Role of the cholinergic antiinflammatory pathway in murine autoimmune myocarditis

Circulation Research

Volumn 109, Issue 2, 2011, Pages 130-140

  Leib, Christoph ^a   Göser, Stefan ^a   Lüthje, Dorit ^a   Öttl, Renate ^a   Tretter, Theresa ^a   Lasitschka, Felix ^a   Zittrich, Stefan ^b   Pfitzer, Gabriele ^b   Katus, Hugo A ^a   Kaya, Ziya ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

cholinergic antiinflammatory pathway; myocarditis; nicotine; troponin

Indexed keywords

CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; DRINKING WATER; GELATINASE A; GELATINASE B; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MATRIX METALLOPROTEINASE 14; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NATRIURETIC PEPTIDE PRECURSOR A; NATRIURETIC PEPTIDE PRECURSOR B; NATRIURETIC PEPTIDE RECEPTOR A; NATRIURETIC PEPTIDE RECEPTOR B; NEOSTIGMINE; NICOTINE TARTRATE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR 7ALPHA; OSTEOPONTIN; RANTES; RECOMBINANT INTERLEUKIN 6; STAT3 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TROPONIN I; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNE MYOCARDITIS; CELL INFILTRATION; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFERENT NERVE; FEMALE; GENETIC TRANSCRIPTION; HEART FAILURE; HEART MUSCLE; HEART MUSCLE FIBROSIS; HEART PROTECTION; HISTOPATHOLOGY; IMMUNIZATION; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SPLEEN CELL; VAGUS NERVE STIMULATION;

ANIMALS; AUTOIMMUNE DISEASES; CHOLINERGIC AGENTS; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; INFLAMMATION; INFLAMMATION MEDIATORS; MICE; MYOCARDITIS; NICOTINE; PROTEINS; RNA, MESSENGER; TROPONIN I; VAGUS NERVE;

EID: 79960383122     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.245563     Document Type: Article

References (54)

1. Tracey KJ. The inflammatory reflex. Nature. 2002;420:853-859. (Pubitemid 36019638)
2. de Jonge WJ, Ulloa L. The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol. 2007;151: 915-929. (Pubitemid 47195518)
3. Nizri E, Irony-Tur-Sinai M, Lory O, Orr-Urtreger A, Lavi E, Brenner T. Activation of the cholinergic anti-inflammatory system by nicotine attenuates neuroinflammation via suppression of Th1 and Th17 responses. J Immunol. 2009;183:6681-6688.
4. Wilund KR, Rosenblat M, Chung HR, Volkova N, Kaplan M, Woods JA, Aviram M. Macrophages from alpha 7 nicotinic acetylcholine receptor knockout mice demonstrate increased cholesterol accumulation and decreased cellular paraoxonase expression: a possible link between the nervous system and atherosclerosis development. Biochem Biophys Res Commun. 2009;390:148-154.
5. Matthay MA, Ware LB. Can nicotine treat sepsis? Nat Med. 2004;10: 1161-1162. (Pubitemid 39540424)
6. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, Wang H, Abumrad N, Eaton JW, Tracey KJ. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405:458-462. (Pubitemid 30367422)
7. Ulloa L. The vagus nerve and the nicotinic anti-inflammatory pathway. Nat Rev Drug Discov. 2005;4:673-684. (Pubitemid 41149761)
8. Marrero MB, Bencherif M. Convergence of alpha 7 nicotinic acetyl-choline receptor-activated pathways for anti-apoptosis and anti-inflammation: central role for JAK2 activation of STAT3 and NF-kappaB. Brain Res. 2009;1256:1-7.
9. Hofer S, Eisenbach C, Lukic IK, Schneider L, Bode K, Brueckmann M, Mautner S, Wente MN, Encke J, Werner J, Dalpke AH, Stremmel W, Nawroth PP, Martin E, Krammer PH, Bierhaus A, Weigand MA. Phar-macologic cholinesterase inhibition improves survival in experimental sepsis. Crit Care Med. 2008;36:404-408. (Pubitemid 351158611)
10. Saeed RW, Varma S, Peng-Nemeroff T, Sherry B, Balakhaneh D, Huston J, Tracey KJ, Al-Abed Y, Metz CN. Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation. J Exp Med. 2005;201:1113-1123. (Pubitemid 40524679)
11. Pavlov VA, Ochani M, Yang LH, Gallowitsch-Puerta M, Ochani K, Lin X, Levi J, Parrish WR, Rosas-Ballina M, Czura CJ, Larosa GJ, Miller EJ, Tracey KJ, Al-Abed Y. Selective alpha7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Crit Care Med. 2007;35:1139-1144. (Pubitemid 46598966)
12. Huston JM, Gallowitsch-Puerta M, Ochani M, Ochani K, Yuan R, Rosas-Ballina M, Ashok M, Goldstein RS, Chavan S, Pavlov VA, Metz CN, Yang H, Czura CJ, Wang H, Tracey KJ. Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis. Crit Care Med. 2007;35:2762-2768. (Pubitemid 350175773)
13. Pavlov VA, Parrish WR, Rosas-Ballina M, Ochani M, Puerta M, Ochani K, Chavan S, Al-Abed Y, Tracey KJ. Brain acetylcholinesterase activity controls systemic cytokine levels through the cholinergic anti-inflammatory pathway. Brain Behav Immun. 2009;23:41-45.
14. Francis J, Zhang ZH, Weiss RM, Felder RB. Neural regulation of the proinflammatory cytokine response to acute myocardial infarction. Am J Physiol Heart Circ Physiol. 2004;287:H791-H797. (Pubitemid 38955314)
15. Zhang Y, Popovic ZB, Bibevski S, Fakhry I, Sica DA, Van Wagoner DR, Mazgalev TN. Chronic vagus nerve stimulation improves autonomic control and attenuates systemic inflammation and heart failure progression in a canine high-rate pacing model. Circ Heart Fail. 2009;2:692-699.
16. Li M, Zheng C, Sato T, Kawada T, Sugimachi M, Sunagawa K. Vagal nerve stimulation markedly improves long-term survival after chronic heart failure in rats. Circulation. 2004;109:120-124. (Pubitemid 38056032)
17. Mioni C, Bazzani C, Giuliani D, Altavilla D, Leone S, Ferrari A, Minutoli L, Bitto A, Marini H, Zaffe D, Botticelli AR, Iannone A, Tomasi A, Bigiani A, Bertolini A, Squadrito F, Guarini S. Activation of an efferent cholinergic pathway produces strong protection against myocardial ische-mia/reperfusion injury in rats. Crit Care Med. 2005;33:2621-2628. (Pubitemid 41682117)
18. Goser S, Andrassy M, Buss SJ, Leuschner F, Volz CH, Ottl R, Zittrich S, Blaudeck N, Hardt SE, Pfitzer G, Rose NR, Katus HA, Kaya Z. Cardiac troponin I but not cardiac troponin T induces severe autoimmune inflammation in the myocardium. Circulation. 2006;114:1693-1702. (Pubitemid 44607117)
19. Kruger M, Pfitzer G, Stehle R. Expression and purification of human cardiac troponin subunits and their functional incorporation into isolated cardiac mouse myofibrils. J Chromatogr B Analyt Technol Biomed Life Sci. 2003;786:287-296. (Pubitemid 36324585)
20. Al-Hillawi E, Minchin SD, Trayer IP. Overexpression of human cardiac troponin-I and troponin-C in Escherichia coli and their purification and characterisation: two point mutations allow high-level expression of troponin-I. Eur J Biochem. 1994;225:1195-1201. (Pubitemid 24342566)
21. Goser S, Ottl R, Brodner A, Dengler TJ, Torzewski J, Egashira K, Rose NR, Katus HA, Kaya Z. Critical role for monocyte chemoattractant protein-1 and macrophage inflammatory protein-1α in induction of experimental autoimmune myocarditis and effective anti-monocyte chemoattractant protein-1 gene therapy. Circulation. 2005;112:3400-3407. (Pubitemid 43739554)
22. Frangogiannis NG. Chemokines in the ischemic myocardium: from inflammation to fibrosis. Inflamm Res. 2004;53:585-595. (Pubitemid 40385316)
23. D'Ambrosio D, Panina-Bordignon P, Sinigaglia F. Chemokine receptors in inflammation: an overview. J Immunol Methods. 2003;273:3-13. (Pubitemid 36078458)
24. Ravikumar R, Flora G, Geddes JW, Hennig B, Toborek M. Nicotine attenuates oxidative stress, activation of redox-regulated transcription factors and induction of proinflammatory genes in compressive spinal cord trauma. Brain Res Mol Brain Res. 2004;124:188-198. (Pubitemid 38591571)
25. Kobayashi Y, Kubo A, Iwano M, Sakaguchi Y, Samejima K, Kyoda Y, Yonemasu K, Hashimoto T. Levels of MCP-1 and GM-CSF mRNA correlated with inflammatory cytokines mRNA levels in experimental autoimmune myocarditis in rats. Autoimmunity. 2002;35:97-104. (Pubitemid 34678728)
26. van Maanen MA, Vervoordeldonk MJ, Tak PP. The cholinergic anti-inflammatory pathway: towards innovative treatment of rheumatoid arthritis. Nat Rev Rheumatol. 2009;5:229-232.
27. Ghia JE, Blennerhassett P, Kumar-Ondiveeran H, Verdu EF, Collins SM. The vagus nerve: a tonic inhibitory influence associated with inflammatory bowel disease in a murine model. Gastroenterology. 2006;131: 1122-1130. (Pubitemid 44498700)
28. Song XM, Li JG, Wang YL, Hu ZF, Zhou Q, Du ZH, Jia BH. The protective effect of the cholinergic anti-inflammatory pathway against septic shock in rats. Shock. 2008;30:468-472.
29. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature. 2003;421:384-388. (Pubitemid 36157937)
30. van Westerloo DJ, Giebelen IA, Florquin S, Daalhuisen J, Bruno MJ, de Vos AF, Tracey KJ, van der PT. The cholinergic anti-inflammatory pathway regulates the host response during septic peritonitis. J Infect Dis. 2005;191:2138-2148. (Pubitemid 40800586)
31. van Maanen MA, Lebre MC, van der PT, Larosa GJ, Elbaum D, Vervoordeldonk MJ, Tak PP. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum. 2009;60: 114-122.
32. Calabrese F, Carturan E, Chimenti C, Pieroni M, Agostini C, Angelini A, Crosato M, Valente M, Boffa GM, Frustaci A, Thiene G. Overexpression of tumor necrosis factor (TNF)alpha and TNFalpha receptor I in human viral myocarditis: clinicopathologic correlations. Mod Pathol. 2004;17: 1108-1118. (Pubitemid 39128237)
33. Satoh M, Tamura G, Segawa I, Tashiro A, Hiramori K, Satodate R. Expression of cytokine genes and presence of enteroviral genomic RNA in endomyocardial biopsy tissues of myocarditis and dilated cardiomy-opathy. Virchows Arch. 1996;427:503-509. (Pubitemid 126828182)
34. Matsumori A, Yamada T, Suzuki H, Matoba Y, Sasayama S. Increased circulating cytokines in patients with myocarditis and cardiomyopathy. Br Heart J. 1994;72:561-566.
35. Kubota T, McTiernan CF, Frye CS, Slawson SE, Lemster BH, Koretsky AP, Demetris AJ, Feldman AM. Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha. Circ Res. 1997;81:627-635. (Pubitemid 27432751)
36. Bryant D, Becker L, Richardson J, Shelton J, Franco F, Peshock R, Thompson M, Giroir B. Cardiac failure in transgenic mice with myocardial expression of tumor necrosis factor-alpha. Circulation. 1998;97:1375-1381. (Pubitemid 28182676)
37. Kubota T, McTiernan CF, Frye CS, Demetris AJ, Feldman AM. Cardiac-specific overexpression of tumor necrosis factor-alpha causes lethal myocarditis in transgenic mice. J Card Fail. 1997;3:117-124. (Pubitemid 127675015)
38. Lenzo JC, Fairweather D, Shellam GR, Lawson CM. Immunomodulation of murine cytomegalovirus-induced myocarditis in mice treated with lipopoly-saccharide and tumor necrosis factor. Cell Immunol. 2001;213:52-61. (Pubitemid 34074970)
39. Kubota T, Bounoutas GS, Miyagishima M, Kadokami T, Sanders VJ, Bruton C, Robbins PD, McTiernan CF, Feldman AM. Soluble tumor necrosis factor receptor abrogates myocardial inflammation but not hypertrophy in cytokine-induced cardiomyopathy. Circulation. 2000;101: 2518-2525. (Pubitemid 30366257)
40. Tanaka T, Kanda T, McManus BM, Kanai H, Akiyama H, Sekiguchi K, Yokoyama T, Kurabayashi M. Overexpression of interleukin-6 aggravates viral myocarditis: impaired increase in tumor necrosis factor-alpha. J Mol Cell Cardiol. 2001;33:1627-1635. (Pubitemid 32844221)
41. Ito H, Ono K, Nishio R, Sasayama S, Matsumori A. Amiodarone inhibits interleukin 6 production and attenuates myocardial injury induced by viral myocarditis in mice. Cytokine. 2002;17:197-202.
42. Eriksson U, Kurrer MO, Schmitz N, Marsch SC, Fontana A, Eugster HP, Kopf M. Interleukin-6-deficient mice resist development of autoimmune myocarditis associated with impaired upregulation of complement C3. Circulation. 2003;107:320-325. (Pubitemid 36135231)
43. Vanhoutte D, Heymans S. TIMPs and cardiac remodeling: "Embracing the MMP-independent-side of the family." J Mol Cell Cardiol. 2010;48: 445-453.
44. Freeling J, Wattier K, LaCroix C, Li YF. Neostigmine and pilocarpine attenuated tumour necrosis factor alpha expression and cardiac hypertrophy in the heart with pressure overload. Exp Physiol. 2008;93:75-82 (Pubitemid 350293968)
45. Akinci SB, Ulu N, Yondem OZ, Firat P, Guc MO, Kanbak M, Aypar U. Effect of neostigmine on organ injury in murine endotoxemia: missing facts about the cholinergic antiinflammatory pathway. World J Surg. 2005;29:1483-1489. (Pubitemid 41712686)
46. Nakahara T, Kawada T, Sugimachi M, Miyano H, Sato T, Shishido T, Yoshimura R, Miyashita H, Sunagawa K. Cholinesterase affects dynamic transduction properties from vagal stimulation to heart rate. Am J Physiol. 1998;275:R541-R547.
47. Endou M, Tanito Y, Okumura F. A comparison between chronotropic effects of neostigmine and edrophonium in isolated guinea pig right atrium. J Pharmacol Exp Ther. 1997;282:1480-1486. (Pubitemid 27408331)
48. Zheng JQ, He XP, Yang AZ, Liu CG. Neostigmine competitively inhibited nicotinic acetylcholine receptors in sympathetic neurons. Life Sci. 1998;62:1171-1178.
49. Yoon SY, Kwon YB, Kim HW, Roh DH, Kang SY, Kim CY, Han HJ, Kim KW, Yang IS, Beitz AJ, Lee JH. Intrathecal neostigmine reduces the zymosan-induced inflammatory response in a mouse air pouch model via adrenomedullary activity: involvement of spinal muscarinic type 2 receptors. Neuropharmacology. 2005;49:275-282. (Pubitemid 41112815)
50. Yoon SY, Kwon YB, Kim HW, Roh DH, Seo HS, Han HJ, Beitz AJ, Lee JH. A spinal muscarinic M2 receptor-GABAergic disinhibition pathway that modulates peripheral inflammation in mice. Neuropharmacology. 2007;53:677-686. (Pubitemid 47513173)
51. Pavlov VA, Ochani M, Gallowitsch-Puerta M, Ochani K, Huston JM, Czura CJ, Al-Abed Y, Tracey KJ. Central muscarinic cholinergic regulation of the systemic inflammatory response during endotoxemia. Proc Natl Acad Sci USA. 2006;103:5219-5223.
52. Yasukawa H, Yajima T, Duplain H, Iwatate M, Kido M, Hoshijima M, Weitzman MD, Nakamura T, Woodard S, Xiong D, Yoshimura A, Chien KR, Knowlton KU. The suppressor of cytokine signaling-1 (SOCS1) is a novel therapeutic target for enterovirus-induced cardiac injury. J Clin Invest. 2003;111:469-478. (Pubitemid 36228004)
53. Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol. 2006;80:227-236. (Pubitemid 44835496)
54. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9:798-809.