The NLRP3 Inflammasome Is a Pathogen Sensor for Invasive Entamoeba histolytica via Activation of α5β1 Integrin at the Macrophage-Amebae Intercellular Junction

PLoS Pathogens

Volumn 11, Issue 5, 2015, Pages

  Mortimer, Leanne ^a   Moreau, France ^a   Cornick, Steve ^a   Chadee, Kris ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CRYOPYRIN; CYSTEINE PROTEINASE; INFLAMMASOME; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MEMBRANE PROTEIN; PANNEXIN 1; PURINERGIC P2X7 RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; CARRIER PROTEIN; NLRP3 PROTEIN, HUMAN; NLRP3 PROTEIN, MOUSE; PROTOZOAL PROTEIN; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CELL STIMULATION; COLON BIOPSY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENTAMOEBA HISTOLYTICA; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; MACROPHAGE; MOUSE; NONHUMAN; AGONISTS; AMEBIASIS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL ADHESION; CELL CULTURE; CHEMISTRY; CYTOLOGY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; METABOLISM; MUTATION; PARASITOLOGY; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN TRANSPORT; RNA INTERFERENCE;

ENTAMOEBA HISTOLYTICA; PROTOZOA;

ANIMALS; CARRIER PROTEINS; CELL ADHESION; CELLS, CULTURED; CYSTEINE PROTEASES; ENTAMOEBA HISTOLYTICA; ENTAMOEBIASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; INTEGRIN ALPHA5BETA1; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; PROTEOLYSIS; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; RNA INTERFERENCE;

EID: 84930321889     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004887     Document Type: Article

References (46)

1. Stanley S.L., Ameobiasis. Lancet. 2003; 361: 1025–1034. 12660071
2. Mortimer L., Chadee K., The Immunopathogenesis of Entamoeba histolytica. Exp. Parasitol. 2010; 126: 366–380. doi: 10.1016/j.exppara.2010.03.005 20303955
3. Prathap K., Gilman R., The histopathology of acute intestinal amebiasis. A rectal biopsy study. Am. J. Pathol. 1970; 60: 229–246. 5457212
4. Chadee K., Meerovitch E., Entamoeba histolytica: early progressive pathology in the cecum of the gerbil (Meriones unguiculatus). Am. J. Trop. Med. Hyg. 1985; 34: 283–291. 2858986
5. Lin J.Y, Chadee K., Macrophage cytotoxicity against Entamoeba histolytica trophozoites is mediated by nitric oxide from L-arginine. J. Immunol. 1992; 148: 3999–4005. 1318338
6. Seguin R., Mann B., Keller K., Chadee K., Identification of the galactose-adherence lectin epitopes of Entamoeba histolytica that stimulate tumor necrosis factor-alpha production in macrophages. Proc. Natl. Acad. Sci. USA. 1995; 92: 12175–12179. 8618866
7. Underhill D.M., Goodrige H., Information processing during phagocytosis. Nat. Rev. Immunol. 2012; 12: 492–502. doi: 10.1038/nri3244 22699831
8. Mortimer L., Moreau F., Cornick S., Chadee K., Gal-lectin-dependent contact activates the inflammasome by invasive Entamoeba histolytica. Mucosal Immunol. 2014; 4: 829–841. doi: 10.1038/mi.2013.100 24253103
9. Latz E., Xiao S.T., Stutz A., Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 2013; 13: 397–411. doi: 10.1038/nri3452 23702978
10. Yamin T., Ayala J.M., Miller D.K., Activation of the native 45 kDa precursor form of interlekuin-1 converting enzyme. J. Biol. Chem. 1996: 271: 13273–13282. 8662843
11. Hornung V., Bauernfeind F., Halle A., Samstad E.O., Kono H., Rock K.L., et al. Silica crystals and aluminum salts mediate NALP-3 inflammasome activation via phagosomal destabilization. Nat. Immunol. 2008; 9: 847–856. doi: 10.1038/ni.1631 18604214
12. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-b. Nat. Immunol. 2008; 9: 857–865. doi: 10.1038/ni.1636 18604209
13. Duewell P., Kono H., Rayner K., Sirois C., Vladimer G., Bauernfeind F.G., et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 2010; 464: 1357–1361. doi: 10.1038/nature08938 20428172
14. Misawa T., Takahama M., Kozaki T., Lee H., Zou J., Saitoh T., et al. Microtubule-driven spatial arrangement of mitochondria promotes activation of the NLRP3 inflammasome. Nat. Immunol. 2013; 14: 454–460. doi: 10.1038/ni.2550 23502856
15. Hou Y., Mortimer L., Chadee K., Entamoeba histolytica cysteine proteinase 5 binds integrin on colonic cells and stimulates NFkappaB-mediated pro-inflammatory responses. J. Biol. Chem. 2010; 285: 35497–35504. doi: 10.1074/jbc.M109.066035 20837477
16. Kinashi T., Intracellular signaling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 2005; 5: 546–559. 15965491
17. Ruoslahti E., RGD and other recognition sequences for integrins. Annu. Rev. Cell. Dev. Biol. 1996; 12: 697–715 8970741
18. Bouvard D., Pouwels J., De Franceschi N., Ivaska J., Integrin inactivators: balancing cellular functions in vitro and in vivo. Nat. Rev. Mol. Cell. Bio. 2013; 14: 430–442. doi: 10.1038/nrm3599 23719537
19. Hirst R., Horwitz A., Bucko C., Rohrschneider L., Phosphorylation of the fibronectin receptor complex in cells transformed by oncogenes that encode tyrosine kinases. Proc. Nat. Acad. Sci. USA. 1986; 83: 6470–6474. 3018734
20. Kerur N., Veettil M.V., Sharma-Walia N., Sadagapan S., Bottero V., Paul A.G., et al. Characterization of entry and infection of monocytic THP-1 cells by Kaposi's sarcoma associated herpesvirus (KSHV): Role of heparan sulfate, DC-SIGN, integrins and signaling. Virology. 2010; 406: 103–116. doi: 10.1016/j.virol.2010.07.012 20674951
21. Chu C., Celik E., Rico F., Moy V.T., Elongated membrane tethers, individually anchored by high affinity alpha(4)beta(1)/VCAM-1 complexes, are the quantal units of monocyte arrests. PLoS One. 2013; 8: e64187. doi: 10.1371/journal.pone.0064187 23691169
22. Ashida N., Arai H., Yamasaki M., Kita T., Distinct signaling pathways for MCP-1-dependent integrin activation and chemotaxis. J. Biol. Chem. 2001; 276: 16555–16560. 11278464
23. Kim M., Jiang L.H., Wilson H.L., North R.A., Surprenant A., Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J. 2001; 20: 6347–6358. 11707406
24. Yegutkin G.G., Henttinen T., Samburski S.S., Spychala J., Jalkanen S., The evidence for two opposite, ATP-generating and ATP-consuming, extracellular pathways on endothelial and lymphoid cells. Biochem. J. 2002; 367: 121–128. 12099890
25. Lohman A.W., Isakson B.E., Differentiating connexin hemichannels and pannexin channels in cellular ATP release. FEBS Lett. 2014; 588: 1379–1388. doi: 10.1016/j.febslet.2014.02.004 24548565
26. Adamson S.E., Leitinger N., The role of pannexin1 in the induction and resolution of inflammation. FEBS Lett. 2014; 588: 1416–1422. doi: 10.1016/j.febslet.2014.03.009 24642372
27. Pelegrin P., Surprenant A., Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 2006; 25: 5071–5082. 17036048
28. Qu Y., Misaghi S., Newton K., Gilmour L.L., Louie S., Cupp J.E., et al. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J. Immunol. 2011; 186: 6553–6561. doi: 10.4049/jimmunol.1100478 21508259
29. Wang H., Xing Y., Mao L., Luo Y., Kang L., Meng G., Pannexin-1 influences peritoneal cavity cell population but is not involved in NLRP3 inflammasome activation. Protein Cell. 2013; 4: 259–265. doi: 10.1007/s13238-013-2114-1 23549611
30. Chekeni F., Elliot M.R., Sandilos J.K., Walk S.F., Kinchen J.M., Lazarowski E.R., et al. Pannexin 1 channelsmediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature. 2010; 467: 863–867. doi: 10.1038/nature09413 20944749
31. Huston C.D, Boettner D.R., Miller-Sims V., Petri W.A., Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica. Infect Imm. 2003; 71: 964–972. 12540579
32. Weilinger N.L, Tang P.L., Thompson R.J., Anoxia-induced NMDA receptor activation opens pannexin channels via Src family kinases. J. Neurosci. 2012; 36: 12579–12588. doi: 10.1523/JNEUROSCI.1267-12.2012 22956847
33. Iglesias R., Locovei S., Roque A., Alberto A.P., Dahl G., Spray D.C., et al. P2X7 receptor-Pannexin1 complex: pharmacology and signaling. Am. J. Physiol. Cell Physiol, 2008; 295: C752–C760. doi: 10.1152/ajpcell.00228.2008 18596211
34. Hellberg A., Nowak N., Leippe M., Tannich E., Bruchhaus I., Recombinant expression and purification of an enzymatically active cysteine proteinase of the protozoan parasite Entamoeba histolytica. Protein Expr. Purif. 2002; 24: 131–137. 11812234
35. Nowak N., Lotter H., Tannich E., Bruchhaus I., Resistance of Entamoeba histolytica to the cysteine proteinase inhibitor E64 is associated with secretion of pro-enzymes and reduced pathogenicity. J. Biol. Chem. 2004; 279: 38260–38266. 15215238
36. Kissoon-Singh V., Moreau F., Tusevych E., Chadee K., Entamoeba histolytica exacerbates epithelial tight junction permeability and proinflammatory responses in Muc2(-/-) mice. Am. J. Pathol. 2013; 182: 852–865. doi: 10.1016/j.ajpath.2012.11.035 23357502
37. Tillack M., Nowak N., Lotter H., Bracha R., Mirelman D., Tannich E., Bruchhaus I., Increased expression of the major cysteine proteinases by stable episomal transfection underlines the important role of EhCP5 for the pathogenicity of Entamoeba histolytica. Mol Biochem Parasitol 2006; 149: 58–64. 16753229
38. Ankri S., Stolarsky T., Bracha R., Padilla-Vaca F., Mirelman D., Antisense inhibition of expression of cysteine proteinases affects Entamoeba histolytica-induced formation of liver abscess in hamsters. Infect. Immun. 1999; 67: 421–422. 9864246
39. Zhang Z., Yan L., Wang L., Seydel K.B., Li E., Ankri S., Mirelman D., Stanley S.L., Entamoeba histolytica cysteine proteinases with interleukin-1 beta converting enzyme (ICE) activity cause intestinal inflammation and tissue damage in amoebiasis. Mol. Microbiol. 2000; 37: 542–548. 10931347
40. Dustin M.L., Groves J.T., Receptor signaling clusters at immune synapses. Annu. Rev. Biophys. 2012; 41: 543–556. doi: 10.1146/annurev-biophys-042910-155238 22404679
41. Goodridge H., Reyes C.N., Becker C.A., Katsumoto T.R., Ma J., Wolf A.J., et al. Activation of the innate immune receptor Dectin-1 upon formation of a ‘phagocytic synapse.’ Nature. 2011; 472: 471–475. doi: 10.1038/nature10071 21525931
42. Schenk U., Westendorf A.M., Radaelli E., Casati A., Ferro M., Fumagalli M., et al. Purinergic control of T cell activation by ATP released through Pannexin-1 Hemichannels. Sci. Signal. 2008; 1: 1–13. doi: 10.1126/stke.112pt1 18364512
43. Woehrle T., Yip L., Elkhal A., Sumi Y., Chen Y., Yao Y., et al. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood. 2010; 116: 3475–3484. doi: 10.1182/blood-2010-04-277707 20660288
44. Jun K., Lee S., Lee H., Choi B., Integrin a5b1 activates the NLRP3 inflammasome by direct interaction with a bacterial surface protein. Immunity. 2012: 36: 1–14. doi: 10.1016/j.immuni.2012.01.001 22284412
45. Diamond L.S., Harlow D.R., Cunnick C.C., A new medium for the axenic cultivation of Entamoeba histolytica. Trans. R. Soc. Trop. Med. Hyg. 1978; 72: 431–432. 212851
46. Denis M., Chadee K., Cytokine activation of murine macrophages for in vitro killing of Entamoeba histolytica trophozoites. Infect. Immun. 1989; 57: 1750–1756. 2542164