Regulation of inflammation and myocardial fibrosis in experimental autoimmune myocarditis

Inflammation and Allergy - Drug Targets

Volumn 10, Issue 3, 2011, Pages 218-225

  Watanabe, Kenichi ^a   Sukumaran, Vijayakumar ^a   Veeraveedu, Punniyakoti T ^a,b   Thandavarayan, Rajarajan A ^a   Gurusamy, Narasimman ^c   Ma, Meilei ^a   Arozal, Wawaimuli ^a   Sari, Flori R ^a   Lakshmanan, Arun Prasath ^a   Arumugam, Somasundaram ^a   Soetikno, Vivian ^a   Rajavel, Varatharajan ^d   Suzuki, Kenji ^e  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d UNIVERSITY OF MALAYA   (Malaysia)

^e NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

Angiotensin converting enzyme inhibitors; Angiotensin receptor blockers; Dilated cardiomyopathy; Experimental autoimmune myocarditis; Inflammation; Myocardial fibrosis

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GROWTH FACTOR; INTERLEUKIN 1; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPONTIN; VASCULAR CELL ADHESION MOLECULE 1;

CONGESTIVE CARDIOMYOPATHY; DRUG EFFECT; HEART FAILURE; HEART MUSCLE FIBROSIS; HEART MUSCLE INJURY; HUMAN; INFLAMMATION; MYOCARDITIS; NONHUMAN; PATHOGENESIS; REVIEW; TH1 CELL; TH2 CELL;

EID: 79958185781     PISSN: 18715281     EISSN: 18715281     Source Type: Journal    
DOI: 10.2174/187152811795564091     Document Type: Review

References (69)

1. Jones, S.M.; Kirby, M.S.; Harding, S.E.; Vescova, G.; Wanless, R.B.; Dalla Libera, L.D.; Poole-Wilson, P.A. Adriamycin cardiomyopathy in the rabbit: alterations in contractile proteins and myocyte function. Cardiovasc Res., 1990, 24, 834-842.
2. Feldman, A.M.; McNamara, D. Myocarditis. N Engl J Med., 2000, 343, 1388-1398.
3. Kodama, M.; Matsumoto, Y.; Fujiwara, M.; Masani, F.; Izumi, T.; Shibata, A. A novel experimental model of giant cell myocarditis induced in rats by immunization with cardiac myosin fraction. Clin. Immunol. Immunopathol., 1990, 57, 250-262.
4. Kodama, M.; Matsumoto, Y.; Fujiwara, M.; Zhang, S.S.; Hanawa, H.; Itoh, E.; Tsuda, T.; Izumi, T.; Shibata, A. Characteristics of giant cells and factors related to the formation of giant cells in myocarditis. Circ. Res., 1991, 69, 1042-1050.
5. Kodama, M.; Matsumoto, Y.; Fujiwara, M. In vivo lymphocytemediated myocardial injures demonstrated by adoptive transfer of experimental autoimmune myocarditis. Circulation, 1992, 85, 1918-1926.
6. Fuse, K.; Kodama, M.; Ito, M.; Okura, Y.; Kato, K.; Hanawa, H.; Aoki, S.; Aizawa, Y. Polarity of helper T cell subsets represents disease nature and clinical course of experimental autoimmune myocarditis in rats. Clin. Exp. Immunol., 2003, 134, 403-408.
7. Binah, O. Pharmacologic modulation of the immune interaction between cytotoxic lymphocytes and ventricular myocytes. J. Cardiovasc. Pharmacol., 2001, 38, 298-316.
8. Ferrario, C.M.; Strawn, W.B. Role of the renin-angiotensinaldosterone system and proinflammatory mediators in cardiovascular disease. Am. J. Cardiol., 2006, 98, 121-128.
9. Schmieder, R.E.; Hilgers, K.F.; Schlaich, M.P.; Schmidt, B.M. Renin-angiotensin system and cardiovascular risk. Lancet, 2007, 369, 1208-1219.
10. Seko, Y. Effect of the angiotensin II receptor blocker olmesartan on the development of murine acute myocarditis caused by coxsackievirus B3. Clin. Sci., 2006, 110, 379-386.
11. Kaplan, M.H.; Craig, J.M. Immunologic studies of heart tissue via cardiac lesions in rabbits associated with autoantibodies to heart induced by immunization with heterologous heart. J Immunol, 1963, 90, 725-733.
12. Neu, N.; Ploier, B.; Ofner, C. Cardiac myosin-induced myocarditis. Heart autoantibodies are not involved the induction of the disease. J. Immunol., 1990, 145, 4094-4100.
13. Bachmaier, K.; Neu, N.; Yeung, R.S.; Mak, T.W.; Liu, P.; Penninger, J.M. Generation of humanized mice susceptible to peptide-induced inflammatory heart disease. Circulation, 1999, 99, 1885-1891.
14. Wegmann, K.W.; Zhao, W.; Griffin, A.C.; Hickey, W.F. Identification of myocarditogenic peptides derived from cardiac myosin capable of inducing experimental allergic myocarditis in the Lewis rat. The utility of a class II binding motif in selecting self-reactive peptides. J. Immunol., 1994, 153, 892-900.
15. Inomata, T.; Hanawa, H.; Miyanishi, T.; Yajima, E.; Nakayama, S.; Maita, T.; Kodama, M.; Izumi, T.; Shibata, A.; Abo, T. Localization of porcine cardiac myosin epitopes that induce experimental autoimmune myocarditis. Circ. Res., 1995, 76, 726-733.
16. Liao, L.; Sindhwani, R.; Rojkind, M.; Factor, S.; Leinwand, L.; Diamond, B. Antibody-mediated autoimmune myocarditis depends on genetically determined target organ sensitivity. J. Exp. Med., 1995, 181, 1123-1131.
17. Pummerer, C.; Berger, P.; Fruhwirth, M.; Ofner, C.; Neu, N. Cellular infiltrate, major histocompatibility antigen expression and immunopathogenic mechanisms in cardiac myosin-induced myocarditis. Lab. Invest., 1991, 65, 538-547.
18. Pummerer, C.L.; Grassl, G.; Sailer, M.; Bachmaier, K.W.; Penninger, J.M.; Neu, N. Cardiac myosin-induced myocarditis: target recognition by autoreactive T cells requires prior activation of cardiac interstitial cells. Lab. Invest., 1996, 74, 845-852.
19. Okura, Y.; Takeda, K.; Honda, S.; Hanawa, H.; Watanabe, H.; Kodama, M.; Izumi, T.; Aizawa, Y.; Seki, S.; Abo, T. Recombinant murine interleukin-12 facilitates induction of cardiac myosinspecific type 1 helper T cells in rats. Circ. Res., 1998, 82, 1035-1042.
20. Kodama, M.; Zhang, S.; Hanawa, H.; Shibata, A. Immunohistochemical characterization of infiltrating mononuclear cells in the rat heart with experimental autoimmune giant cell myocarditis. Clin. Exp. Immunol., 1992, 90, 330-335.
21. Hanawa, H.; Tsuchida, M.; Matsumoto, Y.; Watanabe, H.; Abo, T.; Sekikawa, H.; Kodama, M.; Zhang, S.; Izumi, T.; Shibata, A. Characterization of T cells infiltrating the heart in rats with experimental autoimmune myocarditis. Their similarity to extrathymic T cells in mice and the site of proliferation. J. Immunol., 1993, 150, 5682-5695.
22. Hanawa, H.; Inomata, T.; Sekikawa, H.; Abo, T.; Kodama, M.; Izumi, T.; Shibata, A. Analysis of heart-infiltrating T-cell clonotypes in experimental autoimmune myocarditis in rats. Circ. Res., 1996, 78, 118-125.
23. Smith, S.C.; Allen, P.M. Expression of myosin-class II major histocompatibility complexes in the normal myocardium occurs before induction of autoimmune myocarditis. Proc. Natl. Acad. Sci. USA, 1992, 89, 9131-9135.
24. Smith, S.C.; Allen, P.M. Neutralization of endogenous tumor necrosis factor ameliorates the severity of myosin-induced myocarditis. Circ. Res., 1992, 70, 856-863
25. Goren, N.; Leiros, C.P.; Sterin-Borda, L.; Borda, E. Nitric oxide synthase in experimental autoimmune myocarditis dysfunction. J. Mol. Cell. Cardiol., 1998, 30, 2467-2474.
26. Ishiyama, S.; Hiroe, M.; Nishikawa, T.; Shimojo, T.; Abe, S.; Fujisaki, H.; Ito, H.; Yamakawa, K.; Kobayashi, N.; Kasajima, T.; Marumo, F. The Fas/Fas ligand system is involved in the pathogenesis of autoimmune myocarditis in rats. J. Immunol., 1998, 161, 4695-4701.
27. Springer, T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell, 1994, 76, 301-314.
28. 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.
29. Nakamura, H.; Yamamura, T.; Umemoto, S.; Fukuta, S.; Shioi, T.; Matsumori, A.; Sasayama, S.; Matsuzaki, M. Autoimmune response in chronic ongoing myocarditis demonstrated by heterotopic cardiac transplantation in mice. Circulation, 1996, 94, 3348-3354.
30. Kubota, T.; McTiernan, C.F.; Frye, C.S.; Demetris, A.J.; Feldman, A.M. Cardiac-specific overexpression of tumor necrosis factoralpha causes lethal myocarditis in transgenic mice. J. Card. Fail, 1997, 3, 117-124.
31. Kishimoto, C.; Takada, H.; Kawamata, H.; Umatake, M.; Ochiai, H. Immunoglobulin treatment prevents congestive heart failure in murine encephalomyocarditis viral myocarditis associated with reduction of inflammatory cytokines. J. Pharmacol. Exp. Ther., 2001, 299, 645-651.
32. Sukumaran, V.; Watanabe, K.; Veeraveedu, P.T.; Thandavarayan, R.A,; Gurusamy, N.; Ma, M.; Yamaguchi, K.; Suzuki, K.; Kodama, M.; Aizawa, Y. Beneficial effects of olmesartan, an angiotensin II receptor type 1 antagonist, in rats with dilated cardiomyopathy. Exp. Biol. Med. (Maywood), 2010, 235, 1338-1346.
33. Sukumaran, V.; Watanabe, K.; Veeraveedu, P.T.; Thandavarayan, R.A,; Gurusamy, N.; Ma, M.; Yamaguchi, K.; Suzuki, K.; Kodama, M.; Aizawa, Y. Telmisartan, an angiotensin-II receptor blocker ameliorates cardiac remodeling in rats with dilated cardiomyopathy. Hypertens. Res. 2010, 33, 695-702.
34. Sukumaran, V.; Watanabe, K.; Veeraveedu, P.T.; Ma, M.; Gurusamy, N.; Rajavel, V.; Suzuki, K.; Yamaguchi, K.; Kodama, M.; Aizawa, Y. Telmisartan ameliorates experimental autoimmune myocarditis associated with inhibition of inflammation and oxidative stress. Eur. J. Pharmacol., 2011, 652, 126-135.
35. Sukumaran, V.; Watanabe, K.; Veeraveedu, P.T.; Gurusamy, N.; Ma, M.; Thandavarayan, R.A,; Lakshmanan AP, Yamaguchi, K.; Suzuki, K.; Kodama, M. Olmesartan, an AT1 Antagonist, Attenuates Oxidative Stress, Endoplasmic Reticulum Stress and Cardiac Inflammatory Mediators in Rats with Heart Failure Induced by Experimental Autoimmune Myocarditis. Int. J. Biol. Sci. 2011, 7, 154-167.
36. Kjeldsen, S.E.; Julius, S. Hypertension mega-trials with cardiovascular end points: effect of angiotensin-converting enzyme inhibitors and angiotensin receptor blockers. Am. Heart J., 2004, 148, 747-754.
37. Kramer, C.; Sunkomat, J.; Witte, J.; Luchtefeld, M.; Walden, M.; Schmidt, B. Angiotensin II receptor-independent anti-inflammatory and anti-aggregatory properties of losartan: role of the active metabolite EXP 3179. Circ. Res., 2002, 90, 770-776.
38. Neri Serneri, G.G.; Boddi, M.; Modesti, P.A.; Coppo, M.; Cecioni, I.; Toscano, T.; Papa, M.L.; Bandinelli, M.; Lisi, G.F.; Chiavarelli, M. Cardiac angiotensin II participates in coronary microvessel inflammation of unstable angina and strengthens the immunomediated component. Circ. Res., 2004, 94, 1630-1637.
39. Smith, S.C.; Allen, P.M. Myosin-induced acute myocarditis is a T cell mediated disease. J. Immunol., 1991, 147, 2141-2147.
40. Bergelson, J.M.; Cunningham, J.A.; Droguett, G.; Kurt-Jones, E.A.; Krithivas, A.; Hong, J.S.; Horwitz, M.S.; Crowell, R.L.; Finberg, R.W. Isolation of common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science, 1997, 275, 1320-1323.
41. Schieffer, B.; Bunte, C.; Witte, J.; Hoeper, K.; Böger, R.H.; Schwedhelm, E.; Drexler, H. Comparative effects of AT1-antagonism and angiotensin-converting enzyme inhibition on markers of inflammation and platelet aggregation in patients with coronary artery disease. J. Am. Coll. Cardiol., 2004, 44, 362-368.
42. Gage, J.R.; Fonarow, G.; Hamilton, M.; Widawski, M.; Martinez-Maza, O.; Vredevoe, DL. β-blocker and angiotensin-converting enzyme inhibitor therapy is associated with decreased Th1/Th2 cytokine ratios and inflammatory cytokine production in patients with chronic heart failure. Neuroimmunomodulation, 2004, 11, 173-180.
43. Liu, X.; Zhu, X.; Wang, A.; Fan, H.; Yuan, H. Effects of angiotensin-II receptor blockers on experimental autoimmune myocarditis. Int. J. Cardiol., 2009, 137, 282-288.
44. Midei, M.G.; DeMent, S.H.; Feldman, A.M.; Hutchins, G.M.; Baughman, K.L. Peripartum myocarditis and cardiomyopathy. Circulation, 1990, 81, 922-928.
45. Finkel, M.S.; Oddis, C.V.; Jacob, T.D; Watkins, S.C.; Hattler, B.G.; Simmons, R.L. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science, 1992, 257, 387-389.
46. Tanaka, A.; Matsumori, A.; Wang, W.; Sasayama, S. An angiotensin II receptor antagonist reduces myocardial damage in an animal model of myocarditis. Circulation 1994, 90, 2051-2055.
47. Fairweather, D.; Frisancho-Kiss, S.; Yusung, S.A.; Barrett, M.A.; Davis, S.E.; Steele, R.A.; Gatewood, S.J.; Rose, N.R. IL-12 protects against coxsackievirus B3-induced myocarditis by increasing IFN-gamma and macrophage and neutrophil populations in the heart. J. Immunol., 2005, 174, 261-269.
48. Manabe, I.; Shindo, T.; Nagai, R. Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy. Circ. Res., 2002, 91, 1103-1113.
49. Weber, K.T.; Eghbali, M. Collagen matrix synthesis and degradation in the development and regression of left ventricular hypertrophy. Cardiovasc. Rev. Rep., 1991, 12, 61-69.
50. Kashimura, T.; Hayashi, M.; Kodama, M.; Nakazawa, M.; Abe, S.; Yoshida, T.; Tachikawa, H.; Hanawa, H.; Kato, K.; Watanabe, K.; Aizawa, Y. Effects of imidapril and TA-606 on rat dilated cardiomyopathy after myocarditis. Jpn. Heart J. 2003, 44, 735-744.
51. Juan, W.; Nakazawa, M.; Watanabe, K.; Ma, M.; Wahed, M.I.; Hasegawa, G.; Naito, M.; Yamamoto, T.; Fuse, K.; Kato, K.; Kodama, M.; Aizawa, Y. Quinapril inhibits progression of heart failure and fibrosis in rats with dilated cardiomyopathy after myocarditis. Mol. Cell. Biochem., 2003, 251, 77-82.
52. Weber, K.T. Fibrosis, a common pathway to organ failure: angiotensin II and tissue repair. Semin. Nephrol., 1997, 17, 467-491.
53. Heeneman, S.; Cleutjens, J.P.; Faber, B.C.; Creemers, E.E.; van Suylen, R.J.; Lutgens, E.; Cleutjens, K.B.; Daemen, M.J. The dynamic extracellular matrix: intervention strategies during heart failure and atherosclerosis. J. Pathol., 2003, 200, 516-525.
54. Kuno, A.; Yamada, T.; Masuda, K.; Ogawa, K.; Sogawa, M.; Nakamura, S.; Nakazawa, T.; Ohara, H.; Nomura, T.; Joh, T.; Shirai, T.; Itoh, M. Angiotensin-converting enzyme inhibitor attenuates pancreatic inflammation and fibrosis in male Wistar Bonn/Kobori rats. Gastroenterology, 2003, 124, 1010-1019.
55. Yamada, T.; Kuno, A.; Masuda, K.; Ogawa, K.; Sogawa, M.; Nakamura, S.; Ando, T.; Sano, H.; Nakazawa, T.; Ohara, H.; Nomura, T.; Joh, T.; Itoh, M. Candesartan, an angiotensin II receptor antagonist, suppresses pancreatic inflammation and fibrosis in rats. J. Pharmacol. Exp. Ther., 2003, 307, 17-23.
56. Szalay, G.; Sauter, M.; Haberland, M.; Zuegel, U.; Steinmeyer, A.; Kandolf, R.; Klingel, K. Osteopontin: a fibrosis-related marker molecule in cardiac remodeling of enterovirus myocarditis in the susceptible host. Circ. Res., 2009, 104, 851-859.
57. Hanawa, H.; Abe, S.; Hayashi, M.; Yoshida, T.; Yoshida, K.; Shiono, T.; Fuse, K.; Ito, M.; Tachikawa, H.; Kashimura, T.; Okura, Y.; Kato, K.; Kodama, M.; Maruyama, S.; Yamamoto, T.; Aizawa, Y. Time course of gene expression in rat experimental autoimmune myocarditis. Clin. Sci (Lond)., 2002, 103, 623-632.
58. Renault, M.A.; Robbesyn, F.; Réant, P.; Douin, V.; Daret, D.; Allières, C.; Belloc, I.; Couffinhal, T.; Arnal, J.F.; Klingel, K.; Desgranges, C.; Dos Santos, P.; Charpentier, F.; Gadeau, A.P. Osteopontin Expression in Cardiomyocytes Induces Dilated Cardiomyopathy. Circ. Heart Fail, 2010, 3, 431-439.
59. Schnee, J.M.; Hsueh, W.A. Angiotensin II, adhesion, and cardiac fibrosis. Cardiovasc. Res., 2000, 46, 264-268.
60. Ashizawa, N.; Graf, K.; Do, Y.S.; Nunohiro, T.; Giachelli, C.M.; Meehan, W.P.; Tuan, T.L.; Hsueh, W.A. Osteopontin is produced by rat cardiac fibroblasts and mediates A (II)-induced DNA synthesis and collagen gel contraction. J. Clin. Invest., 1996, 98, 2218-2227.
61. Matsui, Y.; Jia, N.; Okamoto, H.; Kon, S.; Onozuka, H.; Akino, M.; Liu, L.; Morimoto, J.; Rittling, S.R.; Denhardt, D.; Kitabatake, A.; Uede, T. Role of osteopontin in cardiac fibrosis and remodeling in angiotensin II-induced cardiac hypertrophy. Hypertension, 2004, 43, 1195-1201.
62. Regitz-Zagrosek, V.; Leuchs, B.; Krülls-Münch, J.; Fleck, E. Angiotensin-converting enzyme inhibitors and beta-blockers in long-term treatment of dilated cardiomyopathy. Am. Heart J., 1995, 129, 754-761.
63. Baker, D.W.; Konstam, M.A.; Bottorff, M.; Pitt, B. Management of heart failure. I. Pharmacologic treatment. JAMA 1994, 272, 1361-1366.
64. Takada, H.; Kishimoto, C.; Hiraoka, Y.; Kurokawa, M.; Shiraki, K.; Sasayama, S. Captopril suppresses interstitial fibrin deposition in coxsackievirus B3 myocarditis. Am. J. Physiol., 1997, 272, H211-219.
65. Johnston, CI. Angiotensin II type 1 receptor blockade: a novel therapeutic concept. Blood Press, 2000, 1(suppl), 9-13.
66. Brilla, C.G.; Reams, G.P.; Maisch, B.; Weber, K.T. Reninangiotensin system and myocardial fibrosis in hypertension: regulation of the myocardial collagen matrix. Eur. Heart J., 1993, 14(Suppl J), 57-61.
67. Navalkar, S.; Parthasarathy, S.; Santanam, N.; Khan, B.V. Irbesartan, an angiotensin type 1 receptor inhibitor, regulates markers of inflammation in patients with premature atherosclerosis. J. Am. Coll. Cardiol., 2001, 37, 440-444.
68. Koh, K.K.; Ahn, J.Y.; Han, S.H.; Kim, D.S.; Jin, D.K.; Kim, H.S.; Shin, M.S.; Ahn, T.H.; Choi, I.S.; Shin, E.K. Pleiotropic effects of angiotensin II receptor blocker in hypertensive patients. J. Am. Coll. Cardiol., 2003, 42, 905-910.
69. Fliser, D.; Buchholz, K.; Haller, H. Antiinflammatory effects of angiotensin II subtype 1 receptor blockade in hypertensive patients with microinflammation. Circulation, 2004, 110, 1103-1107.