A P2X7 receptor antagonist attenuates experimental autoimmune myocarditis via suppressed myocardial CD4+ T and macrophage infiltration and NADPH oxidase 2/4 expression in mice

Heart and Vessels

Volumn 30, Issue 4, 2015, Pages 527-533

  Zempo, Hirofumi ^a   Sugita, Yoichiro ^a   Ogawa, Masahito ^a   Watanabe, Ryo ^a   Suzuki, Jun ichi ^b   Isobe, Mitsuaki ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

A740003; Experimental autoimmune myocarditis; Fibrosis; Inflammation; P2X7 receptor

Indexed keywords

INTERLEUKIN 1BETA; MESSENGER RNA; N [1 [[(CYANOIMINO)(5 QUINOLINYLAMINO)METHYL]AMINO] 2,2 DIMETHYLPROPYL] 2 (3,4 DIMETHOXYPHENYL)ACETAMIDE; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X7 RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; UNCLASSIFIED DRUG; (N-(1-(((CYANOIMINO)(5-QUINOLINYLAMINO) METHYL) AMINO)-2,2-DIMETHYLPROPYL)-2-(3,4-DIMETHOXYPHENYL)ACETAMIDE); ACETAMIDE DERIVATIVE; QUINOLINE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; BODY WEIGHT; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFECT; EXPERIMENTAL AUTOIMMUNE MYOCARDITIS; HEART CONTRACTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART WEIGHT; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MALE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; AUTOIMMUNE DISEASES; BAGG ALBINO MOUSE; CARDIAC MUSCLE; DISEASE MODEL; INFLAMMATION; METABOLISM; PATHOLOGY;

ACETAMIDES; ANIMALS; AUTOIMMUNE DISEASES; DISEASE MODELS, ANIMAL; INFLAMMATION; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MYOCARDITIS; MYOCARDIUM; NADPH OXIDASE; PURINERGIC P2X RECEPTOR ANTAGONISTS; QUINOLINES; RECEPTORS, PURINERGIC P2X7;

EID: 84938418145     PISSN: 09108327     EISSN: 16152573     Source Type: Journal    
DOI: 10.1007/s00380-014-0527-2     Document Type: Article

References (37)

1. Andreka P, Nadhazi Z, Muzes G, Szantho G, Vandor L, Konya L, Turner MS, Tulassay Z, Bishopric NH (2004) Possible therapeutic targets in cardiac myocyte apoptosis. Curr Pharm Des 10:2445–2461
2. Suzuki J, Ogawa M, Futamatsu H, Kosuge H, Sagesaka YM, Isobe M (2007) Tea catechins improve left ventricular dysfunction, suppress myocardial inflammation and fibrosis, and alter cytokine expression in rat autoimmune myocarditis. Eur J Heart Fail 9:152–159
3. Ashigaki N, Suzuki J, Ogawa M, Watanabe R, Aoyama N, Kobayashi N, Hanatani T, Sekinishi A, Zempo H, Tada Y, Takamura C, Wakayama K, Hirata Y, Nagai R, Izumi Y, Isobe M (2013) Periodontal bacteria aggravate experimental autoimmune myocarditis in mice. Am J Physiol Heart Circ Physiol 304:H740–H748
4. Sagar S, Liu PP, Cooper LT (2012) Myocarditis. Lancet 379:738–747
5. Kawai C (1999) From myocarditis to cardiomyopathy: mechanisms of inflammation and cell death: learning from the past for the future. Circulation 99:1091–1100
6. Caforio AL, Marcolongo R, Jahns R, Fu M, Felix SB, Iliceto S (2012) Immune-mediated and autoimmune myocarditis: clinical presentation, diagnosis and management. Heart Fail Rev 18:715–732
7. Lv H, Havari E, Pinto S, Gottumukkala RV, Cornivelli L, Raddassi K, Matsui T, Rosenzweig A, Bronson RT, Smith R, Fletcher AL, Turley SJ, Wucherpfennig K, Kyewski B, Lipes MA (2011) Impaired thymic tolerance to α-myosin directs autoimmunity to the heart in mice and humans. J Clin Invest 121:1561–1573
8. Marchant DJ, Boyd JH, Lin DC, Granville DJ, Garmaroudi FS, McManus BM (2012) Inflammation in myocardial diseases. Circ Res 110:126–144
9. Kishimoto C, Shioji K, Hashimoto T, Nonogi H, Lee JD, Kato S, Hiramitsu S, Morimoto SI (2013) Therapy with immunoglobulin in patients with acute myocarditis and cardiomyopathy: analysis of leukocyte balance. Heart Vessels. doi:10.1007/s00380-013-0368-4
10. Yuan J, Cao AL, Yu M, Lin QW, Yu X, Zhang JH, Wang M, Guo HP, Liao YH (2010) Th17 cells facilitate the humoral immune response in patients with acute viral myocarditis. J Clin Immunol 30:226–234
11. Suzuki J, Ogawa M, Watanabe R, Morishita R, Hirata Y, Nagai R, Isobe M (2011) Autoimmune giant cell myocarditis: clinical characteristics, experimental models and future treatments. Expert Opin Ther Targets 15:1163–1172
12. Wiley JS, Sluyter R, Gu BJ, Stokes L, Fuller SJ (2011) The human P2X7 receptor and its role in innate immunity. Tissue Antigens 78:321–332
13. Rathinam VA, Vanaja SK, Fitzgerald KA (2012) Regulation of inflammasome signaling. Nat Immunol 13:333–342
14. Matute C, Torre I, Pérez-Cerdá F, Pérez-Samartín A, Alberdi E, Etxebarria E, Arranz AM, Ravid R, Rodríguez-Antigüedad A, Sánchez-Gómez M, Domercq M (2007) P2X(7) receptor blockade prevents ATP excitotoxicity in oligodendrocytes and ameliorates experimental autoimmune encephalomyelitis. J Neurosci 27:9525–9533
15. 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 (2012) Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nat Commun 3:1034
16. Vergani A, Tezza S, D’Addio F, Fotino C, Liu K, Niewczas M, Bassi R, Molano RD, Kleffel S, Petrelli A, Soleti A, Ammirati E, Frigerio M, Visner G, Grassi F, Ferrero ME, Corradi D, Abdi R, Ricordi C, Sayegh MH, Pileggi A, Fiorina P (2013) Long-term heart transplant survival by targeting the ionotropic purinergic receptor P2X7. Circulation 127:463–475
17. Pummerer CL, Luze K, Grässl G, Bachmaier K, Offner F, Burrell SK, Lenz DM, Zamborelli TJ, Penninger JM, Neu N (1996) Identification of cardiac myosin peptides capable of inducing autoimmune myocarditis in BALB/c mice. J Clin Invest 97:2057–2062
18. Honore P, Donnelly-Roberts D, Namovic MT, Hsieh G, Zhu CZ, Mikusa JP, Hernandez G, Zhong C, Gauvin DM, Chandran P, Harris R, Medrano AP, Carroll W, Marsh K, Sullivan JP, Faltynek CR, Jarvis MF (2006) 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 319:1376–1385
19. Seko Y, Takahashi N, Azuma M, Yagita H, Okumura K, Yazaki Y (1998) Effects of in vivo administration of anti-B7-1/B7-2 monoclonal antibodies on murine acute myocarditis caused by coxsackievirus B3. Circ Res 82:613–618
20. Shimoyama M, Hayashi D, Zou Y, Takimoto E, Mizukami M, Monzen K, Kudoh S, Hiroi Y, Yazaki Y, Nagai R, Komuro I (2000) Calcineurin inhibitor attenuates the development and induces the regression of cardiac hypertrophy in rats with salt-sensitive hypertension. Circulation 102:1996–2004
21. Futamatsu H, Suzuki J, Mizuno S, Koga N, Adachi S, Kosuge H, Maejima Y, Hirao K, Nakamura T, Isobe M (2005) Hepatocyte growth factor ameliorates the progression of experimental autoimmune myocarditis: a potential role for induction of T helper 2 cytokines. Circ Res 96:823–830
22. Volonte C, Apolloni S, Skaper SD, Burnstock G (2012) P2X7 receptors: channels, pores and more. CNS Neurol Disord Drug Targets 11:705–721
23. Lassegue B, San Martin A, Griendling KK (2012) Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 110:1364–1390
24. Han LN, Li TL, Zhang YJ, Yang TS, Ding Y (2011) Experimental study of MMP-2 inhibitor treatment of experimental autoimmune myocarditis in Lewis rats. Zhongguo Ying Yong Sheng Li Xue Za Zhi 27:452–456
25. Han LN, Li TL, Zhang YJ, Yang TS, Ding Y, Zhao XN, Guo SL (2011) Effects of matrix metalloproteinase-9 inhibitor in Lewis rats with experimental autoimmune myocarditis. Zhonghua Xin Xue Guan Bing Za Zhi 39:118–123
26. Kania G, Blyszczuk P, Eriksson U (2009) Mechanisms of cardiac fibrosis in inflammatory heart disease. Trends Cardiovasc Med 19:247–252
27. Nabeta T, Inomata T, Iida Y, Ikeda Y, Iwamoto M, Ishii S, Sato T, Watanabe I, Naruke T, Shinagawa H, Koitabashi T, Takeuchi I, Nishii M, Inoue Y, Izumi T (2013) Baseline cardiac magnetic resonance imaging versus baseline endomyocardial biopsy for the prediction of left ventricular reverse remodeling and prognosis in response to therapy in patients with idiopathic dilated cardiomyopathy. Heart Vessels. doi:10.1007/s00380-013-0415-1
28. Smith SC, Allen PM (1991) Myosin-induced acute myocarditis is a T cell-mediated disease. J Immunol 147:2141–2147
29. Maier R, Miller S, Kurrer M, Krebs P, de Giuli R, Kremer M, Scandella E, Ludewig B (2005) Quantification and characterization of myosin peptide-specific CD4+ T cells in autoimmune myocarditis. J Immunol Methods 304:117–125
30. Göser S, Ottl R, Brodner A, Dengler TJ, Torzewski J, Egashira K, Rose NR, Katus HA, Kaya Z (2005) Critical role for monocyte chemoattractant protein-1 and macrophage inflammatory protein-1alpha in induction of experimental autoimmune myocarditis and effective anti-monocyte chemoattractant protein-1 gene therapy. Circulation 112:3400–3407
31. Lang PA, Merkler D, Funkner P, Shaabani N, Meryk A, Krings C, Barthuber C, Recher M, Brück W, Häussinger D, Ohashi PS, Lang KS (2010) Oxidized ATP inhibits T-cell-mediated autoimmunity. Eur J Immunol 40:2401–2408
32. Lemaire I, Falzoni S, Zhang B, Pellegatti P, Di Virgilio F (2011) The P2X7 receptor and Pannexin-1 are both required for the promotion of multinucleated macrophages by the inflammatory cytokine GM-CSF. J Immunol 187:3878–3887
33. Martel-Gallegos G, Rosales-Saavedra MT, Reyes JP, Casas-Pruneda G, Toro-Castillo C, Pérez-Cornejo P, Arreola J (2010) Human neutrophils do not express purinergic P2X7 receptors. Purinergic Signal 6:297–306
34. Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, Yagita H, Ishii N, Evans R, Honda K, Takeda K (2008) ATP drives lamina propria T(H)17 cell differentiation. Nature 455:808–812
35. Ishiyama S, Hiroe M, Nishikawa T, Shimojo T, Abe S, Fujisaki H, Ito H, Yamakawa K, Kobayashi N, Kasajima T, Marumo F (1998) The Fas/Fas ligand system is involved in the pathogenesis of autoimmune myocarditis in rats. J Immunol 161:4695–4701
36. Schenk U, Frascoli M, Proietti M, Geffers R, Traggiai E, Buer J, Ricordi C, Westendorf AM, Grassi F (2011) ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci Signal 4:ra12
37. Killeen ME, Ferris L, Kupetsky EA, Falo L Jr, Mathers AR (2013) Signaling through purinergic receptors for ATP induces human cutaneous innate and adaptive Th17 responses: implications in the pathogenesis of psoriasis. J Immunol 190:4324–4336