Identification of novel mimicry epitopes for cardiac myosin heavy chain-α that induce autoimmune myocarditis in A/J mice

Cellular Immunology

Volumn 271, Issue 2, 2011, Pages 438-449

  Massilamany, Chandirasegaran ^a   Gangaplara, Arunakumar ^a   Steffen, David ^a   Reddy, Jay ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Antigens peptides; Autoimmunity; Inflammation; MHC; T cells

Indexed keywords

EPITOPE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 2; INTERLEUKIN 22; INTERLEUKIN 4; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN ALPHA[334-352]; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNE MYOCARDITIS; BACILLUS; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; CRYPTOCOCCUS NEOFORMANS; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; FEMALE; IMMUNOPATHOGENESIS; MAGNETOSPIRILLUM; MAIZE; MOLECULAR MIMICRY; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH17 CELL;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, FUNGAL; ANTIGENS, PLANT; AUTOIMMUNE DISEASES; BACILLUS; CARDIAC MYOSINS; CROSS REACTIONS; CRYPTOCOCCUS NEOFORMANS; CYTOKINES; EPITOPES; HISTOCOMPATIBILITY ANTIGENS CLASS II; MAGNETOSPIRILLUM; MICE; MICE, INBRED A; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; MYOCARDITIS; MYOSIN HEAVY CHAINS; T-LYMPHOCYTES; ZEA MAYS;

FILOBASIDIELLA NEOFORMANS; MAGNETOSPIRILLUM GRYPHISWALDENSE; MUS; ZEA MAYS;

EID: 80054017674     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2011.08.013     Document Type: Article

References (68)

1. Drory Y., Turetz Y., Hiss Y., Lev B., Fisman E.Z., Pines A., Kramer M.R. Sudden unexpected death in persons less than 40 years of age. Am. J. Cardiol. 1991, 68:1388-1392.
2. Brown C.A., O'Connell J.B. Myocarditis and idiopathic dilated cardiomyopathy. Am. J. Med. 1995, 99:309-314.
3. Fujinami R.S., von Herrath M.G., Christen U., Whitton J.L. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin. Microbiol. Rev. 2006, 19:80-94.
4. Taylor D.O., Edwards L.B., Boucek M.M., Trulock E.P., Aurora P., Christie J., Dobbels F., Rahmel A.O., Keck B.M., Hertz M.I. Registry of the international society for heart and lung transplantation: 24th official adult heart transplant report -- 2007. J. Heart Lung Transplant. 2007, 26:769-781.
5. W. Dec, Introduction to clinical myocarditis, in: L. Cooper, T. (Ed.), Myocarditis from Bench to Bedside, Humana Press, Totowa, New Jersey, 2003, pp. 257-281.
6. Bachmaier K., Neu N., de la Maza L.M., Pal S., Hessel A., Penninger J.M. Chlamydia infections and heart disease linked through antigenic mimicry. Science 1999, 283:1335-1339.
7. Cunningham M.W. T cell mimicry in inflammatory heart disease. Mol. Immunol. 2004, 40:1121-1127.
8. Kim K.S., Hufnagel G., Chapman N.M., Tracy S. The group B coxsackieviruses and myocarditis. Rev. Med. Virol. 2001, 11:355-368.
9. Lawson C.M. Evidence for mimicry by viral antigens in animal models of autoimmune disease including myocarditis. Cell. Mol. Life Sci. 2000, 57:552-560.
10. Bachmaier K., Penninger J.M. Chlamydia and antigenic mimicry. Curr. Top. Microbiol. Immunol. 2005, 296:153-163.
11. Fairweather D., Kaya Z., Shellam G.R., Lawson C.M., Rose N.R. From infection to autoimmunity. J. Autoimmun. 2001, 16:175-186.
12. Horwitz M.S., Knudsen M., Ilic A., Fine C., Sarvetnick N. Transforming growth factor-beta inhibits coxsackievirus-mediated autoimmune myocarditis. Viral. Immunol. 2006, 19:722-733.
13. Huber S.A. Autoimmunity in coxsackievirus B3 induced myocarditis. Autoimmunity 2006, 39:55-61.
14. Massilamany C., Steffen D., Reddy J. An epitope from Acanthamoeba castellanii that cross-react with proteolipid protein 139-151-reactive T cells induces autoimmune encephalomyelitis in SJL mice. J. Neuroimmunol. 2010, 219:17-24.
15. Miller S.D., Vanderlugt C.L., Begolka W.S., Pao W., Yauch R.L., Neville K.L., Katz-Levy Y., Carrizosa A., Kim B.S. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat. Med. 1997, 3:1133-1136.
16. Oldstone M.B. Molecular mimicry, microbial infection, and autoimmune disease: evolution of the concept. Curr. Top. Microbiol. Immunol. 2005, 296:1-17.
17. Rose N.R. Infection, mimics, and autoimmune disease. J. Clin. Invest. 2001, 107:943-944.
18. Li Y., Heuser J.S., Kosanke S.D., Hemric M., Cunningham M.W. Cryptic epitope identified in rat and human cardiac myosin S2 region induces myocarditis in the Lewis rat. J. Immunol. 2004, 172:3225-3234.
19. Gauntt C.J., Arizpe H.M., Higdon A.L., Rozek M.M., Crawley R., Cunningham M.W. Anti-coxsackievirus B3 neutralizing antibodies with pathological potential. Eur. Heart J. 1991, 12(Suppl. D):124-129.
20. Gauntt C.J., Arizpe H.M., Higdon A.L., Wood H.J., Bowers D.F., Rozek M.M., Crawley R. Molecular mimicry, anti-coxsackievirus B3 neutralizing monoclonal antibodies, and myocarditis. J. Immunol. 1995, 154:2983-2995.
21. Gauntt C.J., Higdon A.L., Arizpe H.M., Tamayo M.R., Crawley R., Henkel R.D., Pereira M.E., Tracy S.M., Cunningham M.W. Epitopes shared between coxsackievirus B3 (CVB3) and normal heart tissue contribute to CVB3-induced murine myocarditis. Clin. Immunol. Immunopathol. 1993, 68:129-134.
22. Ansari A.A., Wang Y.C., Danner D.J., Gravanis M.B., Mayne A., Neckelmann N., Sell K.W., Herskowitz A. Abnormal expression of histocompatibility and mitochondrial antigens by cardiac tissue from patients with myocarditis and dilated cardiomyopathy. Am. J. Pathol. 1991, 139:337-354.
23. Caforio A.L., Mahon N.J., McKenna W.J. Cardiac autoantibodies to myosin and other heart-specific autoantigens in myocarditis and dilated cardiomyopathy. Autoimmunity 2001, 34:199-204.
24. De Scheerder I.K., De Buyzere M., Delanghe J., Maas A., Clement D.L., Wieme R. Humoral immune response against contractile proteins (actin and myosin) during cardiovascular disease. Eur. Heart J. 1991, 12(Suppl. D):88-94.
25. Schultheiss H.P., Berg P., Klingenberg M. The mitochondrial adenine nucleotide translocator is an antigen in primary biliary cirrhosis. Clin. Exp. Immunol. 1983, 54:648-654.
26. Cunningham M.W. Cardiac myosin and the TH1/TH2 paradigm in autoimmune myocarditis. Am. J. Pathol. 2001, 159:5-12.
27. Cihakova D., Rose N.R. Pathogenesis of myocarditis and dilated cardiomyopathy. Adv. Immunol. 2008, 99:95-114.
28. Donermeyer D.L., Beisel K.W., Allen P.M., Smith S.C. Myocarditis-inducing epitope of myosin binds constitutively and stably to I-Ak on antigen-presenting cells in the heart. J. Exp. Med. 1995, 182:1291-1300.
29. S.C. Smith, P.M. Allen, Expression of myosin-class II major histocompatibility complexes in the normal myocardium occurs before induction of autoimmune myocarditis, Proc. Natl. Acad. Sci. USA 89 (1992) 9131-9135.
30. Guilherme L., Kalil J., Cunningham M. Molecular mimicry in the autoimmune pathogenesis of rheumatic heart disease. Autoimmunity 2006, 39:31-39.
31. Abel L.C., Kalil J., Cunha Neto E. Molecular mimicry between cardiac myosin and Trypanosoma cruzi antigen B13: identification of a B13-driven human T cell clone that recognizes cardiac myosin. Braz. J. Med. Biol. Res. 1997, 30:1305-1308.
32. Bonney K.M., Taylor J.M., Daniels M.D., Epting C.L., Engman D.M. Heat-killed Trypanosoma cruzi induces acute cardiac damage and polyantigenic autoimmunity. PLoS One 2011, 6:e14571.
33. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
34. Pummerer C.L., Luze K., Grassl G., Bachmaier K., Offner F., Burrell S.K., Lenz D.M., Zamborelli T.J., Penninger J.M., Neu N. Identification of cardiac myosin peptides capable of inducing autoimmune myocarditis in BALB/c mice. J. Clin. Invest. 1996, 97:2057-2062.
35. Afanasyeva M., Wang Y., Kaya Z., Park S., Zilliox M.J., Schofield B.H., Hill S.L., Rose N.R. Experimental autoimmune myocarditis in A/J mice is an interleukin-4-dependent disease with a Th2 phenotype. Am. J. Pathol. 2001, 159:193-203.
36. Smith S.C., Allen P.M. Myosin-induced acute myocarditis is a T cell-mediated disease. J. Immunol. 1991, 147:2141-2147.
37. Reddy J., Bettelli E., Nicholson L., Waldner H., Jang M.H., Wucherpfennig K.W., Kuchroo V.K. Detection of autoreactive myelin proteolipid protein 139-151-specific T cells by using MHC II (IAs) tetramers. J. Immunol. 2003, 170:870-877.
38. Day C.L., Seth N.P., Lucas M., Appel H., Gauthier L., Lauer G.M., Robbins G.K., Szczepiorkowski Z.M., Casson D.R., Chung R.T., Bell S., Harcourt G., Walker B.D., Klenerman P., Wucherpfennig K.W. Ex vivo analysis of human memory CD4 T cells specific for hepatitis C virus using MHC class II tetramers. J. Clin. Invest. 2003, 112:831-842.
39. Jang M.H., Seth N.P., Wucherpfennig K.W. Ex vivo analysis of thymic CD4 T cells in nonobese diabetic mice with tetramers generated from I-A(g7)/class II-associated invariant chain peptide precursors. J. Immunol. 2003, 171:4175-4186.
40. Hausmann D.H., Yu B., Hausmann S., Wucherpfennig K.W. pH-dependent peptide binding properties of the type I diabetes-associated I-Ag7 molecule: rapid release of CLIP at an endosomal pH. J. Exp. Med. 1999, 189:1723-1734.
41. Fugger L., Liang J., Gautam A., Rothbard J.B., McDevitt H.O. Quantitative analysis of peptides from myelin basic protein binding to the MHC class II protein, I-Au, which confers susceptibility to experimental allergic encephalomyelitis. Mol. Med. 1996, 2:181-188.
42. J. Reddy, Z. Illes, X. Zhang, J. Encinas, J. Pyrdol, L. Nicholson, R.A. Sobel, K.W. Wucherpfennig, V.K. Kuchroo, Myelin proteolipid protein-specific CD4+ CD25+ regulatory cells mediate genetic resistance to experimental autoimmune encephalomyelitis, Proc. Natl. Acad. Sci. USA 101 (2004) 15434-15439.
43. Massilamany C., Thulasingam S., Steffen D., Reddy J. Gender differences in CNS autoimmunity induced by mimicry epitope for PLP 139-151 in SJL mice. J. Neuroimmunol. 2011, 230:95-104.
44. Fremont D.H., Monnaie D., Nelson C.A., Hendrickson W.A., Unanue E.R. Crystal structure of I-Ak in complex with a dominant epitope of lysozyme. Immunity 1998, 8:305-317.
45. Lorenz R.G., Tyler A.N., Allen P.M. T cell recognition of bovine ribonuclease. Self/non-self discrimination at the level of binding to the I-Ak molecule. J. Immunol. 1988, 141:4124-4128.
46. Chang S.T., Ghosh D., Kirschner D.E., Linderman J.J. Peptide length-based prediction of peptide-MHC class II binding. Bioinformatics 2006, 22:2761-2767.
47. Esfandiarei M., McManus B.M. Molecular biology and pathogenesis of viral myocarditis. Annu. Rev. Pathol. 2008, 3:127-155.
48. Nussinovitch U., Shoenfeld Y. Autoimmunity and heart diseases: pathogenesis and diagnostic criteria. Arch. Immunol. Ther. Exp (Warsz). 2009, 57:95-104.
49. Whitton J.L., Feuer R. Myocarditis, microbes and autoimmunity. Autoimmunity 2004, 37:375-386.
50. Gravanis M.B., Sternby N.H. Incidence of myocarditis. A 10-year autopsy study from Malmo, Sweden. Arch. Pathol. Lab. Med. 1991, 115:390-392.
51. 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.
52. Pummerer C.L., Grassl G., Sailer M., Bachmaier K.W., Penninger J.M., Neu N. Cardiac myosin-induced myocarditis: target recognition by autoreactive T cells requires prior activation of cardiac interstitial cells. Lab. Invest. 1996, 74:845-852.
53. Kodama M., Matsumoto Y., Fujiwara M., Masani F., Izumi T., Shibata A. A novel experimental model of giant cell myocarditis induced in rats by immunization with cardiac myosin fraction. Clin. Immunol. Immunopathol. 1990, 57:250-262.
54. Liao L., Sindhwani R., Leinwand L., Diamond B., Factor S. Cardiac alpha-myosin heavy chains differ in their induction of myocarditis. Identification of pathogenic epitopes. J. Clin. Invest. 1993, 92:2877-2882.
55. Fairchild P.J., Wildgoose R., Atherton E., Webb S., Wraith D.C. An autoantigenic T cell epitope forms unstable complexes with class II MHC: a novel route for escape from tolerance induction. Int. Immunol. 1993, 5:1151-1158.
56. Joosten I., Wauben M.H., Holewijn M.C., Reske K., Pedersen L.O., Roosenboom C.F., Hensen E.J., van Eden W., Buus S. Direct binding of autoimmune disease related T cell epitopes to purified Lewis rat MHC class II molecules. Int. Immunol. 1994, 6:751-759.
57. Siefert J.L., Larios-Sanz M., Nakamura L.K., Slepecky R.A., Paul J.H., Moore E.R., Fox G.E., Jurtshuk P. Phylogeny of marine Bacillus isolates from the Gulf of Mexico. Curr. Microbiol. 2000, 41:84-88.
58. Blakemore R.P., Maratea D., Wolfe R.S. Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J. Bacteriol. 1979, 140:720-729.
59. Banerjee U., Gupta K., Venugopal P. A case of prosthetic valve endocarditis caused by Cryptococcus neoformans var. neoformans. J. Med. Vet. Mycol. 1997, 35:139-141.
60. Lafont A., Wolff M., Marche C., Clair B., Regnier B. Overwhelming myocarditis due to Cryptococcus neoformans in an AIDS patient. Lancet 1987, 2:1145-1146.
61. Lombardo T.A., Rabson A.S., Dodge H.T. Mycotic endocarditis; report of a case due to Cryptococcus neoformans. Am. J. Med. 1957, 22:664-670.
62. Weichel M., Glaser A.G., Ballmer-Weber B.K., Schmid-Grendelmeier P., Crameri R. Wheat and maize thioredoxins: a novel cross-reactive cereal allergen family related to baker's asthma. J. Allergy. Clin. Immunol. 2006, 117:676-681.
63. Aretz H.T., Billingham M.E., Edwards W.D., Factor S.M., Fallon J.T., Fenoglio J.J., Olsen E.G., Schoen F.J. Myocarditis. A histopathologic definition and classification. Am. J. Cardiovasc. Pathol. 1987, 1:3-14.
64. Cooper L.T., Berry G.J., Shabetai R. Idiopathic giant-cell myocarditis - natural history and treatment. Multicenter giant cell myocarditis study group investigators. N. Engl. J. Med. 1997, 336:1860-1866.
65. Edwards W.D., Holmes D.R., Reeder G.S. Diagnosis of active lymphocytic myocarditis by endomyocardial biopsy: quantitative criteria for light microscopy. Mayo Clin. Proc. 1982, 57:419-425.
66. Galiuto L., Enriquez-Sarano M., Reeder G.S., Tazelaar H.D., Li J.T., Miller F.A., Gleich G.J. Eosinophilic myocarditis manifesting as myocardial infarction: early diagnosis and successful treatment. Mayo Clin. Proc. 1997, 72:603-610.
67. Daniels M.D., Hyland K.V., Wang K., Engman D.M. Recombinant cardiac myosin fragment induces experimental autoimmune myocarditis via activation of Th1 and Th17 immunity. Autoimmunity 2008, 41:490-499.
68. Izumi T., Takehana H., Matsuda C., Yokoyama H., Kohno K., Suzuki K., Inomata T. Experimental autoimmune myocarditis and its pathomechanism. Herz. 2000, 25:274-278.