Prophylactic systemic P2X7 receptor blockade prevents experimental colitis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 1, 2014, Pages 65-78

  Marques, Carla Caldas ^a   Castelo Branco, Morgana T ^a   Pacheco, Rodrigo G ^a   Buongusto, Fernanda ^a   do Rosário, Alyson ^a   Schanaider, Alberto ^a   Coutinho Silva, Robson ^a   De Souza, Heitor S P ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Apoptosis; Brilliant blue G; Innate immunity; P2X7 R; P2X7 R blockade; TNBS induced colitis

Indexed keywords

[N[1 [[(CYANOIMINO)(5 QUINOLINYLAMINO) METHYL]AMINO] 2,2 DIMETHYLPROPYL] 2 (3,4 DIMETHOXYPHENYL)ACETAMIDE]; A 740003; ANTIINFLAMMATORY AGENT; BRILLIANT BLUE; BRILLIANT BLUE G; COLLAGEN FIBER; GASTROINTESTINAL AGENT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MYELOPEROXIDASE; PURINERGIC P2X7 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL DENSITY; COLITIS; COLONOSCOPY; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE SEVERITY; DRUG EFFICACY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FOLLOW UP; GOBLET CELL; HISTOPATHOLOGY; LAMINA PROPRIA; MACROPHAGE; MALE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCORING SYSTEM; T LYMPHOCYTE; TRANSCRIPTION INITIATION; WEIGHT REDUCTION;

APOPTOSIS; BRILLIANT BLUE G; INNATE IMMUNITY; P2X7-R; P2X7-R BLOCKADE; TNBS-INDUCED COLITIS;

ANIMALS; ANTI-INFLAMMATORY AGENTS; APOPTOSIS; COLITIS; COLLAGEN; COLON; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; GOBLET CELLS; INJECTIONS, INTRAPERITONEAL; MACROPHAGES; MALE; NF-KAPPA B; PEROXIDASE; PURINERGIC P2X RECEPTOR ANTAGONISTS; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2X7; ROSANILINE DYES; T-LYMPHOCYTES; TRINITROBENZENESULFONIC ACID;

EID: 84887702141     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.10.012     Document Type: Article

References (83)

1. Podolsky D.K. Inflammatory bowel disease. N. Engl. J. Med. 2002, 347:417-429.
2. Baumgart D.C., Carding S.R. Inflammatory bowel disease: cause and immunobiology. Lancet 2007, 369:1627-1640.
3. Xavier R.J., Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434.
4. Cho J.H. The genetics and immunopathogenesis of inflammatory bowel disease. Nat. Rev. Immunol. 2008, 8:458-466.
5. Papadakis K.A., Targan S.R. The role of chemokines and chemokine receptors in mucosal inflammation. Inflamm. Bowel Dis. 2000, 6:303-313.
6. Neurath M.F., Weigmann B., Finotto S., Glickman J., Nieuwenhuis E., Iijima H., Mizoguchi A., Mizoguchi E., Mudter J., Galle P.R., Bhan A., Autschbach F., Sullivan B.M., Szabo S.J., Glimcher L.H., Blumberg R.S. The transcription factor T-bet regulates mucosal T cell activation in experimental colitis and Crohn's disease. J. Exp. Med. 2002, 195:1129-1143.
7. Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nunez G., Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307:731-734.
8. Atreya I., Atreya R., Neurath M.F. NF-kappaB in inflammatory bowel disease. J. Intern. Med. 2008, 263:591-596.
9. Rogler G., Brand K., Vogl D., Page S., Hofmeister R., Andus T., Knuechel R., Baeuerle P.A., Scholmerich J., Gross V. Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 1998, 115:357-369.
10. Schreiber S., Nikolaus S., Hampe J. Activation of nuclear factor kappa B inflammatory bowel disease. Gut 1998, 42:477-484.
11. Wehkamp J., Schmid M., Stange E.F. Defensins and other antimicrobial peptides in inflammatory bowel disease. Curr. Opin. Gastroenterol. 2007, 23:370-378.
12. Ogura Y., Bonen D.K., Inohara N., Nicolae D.L., Chen F.F., Ramos R., Britton H., Moran T., Karaliuskas R., Duerr R.H., Achkar J.P., Brant S.R., Bayless T.M., Kirschner B.S., Hanauer S.B., Nunez G., Cho J.H. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001, 411:603-606.
13. Hugot J.P., Chamaillard M., Zouali H., Lesage S., Cezard J.P., Belaiche J., Almer S., Tysk C., O'Morain C.A., Gassull M., Binder V., Finkel Y., Cortot A., Modigliani R., Laurent-Puig P., Gower-Rousseau C., Macry J., Colombel J.F., Sahbatou M., Thomas G. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001, 411:599-603.
14. Hampe J., Franke A., Rosenstiel P., Till A., Teuber M., Huse K., Albrecht M., Mayr G., De La Vega F.M., Briggs J., Gunther S., Prescott N.J., Onnie C.M., Hasler R., Sipos B., Folsch U.R., Lengauer T., Platzer M., Mathew C.G., Krawczak M., Schreiber S. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 2007, 39:207-211.
15. Parkes M., Barrett J.C., Prescott N.J., Tremelling M., Anderson C.A., Fisher S.A., Roberts R.G., Nimmo E.R., Cummings F.R., Soars D., Drummond H., Lees C.W., Khawaja S.A., Bagnall R., Burke D.A., Todhunter C.E., Ahmad T., Onnie C.M., McArdle W., Strachan D., Bethel G., Bryan C., Lewis C.M., Deloukas P., Forbes A., Sanderson J., Jewell D.P., Satsangi J., Mansfield J.C., Cardon L., Mathew C.G. Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility. Nat. Genet. 2007, 39:830-832.
16. Coutinho-Silva R., Monteiro da Cruz C., Persechini P.M., Ojcius D.M. The role of P2 receptors in controlling infections by intracellular pathogens. Purinergic Signal 2007, 3:83-90.
17. Ferrari D., Pizzirani C., Adinolfi E., Lemoli R.M., Curti A., Idzko M., Panther E., Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 2006, 176:3877-3883.
18. de Campos N.E., Marques-da-Silva C., Correa G., Castelo-Branco M.T., de Souza H.S., Coutinho-Silva R. Characterizing the presence and sensitivity of the P2X7 receptor in different compartments of the gut. J. Innate. Immun. 2012, 4(5-6):529-541. (Epub 2012 Apr 13). 10.1159/000336628.
19. Souza C.O., Santoro G.F., Figliuolo V.R., Nanini H.F., de Souza H.S., Castelo-Branco M.T., Abalo A.A., Paiva M.M., Coutinho C.M., Coutinho-Silva R. Extracellular ATP induces cell death in human intestinal epithelial cells. Biochim. Biophys. Acta 2012, 1820:1867-1878.
20. Lammas D.A., Stober C., Harvey C.J., Kendrick N., Panchalingam S., Kumararatne D.S. ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z (P2X7) receptors. Immunity 1997, 7:433-444.
21. Coutinho-Silva R., Stahl L., Raymond M.N., Jungas T., Verbeke P., Burnstock G., Darville T., Ojcius D.M. Inhibition of chlamydial infectious activity due to P2X7R-dependent phospholipase D activation. Immunity 2003, 19:403-412.
22. Fairbairn I.P., Stober C.B., Kumararatne D.S., Lammas D.A. ATP-mediated killing of intracellular mycobacteria by macrophages is a P2X(7)-dependent process inducing bacterial death by phagosome-lysosome fusion. J. Immunol. 2001, 167:3300-3307.
23. Di Virgilio F. Novel data point to a broader mechanism of action of oxidized ATP: the P2X7 receptor is not the only target. Br. J. Pharmacol. 2003, 140:441-443.
24. Crane J.K., Naeher T.M., Choudhari S.S., Giroux E.M. Two pathways for ATP release from host cells in enteropathogenic Escherichia coli infection. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G407-G417.
25. + regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: a role for P2X7 receptors. J. Immunol. 2005, 175:3075-3083.
26. Schenk U., Westendorf A.M., Radaelli E., Casati A., Ferro M., Fumagalli M., Verderio C., Buer J., Scanziani E., Grassi F. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 2008, 1:ra6.
27. Kawamura H., Aswad F., Minagawa M., Govindarajan S., Dennert G. P2X7 receptors regulate NKT cells in autoimmune hepatitis. J. Immunol. 2006, 176:2152-2160.
28. Chen Y.G., Scheuplein F., Driver J.P., Hewes A.A., Reifsnyder P.C., Leiter E.H., Serreze D.V. Testing the role of P2X7 receptors in the development of type 1 diabetes in nonobese diabetic mice. J. Immunol. 2006, 186:4278-4284.
29. 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.
30. Pelegrin P., Surprenant A. Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J. 2006, 25:5071-5082.
31. Villani A.C., Lemire M., Fortin G., Louis E., Silverberg M.S., Collette C., Baba N., Libioulle C., Belaiche J., Bitton A., Gaudet D., Cohen A., Langelier D., Fortin P.R., Wither J.E., Sarfati M., Rutgeerts P., Rioux J.D., Vermeire S., Hudson T.J., Franchimont D. Common variants in the NLRP3 region contribute to Crohn's disease susceptibility. Nat. Genet. 2009, 41:71-76.
32. Schoultz I., Verma D., Halfvarsson J., Torkvist L., Fredrikson M., Sjoqvist U., Lordal M., Tysk C., Lerm M., Soderkvist P., Soderholm J.D. Combined polymorphisms in genes encoding the inflammasome components NALP3 and CARD8 confer susceptibility to Crohn's disease in Swedish men. Am. J. Gastroenterol. 2009, 104:1180-1188.
33. Welter-Stahl L., da Silva C.M., Schachter J., Persechini P.M., Souza H.S., Ojcius D.M., Coutinho-Silva R. Expression of purinergic receptors and modulation of P2X7 function by the inflammatory cytokine IFNgamma in human epithelial cells. Biochim. Biophys. Acta 2009, 1788:1176-1187.
34. Belmiro C.L., Castelo-Branco M.T., Melim L.M., Schanaider A., Elia C., Madi K., Pavao M.S., de Souza H.S. Unfractionated heparin and new heparin analogues from ascidians (chordate-tunicate) ameliorate colitis in rats. J. Biol. Chem. 2009, 284:11267-11278.
35. Honore P., Donnelly-Roberts D., Namovic M.T., Hsieh G., Zhu C.Z., Mikusa J.P., Hernandez G., Zhong C., Gauvin D.M., Chandran P., Harris R., Medrano A.P., Carroll W., Marsh K., Sullivan J.P., Faltynek C.R., Jarvis M.F. A-740003 [N-(1-{[(cyanoimino)(5-quinolinylamino) methyl] amino}-2,2-dimethylpropyl)-2-(3,4-dimethoxyphenyl) acetamide], a novel and selective P2X7 receptor antagonist, dose-dependently reduces neuropathic pain in the rat. J. Pharmacol. Exp. Ther. 2006, 319:1376-1385.
36. Diaz-Hernandez M., Diez-Zaera M., Sanchez-Nogueiro J., Gomez-Villafuertes R., Canals J.M., Alberch J., Miras-Portugal M.T., Lucas J.J. Altered P2X7-receptor level and function in mouse models of Huntington's disease and therapeutic efficacy of antagonist administration. FASEB J. 2009, 23:1893-1906.
37. Lienenluke B., Stojanovic T., Fiebig T., Fayyazi A., Germann T., Hecker M. Thalidomide impairment of trinitrobenzene sulphonic acid-induced colitis in the rat - role of endothelial cell-leukocyte interaction. Br. J. Pharmacol. 2001, 133:1414-1423.
38. Becker C., Fantini M.C., Neurath M.F. High resolution colonoscopy in live mice. Nat. Protoc. 2006, 1:2900-2904.
39. Hahm K.B., Im Y.H., Parks T.W., Park S.H., Markowitz S., Jung H.Y., Green J., Kim S.J. Loss of transforming growth factor beta signalling in the intestine contributes to tissue injury in inflammatory bowel disease. Gut 2001, 49:190-198.
40. Dolber P.C., Spach M.S. Conventional and confocal fluorescence microscopy of collagen fibers in the heart. J. Histochem. Cytochem. 1993, 41:465-469.
41. Baumgart D.C., Sandborn W.J. Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet 2007, 369:1641-1657.
42. Sohrabpour A.A., Malekzadeh R., Keshavarzian A. Current therapeutic approaches in inflammatory bowel disease. Curr. Pharm. Des. 2010, 16:3668-3683.
43. Lakatos P.L., Kiss L.S. Current status of thiopurine analogues in the treatment in Crohn's disease. World J. Gastroenterol. 2011, 17:4372-4381.
44. Burger D., Travis S. Conventional medical management of inflammatory bowel disease. Gastroenterology 2011, 140:1827-1837. (e1822).
45. Vermeire S., van Assche G., Rutgeerts P. Review article: altering the natural history of Crohn's disease-evidence for and against current therapies. Aliment. Pharmacol. Ther. 2007, 25:3-12.
46. Billioud V., Sandborn W.J., Peyrin-Biroulet L. Loss of response and need for adalimumab dose intensification in Crohn's disease: a systematic review. Am. J. Gastroenterol. 2011, 106:674-684.
47. Kurashima Y., Amiya T., Nochi T., Fujisawa K., Haraguchi T., Iba H., Tsutsui H., Sato S., Nakajima S., Iijima H., Kubo M., Kunisawa J., Kiyono H. Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat. Commun. 2012, 3:1034.
48. Groschel-Stewart U., Bardini M., Robson T., Burnstock G. P2X receptors in the rat duodenal villus. Cell Tissue Res. 1999, 297:111-117.
49. Cesaro A., Brest P., Hofman V., Hebuterne X., Wildman S., Ferrua B., Marchetti S., Doglio A., Vouret-Craviari V., Galland F., Naquet P., Mograbi B., Unwin R., Hofman P. Amplification loop of the inflammatory process is induced by P2X7R activation in intestinal epithelial cells in response to neutrophil transepithelial migration. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G32-G42.
50. Strober W., Fuss I.J., Blumberg R.S. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 2002, 20:495-549.
51. Gourine A.V., Poputnikov D.M., Zhernosek N., Melenchuk E.V., Gerstberger R., Spyer K.M., Gourine V.N. P2 receptor blockade attenuates fever and cytokine responses induced by lipopolysaccharide in rats. Br. J. Pharmacol. 2005, 146:139-145.
52. Jiang L.H., Mackenzie A.B., North R.A., Surprenant A. Brilliant blue G selectively blocks ATP-gated rat P2X(7) receptors. Mol. Pharmacol. 2000, 58:82-88.
53. Kimbler D.E., Shields J., Yanasak N., Vender J.R., Dhandapani K.M. Activation of P2X7 promotes cerebral edema and neurological injury after traumatic brain injury in mice. PLoS One 2012, 7:e41229.
54. Michel A.D., Chambers L.J., Clay W.C., Condreay J.P., Walter D.S., Chessell I.P. Direct labelling of the human P2X7 receptor and identification of positive and negative cooperativity of binding. Br. J. Pharmacol. 2007, 151:103-114.
55. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 2007, 87:659-797.
56. Gulbransen B.D., Bashashati M., Hirota S.A., Gui X., Roberts J.A., MacDonald J.A., Muruve D.A., McKay D.M., Beck P.L., Mawe G.M., Thompson R.J., Sharkey K.A. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat. Med. 2012, 18:600-604.
57. Qiu F., Dahl G. A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP. Am. J. Physiol. Cell Physiol. 2009, 296:C250-C255.
58. Nelson D.W., Gregg R.J., Kort M.E., Perez-Medrano A., Voight E.A., Wang Y., Grayson G., Namovic M.T., Donnelly-Roberts D.L., Niforatos W., Honore P., Jarvis M.F., Faltynek C.R., Carroll W.A. Structure-activity relationship studies on a series of novel, substituted 1-benzyl-5-phenyltetrazole P2X7 antagonists. J. Med. Chem. 2006, 49:3659-3666.
59. Donnelly-Roberts D.L., Jarvis M.F. Discovery of P2X7 receptor-selective antagonists offers new insights into P2X7 receptor function and indicates a role in chronic pain states. Br. J. Pharmacol. 2007, 151:571-579.
60. Neurath M.F., Pettersson S., Meyer zum Buschenfelde K.H., Strober W. Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat. Med. 1996, 2:998-1004.
61. Bouma G., Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 2003, 3:521-533.
62. Nau G.J., Richmond J.F., Schlesinger A., Jennings E.G., Lander E.S., Young R.A. Human macrophage activation programs induced by bacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1503-1508.
63. Cosnes J., Cattan S., Blain A., Beaugerie L., Carbonnel F., Parc R., Gendre J.P. Long-term evolution of disease behavior of Crohn's disease. Inflamm. Bowel Dis. 2002, 8:244-250.
64. Burke J.P., Mulsow J.J., O'Keane C., Docherty N.G., Watson R.W., O'Connell P.R. Fibrogenesis in Crohn's disease. Am. J. Gastroenterol. 2007, 102:439-448.
65. Beddy D.J., Watson W.R., Fitzpatrick J.M., O'Connell P.R. Critical involvement of stress-activated mitogen-activated protein kinases in the regulation of intracellular adhesion molecule-1 in serosal fibroblasts isolated from patients with Crohn's disease. J. Am. Coll. Surg. 2004, 199:234-242.
66. Theiss A.L., Simmons J.G., Jobin C., Lund P.K. Tumor necrosis factor (TNF) alpha increases collagen accumulation and proliferation in intestinal myofibroblasts via TNF receptor 2. J. Biol. Chem. 2005, 280:36099-36109.
67. Di Sabatino A., Pender S.L., Jackson C.L., Prothero J.D., Gordon J.N., Picariello L., Rovedatti L., Docena G., Monteleone G., Rampton D.S., Tonelli F., Corazza G.R., MacDonald T.T. Functional modulation of Crohn's disease myofibroblasts by anti-tumor necrosis factor antibodies. Gastroenterology 2007, 133:137-149.
68. Riteau N., Gasse P., Fauconnier L., Gombault A., Couegnat M., Fick L., Kanellopoulos J., Quesniaux V.F., Marchand-Adam S., Crestani B., Ryffel B., Couillin I. Extracellular ATP is a danger signal activating P2X7 receptor in lung inflammation and fibrosis. Am. J. Respir. Crit. Care Med. 2010, 182:774-783.
69. Johnson L.A., Luke A., Sauder K., Moons D.S., Horowitz J.C., Higgins P.D. Intestinal fibrosis is reduced by early elimination of inflammation in a mouse model of IBD: impact of a "Top-Down" approach to intestinal fibrosis in mice. Inflamm. Bowel Dis. 2012, 18:460-471.
70. Plevy S.E., Gemberling J.H., Hsu S., Dorner A.J., Smale S.T. Multiple control elements mediate activation of the murine and human interleukin 12 p40 promoters: evidence of functional synergy between C/EBP and Rel proteins. Mol. Cell. Biol. 1997, 17:4572-4588.
71. Becker C., Wirtz S., Blessing M., Pirhonen J., Strand D., Bechthold O., Frick J., Galle P.R., Autenrieth I., Neurath M.F. Constitutive p40 promoter activation and IL-23 production in the terminal ileum mediated by dendritic cells. J. Clin. Invest. 2003, 112:693-706.
72. Lawrance I.C., Wu F., Leite A.Z., Willis J., West G.A., Fiocchi C., Chakravarti S. A murine model of chronic inflammation-induced intestinal fibrosis down-regulated by antisense NF-kappa B. Gastroenterology 2003, 125:1750-1761.
73. Fichtner-Feigl S., Fuss I.J., Preiss J.C., Strober W., Kitani A. Treatment of murine Th1- and Th2-mediated inflammatory bowel disease with NF-kappa B decoy oligonucleotides. J. Clin. Invest. 2005, 115:3057-3071.
74. Hampe J., Schreiber S., Shaw S.H., Lau K.F., Bridger S., Macpherson A.J., Cardon L.R., Sakul H., Harris T.J., Buckler A., Hall J., Stokkers P., van Deventer S.J., Nurnberg P., Mirza M.M., Lee J.C., Lennard-Jones J.E., Mathew C.G., Curran M.E. A genomewide analysis provides evidence for novel linkages in inflammatory bowel disease in a large European cohort. Am. J. Hum. Genet. 1999, 64:808-816.
75. Hugot J.P., Laurent-Puig P., Gower-Rousseau C., Olson J.M., Lee J.C., Beaugerie L., Naom I., Dupas J.L., Van Gossum A., Orholm M., Bonaiti-Pellie C., Weissenbach J., Mathew C.G., Lennard-Jones J.E., Cortot A., Colombel J.F., Thomas G. Mapping of a susceptibility locus for Crohn's disease on chromosome 16. Nature 1996, 379:821-823.
76. Waetzig G.H., Seegert D., Rosenstiel P., Nikolaus S., Schreiber S. p38 mitogen-activated protein kinase is activated and linked to TNF-alpha signaling in inflammatory bowel disease. J. Immunol. 2002, 168:5342-5351.
77. Schenk U., Frascoli M., Proietti M., Geffers R., Traggiai E., Buer J., Ricordi C., Westendorf A.M., Grassi F. ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci. Signal. 2011, 4:ra12.
78. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 2001, 81:807-869.
79. Hsu C.C., Lien J.C., Chang C.W., Chang C.H., Kuo S.C., Huang T.F. Yuwen02f1 suppresses LPS-induced endotoxemia and adjuvant-induced arthritis primarily through blockade of ROS formation, NFkB and MAPK activation. Biochem. Pharmacol. Feb 1 2013, 85(3):385-395. (Epub 2012 Nov 9). 10.1016/j.bcp.2012.11.002.
80. Chen L., Brosnan C.F. Regulation of immune response by P2X7 receptor. Crit. Rev. Immunol. 2006, 26:499-513.
81. Idzko M., Hammad H., van Nimwegen M., Kool M., Willart M.A., Muskens F., Hoogsteden H.C., Luttmann W., Ferrari D., Di Virgilio F., Virchow J.C., Lambrecht B.N. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat. Med. 2007, 13:913-919.
82. Wilhelm K., Ganesan J., Muller T., Durr C., Grimm M., Beilhack A., Krempl C.D., Sorichter S., Gerlach U.V., Juttner E., Zerweck A., Gartner F., Pellegatti P., Di Virgilio F., Ferrari D., Kambham N., Fisch P., Finke J., Idzko M., Zeiser R. Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nat. Med. 2010, 16:1434-1438.
83. Wynn G., Rong W., Xiang Z., Burnstock G. Purinergic mechanisms contribute to mechanosensory transduction in the rat colorectum. Gastroenterology 2003, 125:1398-1409.