Nasal cardiac myosin peptide treatment and OX40 blockade protect mice from acute and chronic virally-induced myocarditis

Journal of Autoimmunity

Volumn 36, Issue 3-4, 2011, Pages 210-220

  Fousteri, Georgia ^a   Dave, Amy ^a   Morin, Bret ^a   Omid, Shaida ^a   Croft, Michael ^a   von Herrath, Matthias G ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Autoimmune myocarditis; Cardiac myosin; Coxsackie virus B3; IL 10; OX40; Peptide therapy; Treg

Indexed keywords

CARDIAC MYOSIN; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OX40 LIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; HEART PROTECTION; IMMUNOPATHOLOGY; MALE; MORTALITY; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RECEPTOR BLOCKING; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; VIRUS MYOCARDITIS;

ACUTE DISEASE; ADMINISTRATION, INTRANASAL; ANIMALS; AUTOIMMUNE DISEASES; CARDIAC MYOSINS; CHRONIC DISEASE; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; INTERLEUKIN-10; MALE; MICE; MICE, INBRED BALB C; MYOCARDITIS; RECEPTORS, OX40; SPLEEN; T-LYMPHOCYTES, REGULATORY;

EID: 79954882375     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2011.01.006     Document Type: Article

References (60)

1. Afanasyeva M., Georgakopoulos D., Rose N.R. Autoimmune myocarditis: cellular mediators of cardiac dysfunction. Autoimmun Rev 2004, 3:476-486.
2. Leuschner F., Katus H.A., Kaya Z. Autoimmune myocarditis: past, present and future. J Autoimmun 2009, 33:282-289.
3. Rose N.R., Herskowitz A., Neumann D.A. Autoimmunity in myocarditis: models and mechanisms. Clin Immunol Immunopathol 1993, 68:95-99.
4. Taqueti V.R., Mitchell R.N., Lichtman A.H. Protecting the pump: controlling myocardial inflammatory responses. Annu Rev Physiol 2006, 68:67-95.
5. Cihakova D., Rose N.R. Pathogenesis of myocarditis and dilated cardiomyopathy. Adv Immunol 2008, 99:95-114.
6. + T lymphocytes in coxsackievirus B3-induced myocarditis. J Virol 1995, 69:6720-6728.
7. Huber S.A., Gauntt C.J., Sakkinen P. Enteroviruses and myocarditis: viral pathogenesis through replication, cytokine induction, and immunopathogenicity. Adv Virus Res 1998, 51:35-80.
8. Fairweather D., Rose N.R. Coxsackievirus-induced myocarditis in mice: a model of autoimmune disease for studying immunotoxicity. Methods 2007, 41:118-122.
9. Cihakova D., Sharma R.B., Fairweather D., Afanasyeva M., Rose N.R. Animal models for autoimmune myocarditis and autoimmune thyroiditis. Methods Mol Med 2004, 102:175-193.
10. Neu N., Beisel K.W., Traystman M.D., Rose N.R., Craig S.W. Autoantibodies specific for the cardiac myosin isoform are found in mice susceptible to Coxsackievirus B3-induced myocarditis. J Immunol 1987, 138:2488-2492.
11. Neumann D.A., Lane J.R., LaFond-Walker A., Allen G.S., Wulff S.M., Herskowitz A., et al. Heart-specific autoantibodies can be eluted from the hearts of Coxsackievirus B3-infected mice. Clin Exp Immunol 1991, 86:405-412.
12. Neumann D.A., Rose N.R., Ansari A.A., Herskowitz A. Induction of multiple heart autoantibodies in mice with coxsackievirus B3- and cardiac myosin-induced autoimmune myocarditis. J Immunol 1994, 152:343-350.
13. Lane J.R., Neumann D.A., Lafond-Walker A., Herskowitz A., Rose N.R. LPS promotes CB3-induced myocarditis in resistant B10.A mice. Cell Immunol 1991, 136:219-233.
14. Pummerer C.L., Luze K., Grassl G., Bachmaier K., Offner F., Burrell S.K., et al. Identification of cardiac myosin peptides capable of inducing autoimmune myocarditis in BALB/c mice. J Clin Invest 1996, 97:2057-2062.
15. Nagler-Anderson C., Terhoust C., Bhan A.K., Podolsky D.K. Mucosal antigen presentation and the control of tolerance and immunity. Trends Immunol 2001, 22:120-122.
16. Mestecky J., Russell M.W., Elson C.O. Perspectives on mucosal vaccines: is mucosal tolerance a barrier?. J Immunol 2007, 179:5633-5638.
17. von Herrath M.G., Harrison L.C. Antigen-induced regulatory T cells in autoimmunity. Nat Rev Immunol 2003, 3:223-232.
18. Gonnella P.A., Del Nido P.J., McGowan F.X. Oral tolerization with cardiac myosin peptide (614-629) ameliorates experimental autoimmune myocarditis: role of STAT 6 genes in BALB/CJ mice. J Clin Immunol 2009, 29:434-443.
19. Kaya Z., Dohmen K.M., Wang Y., Schlichting J., Afanasyeva M., Leuschner F., et al. Cutting edge: a critical role for IL-10 in induction of nasal tolerance in experimental autoimmune myocarditis. J Immunol 2002, 168:1552-1556.
20. Huber S.A. Coxsackievirus B3-induced myocarditis: infection of females during the estrus phase of the ovarian cycle leads to activation of T regulatory cells. Virology 2008, 378:292-298.
21. 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.
22. Bachmaier K., Pummerer C., Kozieradzki I., Pfeffer K., Mak T.W., Neu N., et al. Low-molecular-weight tumor necrosis factor receptor p55 controls induction of autoimmune heart disease. Circulation 1997, 95:655-661.
23. Poffenberger M.C., Straka N., El Warry N., Fang D., Shanina I., Horwitz M.S. Lack of IL-6 during coxsackievirus infection heightens the early immune response resulting in increased severity of chronic autoimmune myocarditis. PLoS One 2009, 4:e6207.
24. Seko Y., Ishiyama S., Nishikawa T., Kasajima T., Hiroe M., Suzuki S., et al. Expression of tumor necrosis factor ligand superfamily costimulatory molecules CD27L, CD30L, OX40L and 4-1BBL in the heart of patients with acute myocarditis and dilated cardiomyopathy. Cardiovasc Pathol 2002, 11:166-170.
25. Seko Y., Takahashi N., Oshima H., Shimozato O., Akiba H., Kobata T., et al. Expression of tumour necrosis factor (TNF) receptor/ligand superfamily co-stimulatory molecules CD40, CD30L, CD27L, and OX40L in murine hearts with chronic ongoing myocarditis caused by coxsackie virus B3. J Pathol 1999, 188:423-430.
26. Seko Y., Takahashi N., Oshima H., Shimozato O., Akiba H., Takeda K., et al. Expression of tumour necrosis factor (TNF) ligand superfamily co-stimulatory molecules CD30L, CD27L, OX40L, and 4-1BBL in murine hearts with acute myocarditis caused by Coxsackievirus B3. J Pathol 2001, 195:593-603.
27. Filippi C.M., Estes E.A., Oldham J.E., von Herrath M.G. Immunoregulatory mechanisms triggered by viral infections protect from type 1 diabetes in mice. J Clin Invest 2009, 119:1515-1523.
28. Fousteri G, Dave A, Bot A, Juntti T, Omid S, von Herrath M. Subcutaneous insulin B:9-23/IFA immunisation induces Tregs that control late-stage prediabetes in NOD mice through IL-10 and IFNgamma. Diabetologia 2010; 53:1958-1970.
29. Chatzidakis I., Fousteri G., Tsoukatou D., Kollias G., Mamalaki C. An essential role for TNF in modulating thresholds for survival, activation, and tolerance of CD8+ T cells. J Immunol 2007, 178:6735-6745.
30. Seko Y., Takahashi N., Azuma M., Yagita H., Okumura K., Yazaki Y. Expression of costimulatory molecule CD40 in murine heart with acute myocarditis and reduction of inflammation by treatment with anti-CD40L/B7-1 monoclonal antibodies. Circ Res 1998, 83:463-469.
31. Seko Y., Takahashi N., Azuma M., Yagita H., Okumura K., Yazaki Y. Effects of in vivo administration of anti-B7-1/B7-2 monoclonal antibodies on murine acute myocarditis caused by coxsackievirus B3. Circ Res 1998, 82:613-618.
32. Haga T., Suzuki J., Kosuge H., Ogawa M., Saiki H., Haraguchi G., et al. Attenuation of experimental autoimmune myocarditis by blocking T cell activation through 4-1BB pathway. J Mol Cell Cardiol 2009, 46:719-727.
33. Baldeviano GC, Barin JG, Talor MV, Srinivasan S, Bedja D, Zheng D, et al. Interleukin-17A is dispensable for myocarditis but essential for the progression to dilated cardiomyopathy. Circ Res 2010; 106:1646-1655.
34. Feldman A.M., McNamara D. Myocarditis. N Engl J Med 2000, 343:1388-1398.
35. Guilherme L, Kalil J. Rheumatic fever and rheumatic heart disease: cellular mechanisms leading autoimmune reactivity and disease. J Clin Immunol 2010; 30:17-23.
36. Kuhl U., Pauschinger M., Seeberg B., Lassner D., Noutsias M., Poller W., et al. Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation 2005, 112:1965-1970.
37. Neumann D.A., Burek C.L., Baughman K.L., Rose N.R., Herskowitz A. Circulating heart-reactive antibodies in patients with myocarditis or cardiomyopathy. J Am Coll Cardiol 1990, 16:839-846.
38. Fousteri G., von Herrath M., Bresson D. Mucosal exposure to antigen: cause or cure of type 1 diabetes?. Curr Diab Rep 2007, 7:91-98.
39. Collins L.V., Eriksson K., Ulrich R.G., Tarkowski A. Mucosal tolerance to a bacterial superantigen indicates a novel pathway to prevent toxic shock. Infect Immun 2002, 70:2282-2287.
40. Rangachari M., Mauermann N., Marty R.R., Dirnhofer S., Kurrer M.O., Komnenovic V., et al. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J Exp Med 2006, 203:2009-2019.
41. George Chandy A., Hultkrantz S., Raghavan S., Czerkinsky C., Lebens M., Telemo E., Holmgren J. Oral tolerance induction by mucosal administration of cholera toxin B-coupled antigen involves T-cell proliferation in vivo and is not affected by depletion of CD25+ T cells. Immunology 2006, 118:311-320.
42. Alvarez D., Swirski F.K., Yang T.C., Fattouh R., Croitoru K., Bramson J.L., et al. Inhalation tolerance is induced selectively in thoracic lymph nodes but executed pervasively at distant mucosal and nonmucosal tissues. J Immunol 2006, 176:2568-2580.
43. Battaglia M., Gianfrani C., Gregori S., Roncarolo M.G. IL-10-producing T regulatory type 1 cells and oral tolerance. Ann N Y Acad Sci 2004, 1029:142-153.
44. Ejrnaes M., Filippi C.M., Martinic M.M., Ling E.M., Togher L.M., Crotty S., et al. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J Exp Med 2006, 203:2461-2472.
45. Brooks D.G., Trifilo M.J., Edelmann K.H., Teyton L., McGavern D.B., Oldstone M.B. Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 2006, 12:1301-1309.
46. Brooks D.G., Walsh K.B., Elsaesser H., Oldstone M.B. IL-10 directly suppresses CD4 but not CD8 T cell effector and memory responses following acute viral infection. Proc Natl Acad Sci U S A 2010, 107:3018-3023.
47. Nohara C., Akiba H., Nakajima A., Inoue A., Koh C.S., Ohshima H., et al. Amelioration of experimental autoimmune encephalomyelitis with anti-OX40 ligand monoclonal antibody: a critical role for OX40 ligand in migration, but not development, of pathogenic T cells. J Immunol 2001, 166:2108-2115.
48. Zhang Z, Rosenbaum JT, Zhong W, Lim C, Hinrichs DJ. Costimulation of Th17 cells: adding fuel or putting out the fire in the inflamed gut? Semin Immunopathol 2010; 32:55-70.
49. Croft M. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity?. Nat Rev Immunol 2003, 3:609-620.
50. Kotani A., Hori T., Matsumura Y., Uchiyama T. Signaling of gp34 (OX40 ligand) induces vascular endothelial cells to produce a CC chemokine RANTES/CCL5. Immunol Lett 2002, 84:1-7.
51. Kawai T., Seki M., Hiromatsu K., Eastcott J.W., Watts G.F., Sugai M., et al. Selective diapedesis of Th1 cells induced by endothelial cell RANTES. J Immunol 1999, 163:3269-3278.
52. Ford M.L., Larsen C.P. Translating costimulation blockade to the clinic: lessons learned from three pathways. Immunol Rev 2009, 229:294-306.
53. Futamatsu H., Suzuki J., Kosuge H., Yokoseki O., Kamada M., Ito H., et al. Attenuation of experimental autoimmune myocarditis by blocking activated T cells through inducible costimulatory molecule pathway. Cardiovasc Res 2003, 59:95-104.
54. Seko Y., Takahashi N., Ishiyama S., Nishikawa T., Kasajima T., Hiroe M., et al. Expression of costimulatory molecules B7-1, B7-2, and CD40 in the heart of patients with acute myocarditis and dilated cardiomyopathy. Circulation 1998, 97:637-639.
55. Imura A., Hori T., Imada K., Ishikawa T., Tanaka Y., Maeda M., et al. The human OX40/gp34 system directly mediates adhesion of activated T cells to vascular endothelial cells. J Exp Med 1996, 183:2185-2195.
56. + T regulatory cells. J Immunol 2008, 181:8650-8659.
57. Gramaglia I., Weinberg A.D., Lemon M., Croft M. Ox-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. J Immunol 1998, 161:6510-6517.
58. + T cells. J Immunol 2007, 179:1427-1430.
59. Griseri T., Asquith M., Thompson C., Powrie F. OX40 is required for regulatory T cell-mediated control of colitis. J Exp Med 2010, 207:699-709.
60. Piconese S., Pittoni P., Burocchi A., Gorzanelli A., Care A., Tripodo C., et al. A non-redundant role for OX40 in the competitive fitness of Treg in response to IL-2. Eur J Immunol 2010, 40:2902-2913.