Regulatory T cells protect mice against coxsackievirus-induced myocarditis through the transforming growth factor β-coxsackie-adenovirus receptor pathway

Circulation

Volumn 121, Issue 24, 2010, Pages 2624-2634

  Shi, Yu ^a   Fukuoka, Masahiro ^a   Li, Guohua ^a   Liu, Youan ^a   Chen, Manyin ^a   Konviser, Michael ^a   Chen, Xin ^a   Opavsky, Mary Anne ^b   Liu, Peter P ^a,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c CANADIAN INSTITUTES OF HEALTH RESEARCH   (Canada)

Author keywords

cardiomyopathy; coxsackieviruses B; heart failure; inflammation; myocarditis; viruses

Indexed keywords

CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFER; COXSACKIE VIRUS; HEART PROTECTION; HISTOPATHOLOGY; IMMUNE RESPONSE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENTEROVIRUS B, HUMAN; KAPLAN-MEIERS ESTIMATE; MICE; MICE, INBRED C57BL; MYOCARDITIS; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77954086395     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.893248     Document Type: Article

References (40)

1. Tam PE. Coxsackievirus myocarditis: interplay between virus and host in the pathogenesis of heart disease. Viral Immunol. 2006;19:133-146.
2. Liu PP, Mason JW. Advances in the understanding of myocarditis. Circulation. 2001;104:1076-1082.
3. Huber SA. Autoimmunity in coxsackievirus B3 induced myocarditis. Autoimmunity. 2006;39:55-61.
4. Liu P, Aitken K, Kong YY, Opavsky MA, Martino T, Dawood F, Wen WH, Kozieradzki I, Bachmaier K, Straus D, Mak TW, Penninger JM. The tyrosine kinase p56lck is essential in coxsackievirus B3-mediated heart disease. Nat Med. 2000;6:429-434.
5. Sakaguchi S. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol. 2004;22:531-562.
6. Rouse BT, Sarangi PP, Suvas S. Regulatory T cells in virus infections. Immunol Rev. 2006;212:272-286.
7. Manigold T, Racanelli V. T-cell regulation by CD4 regulatory T cells during hepatitis B and C virus infections: facts and controversies. Lancet Infect Dis. 2007;7:804-813.
8. Opavsky MA, Martino T, Rabinovitch M, Penninger J, Richardson C, Petric M, Trinidad C, Butcher L, Chan J, Liu PP. Enhanced ERK-1/2 activation in mice susceptible to coxsackievirus-induced myocarditis. J Clin Invest. 2002;109:1561-1569.
9. Szalay G, Sauter M, Hald J, Weinzierl A, Kandolf R, Klingel K. Sustained nitric oxide synthesis contributes to immunopathology in ongoing myocarditis attributable to interleukin-10 disorders. Am J Pathol. 2006; 169:2085-2093.
10. Ohashi S, Nishio A, Nakamura H, Asada M, Tamaki H, Kawasaki K, Fukui T, Yodoi J, Chiba T. Overexpression of redox-active protein thioredoxin-1 prevents development of chronic pancreatitis in mice. Antioxid Redox Signal. 2006;8:1835-1845.
11. Ohashi S, Nishio A, Nakamura H, Kido M, Ueno S, Uza N, Inoue S, Kitamura H, Kiriya K, Asada M, Tamaki H, Matsuura M, Kawasaki K, Fukui T, Watanabe N, Nakase H, Yodoi J, Okazaki K, Chiba T. Protective roles of redox-active protein thioredoxin-1 for severe acute pancreatitis. Am J Physiol Gastrointest Liver Physiol. 2006;290:G772-G781.
12. Boerma M, van der Wees CG, Wondergem J, van der Laarse A, Persoon M, van Zeeland AA, Mullenders LH. Separation of neonatal rat ventricular myocytes and non-myocytes by centrifugal elutriation. Pflugers Arch. 2002;444:452-456.
13. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyo-cyte. Proc Natl Acad Sci USA. 1998;95:2979-2984.
14. Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, Zhu S, Gottlieb PA, Kapranov P, Gingeras TR, Fazekas de St Groth B, Clayberger C, Soper DM, Ziegler SF, Bluestone JA. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4 + T reg cells. J Exp Med. 2006;203:1701-1711.
15. Klunker S, Chong MM, Mantel PY, Palomares O, Bassin C, Ziegler M, Ruckert B, Meiler F, Akdis M, Littman DR, Akdis CA. Transcription factors RUNX1 and RUNX3 in the induction and suppressive function of Foxp3+ inducible regulatory T cells. J Exp Med. 2009;206:2701-2715.
16. Aretz HT, Billingham ME, Edwards WD, Factor SM, Fallon JT, Fenoglio JJ Jr, Olsen EG, Schoen FJ. Myocarditis: a histopathologic definition and classification. Am J Cardiovasc Pathol. 1987;1:3-14.
17. Fehervari Z, Sakaguchi S. CD4+ Tregs and immune control. J Clin Invest. 2004;114:1209-1217.
18. Kim HH, Shin HS, Kwak HJ, Ahn KY, Kim JH, Lee HJ, Lee MS, Lee ZH, Koh GY. RANKL regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. FASEB J. 2003;17:2163-2165.
19. White SM, Constantin PE, Claycomb WC. Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol. 2004;286:H823-H829.
20. Shames BD, Barton HH, Reznikov LL, Cairns CB, Banerjee A, Harken AH, Meng X. Ischemia alone is sufficient to induce TNF-alpha mRNA and peptide in the myocardium. Shock. 2002;17:114-119.
21. Gurevitch J, Frolkis I, Yuhas Y, Paz Y, Matsa M, Mohr R, Yakirevich V. Tumor necrosis factor-alpha is released from the isolated heart undergoing ischemia and reperfusion. J Am Coll Cardiol. 1996;28:247-252.
22. Hickson-Bick DL, Jones C, Buja LM. The response of neonatal rat ventricular myocytes to lipopolysaccharide-induced stress. Shock. 2006; 25:546-552.
23. Lim BK, Xiong D, Dorner A, Youn TJ, Yung A, Liu TI, Gu Y, Dalton ND, Wright AT, Evans SM, Chen J, Peterson KL, McCulloch AD, Yajima T, Knowlton KU. Coxsackievirus and adenovirus receptor (CAR) mediates atrioventricular-node function and connexin 45 localization in the murine heart. J Clin Invest. 2008;118:2758-2770.
24. Lisewski U, Shi Y, Wrackmeyer U, Fischer R, Chen C, Schirdewan A, Juttner R, Rathjen F, Poller W, Radke MH, Gotthardt M. The tight junction protein CAR regulates cardiac conduction and cell-cell communication. J Exp Med. 2008;205:2369-2379.
25. Huber SA, Feldman AM, Sartini D. Coxsackievirus B3 induces T regulatory cells, which inhibit cardiomyopathy in tumor necrosis factor-alpha transgenic mice. Circ Res. 2006;99:1109-1116.
26. Opavsky MA, Penninger J, Aitken K, Wen WH, 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.
27. Blay R, Simpson K, Leslie K, Huber S. Coxsackievirus-induced disease. CD4+ cells initiate both myocarditis and pancreatitis in DBA/2 mice. Am J Pathol. 1989;135:899-907.
28. Henke A, Huber S, Stelzner A, Whitton JL. The role of CD8+ T lymphocytes in coxsackievirus B3-induced myocarditis. J Virol. 1995; 69:6720-6728.
29. Dong C. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol. 2008;8:337-348.
30. Anderson BE, McNiff J, Yan J, Doyle H, Mamula M, Shlomchik MJ, Shlomchik WD. Memory CD4+ T cells do not induce graft-versus-host disease. J Clin Invest. 2003;112:101-108.
31. Lesley R, Kelly LM, Xu Y, Cyster JG. Naive CD4 T cells constitutively express CD40L and augment autoreactive B cell survival. Proc Natl Acad Sci USA. 2006;103:10717-10722.
32. Toubi E, Shoenfeld Y. The role of CD40-CD154 interactions in autoimmunity and the benefit of disrupting this pathway. Autoimmunity. 2004; 37:457-464.
33. Lindsley CW, Barnett SF, Layton ME, Bilodeau MT. The PI3K/Akt pathway: recent progress in the development of ATP-competitive and allosteric Akt kinase inhibitors. Curr Cancer Drug Targets. 2008;8:7-18.
34. Shin I, Bakin AV, Rodeck U, Brunet A, Arteaga CL. Transforming growth factor beta enhances epithelial cell survival via Akt-dependent regulation of FKHRL1. Mol Biol Cell. 2001;12:3328-3339.
35. Bruning A, Runnebaum IB. CAR is a cell-cell adhesion protein in human cancer cells and is expressionally modulated by dexamethasone, TNFalpha, and TGFbeta. Gene Ther. 2003;10:198-205.
36. Ito M, Kodama M, Masuko M, Yamaura M, Fuse K, Uesugi Y, Hirono S, Okura Y, Kato K, Hotta Y, Honda T, Kuwano R, Aizawa Y. Expression of coxsackievirus and adenovirus receptor in hearts of rats with experimental autoimmune myocarditis. Circ Res. 2000;86:275-280.
37. Fuse K, Chan G, Liu Y, Gudgeon P, Husain M, Chen M, Yeh WC, Akira S, Liu PP. Myeloid differentiation factor-88 plays a crucial role in the pathogenesis of Coxsackievirus B3-induced myocarditis and influences type I interferon production. Circulation. 2005;112:2276-2285.
38. Latif N, Zhang H, Archard LC, Yacoub MH, Dunn MJ. Characterization of anti-heart antibodies in mice after infection with coxsackie B3 virus. Clin Immunol. 1999;91:90-98.
39. Rose NR, Hill SL. The pathogenesis of postinfectious myocarditis. Clin Immunol Immunopathol. 1996;80:S92-S99.
40. Burroughs NJ, Miguel Paz Mendes de Oliveira B, Adrego Pinto A. Regulatory T cell adjustment of quorum growth thresholds and the control of local immune responses. J Theor Biol. 2006;241:134-141.