Interferon-γ protects against chronic viral myocarditis by reducing mast cell degranulation, fibrosis, and the profibrotic cytokines transforming growth factor-β1, interleukin-1β, and interleukin-4 in the heart

American Journal of Pathology

Volumn 165, Issue 6, 2004, Pages 1883-1894

  Fairweather, DeLisa ^a   Frisancho Kiss, Sylvia ^a   Yusung, Susy A ^a   Barrett, Masheka A ^a   Davis, Sarah E ^a   Gatewood, Shannon J L ^a   Njoku, Dolores B ^a   Rose, Noel R ^a,b  

^a DEPARTMENT OF PATHOLOGY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 4; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE COURSE; FIBROSIS; HEART; HISTAMINE BLOOD LEVEL; KNOCKOUT MOUSE; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; PERICARDITIS; PERICARDIUM; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; SURVIVAL; VIRUS MYOCARDITIS;

EID: 9644254471     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63241-5     Document Type: Article

References (71)

1. Cotran RS: Tissue repair: cellular growth, fibrosis, and wound healing. Robbins Pathologic Basis of Disease. Edited by RS Cotran, V Kumar, T Collins. Philadelphia, Saunders Co., 1999, pp 89-112
2. Lee CG, Homer RJ, Zhu Z, Lanone S, Wang X, Koteliansky V, Shipley JM, Gotwals P, Noble P, Chen Q, Senior RM, Elias JA: Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor β1. J Exp Med 2001, 194:809-821
3. Schultz JEJ, Witt SA, Glascock BJ, Nieman ML, Reiser PJ, Nix SL, Kimball TR, Doetschman T: TGF-β1 mediates the hypertrophic cardiomyocytes growth induced by angiotensin II. J Clin Invest 2002, 109:787-796
4. Kuwahara F, Kai H, Tokuda K, Kai M, Takeshita A, Egashira K, Imaizumi T: Transforming growth factor-β function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overloaded rats. Circulation 2002, 106:130-135
5. Bouzegrhane F, Thibault G: Is angiotensin II a proliferative factor of cardiac fibroblasts? Cardiovasc Res 2002, 53:304-312
6. Manabe I, Shindo T, Nagai R: Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy. Circ Res 2002, 91:1103-1113
7. 1 receptor upregulation enhances angiotensin II-mediated cardiac fibroblast responses that favor fibrosis. Circ Res 2002, 91:1119-1126
8. Feldman AM, McNamara D: Myocarditis. N Engl J Med 2000, 343:1388-1398
9. Fairweather D, Kaya Z, Shellam GR, Lawson CM, Rose NR: From infection to autoimmunity. J Autoimmun 2001, 16:175-186
10. Lane JR, Neumann DA, LaFond-Walker A, Herskowitz A, Rose NR: Interleukin 1 or tumor necrosis factor can promote Coxsackievirus B3-induced myocarditis in resistant B10.A mice. J Exp Med 1992, 175:1123-1129
11. Lane JR, Neumann DA, LaFond-Walker A, Herskowitz A, Rose NR: Role of IL-1 and tumor necrosis factor in Coxsackievirus-induced autoimmune myocarditis. J Immunol 1993, 151:1682-1690
12. Fairweather D, Yusung S, Frisancho-Kiss S, Barrett M, Gatewood S, Steele R, Rose NR: IL-12Rβ1 and TLR4 increase IL-1β and IL-18-associated myocarditis and Coxsackievirus replication. J Immunol 2003, 170:4731-4737
13. Ma X, Trinchieri G: Regulation of interleukin-12 production by antigen-presenting cells. Adv Immunol 2001, 79:55-92
14. Segal BM, Klinman DM, Shevach EM: Cutting edge: microbial products induce autoimmune disease by an IL-12-dependent pathway. J Immunol 1997, 158:5087-5090
15. Caspi RR: IL-12 in autoimmunity. Clin Immunol Immunopathol 1998, 88:4-13
16. Huber S, Shi C, Budd RC: Gammadelta T cells promote a Th1 response during Coxsackievirus B3 infection in vivo: role of Fas and Fas ligand. J Virol 1998, 76:6487-6494
17. O'Garra A: Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 1998, 8:275-283
18. Moser M, Murphy KM: Dendritic cell regulation of Th1-Th2 development. Nat Immunol 2000, 1:199-205
19. Gurujeyalakshmi G, Giri SN: Molecular mechanisms of antifibrotic effect of interferon gamma in bleomycin-mouse model of lung fibrosis: down-regulation of TGF-beta and procollagen I and III gene expression. Exp Lung Res 1995, 21:791-808
20. Oldroyd SD, Thomas GL, Gabbiani G, El Nahas AM: Interferon-γ inhibits experimental renal fibrosis. Kidney Int 1999, 56:2116-2127
21. Eickelberg O, Pansky A, Koehler E, Bihl M, Tamm M, Hildebrand P, Perruchoud AP, Kashgarian M, Roth M: Molecular mechanisms of TGF-(beta) antagonism by interferon (gamma) and cyclosporin A in lung fibroblasts. FASEB J 2001, 15:797-806
22. Schoen FJ: The heart. Robbins Pathologic Basis of Disease. Edited by RS Cotran, V Kumar, T Collins. Philadelphia, Saunders Co., 1999, pp 543-599
23. Kaya Z, Afanasyeva M, Wang Y, Dohmen KM, Schlichting J, Tretter T, Fairweather D, Holers VM, Rose NR: Contribution of the innate immune system to autoimmune myocarditis: a role for complement. Nat Immunol 2001, 2:739-745
24. Rose NR, Hill SL, Neumann DA: Experimental myocarditis. Autoimmune Disease Models: A Guidebook. San Diego, Academic Press, 1994, pp 175-189
25. Lenzo JC, Fairweather D, Cull V, Shellam GR, Lawson CM: Characterisation of murine cytomegalovirus myocarditis: cellular infiltration of the heart and virus persistence. J Mol Cell Cardiol 2002, 34:629-640
26. Fairweather D, Frisancho-Kiss S, Gatewood S, Njoku D, Steele R, Barrett M, Rose NR: Mast cells and innate cytokines are associated with susceptibility to autoimmune heart disease following Coxsackievirus B3 infection. Autoimmunity 2004, 37:131-145
27. Fairweather D, Rose NR: Type I diabetes: virus infection or autoimmune disease? Nat Immunol 2002, 3:338-340
28. Fairweather D, Afanasyeva M, Rose NR: Cellular immunity: a role for cytokines. The Handbook of Systemic Autoimmune Diseases: The Heart in Systemic Autoimmune Diseases. Edited by A Doria, P Pauletto. Amsterdam, Elsevier Science, 2004, pp 3-17
29. Wu C-Y, Faerrante J, Gately MK, Magram J: Characterization of IL-12 receptor β1 chain (IL-12Rβ1)-deficient mice: IL-12Rβ1 is an essential component of the functional mouse IL-12 receptor. J Immunol 1997, 159:1658-1665
30. 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-γ-independent pathway. Circulation 2001, 104:3145-3151
31. Li J-M, Brooks G: Differential protein expression and subcellular distribution of TGFβ1, β2 and β3 in cardiomyocytes during pressure overload-induced hypertrophy. J Mol Cell Cardiol 1997, 29:2213-2224
32. Clark DA, Coker R: Molecules in focus: transforming growth factor-beta (TGF-β). Int J Biochem Cell Biol 1998, 30:293-298
33. Letterio JJ, Roberts AB: Regulation of immune responses by TGF-β. Annu Rev Immunol 1998, 16:137-161
34. Attisano L, Wrana JL: Signal transduction by the TGF-β superfamily. Science 2002, 296:1646-1647
35. Li YY, McTiernan CF, Feldman AM: Proinflammatory cytokines regulate tissue inhibitors of metalloproteinases and disintegrin metalloproteinase in cardiac cells. Cardiovasc Res 1999, 42:162-172
36. Sano M, Fukuda K, Kodama H, Pan J, Saito M, Matsuzaki J, Takahashi T, Makino S, Kato T, Ogawa S: Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardiomyocytes. J Biol Chem 2000, 275:29717-29723
37. Blair RJ, Meng H, Marchese MJ, Ren S, Schwanz LB, Tonnesen MG, Gruber BL: Human mast cells stimulate vascular tube formation: tryptase is a novel, potent angiogenic factor. J Clin Invest 1997, 99:2691-2700
38. Cairns JA, Walls AF: Mast cell tryptase stimulates the synthesis of type I collagen in human lung fibroblasts. J Clin Invest 1997, 99:1313-1321
39. He S, Gaca MDA, Walls AF: The activation of synovial mast cells: modulation of histamine release by tryptase and chymase and their inhibitors. Eur J Pharmacol 2001, 412:223-229
40. Garbuzenko E, Nagler A, Piokholtz D, Gillery P, Reich R, Maquart F-X, Levi-Schaffer F: Human mast cells stimulate fibroblast proliferation, collagen synthesis and lattice contraction: a direct role for mast cells in skin fibrosis. Clin Exp Allergy 2002, 32:237-246
41. Dvorak AM: Mast cell degranulation in human hearts. N Engl J Med 1986, 315:969-970
42. Marone G, deCrescenzo G, Adt M, Patella V, Arbustini E, Genovese A: Immunological characterization and functional importance of human heart mast cells. Immunopharmacology 1995, 31:1-18
43. Arbustini E, Gavazzi A, Dal Bello B, Morbini P, Campana C, Diegli M, Grasso M, Fasani R, Banchieri N, Porcu E, Pilotto A, Ponzetta M, Bellin O, Lucreziotti S, Vigano M: Ten-year experience with endomyocardial biopsy in myocarditis presenting with congestive heart failure: frequency, pathologic characteristics, treatment and follow-up. G Ital Cardiol 1997, 27:209-223
44. Hara M, Ono K, Hwang M-W, Iwasaki A, Okada M, Nakatani K, Sasayama S, Matsumori A: Evidence for a role of mast cells in the evolution to congestive heart failure. J Exp Med 2002, 195:375-381
45. 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
46. Eriksson U, Kurrer MO, Bingisser R, Eugster HP, Saremaslani P, Follath F, Marsch S, Widmer U: Lethal autoimmune myocarditis in interferon-gamma receptor-deficient mice: enhanced disease severity by impaired inducible nitric oxide synthase induction. Circulation 2001, 103:18-21
47. Gor DO, Rose NR, Greenspan NS: Th1-Th2: a procrustean paradigm. Nat Immunol 2003, 4:503-505
48. Camoglio L, Juffermans NP, Peppelenbosch M, te Velde AA, ten Kate FJ, van Deventer SJH, Kopf M: Contrasting roles of IL-12p40 and IL-12p35 in the development of hapten-induced colitis. Eur J Immunol 2002, 32:261-269
49. Zhang G-X, Gran B, Yu S, Li J, Siglienti I, Chen X, Kamoun M, Rostami A: Induction of experimental autoimmune encephalomyelitis in IL-12 receptor-β2-deficient mice: IL-12 responsiveness is not required in the pathogenesis of inflammatory demyelination in the central nervous system. J Immunol 2003, 170:2153-2160
50. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD: Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748
51. Watford WT, O'Shea JJ: A case of mistaken identity. Nature 2003, 421:706-708
52. Fairweather D, Rose NR: Women and autoimmune diseases. Emerg Int Dis 2004, 10:2005-2011
53. Dinarello CA: Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int Rev Immunol 1998, 16:457-499
54. Joosten LA, Helsen MM, Saxne T, van De Loo FA, Heinegard D, van Den Berg WB: IL-1 alpha/beta blockade prevents cartilage and bone destruction in murine type II collagen-induced arthritis, whereas TNF-alpha blockade only ameliorates joint inflammation. J Immunol 1999, 163:5049-5055
55. Piccotti JR, Li K, Chan SY, Ferrante J, Magram J, Eichwald EJ, Bishop DK: Alloantigen-reactive Th1 development in IL-12-deficient mice. J Immunol 1998, 160:1132-1138
56. Frangogiannis NG, Smith CW, Entman ML: The inflammatory response in myocardial infarction. Cardiovasc Res 2002, 53:31-47
57. Hawkins RA, Claman HN, Clark RA, Steigerwald JC: Increased dermal mast cell populations in progressive systemic sclerosis: a link in chronic fibrosis? Ann Intern Med 1985, 102:182-186
58. Secor VH, Secor WE, Gutekunst C-A, Brown MA: Mast cells are essential for early onset and severe disease in a murine model of multiple sclerosis. J Exp Med 2000, 191:813-821
59. Woolley DE, Tetlow LC: Mast cell activation and its relation to proinflammatory cytokine production in the rheumatoid lesion. Arthritis Res 2000, 2:65-74
60. Lorentz A, Schuppan D, Gebert A, Manns MP, Bischoff SC: Regulatory effects of stem cell factor and interleukin-4 on adhesion of human mast cells to extracellular matrix proteins. Blood 2002, 99:966-972
61. Subramanian N, Bray MA: Interleukin 1 releases histamine from human basophils and mast cells in vitro. J Immunol 1987, 138:271-275
62. Strait RT, Morris SC, Smiley K, Urban Jr JF, Finkelman FD: IL-4 exacerbates anaphylaxis. J Immunol 2003, 170:3835-3842
63. Boyce JA: Mast cells: beyond IgE. J Allergy Clin Immunol 2003, 111:24-32
64. Prussin C, Metcalfe DD: IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol 2003, 111:S486-S494
65. Ahdieh M, Vandenbos T, Youakin A: Lung epithelial barrier function and wound healing are decreased by IL-4 and IL-13 and enhanced by IFN-γ. Am J Physiol 2001, 281:C2029-C2038
66. Selman M: A dark side of interferon-γ in the treatment of idiopathic pulmonary fibrosis? Am J Respir Crit Care Med 2003, 167:945-947
67. Wheeler DS, Kooy NW: A formidable challenge: the diagnosis and treatment of viral myocarditis in children. Crit Care Clin 2003, 19:365-391
68. Rafaeli Y, Van Parijs L, Alexander SI, Abbas AK: Interferon gamma is required for activation-induced death of T lymphocytes. J Exp Med 2002, 196:999-1005
69. Chu CQ, Wittmer S, Dalton DK: Failure to suppress the expansion of the activated CD4 T cell population in interferon gamma-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J Exp Med 2000, 192:123-128
70. Horwitz MS, La Cava A, Fine C, Rodriguez E, Ilic A, Sarvetnick N: Pancreatic expression of interferon-γ protects mice from lethal coxsackievirus B3 infection and subsequent myocarditis. Nat Med 2000, 6:693-697
71. Honore I, Nunes H, Groussard O, Kambouchner M, Chambellan A, Aubier M, Valeyre D, Crestani B: Acute respiratory failure after interferon-γ therapy of end-stage pulmonary fibrosis. Am J Resp Crit Care Med 2003, 167:953-957