A Shigella Effector Dampens Inflammation by Regulating Epithelial Release of Danger Signal ATP through Production of the Lipid Mediator PtdIns5P

Immunity

Volumn 39, Issue 6, 2013, Pages 1121-1131

  Puhar, Andrea ^a,b   Tronchère, Hélène ^c,d   Payrastre, Bernard ^c,d,e   Tran Van Nhieu, Guy ^f,g   Sansonetti, Philippe J ^a,b  

^a INSERM   (France)

^b INSTITUT PASTEUR   (France)

^c Université de Toulouse   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e TOULOUSE UNIVERSITY HOSPITAL   (France)

^f PSL RESEARCH UNIVERSITY   (France)

^g Centre de Recherche Interdisciplinaire en Biologie   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOKINE; GAMMA INTERFERON; GAP JUNCTION PROTEIN; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; INTERLEUKIN 8; LIPID; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENTEROPATHOGENIC ESCHERICHIA COLI; HELA CELL; HISTOLOGY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; RABBIT; SALMONELLA; SHIGELLA FLEXNERI; TYPE III SECRETION SYSTEM;

EID: 84890134936     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.11.013     Document Type: Article

References (51)

1. Abramoff M.D., Magelhaes P.J., Ram S.J. Image Processing with ImageJ. Biophotonics International 2004, 11:36-42.
2. Ali S.R., Timmer A.M., Bilgrami S., Park E.J., Eckmann L., Nizet V., Karin M. Anthrax toxin induces macrophage death by p38 MAPK inhibition but leads to inflammasome activation via ATP leakage. Immunity 2011, 35:34-44.
3. Allaoui A., Mounier J., Prévost M.C., Sansonetti P.J., Parsot C. icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread. Mol. Microbiol. 1992, 6:1605-1616.
4. Allaoui A., Ménard R., Sansonetti P.J., Parsot C. Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus. Infect. Immun. 1993, 61:1707-1714.
5. Allaoui A., Sansonetti P.J., Parsot C. MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri lpa invasins. Mol. Microbiol. 1993, 7:59-68.
6. Arondel J., Singer M., Matsukawa A., Zychlinsky A., Sansonetti P.J. Increased interleukin-1 (IL-1) and imbalance between IL-1 and IL-1 receptor antagonist during acute inflammation in experimental Shigellosis. Infect. Immun. 1999, 67:6056-6066.
7. H17 cell differentiation. Nature 2008, 455:808-812.
8. Bours M.J., Swennen E.L., Di Virgilio F., Cronstein B.N., Dagnelie P.C. Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 2006, 112:358-404.
9. Clair C., Combettes L., Pierre F., Sansonetti P., Tran Van Nhieu G. Extracellular-loop peptide antibodies reveal a predominant hemichannel organization of connexins in polarized intestinal cells. Exp. Cell Res. 2008, 314:1250-1265.
10. Clerc P., Sansonetti P.J. Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect. Immun. 1987, 55:2681-2688.
11. Coronas S., Ramel D., Pendaries C., Gaits-Iacovoni F., Tronchère H., Payrastre B. PtdIns5P: a little phosphoinositide with big functions?. Biochem. Soc. Symp. 2007, 74:117-128.
12. De Vuyst E., Decrock E., De Bock M., Yamasaki H., Naus C.C., Evans W.H., Leybaert L. Connexin hemichannels and gap junction channels are differentially influenced by lipopolysaccharide and basic fibroblast growth factor. Mol. Biol. Cell 2007, 18:34-46.
13. Dinarello C.A. Anti-inflammatory Agents: Present and Future. Cell 2010, 140:935-950.
14. Elfgang C., Eckert R., Lichtenberg-Fraté H., Butterweck A., Traub O., Klein R.A., Hülser D.F., Willecke K. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J.Cell Biol. 1995, 129:805-817.
15. Evans W.H., De Vuyst E., Leybaert L. The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem. J. 2006, 397:1-14.
16. Humphreys D., Hume P.J., Koronakis V. The Salmonella effector SptP dephosphorylates host AAA+ ATPase VCP to promote development of its intracellular replicative niche. Cell Host Microbe 2009, 5:225-233.
17. 12 receptor agonists are not chemoattractants and macrophage chemotaxis to complement C5a is phosphatidylinositol 3-kinase (PI3K)- and p38 mitogen-activated protein kinase (MAPK)-independent. J.Biol. Chem. 2011, 286:44776-44787.
18. Jun H.K., Lee S.H., Lee H.R., Choi B.K. Integrin α5β1 activates the NLRP3 inflammasome by direct interaction with a bacterial surface protein. Immunity 2012, 36:755-768.
19. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011, 34:637-650.
20. Keune Wj., Bultsma Y., Sommer L., Jones D., Divecha N. Phosphoinositide signalling in the nucleus. Adv. Enzyme Regul. 2011, 51:91-99.
21. Konradt C., Frigimelica E., Nothelfer K., Puhar A., Salgado-Pabon W., di Bartolo V., Scott-Algara D., Rodrigues C.D., Sansonetti P.J., Phalipon A. The Shigella flexneri type three secretion system effector IpgD inhibits Tcell migration by manipulating host phosphoinositide metabolism. Cell Host Microbe 2011, 9:263-272.
22. Madara J.L., Patapoff T.W., Gillece-Castro B., Colgan S.P., Parkos C.A., Delp C., Mrsny R.J. 5'-adenosine monophosphate is the neutrophil-derived paracrine factor that elicits chloride secretion from T84 intestinal epithelial cell monolayers. J.Clin. Invest. 1993, 91:2320-2325.
23. Marcus S.L., Wenk M.R., Steele-Mortimer O., Finlay B.B. A synaptojanin-homologous region of Salmonella typhimurium SigD is essential for inositol phosphatase activity and Akt activation. FEBS Lett. 2001, 494:201-207.
24. Mariathasan S., Weiss D.S., Newton K., McBride J., O'Rourke K., Roose-Girma M., Lee W.P., Weinrauch Y., Monack D.M., Dixit V.M. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006, 440:228-232.
25. Niebuhr K., Jouihri N., Allaoui A., Gounon P., Sansonetti P.J., Parsot C. IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation. Mol. Microbiol. 2000, 38:8-19.
26. 2 into PtdIns(5)P by the S.flexneri effector IpgD reorganizes host cell morphology. EMBO J. 2002, 21:5069-5078.
27. Norris F.A., Wilson M.P., Wallis T.S., Galyov E.E., Majerus P.W. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl. Acad. Sci. USA 1998, 95:14057-14059.
28. North R.A., Jarvis M.F. P2X receptors as drug targets. Mol. Pharmacol. 2013, 83:759-769.
29. Paemeleire K., Martin P.E., Coleman S.L., Fogarty K.E., Carrington W.A., Leybaert L., Tuft R.A., Evans W.H., Sanderson M.J. Intercellular calcium waves in HeLa cells expressing GFP-labeled connexin 43, 32, or 26. Mol. Biol. Cell 2000, 11:1815-1827.
30. Parsot C. Shigella type III secretion effectors: how, where, when, for what purposes?. Curr. Opin. Microbiol. 2009, 12:110-116.
31. Pendaries C., Tronchère H., Arbibe L., Mounier J., Gozani O., Cantley L., Fry M.J., Gaits-Iacovoni F., Sansonetti P.J., Payrastre B. PtdIns5P activates the host cell PI3-kinase/Akt pathway during Shigella flexneri infection. EMBO J. 2006, 25:1024-1034.
32. 4 receptors. Infect. Immun. 2012, 80:4232-4238.
33. Phalipon A., Sansonetti P.J. Shigella's ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival?. Immunol. Cell Biol. 2007, 85:119-129.
34. Phalipon A., Kaufmann M., Michetti P., Cavaillon J.M., Huerre M., Sansonetti P., Kraehenbuhl J.P. Monoclonal immunoglobulin A antibody directed against serotype-specific epitope of Shigella flexneri lipopolysaccharide protects against murine experimental shigellosis. J.Exp. Med. 1995, 182:769-778.
35. Ramel D., Lagarrigue F., Pons V., Mounier J., Dupuis-Coronas S., Chicanne G., Sansonetti P.J., Gaits-Iacovoni F., Tronchère H., Payrastre B. Shigella flexneri infection generates the lipid PI5P to alter endocytosis and prevent termination of EGFR signaling. Sci. Signal. 2011, 4:ra61.
36. Raucher D., Stauffer T., Chen W., Shen K., Guo S., York J.D., Sheetz M.P., Meyer T. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 2000, 100:221-228.
37. Retamal M.A., Schalper K.A., Shoji K.F., Bennett M.V., Sáez J.C. Opening of connexin 43 hemichannels is increased by lowering intracellular redox potential. Proc. Natl. Acad. Sci. USA 2007, 104:8322-8327.
38. Robertson J., Lang S., Lambert P.A., Martin P.E. Peptidoglycan derived from Staphylococcus epidermidis induces Connexin43 hemichannel activity with consequences on the innate immune response in endothelial cells. Biochem. J. 2010, 432:133-143.
39. Romero S., Grompone G., Carayol N., Mounier J., Guadagnini S., Prevost M.C., Sansonetti P.J., Van Nhieu G.T. ATP-mediated Erk1/2 activation stimulates bacterial capture by filopodia, which precedes Shigella invasion of epithelial cells. Cell Host Microbe 2011, 9:508-519.
40. Sansonetti P.J. To be or not to be a pathogen: that is the mucosally relevant question. Mucosal Immunol. 2011, 4:8-14.
41. Sansonetti P.J., Di Santo J.P. Debugging how bacteria manipulate the immune response. Immunity 2007, 26:149-161.
42. Sarkes D., Rameh L.E. A novel HPLC-based approach makes possible the spatial characterization of cellular PtdIns5P and other phosphoinositides. Biochem. J. 2010, 428:375-384.
43. Säve S., Persson K. Extracellular ATP and P2Y receptor activation induce a proinflammatory host response in the human urinary tract. Infect. Immun. 2010, 78:3609-3615.
44. Schnupf P., Sansonetti P.J. Quantitative RT-PCR profiling of the Rabbit Immune Response: Assessment of Acute Shigella flexneri Infection. PLoS One 2012, 7(6):e36446.
45. 17 cells are the dominant Tcell subtype primed by Shigella flexneri mediating protective immunity. J.Immunol. 2010, 184:2076-2085.
46. 2 purinergic receptors to facilitate HIV-1 infection. J.Exp. Med. 2011, 208:1823-1834.
47. Tran S.L., Guillemet E., Ngo-Camus M., Clybouw C., Puhar A., Moris A., Gohar M., Lereclus D., Ramarao N. Haemolysin II is a Bacillus cereus virulence factor that induces apoptosis of macrophages. Cell. Microbiol. 2011, 13:92-108.
48. Tran S.L., Puhar A., Ngo-Camus M., Ramarao N. Trypan blue dye enters viable cells incubated with the pore-forming toxin HlyII of Bacillus cereus. PLoS ONE 2011, 6:e22876.
49. Tran Van Nhieu G., Clair C., Bruzzone R., Mesnil M., Sansonetti P., Combettes L. Connexin-dependent inter-cellular communication increases invasion and dissemination of Shigella in epithelial cells. Nat. Cell Biol. 2003, 5:720-726.
50. Ungewickell A., Hugge C., Kisseleva M., Chang S.C., Zou J., Feng Y., Galyov E.E., Wilson M., Majerus P.W. The identification and characterization of two phosphatidylinositol-4,5-bisphosphate 4-phosphatases. Proc. Natl. Acad. Sci. USA 2005, 102:18854-18859.
51. Zhou D., Chen L.M., Hernandez L., Shears S.B., Galán J.E. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 2001, 39:248-259.