Interleukin-17A is dispensable for myocarditis but essential for the progression to dilated cardiomyopathy

Circulation Research

Volumn 106, Issue 10, 2010, Pages 1646-1655

  Baldeviano, G Christian ^a,d   Barin, Jobert G ^c   Talor, Monica V ^a   Srinivasan, Sachin ^d   Bedja, Djahida ^b   Zheng, Dongfeng ^a   Gabrielson, Kathleen ^b   Iwakura, Yoichiro ^e   Rose, Noel R ^a,d   Cihakova, Daniela ^a  

^a Departments of Pathology   (United States)

^b Molecular and Comparative Pathobiology   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

Autoimmunity; Dilated cardiomyopathy; IL 17A; Myocarditis; Th17

Indexed keywords

CD11B ANTIGEN; GAMMA INTERFERON; GELATINASE; GELATINASE A; GELATINASE B; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDITIS; CELL POPULATION; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DRUG MECHANISM; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GRANULOCYTE; HEART MUSCLE FIBROSIS; HEART VENTRICLE FUNCTION; IMMUNOPATHOGENESIS; LYMPHOCYTIC INFILTRATION; MALE; MONOCYTE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; TH17 CELL; TISSUE SPECIFICITY; UPREGULATION; WILD TYPE;

ANIMALS; ANTIGENS, CD; CARDIOMYOPATHIES; CD4-POSITIVE T-LYMPHOCYTES; CHEMOKINES; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FLOW CYTOMETRY; IMMUNIZATION; INFLAMMATION; INTERLEUKIN-17; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCARDITIS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 77953021137     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.213157     Document Type: Article

References (45)

1. Cooper LT Jr. Myocarditis. N Engl J Med. 2009;360:1526-1538.
2. Cihakova D, Rose NR. Pathogenesis of myocarditis and dilated cardiomyopathy. Adv Immunol. 2008;99:95-114.
3. Rose NR. The significance of autoimmunity in myocarditis. Ernst Schering Res Found Workshop. 2006;(55):141-154.
4. Eriksson U, Kurrer MO, Schmitz N, Marsch SC, Fontana A, Eugster HP, Kopf M. Interleukin-6-deficient mice resist development of autoimmune myocarditis associated with impaired upregulation of complement C3. Circulation. 2003;107:320-325.
5. Bujak M, Frangogiannis NG. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res. 2007;74: 184-195.
6. Brauer PR. MM. Ps-role in cardiovascular development and disease. Front Biosci. 2006;11:447-478.
7. Spinale FG. Myocardial matrix remodeling and the matrix metallopro-teinases: influence on cardiac form and function. Physiol Rev. 2007;87: 1285-1342.
8. Gor DO, Rose NR, Greenspan NS. TH1-TH2: a procrustean paradigm. Nat Immunol. 2003;4:503-505.
9. + T cells in IFN-gamma knockout mice is associated with progression of myocarditis to heart failure. Proc Natl Acad Sci USA. 2005;102:180-185.
10. Afanasyeva M, Wang Y, Kaya Z, Stafford EA, Dohmen KM, Sadighi Akha AA, Rose NR. 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.
11. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 cells. Annu Rev Immunol. 2009;27:485-517.
12. Dong C. TH17 cells in development: An updated view of their molecular identity and genetic programming. Nat Rev Immunol. 2008;8:337-348.
13. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6: 1133-1141.
14. Steinman L. A rush to judgment on Th17. J Exp Med. 2008;205: 1517-1522.
15. Luger D, Silver PB, Tang J, Cua D, Chen Z, Iwakura Y, Bowman EP, Sgambellone NM, Chan CC, Caspi RR. Either a Th17 or a Th1 effector response can drive autoimmunity: conditions of disease induction affect dominant effector category. J Exp Med. 2008;205:799-810.
16. Komiyama Y, Nakae S, Matsuki T, Nambu A, Ishigame H, Kakuta S, Sudo K, Iwakura Y. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol. 2006;177: 566-573.
17. Haak S, Croxford AL, Kreymborg K, Heppner FL, Pouly S, Becher B, Waisman A. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J Clin Invest. 2009;119:61-69.
18. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, Homma I, Sekikawa K, Asano M, Iwakura Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity. 2002;17:375-387.
19. Cihakova D, Barin JG, Afanasyeva M, Kimura M, Fairweather D, Berg M, Talor MV, Baldeviano GC, Frisancho S, Gabrielson K, Bedja D, Rose NR. Interleukin-13 protects against experimental autoimmune myocarditis by regulating macrophage differentiation. Am J Pathol. 2008;172: 1195-1208.
20. Rangachari M, Mauermann N, Marty RR, Dirnhofer S, Kurrer MO, Komnenovic V, Penninger JM, Eriksson U. T-bet negatively regulates autoimmune myocarditis by suppressing local production of interleukin 17. J Exp Med. 2006;203:2009-2019.
21. Marta Toth, Rafael Fridman. Assessment of gelatinases (MMP-2 and MMP-9) by gelatin zymography. In: Brooks SA, Schumacher U, eds. Methods in Molecular Medicine: Metastasis Research Protocols. Volume I: Analysis of Cells and Tissues. Totowa, NJ: Humana Press; 2001:163: 163-174.
22. Yang XP, Liu YH, Rhaleb NE, Kurihara N, Kim HE, Carretero OA. Echocardiographic assessment of cardiac function in conscious and anesthetized mice. Am J Physiol. 1999;277:H1967-H1974.
23. Kubota T, McTiernan CF, Frye CS, Demetris AJ, Feldman AM. Cardiac-specific overexpression of tumor necrosis factor-alpha causes lethal myocarditis in transgenic mice. J Card Fail. 1997;3:117-124.
24. Tanaka T, Kanda T, McManus BM, Kanai H, Akiyama H, Sekiguchi K, Yokoyama T, Kurabayashi M. Overexpression of interleukin-6 aggravates viral myocarditis: Impaired increase in tumor necrosis factor-alpha. JMol Cell Cardiol. 2001;33:1627-1635.
25. Cornish T, Morgan J, Gurel B, De Marzo AM. FrIDA: an open source framework for image dataset analysis. Arch Pathol Lab Med. 2008;132: 854-855.
26. Gurel B, Iwata T, Koh CM, Jenkins RB, Lan F, Van Dang C, Hicks JL, Morgan J, Cornish TC, Sutcliffe S, Isaacs WB, Luo J, De Marzo AM. Nuclear MYC protein overexpression is an early alteration in human prostate carcinogenesis. Mod Pathol. 2008;21:1156-1167.
27. Doreau A, Belot A, Bastid J, Riche B, Trescol-Biemont MC, Ranchin B, Fabien N, Cochat P, Pouteil-Noble C, Trolliet P, Durieu I, Tebib J, Kassai B, Ansieau S, Puisieux A, Eliaou JF, Bonnefoy-Berard N. Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat Immunol. 2009;10:778-785.
28. Hsu HC, Yang P, Wang J, Wu Q, Myers R, Chen J, Yi J, Guentert T, Tousson A, Stanus AL, Le TV, Lorenz RG, Xu H, Kolls JK, Carter RH, Chaplin DD, Williams RW, Mountz JD. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol. 2008;9: 166-175.
29. Afanasyeva M, Georgakopoulos D, Belardi DF, Ramsundar AC, Barin JG, Kass DA, Rose NR. Quantitative analysis of myocardial inflammation by flow cytometry in murine autoimmune myocarditis: correlation with cardiac function. Am J Pathol. 2004;164:807-815.
30. Afanasyeva M, Georgakopoulos D, Rose NR. Autoimmune myocarditis: cellular mediators of cardiac dysfunction. Autoimmun Rev. 2004;3: 476-486.
31. Gallagher GL, Jackson CJ, Hunyor SN. Myocardial extracellular matrix remodeling in ischemic heart failure. Front Biosci. 2007;12:1410-1419.
32. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 2005;6:1123-1132.
33. O'Connor W Jr, Kamanaka M, Booth CJ, Town T, Nakae S, Iwakura Y, Kolls JK, Flavell RA. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol. 2009;10:603-609.
34. Sonderegger I, Rohn TA, Kurrer MO, Iezzi G, Zou Y, Kastelein RA, Bachmann MF, Kopf M. Neutralization of IL-17 by active vaccination inhibits IL-23-dependent autoimmune myocarditis. Eur J Immunol. 2006; 36:2849-2856.
35. Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y, Fujikado N, Tanahashi Y, Akitsu A, Kotaki H, Sudo K, Nakae S, Sasakawa C, Iwakura Y. Differential roles of interleukin-17A and-17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity. 2009;30:108-119.
36. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol. 2009;9:556-567.
37. McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, Cua DJ. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol. 2007;8:1390-1397.
38. Diaz JA, Booth AJ, Lu G, Wood SC, Pinsky DJ, Bishop DK. Critical role for IL-6 in hypertrophy and fibrosis in chronic cardiac allograft rejection. Am J Transplant. 2009;9:1773-1783.
39. Afanasyeva M, Wang Y, Kaya Z, Park S, Zilliox MJ, Schofield BH, Hill SL, Rose NR. Experimental autoimmune myocarditis in A/J mice is an interleukin-4-dependent disease with a Th2 phenotype. Am J Pathol. 2001;159:193-203.
40. Rouet-Benzineb P, Buhler JM, Dreyfus P, Delcourt A, Dorent R, Perennec J, Crozatier B, Harf A, Lafuma C. Altered balance between matrix gelatinases (MMP-2 and MMP-9) and their tissue inhibitors in human dilated cardiomyopathy: potential role of MMP-9 in myosin-heavy chain degradation. Eur J Heart Fail. 1999;1:337-352.
41. Matsumoto Y, Park IK, Kohyama K. Matrix metalloproteinase (MMP)-9, but not MMP-2, is involved in the development and progression of C protein-induced myocarditis and subsequent dilated cardiomyopathy. J Immunol. 2009;183:4773-4781.
42. Cortez DM, Feldman MD, Mummidi S, Valente AJ, Steffensen B, Vincenti M, Barnes JL, Chandrasekar B. IL-17 stimulates MMP-1 expression in primary human cardiac fibroblasts via p38 MAPK-and ERK1/2-dependent C/EBP-beta, NF-kappaB, and AP-1 activation. Am J Physiol Heart Circ Physiol. 2007;293:H3356-H3365.
43. Wilson MS, Madala SK, Ramalingam TR, Gochuico BR, Rosas IO, Cheever AW, Wynn TA. Bleomycin and IL-1{beta}-mediated pulmonary fibrosis is IL-17A dependent. J Exp Med. 2010;207:535-552.
44. Frustaci A, Russo MA, Chimenti C. Randomized study on the efficacy of immunosuppressive therapy in patients with virus-negative inflammatory cardiomyopathy: The TIMIC study. Eur Heart J. 2009;30:1995-2002.
45. Yi A, Jian L, Xiaojing H, Hui X. The prevalence of Th17 cells in patients with dilated cardiomyopathy. Clin Invest Med. 2009;32:E144-E150.