Vaccination with Flt3L-induced CD8α+ dendritic cells prevents CD4+ T helper cell-mediated experimental autoimmune myocarditis

Vaccine

Volumn 31, Issue 42, 2013, Pages 4802-4811

  Valaperti, Alan ^a,b   Nishii, Mototsugu ^b,c   Germano, Davide ^a,d   Liu, Peter P ^b   Eriksson, Urs ^a,e  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF TORONTO   (Canada)

^c KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d NOVARTIS PHARMA AG   (Switzerland)

^e Division of Cardiology GZO Zurich Regional Health Center   (Switzerland)

Author keywords

Autoimmunity; Dendritic cells; Flt3L; Myocarditis; Th1; Th17

Indexed keywords

DENDRITIC CELL VACCINE; FLT3 LIGAND; FREUND ADJUVANT; GAMMA INTERFERON; INTERLEUKIN 12P35; INTERLEUKIN 17; MYOSIN HEAVY CHAIN ALPHA; OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL AUTOIMMUNE MYOCARDITIS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HELPER CELL; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; VACCINATION;

AUTOIMMUNITY; CD4(+) T HELPER; DENDRITIC CELLS; EAM; EXPERIMENTAL AUTOIMMUNE MYOCARDITIS; FLT3L; FMS-LIKE TYROSINE KINASE 3 LIGAND; MYHC; MYOCARDITIS; MYOSIN HEAVY-CHAIN; TH; TH1; TH17;

ANIMALS; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; INTERFERON-GAMMA; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MYOCARDITIS; T-LYMPHOCYTES, HELPER-INDUCER; VACCINATION;

EID: 84884209020     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.07.084     Document Type: Article

References (50)

1. Eriksson U., Penninger J.M. Autoimmune heart failure: new understandings of pathogenesis. Int J Biochem Cell Biol 2005, 37:27-32.
2. Feldman A.M., McNamara D. Myocarditis. N Engl J Med 2000, 343:1388-1398.
3. Calabrese F., Thiene G. Myocarditis and inflammatory cardiomyopathy: microbiological and molecular biological aspects. Cardiovasc Res 2003, 60:11-25.
4. Caforio A.L., Bonifacio E., Stewart J.T., Neglia D., Parodi O., Bottazzo G.F., et al. Novel organ-specific circulating cardiac autoantibodies in dilated cardiomyopathy. J Am Coll Cardiol 1990, 15:1527-1534.
5. Frustaci A., Chimenti C., Calabrese F., Pieroni M., Thiene G., Maseri A. Immunosuppressive therapy for active lymphocytic myocarditis: virological and immunologic profile of responders versus nonresponders. Circulation 2003, 107:857-863.
6. 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.
7. Sonderegger I., Rohn T.A., Kurrer M.O., Iezzi G., Zou Y., Kastelein R.A., et al. Neutralization of IL-17 by active vaccination inhibits IL-23-dependent autoimmune myocarditis. Eur J Immunol 2006, 36:2849-2856.
8. Valaperti A., Marty R.R., Kania G., Germano D., Mauermann N., Dirnhofer S., et al. CD11b+ monocytes abrogate Th17 CD4+ T cell-mediated experimental autoimmune myocarditis. J Immunol 2008, 180:2686-2695.
9. Baldeviano G.C., Barin J.G., Talor M.V., 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.
10. Neu N., Rose N.R., Beisel K.W., Herskowitz A., Gurri-Glass G., Craig S.W. Cardiac myosin induces myocarditis in genetically predisposed mice. J Immunol 1987, 139:3630-3636.
11. Eriksson U., Kurrer M.O., Schmitz N., Marsch S.C., Fontana A., Eugster H.P., et al. Interleukin-6-deficient mice resist development of autoimmune myocarditis associated with impaired upregulation of complement C3. Circulation 2003, 107:320-325.
12. Fairweather D., Frisancho-Kiss S., Yusung S.A., Barrett M.A., Davis S.E., Steele R.A., et al. 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.
13. Afanasyeva M., Wang Y., Kaya Z., Stafford E.A., Dohmen K.M., Sadighi Akha A.A., et al. Interleukin-12 receptor/STAT4 signaling is required for the development of autoimmune myocarditis in mice by an interferon-gamma-independent pathway. Circulation 2001, 104:3145-3151.
14. Eriksson U., Kurrer M.O., Sebald W., Brombacher F., Kopf M. Dual role of the IL-12/IFN-gamma axis in the development of autoimmune myocarditis: induction by IL-12 and protection by IFN-gamma. J Immunol 2001, 167:5464-5469.
15. Eriksson U., Kurrer M.O., Bingisser R., Eugster H.P., Saremaslani P., Follath F., et al. Lethal autoimmune myocarditis in interferon-gamma receptor-deficient mice: enhanced disease severity by impaired inducible nitric oxide synthase induction. Circulation 2001, 103:18-21.
16. Fairweather D., Yusung S., Frisancho S., Barrett M., Gatewood S., Steele R., et al. IL-12 receptor beta 1 and Toll-like receptor 4 increase IL-1 beta- and IL-18-associated myocarditis and coxsackievirus replication. J Immunol 2003, 170:4731-4737.
17. Negishi H., Osawa T., Ogami K., Ouyang X., Sakaguchi S., Koshiba R., et al. A critical link between Toll-like receptor 3 and type II interferon signaling pathways in antiviral innate immunity. Proc Natl Acad Sci U S A 2008, 105:20446-20451.
18. Nindl V., Maier R., Ratering D., De Giuli R., Zust R., Thiel V., et al. Cooperation of Th1 and Th17 cells determines transition from autoimmune myocarditis to dilated cardiomyopathy. Eur J Immunol 2012, 42:2311-2321.
19. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005, 6:1123-1132.
20. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., et al. A distinct lineage of CD4T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005, 6:1133-1141.
21. Stockinger B., Veldhoen M. Differentiation and function of Th17T cells. Curr Opin Immunol 2007, 19:281-286.
22. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392(March (6673)):245-252.
23. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000, 18:767-811.
24. Lanzavecchia A., Sallusto F. The instructive role of dendritic cells on T cell responses: lineages, plasticity and kinetics. Curr Opin Immunol 2001, 13:291-298.
25. Guermonprez P., Valladeau J., Zitvogel L., Thery C., Amigorena S. Antigen presentation and T cell stimulation by dendritic cells. Annu Rev Immunol 2002, 20:621-667.
26. Eriksson U., Ricci R., Hunziker L., Kurrer M.O., Oudit G.Y., Watts T.H., et al. Dendritic cell-induced autoimmune heart failure requires cooperation between adaptive and innate immunity. Nat Med 2003, 9:1484-1490.
27. Steinman R.M., Hawiger D., Nussenzweig M.C. Tolerogenic dendritic cells. Annu Rev Immunol 2003, 21:685-711.
28. Lutz M.B., Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity. Trends Immunol 2002, 23:445-449.
29. Eriksson U., Kurrer M.O., Sonderegger I., Iezzi G., Tafuri A., Hunziker L., et al. Activation of dendritic cells through the interleukin 1 receptor 1 is critical for the induction of autoimmune myocarditis. J Exp Med 2003, 197:323-331.
30. Marty R.R., Dirnhofer S., Mauermann N., Schweikert S., Akira S., Hunziker L., et al. MyD88 signaling controls autoimmune myocarditis induction. Circulation 2006, 113:258-265.
31. Tang J., Zhu W., Silver P.B., Su S.B., Chan C.C., Caspi R.R. Autoimmune uveitis elicited with antigen-pulsed dendritic cells has a distinct clinical signature and is driven by unique effector mechanisms: initial encounter with autoantigen defines disease phenotype. J Immunol 2007, 178:5578-5587.
32. Kania G., Siegert S., Behnke S., Prados-Rosales R., Casadevall A., Luscher T.F., et al. Innate signalling promotes formation of regulatory nitric oxide-producing dendritic cells limiting T cell expansion in experimental autoimmune myocarditis. Circulation 2013, 127:2285-2294.
33. Maraskovsky E., Brasel K., Teepe M., Roux E.R., Lyman S.D., Shortman K., et al. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 1996, 184:1953-1962.
34. Pulendran B., Smith J.L., Caspary G., Brasel K., Pettit D., Maraskovsky E., et al. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc Natl Acad Sci U S A 1999, 96:1036-1041.
35. Maldonado-Lopez R., De Smedt T., Michel P., Godfroid J., Pajak B., Heirman C., et al. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J Exp Med 1999, 189:587-592.
36. De Smedt T., Butz E., Smith J., Maldonado-Lopez R., Pajak B., Moser M., et al. CD8alpha(-) and CD8alpha(+) subclasses of dendritic cells undergo phenotypic and functional maturation in vitro and in vivo. J Leukoc Biol 2001, 69:951-958.
37. Maekawa Y., Tsukumo S., Chiba S., Hirai H., Hayashi Y., Okada H., et al. Delta1-Notch3 interactions bias the functional differentiation of activated CD4+ T cells. Immunity 2003, 19:549-559.
38. Ito T., Schaller M., Hogaboam C.M., Standiford T.J., Sandor M., Lukacs N.W., et al. TLR9 regulates the mycobacteria-elicited pulmonary granulomatous immune response in mice through DC-derived Notch ligand delta-like 4. J Clin Invest 2009, 119:33-46.
39. Littman D.R., Rudensky A.Y. Th17 and regulatory T cells in mediating and restraining inflammation. Cell 2010, 140:845-858.
40. Huber S.A., Lodge P.A. Coxsackievirus B-3 myocarditis. Identification of different pathogenic mechanisms in DBA/2 and Balb/c mice. Am J Pathol 1986, 122:284-291.
41. Peng H., Yang X.P., Carretero O.A., Nakagawa P., D'Ambrosio M., Leung P., et al. Angiotensin II-induced dilated cardiomyopathy in Balb/c but not C57BL/6J mice. Exp Physiol 2011, 96:756-764.
42. Sawitzki B., Kingsley C.I., Oliveira V., Karim M., Herber M., Wood K.J. IFN-gamma production by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo. J Exp Med 2005, 201:1925-1935.
43. Ono M., Shimizu J., Miyachi Y., Sakaguchi S. Control of autoimmune myocarditis and multiorgan inflammation by glucocorticoid-induced TNF receptor family-related protein (high), Foxp3-expressing CD25+ and CD25- regulatory T cells. J Immunol 2006, 176:4748-4756.
44. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 cells. Annu Rev Immunol 2009, 27:485-517.
45. Codarri L., Gyulveszi G., Tosevski V., Hesske L., Fontana A., Magnenat L., et al. RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat Immunol 2011, 12:560-567.
46. Bettelli E., Oukka M., Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007, 8:345-350.
47. Frucht D.M., Fukao T., Bogdan C., Schindler H., O'Shea J.J., Koyasu S. IFN-gamma production by antigen-presenting cells: mechanisms emerge. Trends Immunol 2001, 22:556-560.
48. Ohteki T., Fukao T., Suzue K., Maki C., Ito M., Nakamura M., et al. Interleukin 12-dependent interferon gamma production by CD8alpha+ lymphoid dendritic cells. J Exp Med 1999, 189:1981-1986.
49. Boonstra A., Asselin-Paturel C., Gilliet M., Crain C., Trinchieri G., Liu Y.J., et al. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J Exp Med 2003, 197:101-109.
50. Ueno H., Klechevsky E., Morita R., Aspord C., Cao T., Matsui T., et al. Dendritic cell subsets in health and disease. Immunol Rev 2007, 219:118-142.