P2X4 Assembles with P2X7 and Pannexin-1 in Gingival Epithelial Cells and Modulates ATP-induced Reactive Oxygen Species Production and Inflammasome Activation

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Hung, Shu Chen ^a   Choi, Chul Hee ^b   Said Sadier, Najwane ^a   Johnson, Larry ^a   Atanasova, Kalina Rosenova ^b   Sellami, Hanen ^a,c   Yilmaz, Özlem ^b   Ojcius, David M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c HABIB BOURGUIBA HOSPITAL   (Tunisia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MEMBRANE PROTEIN; PANNEXIN 1; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; GAP JUNCTION PROTEIN; NERVE PROTEIN; NLRP3 PROTEIN, HUMAN; PANX1 PROTEIN, HUMAN; SMALL INTERFERING RNA; PROTEIN BINDING;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; EPITHELIUM CELL; GINGIVA; HUMAN; HUMAN CELL; INHIBITION KINETICS; KERATINOCYTE; PORPHYROMONAS GINGIVALIS; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; BIOSYNTHESIS; CELL LINE; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PRIMARY CELL CULTURE; PROTEIN BINDING; SIGNAL TRANSDUCTION; AGONISTS; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS;

ADENOSINE TRIPHOSPHATE; CARRIER PROTEINS; CELL LINE; CONNEXINS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GINGIVA; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; KERATINOCYTES; NERVE TISSUE PROTEINS; PORPHYROMONAS GINGIVALIS; PRIMARY CELL CULTURE; PROTEIN BINDING; REACTIVE OXYGEN SPECIES; RECEPTORS, PURINERGIC P2X4; RECEPTORS, PURINERGIC P2X7; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84880825336     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070210     Document Type: Article

References (67)

1. Hornef MW, Bogdan C, (2005) The role of epithelial Toll-like receptor expression in host defense and microbial tolerance. Journal of endotoxin research 11: 124-128.
2. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, et al. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nature immunology 5: 1166-1174.
3. Chamaillard M, Inohara N, Nunez G, (2004) Battling enteroinvasive bacteria: Nod1 comes to the rescue. Trends in microbiology 12: 529-532.
4. Philpott DJ, Girardin SE, Sansonetti PJ, (2001) Innate immune responses of epithelial cells following infection with bacterial pathogens. Current opinion in immunology 13: 410-416.
5. Gerdes N, Sukhova GK, Libby P, Reynolds RS, Young JL, et al. (2002) Expression of interleukin (IL)-18 and functional IL-18 receptor on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for atherogenesis. The Journal of experimental medicine 195: 245-257.
6. Dinarello CA, (2005) Blocking IL-1 in systemic inflammation. The Journal of experimental medicine 201: 1355-1359.
7. Dinarello CA, (2006) Interleukin 1 and interleukin 18 as mediators of inflammation and the aging process. The American journal of clinical nutrition 83: 447S-455S.
8. Ishii KJ, Koyama S, Nakagawa A, Coban C, Akira S, (2008) Host innate immune receptors and beyond: making sense of microbial infections. Cell host & microbe 3: 352-363.
9. Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G, (2009) The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nature immunology 10: 241-247.
10. Zitvogel L, Kepp O, Galluzzi L, Kroemer G, (2012) Inflammasomes in carcinogenesis and anticancer immune responses. Nature immunology 13: 343-351.
11. Lich JD, Arthur JC, Ting JP, (2006) Cryopyrin: in from the cold. Immunity 24: 241-243.
12. Said-Sadier N, Ojcius DM, (2012) Alarmins, inflammasomes and immunity. Biomed J 35: 437-449.
13. Ciraci C, Janczy JR, Sutterwala FS, Cassel SL, (2012) Control of innate and adaptive immunity by the inflammasome. Microbes Infect 14: 1263-1270.
14. Martinon F, Burns K, Tschopp J, (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Molecular cell 10: 417-426.
15. Kanneganti TD, (2010) Central roles of NLRs and inflammasomes in viral infection. Nature reviews Immunology 10: 688-698.
16. Lupfer C, Kanneganti TD (2012) The role of inflammasome modulation in virulence. Virulence 3.
17. Broz P, Monack DM, (2011) Molecular mechanisms of inflammasome activation during microbial infections. Immunological reviews 243: 174-190.
18. Davis BK, Wen H, Ting JP, (2011) The inflammasome NLRs in immunity, inflammation, and associated diseases. Annual review of immunology 29: 707-735.
19. Schroder K, Tschopp J, (2010) The inflammasomes. Cell 140: 821-832.
20. Meylan E, Tschopp J, Karin M, (2006) Intracellular pattern recognition receptors in the host response. Nature 442: 39-44.
21. Kanneganti TD, Lamkanfi M, Kim YG, Chen G, Park JH, et al. (2007) Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 26: 433-443.
22. Locovei S, Scemes E, Qiu F, Spray DC, Dahl G, (2007) Pannexin1 is part of the pore forming unit of the P2×(7) receptor death complex. FEBS letters 581: 483-488.
23. Kahlenberg JM, Dubyak GR, (2004) Mechanisms of caspase-1 activation by P2×7 receptor-mediated K+ release. American journal of physiology Cell physiology 286: C1100-1108.
24. Shi Y, Mucsi AD, Ng G, (2010) Monosodium urate crystals in inflammation and immunity. Immunological reviews 233: 203-217.
25. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, et al. (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nature immunology 9: 857-865.
26. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, et al. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nature immunology 9: 847-856.
27. Cruz CM, Rinna A, Forman HJ, Ventura AL, Persechini PM, et al. (2007) ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. The Journal of biological chemistry 282: 2871-2879.
28. Arlehamn CS, Petrilli V, Gross O, Tschopp J, Evans TJ, (2010) The role of potassium in inflammasome activation by bacteria. The Journal of biological chemistry 285: 10508-10518.
29. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J, (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nature immunology 11: 136-140.
30. Zhou R, Yazdi AS, Menu P, Tschopp J, (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469: 221-225.
31. Bowler JW, Bailey RJ, North RA, Surprenant A, (2003) P2×4, P2Y1 and P2Y2 receptors on rat alveolar macrophages. British journal of pharmacology 140: 567-575.
32. Rayah A, Kanellopoulos JM, Di Virgilio F, (2012) P2 receptors and immunity. Microbes Infect 14: 1254-1262.
33. North RA, (2002) Molecular physiology of P2X receptors. Physiological reviews 82: 1013-1067.
34. Choi CH, Spooner R, Deguzman J, Koutouzis T, Ojcius DM, et al. (2012) Porphyromonas gingivalis-nucleoside-diphosphate-kinase inhibits ATP-induced reactive-oxygen-species via P2×(7) receptor/NADPH-oxidase signalling and contributes to persistence. Cellular microbiology in press.
35. Lamont RJ, Yilmaz O, (2002) In or out: the invasiveness of oral bacteria. Periodontology 2000 30: 61-69.
36. Nisapakultorn K, Ross KF, Herzberg MC, (2001) Calprotectin expression in vitro by oral epithelial cells confers resistance to infection by Porphyromonas gingivalis. Infection and immunity 69: 4242-4247.
37. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr, (1998) Microbial complexes in subgingival plaque. Journal of clinical periodontology 25: 134-144.
38. Christersson LA, Wikesjo UM, Albini B, Zambon JJ, Genco RJ, (1987) Tissue localization of Actinobacillus actinomycetemcomitans in human periodontitis. II. Correlation between immunofluorescence and culture techniques. Journal of periodontology 58: 540-545.
39. Yilmaz O, Sater AA, Yao L, Koutouzis T, Pettengill M, et al. (2010) ATP-dependent activation of an inflammasome in primary gingival epithelial cells infected by Porphyromonas gingivalis. Cellular microbiology 12: 188-198.
40. Oda D, Bigler L, Lee P, Blanton R, (1996) HPV immortalization of human oral epithelial cells: a model for carcinogenesis. Exp Cell Res 226: 164-169.
41. McMahon L, Schwartz K, Yilmaz O, Brown E, Ryan LK, et al. (2011) Vitamin D-mediated induction of innate immunity in gingival epithelial cells. Infection and immunity 79: 2250-2256.
42. Yilmaz O, Jungas T, Verbeke P, Ojcius DM, (2004) Activation of the phosphatidylinositol 3-kinase/Akt pathway contributes to survival of primary epithelial cells infected with the periodontal pathogen Porphyromonas gingivalis. Infection and immunity 72: 3743-3751.
43. Abdul-Sater AA, Said-Sadier N, Lam VM, Singh B, Pettengill MA, et al. (2010) Enhancement of reactive oxygen species production and chlamydial infection by the mitochondrial Nod-like family member NLRX1. The Journal of biological chemistry 285: 41637-41645.
44. Séror C, Melki MT, Subra F, Raza SQ, Bras M, et al. (2012) Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J Exp Med 208: 1823-1834.
45. Choi CH, Spooner R, Deguzman J, Koutouzis T, Ojcius DM, et al. (2012) Porphyromonas gingivalis-nucleoside-diphosphate-kinase inhibits ATP-induced reactive-oxygen-species via P2×(7) receptor/NADPH-oxidase signalling and contributes to persistence. Cellular Microbiology 15: 961-976.
46. Huang PR, Hung SC, Wang TC, (2010) Telomeric DNA-binding activities of heterogeneous nuclear ribonucleoprotein A3 in vitro and in vivo. Biochimica et biophysica acta 1803: 1164-1174.
47. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, et al. (2008) Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320: 674-677.
48. Desouki MM, Kulawiec M, Bansal S, Das GM, Singh KK, (2005) Cross talk between mitochondria and superoxide generating NADPH oxidase in breast and ovarian tumors. Cancer Biology & Therapy 4: 1367-1373.
49. Cassel SL, Eisenbarth SC, Iyer SS, Sadler JJ, Colegio OR, et al. (2008) The Nalp3 inflammasome is essential for the development of silicosis. Proc Natl Acad Sci USA 105: 9035-9040.
50. Silverman WR, de Rivero Vaccari JP, Locovei S, Qiu F, Carlsson SK, et al. (2009) The pannexin 1 channel activates the inflammasome in neurons and astrocytes. The Journal of biological chemistry 284: 18143-18151.
51. Yilmaz O, Yao L, Maeda K, Rose TM, Lewis EL, et al. (2008) ATP scavenging by the intracellular pathogen Porphyromonas gingivalis inhibits P2×7-mediated host-cell apoptosis. Cellular microbiology 10: 863-875.
52. Negulyaev YA, Markwardt F, (2000) Block by extracellular Mg2+ of single human purinergic P2×4 receptor channels expressed in human embryonic kidney cells. Neuroscience letters 279: 165-168.
53. Soto F, Garcia-Guzman M, Gomez-Hernandez JM, Hollmann M, Karschin C, et al. (1996) P2X4: an ATP-activated ionotropic receptor cloned from rat brain. Proceedings of the National Academy of Sciences of the United States of America 93: 3684-3688.
54. Guo C, Masin M, Qureshi OS, Murrell-Lagnado RD, (2007) Evidence for functional P2×4/P2×7 heteromeric receptors. Molecular pharmacology 72: 1447-1456.
55. Boumechache M, Masin M, Edwardson JM, Gorecki DC, Murrell-Lagnado R, (2009) Analysis of assembly and trafficking of native P2X4 and P2×7 receptor complexes in rodent immune cells. The Journal of biological chemistry 284: 13446-13454.
56. Kawano A, Tsukimoto M, Mori D, Noguchi T, Harada H, et al. (2012) Regulation of P2×7-dependent inflammatory functions by P2×4 receptor in mouse macrophages. Biochemical and biophysical research communications 420: 102-107.
57. Kawano A, Tsukimoto M, Noguchi T, Hotta N, Harada H, et al. (2012) Involvement of P2×4 receptor in P2×7 receptor-dependent cell death of mouse macrophages. Biochemical and biophysical research communications 419: 374-380.
58. Tassi S, Carta S, Vene R, Delfino L, Ciriolo MR, et al. (2009) Pathogen-induced interleukin-1beta processing and secretion is regulated by a biphasic redox response. J Immunol 183: 1456-1462.
59. Meissner F, Molawi K, Zychlinsky A, (2008) Superoxide dismutase 1 regulates caspase-1 and endotoxic shock. Nature Immunol 9: 866-872.
60. Carta S, Tassi S, Pettinati I, Delfino L, Dinarello CA, et al. (2011) The rate of interleukin-1beta secretion in different myeloid cells varies with the extent of redox response to Toll-like receptor triggering. J Biol Chem 286: 27069-27080.
61. Shimada K, Crother TR, Karlin J, Dagvadorj J, Chiba N, et al. (2012) Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 36: 401-414.
62. Shimada K, Crother TR, Arditi M, (2012) Innate immune responses to Chlamydia pneumoniae infection: role of TLRs, NLRs, and the inflammasome. Microbes Infect 14: 1301-1307.
63. Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, et al. (2011) Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 186: 6553-6561.
64. Wang H, Xing Y, Mao L, Luo Y, Kang L, et al. (2013) Pannexin-1 influences peritoneal cavity cell population but is not involved in NLRP3 inflammasome activation. Protein Cell.
65. Dvoriantchikova G, Ivanov D, Barakat D, Grinberg A, Wen R, et al. (2012) Genetic ablation of Pannexin1 protects retinal neurons from ischemic injury. PLoS ONE 7: e31991.
66. de Rivero Vaccari JP, Lotocki G, Marcillo AE, Dietrich WD, Keane RW, (2008) A molecular platform in neurons regulates inflammation after spinal cord injury. J Neurosci 28: 3404-3414.
67. Silverman WR, de Rivero Vaccari JP, Locovei S, Qiu F, Carlsson SK, et al. (2009) The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J Biol Chem 284: 18143-18151.