Coxsackievirus B3 infection leads to the generation of cardiac myosin heavy chain-α-reactive CD4 T cells in A/J mice

Clinical Immunology

Volumn 144, Issue 3, 2012, Pages 237-249

  Gangaplara, Arunakumar ^a   Massilamany, Chandirasegaran ^a   Brown, Deborah M ^b   Delhon, Gustavo ^a   Pattnaik, Asit K ^a   Chapman, Nora ^c   Rose, Noel ^d   Steffen, David ^a   Reddy, Jay ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

Autoimmunity; ; Autoreactive T cells; ; Cardiac myosin heavy chain ; ; Coxsackievirus B3; ; MHC class II dextramers; Myocarditis;

Indexed keywords

INTERLEUKIN 17; MYOSIN HEAVY CHAIN ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CARDIOVASCULAR SYSTEM; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; COXSACKIE VIRUS B; COXSACKIE VIRUS INFECTION; IMMUNE RESPONSE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; STAINING;

ANIMALS; AUTOIMMUNITY; CARDIAC MYOSINS; CARDIOMYOPATHY, DILATED; CD4-POSITIVE T-LYMPHOCYTES; CERCOPITHECUS AETHIOPS; COXSACKIEVIRUS INFECTIONS; ENTEROVIRUS B, HUMAN; HEART; INTERLEUKIN-17; MICE; MYOCARDITIS; MYOSIN HEAVY CHAINS; VERO CELLS;

EID: 84864359627     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2012.07.003     Document Type: Article

References (54)

1. Heidenreich P.A., Trogdon J.G., Khavjou O.A., Butler J., Dracup K., Ezekowitz M.D., Finkelstein E.A., Hong Y., Johnston S.C., Khera A., Lloyd-Jones D.M., Nelson S.A., Nichol G., Orenstein D., Wilson P.W., Woo Y.J. Forecasting the future of cardiovascular disease in the United States: a policy statement from the American Heart Association. Circulation 2011, 123:933-944.
2. 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.
3. 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.
4. Cihakova D., Rose N.R. Pathogenesis of myocarditis and dilated cardiomyopathy. Adv. Immunol. 2008, 99:95-114.
5. 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.
6. Neu N., Klieber R., Fruhwirth M., Berger P. Cardiac myosin-induced myocarditis as a model of postinfectious autoimmunity. Eur. Heart J. 1991, 12(Suppl. D):117-120.
7. Neumann D.A., Lane J.R., LaFond-Walker A., Allen G.S., Wulff S.M., Herskowitz A., Rose N.R. Heart-specific autoantibodies can be eluted from the hearts of Coxsackievirus B3-infected mice. Clin. Exp. Immunol. 1991, 86:405-412.
8. Rose N.R., Wolfgram L.J., Herskowitz A., Beisel K.W. Postinfectious autoimmunity: two distinct phases of coxsackievirus B3-induced myocarditis. Ann. N. Y. Acad. Sci. 1986, 475:146-156.
9. Kim K.S., Tracy S., Tapprich W., Bailey J., Lee C.K., Kim K., Barry W.H., Chapman N.M. 5'-Terminal deletions occur in coxsackievirus B3 during replication in murine hearts and cardiac myocyte cultures and correlate with encapsidation of negative-strand viral RNA. J. Virol. 2005, 79:7024-7041.
10. Pauschinger M., Phan M.D., Doerner A., Kuehl U., Schwimmbeck P.L., Poller W., Kandolf R., Schultheiss H.P. Enteroviral RNA replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation 1999, 99:889-895.
11. Li H.S., Ligons D.L., Rose N.R. Genetic complexity of autoimmune myocarditis. Autoimmun. Rev. 2008, 7:168-173.
12. Fousteri G., Dave A., Morin B., Omid S., Croft M., von Herrath M.G. Nasal cardiac myosin peptide treatment and OX40 blockade protect mice from acute and chronic virally-induced myocarditis. J. Autoimmun. 2011, 36:210-220.
13. Estrin M., Huber S.A. Coxsackievirus B3-induced myocarditis. Autoimmunity is L3T4+ T helper cell and IL-2 independent in BALB/c mice. Am. J. Pathol. 1987, 127:335-341.
14. Huber S.A., Lodge P.A. Coxsackievirus B-3 myocarditis in Balb/c mice. Evidence for autoimmunity to myocyte antigens. Am. J. Pathol. 1984, 116:21-29.
15. Huber S.A., Sartini D., Exley M. Vgamma4(+) T cells promote autoimmune CD8(+) cytolytic T-lymphocyte activation in coxsackievirus B3-induced myocarditis in mice: role for CD4(+) Th1 cells. J. Virol. 2002, 76:10785-10790.
16. 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.
17. Reed L.J., Muench H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 1938, 27:493-497.
18. 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.
19. Massilamany C., Gangaplara A., Steffen D., Reddy J. Identification of novel mimicry epitopes for cardiac myosin heavy chain-alpha that induce autoimmune myocarditis in A/J mice. Cell. Immunol. 2011, 271:438-449.
20. 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.
21. 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.
22. Massilamany C., Upadhyaya B., Gangaplara A., Kuszynski C., Reddy J. Detection of autoreactive CD4 T cells using major histocompatibility complex class II dextramers. BMC Immunol. 2011, 12:40.
23. Massilamany C., Gangaplara A., Chapman N., Rose N., Reddy J. Detection of cardiac myosin heavy chain-alpha-specific CD4 cells by using MHC class II/IA(k) tetramers in A/J mice. J. Immunol. Methods 2011, 372:107-118.
24. Wang J., Okazaki I.M., Yoshida T., Chikuma S., Kato Y., Nakaki F., Hiai H., Honjo T., Okazaki T. PD-1 deficiency results in the development of fatal myocarditis in MRL mice. Int. Immunol. 2010, 22:443-452.
25. 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.
26. Loudon R.P., Moraska A.F., Huber S.A., Schwimmbeck P., Schultheiss P. An attenuated variant of Coxsackievirus B3 preferentially induces immunoregulatory T cells in vivo. J. Virol. 1991, 65:5813-5819.
27. Fujimoto C., Yu C.R., Shi G., Vistica B.P., Wawrousek E.F., Klinman D.M., Chan C.C., Egwuagu C.E., Gery I. Pertussis toxin is superior to TLR ligands in enhancing pathogenic autoimmunity, targeted at a neo-self antigen, by triggering robust expansion of Th1 cells and their cytokine production. J. Immunol. 2006, 177:6896-6903.
28. Agarwal R.K., Sun S.H., Su S.B., Chan C.C., Caspi R.R. Pertussis toxin alters the innate and the adaptive immune responses in a pertussis-dependent model of autoimmunity. J. Neuroimmunol. 2002, 129:133-140.
29. Powell T.J., Brown D.M., Hollenbaugh J.A., Charbonneau T., Kemp R.A., Swain S.L., Dutton R.W. CD8+ T cells responding to influenza infection reach and persist at higher numbers than CD4+ T cells independently of precursor frequency. Clin. Immunol. 2004, 113:89-100.
30. Namba K., Ogasawara K., Kitaichi N., Matsuki N., Takahashi A., Sasamoto Y., Kotake S., Matsuda H., Iwabuchi K., Ohno S., Onoe K. Identification of a peptide inducing experimental autoimmune uveoretinitis (EAU) in H-2Ak-carrying mice. Clin. Exp. Immunol. 1998, 111:442-449.
31. 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.
32. Kaya Z., Goser S., Buss S.J., Leuschner F., Ottl R., Li J., Volkers M., Zittrich S., Pfitzer G., Rose N.R., Katus H.A. Identification of cardiac troponin I sequence motifs leading to heart failure by induction of myocardial inflammation and fibrosis. Circulation 2008, 118:2063-2072.
33. Wolfgram L.J., Beisel K.W., Herskowitz A., Rose N.R. Variations in the susceptibility to Coxsackievirus B3-induced myocarditis among different strains of mice. J. Immunol. 1986, 136:1846-1852.
34. Rose N.R., Hill S.L. The pathogenesis of postinfectious myocarditis. Clin. Immunol. Immunopathol. 1996, 80:S92-S99.
35. Huber S. Tumor necrosis factor-alpha promotes myocarditis in female mice infected with coxsackievirus B3 through upregulation of CD1d on hematopoietic cells. Viral. Immunol. 2010, 23:79-86.
36. Tateyama M. Mechanism of suppression of colchicine in experimental allergic encephalomyelitis. Hokkaido Igaku Zasshi 1988, 63:72-79.
37. 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.
38. Jager A., Dardalhon V., Sobel R.A., Bettelli E., Kuchroo V.K. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 2009, 183:7169-7177.
39. Fan Y., Weifeng W., Yuluan Y., Qing K., Yu P., Yanlan H. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of coxsackievirus b3-induced viral myocarditis reduces myocardium inflammation. Virol. J. 2011, 8:17.
40. Opavsky M.A., Penninger J., Aitken K., Wen W.H., Dawood F., Mak T., Liu P. Susceptibility to myocarditis is dependent on the response of alphabeta T lymphocytes to coxsackieviral infection. Circ. Res. 1999, 85:551-558.
41. Henke A., Huber S., Stelzner A., Whitton J.L. The role of CD8+ T lymphocytes in coxsackievirus B3-induced myocarditis. J. Virol. 1995, 69:6720-6728.
42. Domingues H.S., Mues M., Lassmann H., Wekerle H., Krishnamoorthy G. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS One 2010, 5:e15531.
43. Fairweather D., Frisancho-Kiss S., Yusung S.A., Barrett M.A., Davis S.E., Steele R.A., Gatewood S.J., Rose N.R. 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.
44. Horwitz M.S., La Cava A., Fine C., Rodriguez E., Ilic A., Sarvetnick N. Pancreatic expression of interferon-gamma protects mice from lethal coxsackievirus B3 infection and subsequent myocarditis. Nat. Med. 2000, 6:693-697.
45. Li J., Leschka S., Rutschow S., Schwimmbeck P.L., Husmann L., Noutsias M., Westermann D., Poller W., Zeichhardt H., Klingel K., Tschope C., Schultheiss H.P., Pauschinger M. Immunomodulation by interleukin-4 suppresses matrix metalloproteinases and improves cardiac function in murine myocarditis. Eur. J. Pharmacol. 2007, 554:60-68.
46. Hofmann P., Schmidtke M., Stelzner A., Gemsa D. Suppression of proinflammatory cytokines and induction of IL-10 in human monocytes after coxsackievirus B3 infection. J. Med. Virol. 2001, 64:487-498.
47. Henke A., Mohr C., Sprenger H., Graebner C., Stelzner A., Nain M., Gemsa D. Coxsackievirus B3-induced production of tumor necrosis factor-alpha, IL-1 beta, and IL-6 in human monocytes. J. Immunol. 1992, 148:2270-2277.
48. Seko Y., Takahashi N., Yagita H., Okumura K., Yazaki Y. Expression of cytokine mRNAs in murine hearts with acute myocarditis caused by coxsackievirus b3. J. Pathol. 1997, 183:105-108.
49. Baldeviano G.C., Barin J.G., Talor M.V., Srinivasan S., Bedja D., Zheng D., Gabrielson K., Iwakura Y., Rose N.R., Cihakova D. Interleukin-17A is dispensable for myocarditis but essential for the progression to dilated cardiomyopathy. Circ. Res. 2010, 106:1646-1655.
50. Fairweather D., Rose N.R. Coxsackievirus-induced myocarditis in mice: a model of autoimmune disease for studying immunotoxicity. Methods 2007, 41:118-122.
51. Tracy S., Hofling K., Pirruccello S., Lane P.H., Reyna S.M., Gauntt C.J. Group B coxsackievirus myocarditis and pancreatitis: connection between viral virulence phenotypes in mice. J. Med. Virol. 2000, 62:70-81.
52. Nakamura H., Yamamoto T., Yamamura T., Nakao F., Umemoto S., Shintaku T., Yamaguchi K., Liu P., Matsuzaki M. Repetitive coxsackievirus infection induces cardiac dilatation in post-myocarditic mice. Jpn. Circ. J. 1999, 63:794-802.
53. Cunningham M.W. T cell mimicry in inflammatory heart disease. Mol. Immunol. 2004, 40:1121-1127.
54. McMahon E.J., Bailey S.L., Castenada C.V., Waldner H., Miller S.D. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat. Med. 2005, 11:335-339.