggregates rafts via oligomerization. Cell Microbiol 7: 1345-1356.
19. Gordon, J.R., and Galli, S.J., (1991) Release of both preformed and newly synthesized tumor necrosis factor alpha (TNF-alpha)/cachectin by mouse mast cells stimulated via the Fc epsilon RI. A mechanism for the sustained action of mast cell-derived TNF-alpha during IgE-dependent biological responses. J Exp Med 174: 103-107.
20. Grimminger, F., Sibelius, U., Bhakdi, S., Suttorp, N., and Seeger, W. (1991) Escherichia coli hemolysin is a potent inductor of phosphoinositide hydrolysis and related metabolic responses in human neutrophils. J Clin Invest 88: 1531-1539.
21. Jacobs, T., Darji, A., Frahm, N., Rohde, M., Wehland, J., Chakraborty, T., and Weiss, S. (1998) Listeriolysin O: Cholesterol inhibits cytolysis but not binding to cellular membranes. Mol Microbiol 28: 1081-1089.
22. Kathariou, S., Metz, P., Hof, H., and Goebel, W. (1987) Tn916-induced mutations in the hemolysin determinant affecting virulence of Listeria monocytogenes. J Bacteriol 169: 1291-1297.
23. Kayal, S., Lilienbaum, A., Poyart, C., Memet, S., Israel, A., and Berche, P. (1999) Listeriolysin O-dependent activation of endothelial cells during infection with Listeria monocytogenes: Activation of NF-kappa B and upregulation of adhesion molecules and chemokines. Mol Microbiol 31: 1709-1722.
24. 2+ release from intracellular stores in human granulocytes. J Biol Chem 273: 18122-18129.
25. Lange, Y., Ye, J., Rigney, M., and Steck, T.L. (1999) Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J Lipid Res 40: 2264-2270.
26. McLachlan, J.B., Hart, J.P., Pizzo, S.V., Shelburne, C.P., Staats, H.F., Gunn, M.D., and Abraham, S.N. (2003) Mast cell-derived tumor necrosis factor induces hypertrophy of draining lymph nodes during infection. Nat Immunol 4: 1199-1205.
27. McNeil, P.L., and Kirchhausen, T. (2005) An emergency response team for membrane repair. Nat Rev Mol Cell Biol 6: 499-505.
28. McNeil, P.L., and Steinhardt, R.A. (2003) Plasma membrane disruption: repair, prevention, adaptation. Annu Rev Cell Dev Biol 19: 697-731.
29. Malaviya, R., Ikeda, T., Ross, E., and Abraham, S.N., (1996) Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 381: 77-80.
30. Marshall, J.S. (2004) Mast-cell responses to pathogens. Nat Rev Immunol 4: 787-799.
31. Palmer, M. (2001) The family of thiol-activated, cholesterol-binding cytolysins. Toxicon 39: 1681-1689.
32. Pasparakis, M., Alexopoulou, L., Episkopou, V., and Kollias, G. (1996) Immune and inflammatory responses in TNF alpha-deficient mice: A critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J Exp Med 184: 1397-1411.
33. Pfeffer, K., Matsuyama, T., Kundig, T.M., Wakeham, A., Kishihara, K., Shahinian, A., et al. (1993) Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73: 457-467.
34. Portnoy, D.A., Jacks, P.S., and Hinrichs, D.J., (1988) Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med 167: 1459-1471.
35. Razin, E., Ihle, J.N., Seldin, D., Mencia-Huerta, J.M., Katz, H.R., LeBlanc, P.A., et al. (1984) Interleukin 3: A differentiation and growth factor for the mouse mast cell that contains chondroitin sulfate E proteoglycan. J Immunol 132: 1479-1486.
36. 2+ oscillations. Cell Microbiol 4: 483-491.
37. Rivers, D.B., Crawley, T., and Bauser, H. (2005) Localization of intracellular calcium release in cells injured by venom from the ectoparasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) and dependence of calcium mobilization on G-protein activation. J Insect Physiol 51: 149-160.
38. Rothe, J., Lesslauer, W., Lotscher, H., Lang, Y., Koebel, P., Kontgen, F., et al. (1993) Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364: 798-802.
39. Shaughnessy, L.M., Hoppe, A.D., Christensen, K.A., and Swanson, J.A. (2006) Membrane perforations inhibit lysosome fusion by altering pH and calcium in Listeria monocytogenes vacuoles. Cell Microbiol 8: 781-792.
40. Sibelius, U., Chakraborty, T., Krogel, B., Wolf, J., Rose, F., Schmidt, R., et al. (1996) The listerial exotoxins listeriolysin and phosphatidylinositol-specific phospholipase C synergize to elicit endothelial cell phosphoinositide metabolism. J Immunol 157: 4055-4060.
41. Steinberg, T.H., Newman, A.S., Swanson, J.A., and Silverstein, S.C. (1987) Macrophages possess probenecid-inhibitable organic anion transporters that remove fluorescent dyes from the cytoplasmic matrix. J Cell Biol 105: 2695-2702.
42. Tran Van-Nhieu, G., Clair, C., Grompone, G., and Sansonetti, P. (2004) Calcium signalling during cell interactions with bacterial pathogens. Biol Cell 96: 93-101.
43. Van Epps, D.E., and Andersen, B.R. (1974) Streptolysin O inhibition of neutrophil chemotaxis and mobility: Nonimmune phenomenon with species specificity. Infect Immun 9: 27-33.
44. Wadsworth, S.J., and Goldfine, H. (1999) Listeria monocytogenes phospholipase C-dependent calcium signaling modulates bacterial entry into J774 macrophage-like cells. Infect Immun 67: 1770-1778.
45. Walev, I., Bhakdi, S.C., Hofmann, F., Djonder, N., Valeva, A., Aktories, K., and Bhakdi, S. (2001) Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O. Proc Natl Acad Sci USA 98: 3185-3190.