Porphyromonas gingivalis fimbriae dampen P2X7-dependent interleukin-1β secretion

Journal of Innate Immunity

Volumn 6, Issue 6, 2014, Pages 831-845

  Morandini, Ana Carolina ^a   Ramos Junior, Erivan S ^a   Potempa, Jan ^b,c   Nguyen, Ky Anh ^e   Oliveira, Ana Carolina ^a   Bellio, Maria ^a   Ojcius, David M ^d   Scharfstein, Julio ^a   Coutinho Silva, Robson ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c UNIVERSITY OF LOUISVILLE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Interleukin 1 ; Macrophages; P2X7 receptor; Porphyromonas gingivalis

Indexed keywords

INFLAMMASOME; INTERLEUKIN 1BETA; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHOLIPASE A2; PURINERGIC P2X7 RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; ADENOSINE TRIPHOSPHATE; IL1B PROTEIN, MOUSE; MYD88 PROTEIN, MOUSE; TLR2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BACTERIAL INFECTION; BONE MARROW DERIVED MACROPHAGE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; FIMBRIA; MOUSE; NONHUMAN; PORPHYROMONAS GINGIVALIS; PROTEIN EXPRESSION; ANIMAL; BACTEROIDACEAE INFECTION; DOWN REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; MICROBIOLOGY; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; BACTEROIDACEAE INFECTIONS; DOWN-REGULATION; FIMBRIAE, BACTERIAL; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; PORPHYROMONAS GINGIVALIS; RECEPTORS, PURINERGIC P2X7; TOLL-LIKE RECEPTOR 2;

EID: 84908620824     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000363338     Document Type: Article

References (54)

1. Said-Sadier N, Ojcius DM: Alarmins, inflam-masomes and immunity. Biomed J 2012; 35: 437-449.
2. Fantuzzi G, Dinarello CA: Interleukin-18 and interleukin-1 beta: two cytokine substrates for ice (caspase-1). J Clin Immunol 1999; 19:1-11.
3. Abdul-Sater AA, Said-Sadier N, Ojcius D.M., Yilmaz O., Kelly KA: Inflammasomes bridge signaling between pathogen identification and the immune response. Drugs Today (Barc) 2009; 45(suppl B):105-112.
4. Netea MG, Nold-Petry CA, Nold M.F., Joosten LA, Opitz B, van der Meer JH, van de Veer-donk FL, Ferwerda G, Heinhuis B, Devesa I, Funk CJ, Mason RJ, Kullberg BJ, Rubartelli A, van der Meer JW, Dinarello CA: Differential requirement for the activation of the inflam-masome for processing and release of IL-1be-ta in monocytes and macrophages. Blood 2009; 113:2324-2335.
5. Eder C: Mechanisms of interleukin-1beta release. Immunobiology 2009; 214:543-553.
6. Lamkanfi M, Dixit VM: Inflammasomes: guardians of cytosolic sanctity. Immunol Rev 2009; 227:95-105.
7. Martinon F, Burns K, Tschopp J: The inflam-masome: a molecular platform triggering activation of inflammatory caspases and processing of pro-IL1-beta. Mol Cell 2002; 10: 417-426.
8. Rathinam VA, Vanaja SK, Fitzgerald KA: Regulation of inflammasome signaling. Nat Immunol 2012; 13:333-342.
9. Taxman DJ, Huang MT, Ting JP: Inflamma-some inhibition as a pathogenic stealth mechanism. Cell Host Microbe 2010; 8:7-11.
10. Darveau RP, Hajishengallis G, Curtis MA: Porphyromonas gingivalis as a potential community activist for disease. J Dent Res 2012; 91:816-820.
11. Hajishengallis G, Wang M, Liang S., Triantaf-ilou M, Triantafilou K: Pathogen induction of CXCR4/TLR2 cross-talk impairs host defense function. Proc Natl Acad Sci USA 2008; 105: 13532-13537.
12. Guo Y, Nguyen KA, Potempa J: Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000 2010; 54:15-44.
13. Papadopoulos G, Weinberg EO, Massari P, Gibson FC 3rd, Wetzler LM, Morgan EF, Genco CA: Macrophage-specific TLR2 signaling mediates pathogen-induced TNF-de-pendent inflammatory oral bone loss. J Immunol 2013; 190:1148-1157.
14. Yilmaz O, Sater AA, Yao L, Koutouzis T., Pettengill M, Ojcius DM: ATP-dependent activation of an inflammasome in primary gingival epithelial cells infected by Porphyromonas gingivalis. Cell Microbiol 2010; 12: 188-198.
15. Persechini PM, Bisaggio RC, Alves-Neto JL, Coutinho-Silva R: Extracellular ATP in the lymphohematopoietic system: P2Z purino-ceptors off membrane permeabilization. Braz J Med Biol Res 1998; 31:25-34.
16. Coutinho-Silva R, Ojcius DM: Role of extracellular nucleotides in the immune response against intracellular bacteria and protozoan parasites. Microbes Infect 2012; 14:1271-1277.
17. Taxman DJ, Swanson KV, Broglie P.M., Wen H., Holley-Guthrie E, Huang MT, Callaway J.B., Eitas TK, Duncan JA, Ting JP: Porphy-romonas gingivalis mediates inflammasome repression in polymicrobial cultures through a novel mechanism involving reduced endo-cytosis. J Biol Chem 2012; 287:32791-32799.
18. Davis BK, Wen H, Ting JP: The inflamma-some NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol 2011; 29:707-735.
19. Oliveira AC, de Alencar BC, Tzelepis F, Klezewsky W, da Silva RN, Neves FS, Caval-canti GS, Boscardin S, Nunes MP, Santiago MF, Nobrega A, Rodrigues MM, Bellio M: Impaired innate immunity in Tlr4(-/-) mice but preserved CD8+ T cell responses against Trypanosoma cruzi in Tlr4-, Tlr2-, Tlr9- or MyD88-deficient mice. PLoS Pathog 2010; 6:e1000870.
20. Rapala-Kozik M, Bras G, Chruscicka B., Karkowska-Kuleta J, Sroka A, Herwald H., Nguyen KA, Eick S, Potempa J, Kozik A: Adsorption of components of the plasma kinin-forming system on the surface of Porphy-romonas gingivalis involves gingipains as the major docking platforms. Infect Immun 2011; 79:797-805.
21. Monteiro AC, Scovino A, Raposo S., Gaze VM, Cruz C, Svensjo E, Narciso M.S., Colombo AP, Pesquero JB, Feres-Filho E, Nguyen KA, Sroka A, Potempa J, Scharfstein J: Kinin danger signals proteolytically released by gingipain induce fimbriae-specific IFN-gamma- and IL-17-producing T cells in mice infected intramucosally with Porphyromonas gingivalis. J Immunol 2009; 183: 3700-3711.
22. Hamada N, Sojar HT, Cho M.I., Genco RJ: Isolation and characterization of a minor fimbria from Porphyromonas gingivalis. Infect Immun 1996; 64:4788-4794.
23. Marim FM, Silveira TN, Lima DS Jr, Zamboni DS: A method for generation of bone marrow-derived macrophages from cryopre-served mouse bone marrow cells. PLoS One 2010; 5:e15263.
24. Coutinho-Silva R, Perfettini JL, Persechini P.M., Dautry-Varsat A, Ojcius DM: Modulation of P2Z/P2X(7) receptor activity in macrophages infected with Chlamydia psittaci. Am J Physiol Cell Physiol 2001; 280:C81-C89.
25. Andrei C, Margiocco P, Poggi A., Lotti LV, Torrisi MR, Rubartelli A: Phospholipases C and A2 control lysosome-mediated IL-1 beta secretion: implications for inflammatory processes. Proc Natl Acad Sci USA 2004; 101: 9745-9750.
26. Di Virgilio F, Chiozzi P, Ferrari D., Falzoni S, Sanz JM, Morelli A, Torboli M., Bolognesi G, Baricordi OR: Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 2001; 97:587-600.
27. Franchi L, Chen G, Marina-Garcia N, Abe A., Qu Y, Bao S, Shayman J.A., Turk J., Dubyak GR, Nunez G: Calcium-independent phospholipase A2 beta is dispensable in inflammasome activation and its inhibition by bromoenol lactone. J Innate Immun 2009; 1: 607-617.
28. Coats SR, Jones JW, Do C.T., Braham PH, Bainbridge BW, To TT, Goodlett D.R., Ernst RK, Darveau RP: Human Toll-like receptor 4 responses to P. gingivalis are regulated by lip-id A 1- and 4'-phosphatase activities. Cell Microbiol 2009; 11:1587-1599.
29. Curtis MA, Percival RS, Devine D, Darveau R.P., Coats SR, Rangarajan M, Tarelli E, Marsh PD: Temperature-dependent modulation of Porphyromonas gingivalis lipid A structure and interaction with the innate host defenses. Infect Immun 2011; 79:1187-1193.
30. Jain S, Coats SR, Chang A.M., Darveau RP: A novel class of lipoprotein lipase-sensitive molecules mediates Toll-like receptor 2 activation by Porphyromonas gingivalis. Infect Immun 2013; 81:1277-1286.
31. Shimada K, Crother TR, Karlin J, Dagvadorj J., Chiba N, Chen S, Ramanujan V.K., Wolf AJ, Vergnes L, Ojcius DM, Rentsendorj A, Vargas M, Guerrero C, Wang Y, Fitzgerald KA, Underhill DM, Town T, Arditi M: Oxidized mi-tochondrial DNA activates the NLRP3 in-flammasome during apoptosis. Immunity 2012; 36:401-414.
32. Mao S, Park Y, Hasegawa Y., Tribble GD, James CE, Handfield M, Stavropoulos M.F., Yilmaz O., Lamont RJ: Intrinsic apoptotic pathways of gingival epithelial cells modulated by Porphyromonas gingivalis. Cell Micro-biol 2007; 9:1997-2007.
33. Yilmaz O, Jungas T, Verbeke P., Ojcius DM: Activation of the phosphatidylinositol 3-ki-nase/Akt pathway contributes to survival of primary epithelial cells infected with the peri-odontal pathogen P orphyromonas gingivalis. Infect Immun 2004; 72:3743-3751.
34. Yilmaz O, Verbeke P, Lamont R.J., Ojcius DM: Intercellular spreading of Porphyromonas gingivalis infection in primary gingival epithelial cells. Infect Immun 2006; 74:703-710.
35. Yilmaz O, Yao L, Maeda K., Rose TM, Lewis EL, Duman M, Lamont R.J., Ojcius DM: ATP scavenging by the intracellular pathogen Por-phyromonas gingivalis inhibits P2X7-mediat-ed host-cell apoptosis. Cell Microbiol 2008; 10:863-875.
36. Catlett-Falcone R, Landowski TH, Oshiro M.M., Turkson J., Levitzki A, Savino R, Cilib-erto G, Moscinski L., Fernandez-Luna JL, Nunez G, Dalton WS, Jove R: Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 1999; 10:105-115.
37. Atkinson L, Milligan CJ, Buckley N.J., Deuchars J: An ATP-gated ion channel at the cell nucleus. Nature 2002; 420:42.
38. Bardini M, Lee HY, Burnstock G: Distribution of P2X receptor subtypes in the rat female reproductive tract at late pro-oestrus/early oestrus. Cell Tissue Res 2000; 299:105-113.
39. Lee HY, Bardini M, Burnstock G: Distribution of P2X receptors in the urinary bladder and the ureter of the rat. J Urol 2000; 163: 2002-2007.
40. Antonio LS, Costa RR, Gomes M.D., Varanda WA: Mouse Leydig cells express multiple P2X receptor subunits. Purinergic Signal 2009; 5: 277-287.
41. Belibasakis GN, Guggenheim B, Bostanci N: Down-regulation of NLRP3 inflammasome in gingival fibroblasts by subgingival biofilms: involvement of Porphyromonas gingivalis. Innate Immun 2013; 19:3-9.
42. Bostanci N, Emingil G, Saygan B., Turkoglu O, Atilla G, Curtis M.A., Belibasakis GN: Expression and regulation of the NALP3 inflamma-some complex in periodontal diseases. Clin Exp Immunol 2009; 157:415-422.
43. Hajishengallis G, Martin M, Schifferle R.E., Genco RJ: Counteracting interactions between lipopolysaccharide molecules with differential activation of Toll-like receptors. Infect Immun 2002; 70:6658-6664.
44. Hamedi M, Belibasakis GN, Cruchley A.T., Rangarajan M., Curtis MA, Bostanci N: Por-phyromonas gingivalis culture supernatants differentially regulate interleukin-1beta and interleukin-18 in human monocytic cells. Cytokine 2009; 45:99-104.
45. Sugano N, Ikeda K, Oshikawa M., Sawamoto Y, Tanaka H, Ito K: Differential cytokine induction by two types of Porphyromonas gingi-valis. Oral Microbiol Immunol 2004; 19:121-123.
46. Park E, Na HS, Song Y.R., Shin SY, Kim YM, Chung J: Activation of NLRP3 and AIM2 in-flammasomes by Porphyromonas gingivalis infection. Infect Immun 2014; 82:112-123.
47. Coutinho-Silva R, Stahl L, Raymond M.N., Jungas T., Verbeke P, Burnstock G, Darville T., Ojcius DM: Inhibition of chlamydial infectious activity due to P2X7R-dependent phos-pholipase D activation. Immunity 2003; 19: 403-412.
48. Darville T, Welter-Stahl L, Cruz C., Sater AA, Andrews CW Jr, Ojcius DM: Effect of the pu-rinergic receptor P2X7 on Chlamydia infection in cervical epithelial cells and vaginally infected mice. J Immunol 2007; 179:3707-3714.
49. Choi CH, Spooner R, Deguzman J., Koutouzis T, Ojcius DM, Yilmaz O: Porphyromonas gin-givalis-nucleoside-diphosphate-kinase inhibits ATP-induced reactive-oxygen-species via P2X7 receptor/NADPH-oxidase signalling and contributes to persistence. Cell Microbiol 2013; 15:961-976.
50. Hajishengallis G, Darveau RP, Curtis MA: The keystone-pathogen hypothesis. Nat Rev Microbiol 2012; 10:717-725.
51. Hajishengallis G, McIntosh ML, Nishiyama S.I., Yoshimura F: Mechanism and implications of CXCR4-mediated integrin activation by Porphyromonas gingivalis. Mol Oral Microbiol 2013; 28:239-249.
52. Gaddis DE, Maynard CL, Weaver C.T., Michalek SM, Katz J: Role of TLR2-dependent IL-10 production in the inhibition of the initial IFN-gamma T cell response to Porphy-romonas gingivalis. J Leukoc Biol 2013; 93: 21-31.
53. Mu HH, Pennock ND, Humphreys J, Kirschning C.J., Cole BC: Engagement of Tolllike receptors by mycoplasmal superantigen: downregulation of TLR2 by MAM/TLR4 interaction. Cell Microbiol 2005; 7:789-797.
54. Mu HH, Hasebe A, Van Schelt A, Cole BC: Novel interactions of a microbial superantigen with TLR2 and TLR4 differentially regulate IL-17 and Th17-associated cytokines. Cell Microbiol 2011; 13:374-387.