Ca2+-dependent repair of pneumolysin pores: A new paradigm for host cellular defense against bacterial pore-forming toxins

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 9, 2014, Pages 2045-2054

  Wolfmeier, Heidi ^a   Schoenauer, Roman ^a   Atanassoff, Alexander P ^a   Neill, Daniel R ^b   Kadioglu, Aras ^b   Draeger, Annette ^a   Babiychuk, Eduard B ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Annexin; Calcium; Non immune defense; Plasma membrane

Indexed keywords

CALCIUM; PNEUMOLYSIN; PROTEIN KINASE C ALPHA; BACTERIAL PROTEIN; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; STREPTOLYSIN;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL ACTIVATION; CELL DEATH; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CELL PERMEABILIZATION; CELL REGENERATION; CHANNEL GATING; CONTROLLED STUDY; CYTOLYSIS; CYTOPLASM; CYTOSOL; EMBRYO; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NUCLEAR PORE; PRIORITY JOURNAL; CHEMISTRY; HEK293 CELL LINE; METABOLISM; STREPTOCOCCUS PNEUMONIAE;

BACTERIAL PROTEINS; CALCIUM; CELL MEMBRANE; HEK293 CELLS; HUMANS; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS;

EID: 84952629946     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.09.005     Document Type: Article

References (34)

1. Hirst R.A., Kadioglu A., O'Callaghan C., Andrew P.W. The role of pneumolysin in pneumococcal pneumonia and meningitis. Clin. Exp. Immunol. 2004, 138:195-201.
2. Kadioglu A., Weiser J.N., Paton J.C., Andrew P.W. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 2008, 6:288-301.
3. Bergmann S., Hammerschmidt S. Versatility of pneumococcal surface proteins. Microbiology 2006, 152:295-303.
4. Marriott H.M., Mitchell T.J., Dockrell D.H. Pneumolysin: a double-edged sword during the host-pathogen interaction. Curr. Mol. Med. 2008, 8:497-509.
5. Aroian R., van der Goot F.G. Pore-forming toxins and cellular non-immune defenses (CNIDs). Curr. Opin. Microbiol. 2007, 10:57-61.
6. Cassidy S.K., O'Riordan M.X. More than a pore: the cellular response to cholesterol-dependent cytolysins. Toxins (Basel) 2013, 5:618-636.
7. Rogers P.D., Thornton J., Barker K.S., McDaniel D.O., Sacks G.S., Swiatlo E., McDaniel L.S. Pneumolysin-dependent and -independent gene expression identified by cDNA microarray analysis of THP-1 human mononuclear cells stimulated by Streptococcus pneumoniae. Infect. Immun. 2003, 71:2087-2094.
8. McNeela E.A., Burke A., Neill D.R., Baxter C., Fernandes V.E., Ferreira D., Smeaton S., El-Rachkidy R., McLoughlin R.M., Mori A., Moran B., Fitzgerald K.A., Tschopp J., Petrilli V., Andrew P.W., Kadioglu A., Lavelle E.C. Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4. PLoS Pathog. 2010, 6:e1001191.
9. Malley R., Henneke P., Morse S.C., Cieslewicz M.J., Lipsitch M., Thompson C.M., Kurt-Jones E., Paton J.C., Wessels M.R., Golenbock D.T. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:1966-1971.
10. 2+-dependent inflammatory responses in lung microvessels. PLoS ONE 2013, 8:e63465.
11. Tauseef M., Knezevic N., Chava K.R., Smith M., Sukriti S., Gianaris N., Obukhov A.G., Vogel S.M., Schraufnagel D.E., Dietrich A., Birnbaumer L., Malik A.B., Mehta D. TLR4 activation of TRPC6-dependent calcium signaling mediates endotoxin-induced lung vascular permeability and inflammation. J. Exp. Med. 2012, 209:1953-1968.
12. Racioppi L., Noeldner P.K., Lin F., Arvai S., Means A.R. Calcium/calmodulin-dependent protein kinase kinase 2 regulates macrophage-mediated inflammatory responses. J. Biol. Chem. 2012, 287:11579-11591.
13. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 2003, 4:517-529.
14. Atanassoff A.P., Wolfmeier H., Schoenauer R., Hostettler A., Ring A., Draeger A., Babiychuk E.B. Microvesicle shedding and lysosomal repair fulfill divergent cellular needs during the repair of streptolysin O-induced plasmalemmal damage. PLoS ONE 2014, 9:e89743.
15. 2+ sensitivities. J. Biol. Chem. 2011, 286:17982-17991.
16. Keyel P.A., Loultcheva L., Roth R., Salter R.D., Watkins S.C., Yokoyama W.M., Heuser J.E. Streptolysin O clearance through sequestration into blebs that bud passively from the plasma membrane. J. Cell Sci. 2011, 124:2414-2423.
17. Draeger A., Monastyrskaya K., Babiychuk E.B. Plasma membrane repair and cellular damage control: the annexin survival kit. Biochem. Pharmacol. 2011, 81:703-712.
18. Monastyrskaya K., Babiychuk E.B., Hostettler A., Rescher U., Draeger A. Annexins as intracellular calcium sensors. Cell Calcium 2007, 41:207-219.
19. Fulcher M.L., Gabriel S., Burns K.A., Yankaskas J.R., Randell S.H. Well-differentiated human airway epithelial cell cultures. Methods Mol. Med. 2005, 107:183-206.
20. 2+) operates a switch between repair and lysis of streptolysin O-perforated cells. Cell Death Differ. 2009, 16:1126-1134.
21. Lizarbe M.A., Barrasa J.I., Olmo N., Gavilanes F., Turnay J. Annexin-phospholipid interactions. Functional implications. Int. J. Mol. Sci. 2013, 14:2652-2683.
22. Gerke V., Moss S.E. Annexins: from structure to function. Physiol. Rev. 2002, 82:331-371.
23. Wippel C., Fortsch C., Hupp S., Maier E., Benz R., Ma J., Mitchell T.J., Iliev A.I. Extracellular calcium reduction strongly increases the lytic capacity of pneumolysin from Streptococcus pneumoniae in brain tissue. J. Infect. Dis. 2011, 204:930-936.
24. Rubins J.B., Mitchell T.J., Andrew P.W., Niewoehner D.E. Pneumolysin activates phospholipase A in pulmonary artery endothelial cells. Infect. Immun. 1994, 62:3829-3836.
25. Ratner A.J., Hippe K.R., Aguilar J.L., Bender M.H., Nelson A.L., Weiser J.N. Epithelial cells are sensitive detectors of bacterial pore-forming toxins. J. Biol. Chem. 2006, 281:12994-12998.
26. Kadioglu A., Coward W., Colston M.J., Hewitt C.R., Andrew P.W. CD4-T-lymphocyte interactions with pneumolysin and pneumococci suggest a crucial protective role in the host response to pneumococcal infection. Infect. Immun. 2004, 72:2689-2697.
27. Neill D.R., Coward W.R., Gritzfeld J.F., Richards L., Garcia-Garcia F.J., Dotor J., Gordon S.B., Kadioglu A. Density and duration of pneumococcal carriage is maintained by transforming growth factor beta1 and T regulatory cells. Am. J. Respir. Crit. Care Med. 2014, 189:1250-1259.
28. 2+-dependent endocytosis. J. Cell Biol. 2008, 180:905-914.
29. 2+ response amplitude and duration. Nature 1997, 386:855-858.
30. Smith M.F., Mitchell A., Li G., Ding S., Fitzmaurice A.M., Ryan K., Crowe S., Goldberg J.B. Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J. Biol. Chem. 2003, 278:32552-32560.
31. 2+-calmodulin-dependent protein kinase IV and protein phosphatase 2A. Science 1998, 280:1258-1261.
32. 2+-dependent mitogen-activated protein kinase signaling pathways in airway epithelial cells. J. Biol. Chem. 2001, 276:19267-19275.
33. Bouter A., Gounou C., Berat R., Tan S., Gallois B., Granier T., d'Estaintot B.L., Poschl E., Brachvogel B., Brisson A.R. Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat. Commun. 2011, 2.
34. Schoenauer R., Atanassoff A.P., Wolfmeier H., Pelegrin P., Babiychuk E.B., Draeger A. P2X7 receptors mediate resistance to toxin-induced cell lysis. Biochim. Biophys. Acta 2014, 1843:915-922.