Immunopathogenesis of Myocarditis: The Interplay Between Cardiac Fibroblast Cells, Dendritic Cells, Macrophages and CD4+T Cells

Scandinavian Journal of Immunology

Volumn 82, Issue 1, 2015, Pages 1-9

  Amoah, B Prince ^a,b   Yang, H ^a   Zhang, P ^a   Su, Z ^a,c   Xu, H ^a  

^a JIANGSU UNIVERSITY   (China)

^b UNIVERSITY OF CAPE COAST   (Ghana)

^c The Fourth People's Hospital of Zhenjiang   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALVASCULIN; COLLAGEN RECEPTOR; DISCOIDIN DOMAIN RECEPTOR 1; DISCOIDIN DOMAIN RECEPTOR 2; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL INTERACTION; DENDRITIC CELL; DISEASE COURSE; HEART FIBROBLAST; HUMAN; IMMUNOPATHOGENESIS; INNATE IMMUNITY; MACROPHAGE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; TH1 CELL; TH17 CELL; TH2 CELL; TH22 CELL; FIBROBLAST; HEART MUSCLE CELL; IMMUNOLOGY; PATHOLOGY; TUMOR MICROENVIRONMENT;

CD4-POSITIVE T-LYMPHOCYTES; CELLULAR MICROENVIRONMENT; DENDRITIC CELLS; FIBROBLASTS; HUMANS; MACROPHAGES; MYOCARDITIS; MYOCYTES, CARDIAC;

EID: 84930973150     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/sji.12298     Document Type: Review

References (101)

1. O'Connell JB. The role of myocarditis in end-stage dilated cardiomyopathy. Tex Heart Inst J 1987;14:268.
2. Cooper LT Jr. Myocarditis. N Engl J Med 2009;360:1526-38.
3. Fairweather D, Rose NR. Coxsackievirus-induced myocarditis in mice: a model of autoimmune disease for studying immunotoxicity. Methods 2007;41:118-22.
4. Rose NR. Myocarditis: infection versus autoimmunity. J Clin Immunol 2009;29:730-7.
5. Kakkar R, Lee RT. Intramyocardial fibroblast myocyte communication. Circ Res 2010;106:47-57.
6. Souders CA, Bowers SLK, Baudino TA. Cardiac fibroblast the renaissance cell. Circ Res 2009;105:1164-76.
7. Brilla CG. Renin-angiotensin-aldosterone system and myocardial fibrosis. Cardiovasc Res 2000;47:1-3.
8. Camelliti P, Green C, Kohl P. Structural and Functional Coupling of Cardiac Myocytes and Fibroblasts, Vol. 42. Basel, Switzerland: Karger Publishers, 2006.
9. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6:392-401.
10. Moorman AF, Christoffels VM. Cardiac chamber formation: development, genes, and evolution. Physiol Rev 2003;83:1223-67.
11. Männer J, Perez-Pomares J, Macias D, Munoz-Chapuli R. The origin, formation and developmental significance of the epicardium: a review. Cells Tissues Organs 2001;169:89-103.
12. Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 2003;112:1776-84.
13. Wessels A, Pérez-Pomares J. The epicardium and epicardially derived cells (EPDCs) as cardiac stem cells. Anat Rec A Discov Mol Cell Evol Biol 2004;276:43-57.
14. Norris RA, Borg TK, Butcher JT, Baudino TA, Banerjee I, Markwald RR. Neonatal and adult cardiovascular pathophysiological remodeling and repair. Ann N Y Acad Sci 2008;1123:30-40.
15. Tzanidis A, Hannan RD, Thomas WG et al. Direct actions of urotensin II on the heart implications for cardiac fibrosis and hypertrophy. Circ Res 2003;93:246-53.
16. Weber KT. Monitoring tissue repair and fibrosis from a distance. Circulation 1997;96:2488-92.
17. Goldsmith EC, Hoffman A, Morales MO et al. Organization of fibroblasts in the heart. Dev Dyn 2004;230:787-94.
18. Okada H, Danoff TM, Kalluri R, Neilson EG. Early role of Fsp1 in epithelial-mesenchymal transformation. Am J Physiol Renal Physiol 1997;273:F563-74.
19. Zeisberg EM, Tarnavski O, Zeisberg M et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007;13:952-61.
20. Snider P, Standley KN, Wang J, Azhar M, Doetschman T, Conway SJ. Origin of cardiac fibroblasts and the role of periostin. Circ Res 2009;105:934-47.
21. Li YY, Feldman AM. Matrix metalloproteinases and myocardial remodeling in heart failure, Volume 1, 2003:157-189.
22. Liu H, Chen B, Lilly B. Fibroblasts potentiate blood vessel formation partially through secreted factor TIMP-1. Angiogenesis 2008;11:223-34.
23. Forbes M, Sperelakis N. The membrane systems and cytoskeletal elements of mammalian myocardial cells. In: Cell and Muscle Motility, Springer US, 1983:89-155.
24. Krenning G, Zeisberg EM, Kalluri R. The origin of fibroblasts and mechanism of cardiac fibrosis. J Cell Physiol 2010;225:631-7.
25. Hogaboam CM, Steinhauser ML, Chensue SW, Kunkel SL. Novel roles for chemokines and fibroblasts in interstitial fibrosis. Kidney Int 1998;54:2152-9.
26. Eghbali M, Blumenfeld O, Seifter S et al. Localization of types I, III and IV collagen mRNAs in rat heart cells by in situ hybridization. J Mol Cell Cardiol 1989;21:103-13.
27. Zhu J, Carver W. Effects of interleukin-33 on cardiac fibroblast gene expression and activity. Cytokine 2012;58:368-79.
28. Brodlie M, McKean M, Johnson G et al. Raised interleukin-17 is immunolocalised to neutrophils in cystic fibrosis lung disease. Eur Respir J 2011;37:1378-85.
29. Tapmeier TT, Fearn A, Brown K et al. Pivotal role of CD4+ T cells in renal fibrosis following ureteric obstruction. Kidney Int 2010;78:351-62.
30. Meneghin A, Hogaboam CM. Infectious disease, the innate immune response, and fibrosis. J Clin Invest 2007;117:530-8.
31. Díez J, Querejeta R, López B, González A, Larman M, Ubago JLM. Losartan-dependent regression of myocardial fibrosis is associated with reduction of left ventricular chamber stiffness in hypertensive patients. Circulation 2002;105:2512-7.
32. Long CS, Brown RD. The cardiac fibroblast, another therapeutic target for mending the broken heart? J Mol Cell Cardiol 2002;34:1273-8.
33. Querejeta R, López B, González A et al. Increased collagen type I synthesis in patients with heart failure of hypertensive origin relation to myocardial fibrosis. Circulation 2004;110:1263-8.
34. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-52.
35. Novak N, Koch S, Allam J-P, Bieber T. Dendritic cells: bridging innate and adaptive immunity in atopic dermatitis. J Allergy Clin Immunol 2010;125:50-9.
36. Reis e Sousa C. Activation of dendritic cells: translating innate into adaptive immunity. Curr Opin Immunol 2004;16:21-5.
37. Burchell JT, Strickland DH, Stumbles PA. The role of dendritic cells and regulatory T cells in the regulation of allergic asthma. Pharmacol Ther 2010;125:1-10.
38. Khan S, Greenberg JD, Bhardwaj N. Dendritic cells as targets for therapy in rheumatoid arthritis. Nat Rev Rheumatol 2009;5:566-71.
39. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007;449:419-26.
40. Randolph GJ, Ochando J, Partida-Sánchez S. Migration of dendritic cell subsets and their precursors. Annu Rev Immunol 2008;26:293-316.
41. Shortman K, Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 2006;7:19-30.
42. Kofler S, Petrakopoulou P, Grimm C, Kaczmarek I, Meiser BM, Weis M. Graft-infiltrating dendritic cells and coronary endothelial dysfunction after human heart transplantation. J Heart Lung Transplant 2008;27:387-93.
43. Schlichting C, Schareck W, Weis M. Renal ischemia-reperfusion injury: new implications of dendritic cell-endothelial cell interactions. In: Vol. 38, 3, edn. Transplantation Proceedings: 2006. Amsterdam: Elsevier, 2006:670-73.
44. Saalbach A, Klein C, Schirmer C, Briest W, Anderegg U, Simon JC. Dermal fibroblasts promote the migration of dendritic cells. J Invest Dermatol 2009;130:444-54.
45. Cooper LT Jr. Giant cell myocarditis: diagnosis and treatment. Herz 2000;25:291-8.
46. Theaker J, Gatter K, Heryet A, Evans D, McGee J. Giant cell myocarditis: evidence for the macrophage origin of the giant cells. J Clin Pathol 1985;38:160-4.
47. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 2013;229:176-85.
48. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009;27:451-83.
49. Bagnost T, Ma L, Da Silva RF et al. Cardiovascular effects of arginase inhibition in spontaneously hypertensive rats with fully developed hypertension. Cardiovasc Res 2010;87:569-77.
50. Meznarich J, Malchodi L, Helterline D et al. Urokinase plasminogen activator induces pro-fibrotic/m2 phenotype in murine cardiac macrophages. PLoS ONE 2013;8:e57837.
51. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011;11:723-37.
52. Sica A, Invernizzi P, Mantovani A. Macrophage plasticity and polarization in liver homeostasis and pathology. Hepatology 2014;59:2034-42.
53. Van Linthout S, Miteva K, Tschöpe C. Crosstalk between fibroblasts and inflammatory cells. Cardiovasc Res 2014;102:258-69.
54. Overall CM, Wrana J, Sodek J. Independent regulation of collagenase, 72-kDa progelatinase, and metalloendoproteinase inhibitor expression in human fibroblasts by transforming growth factor-beta. J Biol Chem 1989;264:1860-9.
55. Shah M, Foreman DM, Ferguson M. Neutralisation of TGF-beta 1 and TGF-beta 2 or exogenous addition of TGF-beta 3 to cutaneous rat wounds reduces scarring. J Cell Sci 1995;108:985-1002.
56. Koyanagi M, Egashira K, Kubo-Inoue M et al. Role of transforming growth factor-β1 in cardiovascular inflammatory changes induced by chronic inhibition of nitric oxide synthesis. Hypertension 2000;35:86-90.
57. Brønnum H, Eskildsen T, Andersen DC, Schneider M, Sheikh SP. IL-1β suppresses TGF-β-mediated myofibroblast differentiation in cardiac fibroblasts. Growth Factors 2013;31:81-9.
58. Meyer-ter-Vehn T, Gebhardt S, Sebald W et al. p38 inhibitors prevent TGF-β-induced myofibroblast transdifferentiation in human Tenon fibroblasts. Invest Ophthalmol Vis Sci 2006;47:1500-9.
59. Ikeuchi M, Tsutsui H, Shiomi T et al. Inhibition of TGF-β signaling exacerbates early cardiac dysfunction but prevents late remodeling after infarction. Cardiovasc Res 2004;64:526-35.
60. Okada H, Takemura G, Kosai K-I et al. Postinfarction gene therapy against transforming growth factor-β signal modulates infarct tissue dynamics and attenuates left ventricular remodeling and heart failure. Circulation 2005;111:2430-7.
61. van Amerongen MJ, Harmsen MC, van Rooijen N, Petersen AH, van Luyn MJ. Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol 2007;170:818-29.
62. Sullivan DE, Ferris M, Nguyen H, Abboud E, Brody AR. TNF-α induces TGF-β1 expression in lung fibroblasts at the transcriptional level via AP-1 activation. J Cell Mol Med 2009;13:1866-76.
63. Luedde T, Schwabe RF. NF-κB in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol 2011;8:108-18.
64. Matsumori A, Yamada T, Suzuki H, Matoba Y, Sasayama S. Increased circulating cytokines in patients with myocarditis and cardiomyopathy. Br Heart J 1994;72:561-6.
65. Levine B, Kalman J, Mayer L, Fillit HM, Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N Engl J Med 1990;323:236-41.
66. Wynn T. Cellular and molecular mechanisms of fibrosis. J Pathol 2008;214:199-210.
67. Seki E, De Minicis S, Österreicher CH et al. TLR4 enhances TGF-β signaling and hepatic fibrosis. Nat Med 2007;13:1324-32.
68. Yuan J, Yu M, Lin Q-W et al. Th17 cells contribute to viral replication in coxsackievirus B3-induced acute viral myocarditis. J Immunol 2010;185:4004-10.
69. Xie Y, Chen R, Zhang X et al. The role of Th17 cells and regulatory T cells in Coxsackievirus B3-induced myocarditis. Virology 2011;421:78-84.
70. Qing K, Weifeng W, Fan Y, Yuluan Y, Yu P, Yanlan H. Distinct different expression of Th17 and Th9 cells in coxsackie virus B3-induced mice viral myocarditis. Virol J 2011;8:267.
71. Nathan C, Prendergast TJ, Wiebe M et al. Activation of human macrophages. Comparison of other cytokines with interferon-gamma. J Exp Med 1984;160:600-5.
72. Piguet PF, Collart MA, Grau GE, Kapanci Y, Vassalli P. Tumor necrosis factor/cachectin plays a key role in bleomycin-induced pneumopathy and fibrosis. J Exp Med 1989;170:655-63.
73. Han Y-l, Li Y-L, Jia L-X et al. Reciprocal interaction between macrophages and T cells stimulates IFN-γ and MCP-1 production in Ang II-induced cardiac inflammation and fibrosis. PLoS ONE 2012;7:e35506.
74. Jimenez S, Freundlich B, Rosenbloom J. Selective inhibition of human diploid fibroblast collagen synthesis by interferons. J Clin Invest 1984;74:1112.
75. Shao DD, Suresh R, Vakil V, Gomer RH, Pilling D. Pivotal advance: Th-1 cytokines inhibit, and Th-2 cytokines promote fibrocyte differentiation. J Leukoc Biol 2008;83:1323-33.
76. 2-terminal kinase-dependent pathway. J Allergy Clin Immunol 2001;107:1001-8.
77. Bailey JR, Bland PW, Tarlton JF et al. IL-13 promotes collagen accumulation in Crohn's disease fibrosis by down-regulation of fibroblast MMP synthesis: a role for innate lymphoid cells? PLoS ONE 2012;7:e52332.
78. Feng W, Li W, Liu W, Wang F, Li Y, Yan W. IL-17 induces myocardial fibrosis and enhances RANKL/OPG and MMP/TIMP signaling in isoproterenol-induced heart failure. Exp Mol Pathol 2009;87:212-8.
79. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008;28:454-67.
80. Liu Y, Zhu H, Su Z et al. IL-17 contributes to cardiac fibrosis following experimental autoimmune myocarditis by a PKCβ/Erk1/2/NF-κB-dependent signaling pathway. Int Immunol 2012;24:605-12.
81. Xie Y, Li M, Wang X et al. In vivo delivery of adenoviral vector containing interleukin-17 receptor a reduces cardiac remodeling and improves myocardial function in viral myocarditis leading to dilated cardiomyopathy. PLoS ONE 2013;8:e72158.
82. Liao Y-H, Xia N, Zhou S-F et al. Interleukin-17A contributes to myocardial ischemia/reperfusion injury by regulating cardiomyocyte apoptosis and neutrophil infiltration. J Am Coll Cardiol 2012;59:420-9.
83. Yu M, Hu J, Zhu MX et al. Cardiac fibroblasts recruit Th17 cells infiltration into myocardium by secreting CCL20 in CVB3-induced acute viral myocarditis. Cell Physiol Biochem 2013;32:1437-50.
84. Su Z, Yin J, Wang T et al. Up-regulated HMGB1 in EAM directly led to collagen deposition by a PKCβ/Erk1/2-dependent pathway: cardiac fibroblast/myofibroblast might be another source of HMGB1. J Cell Mol Med 2014;18:1740-51.
85. Su Z, Sun C, Zhou C et al. HMGB1 blockade attenuates experimental autoimmune myocarditis and suppresses Th17-cell expansion. Eur J Immunol 2011;41:3586-95.
86. Duhen T, Geiger R, Jarrossay D, Lanzavecchia A, Sallusto F. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol 2009;10:857-63.
87. Eyerich S, Eyerich K, Pennino D et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 2009;119:3573-85.
88. Kong Q, Wu W, Yang F et al. Increased expressions of IL-22 and Th22 cells in the coxsackievirus B3-Induced mice acute viral myocarditis. Virol J 2012;9:232.
89. Chestovich PJ, Uchida Y, Chang W et al. IL-22: implications for liver ischemia/reperfusion injury. Transplantation 2012;93:485.
90. Zheng Y, Valdez PA, Danilenko DM et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008;14:282-9.
91. Sonnenberg GF, Fouser LA, Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 2011;12:383-90.
92. Chang H, Hanawa H, Liu H et al. Hydrodynamic-based delivery of an interleukin-22-Ig fusion gene ameliorates experimental autoimmune myocarditis in rats. J Immunol 2006;177:3635-43.
93. Fan Y, Weifeng W, Yuluan Y, Qing K, Yu P, Yanlan H. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of coxsackievirus b3-induced viral myocarditis reduces myocardium inflammation. Virol J 2011;8:17.
94. Liu Y-J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 2005;23:275-306.
95. Kanellakis P, Dinh TN, Agrotis A, Bobik A. CD4+ CD25+ Foxp3+ regulatory T cells suppress cardiac fibrosis in the hypertensive heart. J Hypertens 2011;29:1820-8.
96. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999;190:995-1004.
97. Rubtsov YP, Rasmussen JP, Chi EY et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008;28:546-58.
98. Samarakoon R, Overstreet JM, Higgins PJ. TGF-β signaling in tissue fibrosis: redox controls, target genes and therapeutic opportunities. Cell Signal 2013;25:264-8.
99. Cao Y, Xu W, Xiong S. Adoptive transfer of regulatory T cells protects against Coxsackievirus B3-induced cardiac fibrosis. PLoS ONE 2013;8:e74955.
100. Lee S-K, Seo S-H, Kim B-S et al. IFN-gamma regulates the expression of B7-H1 in dermal fibroblast cells. J Dermatol Sci 2005;40:95-103.
101. Fairweather D, Frisancho-Kiss S, Yusung SA et al. IL-12 protects against coxsackievirus B3-induced myocarditis by increasing IFN-γ and macrophage and neutrophil populations in the heart. J Immunol 2005;174:261-9.