Lack of IL-6 during coxsackievirus infection heightens the early immune response resulting in increased severity of chronic autoimmune myocarditis

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Poffenberger, Maya C ^a   Straka, Nadine ^a   El Warry, Nahida ^a   Fang, Dianne ^a   Shanina, Iryna ^a   Horwitz, Marc S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; CXCL9 CHEMOKINE; INTERLEUKIN 10; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; RECOMBINANT INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNE DISEASE; CELL INFILTRATION; CHRONIC INFLAMMATION; CONTROLLED STUDY; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; CYTOKINE PRODUCTION; DISEASE CONTROL; DISEASE SEVERITY; HEART PROTECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; IMMUNOREGULATION; MACROPHAGE MIGRATION; MONOCYTE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION; VIRUS MYOCARDITIS; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CHRONIC DISEASE; ENTEROVIRUS; GENETICS; HOSPITALIZATION; IMMUNOLOGY; MOUSE MUTANT; MYOCARDITIS; PATHOPHYSIOLOGY; PHYSIOLOGY; VIROLOGY;

COXSACKIEVIRUS; MUS;

ANIMALS; AUTOIMMUNE DISEASES; CHRONIC DISEASE; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDITIS; RECOMBINANT PROTEINS; SEVERITY OF ILLNESS INDEX; VIRUS REPLICATION;

EID: 67749099899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006207     Document Type: Article

References (36)

1. Brown CA, O'Connell JB (1995) Myocarditis and idiopathic dilated cardiomyopathy. Am J Med 99: 309-314.
2. Eriksson U, Kurrer MO, Schmitz N, Marsch SC, Fontana A, et al. (2003) Interleukin-6-deficient mice resist development of autoimmune myocarditis associated with impaired upregulation of complement C3. Circulation 107: 320-325.
3. Kanda T, McManus JE, Nagai R, Imai S, Suzuki T, et al. (1996) Modification of viral myocarditis in mice by interleukin-6. Circ Res 78: 848-856.
4. Kanda T, Takahashi T (2004) Interleukin-6 and cardiovascular diseases. Jpn Heart J 45: 183-193.
5. Tanaka T, Kanda T, McManus BM, Kanai H, Akiyama H, et al. (2001) Overexpression of interleukin-6 aggravates viral myocarditis: impaired increase in tumor necrosis factor-alpha. J Mol Cell Cardiol 33: 1627-1635.
6. Kopf M, Ramsay A, Brombacher F, Baumann H, Freer G, et al. (1995) Pleiotropic defects of IL-6-deficient mice including early hematopoiesis, T and B cell function, and acute phase responses. Ann N Y Acad Sci 762: 308-318.
7. Pasare C, Medzhitov R (2003) Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 299: 1033-1036.
8. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, et al. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
9. Korn T, Bettelli E, Gao W, Awasthi A, Jager A, et al. (2007) IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448: 484-487.
10. Yajima T, Yasukawa H, Jeon ES, Xiong D, Dorner A, et al. (2006) Innate defense mechanism against virus infection within the cardiac myocyte requiring gp130-STAT3 signaling. Circulation 114: 2364-2373.
11. Samoilova EB, Horton JL, Hilliard B, Liu TS, Chen Y (1998) IL-6-deficient mice are resistant to experimental autoimmune encephalomyelitis: roles of IL-6 in the activation and differentiation of autoreactive T cells. J Immunol 161: 6480-6486.
12. Richards HB, Satoh M, Shaw M, Libert C, Poli V, et al. (1998) Interleukin 6 dependence of anti-DNA antibody production: evidence for two pathways of autoantibody formation in pristane-induced lupus. J Exp Med 188: 985-990.
13. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, et al. (1998) Interleukin 6 is required for the development of collagen-induced arthritis. J Exp Med 187: 461-468.
14. Ohshima S, Saeki Y, Mima T, Sasai M, Nishioka K, et al. (1998) Interleukin 6 plays a key role in the development of antigen-induced arthritis. Proc Natl Acad Sci U S A 95: 8222-8226.
15. Deng C, Goluszko E, Tuzun E, Yang H, Christadoss P (2002) Resistance to experimental autoimmune myasthenia gravis in IL-6-deficient mice is associated with reduced germinal center formation and C3 production. J Immunol 169: 1077-1083.
16. Horwitz MS, La Cava A, Fine C, Rodriguez E, Ilic A, et al. (2000) Pancreatic expression of interferon-gamma protects mice from lethal coxsackievirus B3 infection and subsequent myocarditis. Nat Med 6: 693-697.
17. Lane JR, Neumann DA, Lafond-Walker A, Herskowitz A, Rose NR (1991) LPS promotes CB3-induced myocarditis in resistant B10.A mice. Cell Immunol 136: 219-233.
18. Shen Y, Xu W, Chu YW, Wang Y, Liu QS, et al. (2004) Coxsackievirus group B type 3 infection upregulates expression of monocyte chemoattractant protein 1 in cardiac myocytes, which leads to enhanced migration of mononuclear cells in viral myocarditis. J Virol 78: 12548-12556.
19. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, et al. (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342.
20. Richer M, Poffenberger MC, Horwitz MS (2007) Early inflammatory responses direct chronic autoimmunity development in the heart following coxsackievirus infection. Future Virology 2: 283-291.
21. Blackburn SD, Wherry EJ (2007) IL-10, T cell exhaustion and viral persistence. Trends Microbiol 15: 143-146.
22. Girndt M, Kohler H (2003) Interleukin-10 (IL-10): an update on its relevance for cardiovascular risk. Nephrol Dial Transplant 18: 1976-1979.
23. Bettelli E, Nicholson LB, Kuchroo VK (2003) IL-10, a key effector regulatory cytokine in experimental autoimmune encephalomyelitis. J Autoimmun 20: 265-267.
24. Watanabe K, Nakazawa M, Fuse K, Hanawa H, Kodama M, et al. (2001) Protection against autoimmune myocarditis by gene transfer of interleukin-10 by electroporation. Circulation 104: 1098-1100.
25. Hofmann P, Schmidtke M, Stelzner A, Gemsa D (2001) Suppression of proinflammatory cytokines and induction of IL-10 in human monocytes after coxsackievirus B3 infection. J Med Virol 64: 487-498.
26. Nishii M, Inomata T, Takehana H, Takeuchi I, Nakano H, et al. (2004) Serum levels of interleukin-10 on admission as a prognostic predictor of human fulminant myocarditis. J Am Coll Cardiol 44: 1292-1297.
27. Gluck B, Schmidtke M, Merkle I, Stelzner A, Gemsa D (2001) Persistent expression of cytokines in the chronic stage of CVB3-induced myocarditis in NMRI mice. J Mol Cell Cardiol 33: 1615-1626.
28. Schmidtke M, Gluck B, Merkle I, Hofmann P, Stelzner A, et al. (2000) Cytokine profiles in heart, spleen, and thymus during the acute stage of experimental coxsackievirus B3-induced chronic myocarditis. J Med Virol 61: 518-526.
29. Lane JR, Neumann DA, Lafond-Walker A, Herskowitz A, Rose NR (1992) Interleukin 1 or tumor necrosis factor can promote Coxsackie B3-induced myocarditis in resistant B10.A mice. J Exp Med 175: 1123-1129.
30. Kubota T, McTiernan CF, Frye CS, Demetris AJ, Feldman AM (1997) Cardiac-specific overexpression of tumor necrosis factor-alpha causes lethal myocarditis in transgenic mice. J Card Fail 3: 117-124.
31. Calabrese F, Carturan E, Chimenti C, Pieroni M, Agostini C, et al. (2004) Overexpression of tumor necrosis factor (TNF)alpha and TNFalpha receptor I in human viral myocarditis: clinicopathologic correlations. Mod Pathol 17: 1108-1118.
32. Zhao HF, Ito T, Gibo J, Kawabe K, Oono T, et al. (2005) Anti-monocyte chemoattractant protein 1 gene therapy attenuates experimental chronic pancreatitis induced by dibutyltin dichloride in rats. Gut 54: 1759-1767.
33. Rollins BJ, Yoshimura T, Leonard EJ, Pober JS (1990) Cytokine-activated human endothelial cells synthesize and secrete a monocyte chemoattractant, MCP-1/JE. Am J Pathol 136: 1229-1233.
34. Rollins BJ (1997) Chemokines. Blood 90: 909-928.
35. Goser S, Ottl R, Brodner A, Dengler TJ, Torzewski J, et al. (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.
36. Kolattukudy PE, Quach T, Bergese S, Breckenridge S, Hensley J, et al. (1998) Myocarditis induced by targeted expression of the MCP-1 gene in murine cardiac muscle. Am J Pathol 152: 101-111.