The innate immune response: An important partner in shaping coxsackievirus-mediated autoimmunity

Journal of Innate Immunity

Volumn 1, Issue 5, 2009, Pages 421-434

  Richer, Martin J ^a   Horwitz, Marc S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Autoimmune myocarditis; Autoimmunity; Coxsackievirus; Innate immunity; Type 1 diabetes

Indexed keywords

CHEMOKINE; CYTOKINE;

ANTIGEN PRESENTING CELL; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CHRONIC DISEASE; CONGESTIVE CARDIOMYOPATHY; COXSACKIE VIRUS; COXSACKIE VIRUS INFECTION; HUMAN; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; MOLECULAR RECOGNITION; MYOCARDITIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VIRUS INDUCTION;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; COXSACKIEVIRUS INFECTIONS; DIABETES MELLITUS, TYPE 1; ENTEROVIRUS; HUMANS; IMMUNITY, INNATE; MICE; MYOCARDITIS;

EID: 77950926741     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000226247     Document Type: Review

References (117)

1. Ercolini AM, Miller SD: The role of infections in autoimmune disease. Clin Exp Immunol 2009;155:1-15.
2. Zandman-Goddard G, Shoenfeld Y: Infections and SLE. Autoimmunity 2005;38:473-485.
3. Lalive PH, Allali G, Truffert A: Myasthenia gravis associated with HTLV-I infection and atypical brain lesions. Muscle Nerve 2007;35:525-528. (Pubitemid 46542974)
4. Ascherio A, Munger KL: Environmental risk factors for multiple sclerosis. 1. The role of infection. Ann Neurol 2007;61:288-299.
5. Rose NR: Autoimmunity in coxsackievirus infection. Curr Top Microbiol Immunol 2008;323:293-314.
6. van der Werf N, Kroese FG, Rozing J, Hillebrands JL: Viral infections as potential triggers of type 1 diabetes. Diabetes Metab Res Rev 2007;23:169-183. (Pubitemid 46437842)
7. Pasare C, Medzhitov R: Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 2003;299:1033-1036. (Pubitemid 36222922)
8. Waldner H, Collins M, Kuchroo VK: Activation of antigen-presenting cells by microbial products breaks self tolerance and induces autoimmune disease. J Clin Invest 2004;113:990-997. (Pubitemid 38544120)
9. Ichikawa HT, Williams LP, Segal BM: Activation of APCs through CD40 or Toll-like receptor 9 overcomes tolerance and precipitates autoimmune disease. J Immunol 2002;169:2781-2787.
10. Whitton JL: Immunopathology during coxsackievirus infection. Springer Semin Immunopathol 2002;24:201-213.
11. Huber S, Ramsingh AI: Coxsackievirus-induced pancreatitis. Viral Immunol 2004;17:358-369.
12. Wolfgram LJ, Beisel KW, Herskowitz A, Rose NR: Variations in the susceptibility to Coxsackievirus B3-induced myocarditis among different strains of mice. J Immunol 1986;136:1846-1852. (Pubitemid 16119600)
13. Yusuf S, Reddy S, Ounpuu S, Anand S: Global burden of cardiovascular diseases. 1. General considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation 2001;104:2746-2753.
14. Taylor DO, Edwards LB, Aurora P, Christie JD, Dobbels F, Kirk R, Rahmel AO, Kucheryavaya AY, Hertz MI: Registry of the International Society for Heart and Lung Transplantation: twenty-fifth official adult heart transplant report, 2008. J Heart Lung Transplant 2008;27:943-956. (Pubitemid 47199081)
15. Huber SA, Gauntt CJ, Sakkinen P: Enteroviruses and myocarditis: viral pathogenesis through replication, cytokine induction, and immunopathogenicity. Adv Virus Res 1998;51:35-80.
16. Fairweather D, Kaya Z, Shellam GR, Lawson CM, Rose NR: From infection to autoimmunity. J Autoimmun 2001;16:175-186.
17. Esfandiarei M, McManus BM: Molecular biology and pathogenesis of viral myocarditis. Annu Rev Pathol 2008;3:127-155.
18. Li HS, Ligons DL, Rose NR: Genetic complexity of autoimmune myocarditis. Autoimmun Rev 2008;7:168-173.
19. Hashimoto I, Tatsumi M, Nakagawa M: The role of T lymphocytes in the pathogenesis of Coxsackie virus B3 heart disease. Br J Exp Pathol 1983;64:497-504. (Pubitemid 14205473)
20. Henke A, Huber S, Stelzner A, Whitton JL: The role of CD8+ T lymphocytes in cox-sackievirus B3-induced myocarditis. J Virol 1995;69:6720-6728.
21. Why HJ, Meany BT, Richardson PJ, Olsen EG, Bowles NE, Cunningham L, Freeke CA, Archard LC: Clinical and prognostic significance of detection of enteroviral RNA in the myocardium of patients with myocarditis or dilated cardiomyopathy. Circulation 1994;89:2582-2589. (Pubitemid 24173674)
22. Pauschinger M, Doerner A, Kuehl U, Schwimmbeck PL, Poller W, Kandolf R, Schultheiss HP: Enteroviral RNA replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation 1999;99:889-895. (Pubitemid 29094302)
23. Kim KS, Tracy S, Tapprich W, Bailey J, Lee CK, Kim K, Barry WH, Chapman NM: 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. (Pubitemid 40677334)
24. Hill NJ, King C, Flodstrom-Tullberg M: Recent acquisitions on the genetic basis of autoimmune disease. Front Biosci 2008;13:4838-4851. (Pubitemid 351599639)
25. Jahromi MM, Eisenbarth GS: Genetic determinants of type 1 diabetes across populations. Ann NY Acad Sci 2006;1079:289-299. (Pubitemid 46001348)
26. Smyth DJ, Cooper JD, Bailey R, Field S, Burren O, Smink LJ, Guja C, Ionescu-Tirgoviste C, Widmer B, Dunger DB, Savage DA, Walker NM, Clayton DG, Todd JA: A genomewide association study of nonsynonymous SNPs identifies a type 1 diabetes locus in the interferon-induced helicase (IFIH1) region. Nat Genet 2006;38:617-619. (Pubitemid 43927300)
27. Gale EA: The rise of childhood type 1 diabetes in the 20th century. Diabetes 2002;51:3353-3361. (Pubitemid 35403436)
28. Hyttinen V, Kaprio J, Kinnunen L, Koskenvuo M, Tuomilehto J: Genetic liability of type 1 diabetes and the onset age among 22,650 young Finnish twin pairs: a nationwide follow-up study. Diabetes 2003;52:1052-1055. (Pubitemid 36384278)
29. Raymond NT, Jones JR, Swift PG, Davies MJ, Lawrence G, McNally PG, Burden ML, Gregory R, Burden AC, Botha JL: Comparative incidence of type I diabetes in children aged under 15 years from South Asian and white or other ethnic backgrounds in Leicestershire, UK, 1989 to 1998. Diabetologia 2001; 44 suppl 3:B32-B36.
30. Jun HS, Yoon JW: A new look at viruses in type 1 diabetes. Diabetes Metab Res Rev 2003;19:8-31. (Pubitemid 36285371)
31. Richer MJ, Horwitz MS: Viral infections in the pathogenesis of autoimmune diseases: focus on type 1 diabetes. Front Biosci 2008;13:4241-4257.
32. Gamble DR, Kinsley ML, FitzGerald MG, Bolton R, Taylor KW: Viral antibodies in diabetes mellitus. Br Med J 1969;3:627-630.
33. King ML, Shaikh A, Bidwell D, Voller A, Banatvala JE: Coxsackie-B-virus-specific IgM responses in children with insulin-dependent (juvenile-onset; type I) diabetes mellitus. Lancet 1983;1:1397-1399.
34. Banatvala JE, Bryant J, Schernthaner G, Borkenstein M, Schober E, Brown D, De Silva LM, Menser MA, Silink M: Coxsackie B, mumps, rubella, and cytomegalovirus specific IgM responses in patients with juvenile-onset insulin-dependent diabetes mellitus in Britain, Austria, and Australia. Lancet 1985;1:1409-1412. (Pubitemid 15057971)
35. Frisk G, Friman G, Tuvemo T, Fohlman J, Diderholm H: Coxsackie B virus IgM in children at onset of type 1 (insulin-dependent) diabetes mellitus: evidence for IgM induction by a recent or current infection. Diabetologia 1992;35:249-253.
36. Clements GB, Galbraith DN, Taylor KW: Coxsackie B virus infection and onset of childhood diabetes. Lancet 1995;346:221-223.
37. Helfand RF, Gary HE Jr, Freeman CY, Anderson LJ, Pallansch MA: Serologic evidence of an association between enteroviruses and the onset of type 1 diabetes mellitus. Pittsburgh Diabetes Research Group. J Infect Dis 1995;172:1206-1211.
38. Andreoletti L, Hober D, Hober-Vandenberghe C, Belaich S, Vantyghem MC, Lefebvre J, Wattre P: Detection of coxsackie B virus RNA sequences in whole blood samples from adult patients at the onset of type I diabetes mellitus. J Med Virol 1997;52:121-127. (Pubitemid 27239308)
39. Lonnrot M, Korpela K, Knip M, Ilonen J, Simell O, Korhonen S, Savola K, Muona P, Simell T, Koskela P, Hyoty H: Enterovirus infection as a risk factor for beta-cell autoimmunity in a prospectively observed birth cohort: the Finnish Diabetes Prediction and Prevention Study. Diabetes 2000;49:1314-1318. (Pubitemid 30624231)
40. Lonnrot M, Salminen K, Knip M, Savola K, Kulmala P, Leinikki P, Hyypia T, Akerblom HK, Hyoty H: Enterovirus RNA in serum is a risk factor for beta-cell autoimmunity and clinical type 1 diabetes: a prospective study. Childhood Diabetes in Finland (DiMe) Study Group. J Med Virol 2000;61:214-220.
41. Sadeharju K, Lonnrot M, Kimpimaki T, Savola K, Erkkila S, Kalliokoski T, Savolainen P, Koskela P, Ilonen J, Simell O, Knip M, Hyoty H: Enterovirus antibody levels during the first two years of life in prediabetic autoantibody-positive children. Diabetologia 2001;44:818-823. (Pubitemid 32642453)
42. Sadeharju K, Hamalainen AM, Knip M, Lonnrot M, Koskela P, Virtanen SM, Ilonen J, Akerblom HK, Hyoty H: Enterovirus infections as a risk factor for type I diabetes: virus analyses in a dietary intervention trial. Clin Exp Immunol 2003;132:271-277. (Pubitemid 36560623)
43. Sarmiento L, Cabrera-Rode E, Lekuleni L, Cuba I, Molina G, Fonseca M, Heng-Hung L, Borroto AD, Gonzalez P, Mas-Lago P, Diaz- Horta O: Occurrence of enterovirus RNA in serum of children with newly diagnosed type 1 diabetes and islet cell autoantibodypositive subjects in a population with a low incidence of type 1 diabetes. Autoimmunity 2007;40:540-545. (Pubitemid 351233176)
44. Yoon JW, Austin M, Onodera T, Notkins AL: Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N Engl J Med 1979;300:1173-1179.
45. Dotta F, Censini S, van Halteren AG, Marselli L, Masini M, Dionisi S, Mosca F, Boggi U, Muda AO, Prato SD, Elliott JF, Covacci A, Rappuoli R, Roep BO, Marchetti P: Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc Natl Acad Sci USA 2007;104:5115-5120. (Pubitemid 47186185)
46. Serreze DV, Ottendorfer EW, Ellis TM, Gauntt CJ, Atkinson MA: Acceleration of type 1 diabetes by a coxsackievirus infection requires a preexisting critical mass of autoreactive T-cells in pancreatic islets. Diabetes 2000;49:708-711.
47. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N: Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med 1998;4:781-785. (Pubitemid 28331018)
48. Horwitz MS, Ilic A, Fine C, Balasa B, Sarvetnick N: Coxsackieviral- mediated diabetes: induction requires antigen-presenting cells and is accompanied by phagocytosis of beta cells. Clin Immunol 2004;110:134-144. (Pubitemid 38296703)
49. Horwitz MS, Fine C, Ilic A, Sarvetnick N: Requirements for viral-mediated autoimmune diabetes: beta-cell damage and immune infiltration. J Autoimmun 2001;16:211-217. (Pubitemid 32566109)
50. Elshebani A, Olsson A, Westman J, Tuvemo T, Korsgren O, Frisk G: Effects on isolated human pancreatic islet cells after infection with strains of enterovirus isolated at clinical presentation of type 1 diabetes. Virus Res 2007;124:193-203. (Pubitemid 46216572)
51. Bowie AG, Unterholzner L: Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 2008;8:911-922.
52. Kawai T, Akira S: Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 2008;1143:1-20.
53. Sadler AJ, Williams BR: Interferon-inducible antiviral effectors. Nat Rev Immunol 2008;8:559-568.
54. Theofilopoulos AN, Baccala R, Beutler B, Kono DH: Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 2005;23:307-336. (Pubitemid 40563172)
55. Zhou S, Kurt-Jones EA, Cerny AM, Chan M, Bronson RT, Finberg RW: MyD88 intrinsically regulates CD4 T-cell responses. J Virol 2009;83:1625-1634.
56. Sutmuller RP, den Brok MH, Kramer M, Bennink EJ, Toonen LW, Kullberg BJ, Joosten LA, Akira S, Netea MG, Adema GJ: Toll-like receptor 2 controls expansion and function of regulatory T cells. J Clin Invest 2006;116:485-494. (Pubitemid 43228366)
57. Le Goffic R, Balloy V, Lagranderie M, Alexopoulou L, Escriou N, Flavell R, Chignard M, Si-Tahar M: Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus- induced acute pneumonia. PLoS Pathog 2006;2:e53. (Pubitemid 43998849)
58. Gowen BB, Hoopes JD, Wong MH, Jung KH, Isakson KC, Alexopoulou L, Flavell RA, Sidwell RW: TLR3 deletion limits mortality and disease severity due to Phlebovirus infection. J Immunol 2006;177:6301-6307. (Pubitemid 44628848)
59. Horwitz MS, Krahl T, Fine C, Lee J, Sarvetnick N: Protection from lethal coxsackievirus-induced pancreatitis by expression of gamma interferon. J Virol 1999;73:1756-1766. (Pubitemid 29098074)
60. Triantafilou K, Triantafilou M: Coxsackievirus B4-induced cytokine production in pancreatic cells is mediated through toll-like receptor 4. J Virol 2004;78:11313-11320. (Pubitemid 39299671)
61. Triantafilou K, Orthopoulos G, Vakakis E, Ahmed MA, Golenbock DT, Lepper PM, Triantafilou M: Human cardiac inflammatory responses triggered by Coxsackie B viruses are mainly Toll-like receptor (TLR) 8-dependent. Cell Microbiol 2005;7:1117-1126. (Pubitemid 41030937)
62. Richer MJ, Lavallee DJ, Shanina I, Horwitz MS: Toll-like receptor 3 signaling on macrophages is required for survival following coxsackievirus B4 infection. PLoS ONE 2009;4:e4127.
63. 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. (Pubitemid 41464570)
64. Negishi H, Osawa T, Ogami K, Ouyang X, Sakaguchi S, Koshiba R, Yanai H, Seko Y, Shitara H, Bishop K, Yonekawa H, Tamura T, Kaisho T, Taya C, Taniguchi T, Honda K: A critical link between Toll-like receptor 3 and type II interferon signaling pathways in antiviral innate immunity. Proc Natl Acad Sci USA 2008;105:20446-20451.
65. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA, Diamond MS, Colonna M: Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci USA 2006;103:8459-8464. (Pubitemid 43838477)
66. Huber S: Host immune responses to coxsackievirus B3. Curr Top Microbiol Immunol 2008;323:199-221.
67. Lowenstein CJ, Hill SL, Lafond-Walker A, Wu J, Allen G, Landavere M, Rose NR, Herskowitz A: Nitric oxide inhibits viral replication in murine myocarditis. J Clin Invest 1996;97:1837-1843. (Pubitemid 26129869)
68. Pasare C, Medzhitov R: Toll-like receptors: linking innate and adaptive immunity. Microbes Infect 2004;6:1382-1387. (Pubitemid 41110581)
69. Marty RR, Dirnhofer S, Mauermann N, Schweikert S, Akira S, Hunziker L, Penninger JM, Eriksson U: MyD88 signaling controls autoimmune myocarditis induction. Circulation 2006;113:258-265. (Pubitemid 43754383)
70. Lane JR, Neumann DA, Lafond-Walker A, Herskowitz A, Rose NR: LPS promotes CB3-induced myocarditis in resistant B10.A mice. Cell Immunol 1991;136:219-233.
71. Lane JR, Neumann DA, Lafond-Walker A, Herskowitz A, Rose NR: Interleukin 1 or tumor necrosis factor can promote Coxsackie B3-induced myocarditis in resistant B10.A mice. J Exp Med 1992;175:1123-1129.
72. Satoh M, Akatsu T, Ishikawa Y, Minami Y, Takahashi Y, Nakamura M: Association between toll-like receptor 8 expression and adverse clinical outcomes in patients with enterovirus-associated dilated cardiomyopathy. Am Heart J 2007;154:581-588. (Pubitemid 47268249)
73. Satoh M, Nakamura M, Akatsu T, Shimoda Y, Segawa I, Hiramori K: Toll-like receptor 4 is expressed with enteroviral replication in myocardium from patients with dilated cardiomyopathy. Lab Invest 2004;84:173-181. (Pubitemid 41656498)
74. Fairweather D, Yusung S, Frisancho S, Barrett M, Gatewood S, Steele R, Rose NR: IL-12 receptor beta 1 and Toll-like receptor 4 increase IL-1 beta-and IL-18-associated myocarditis and coxsackievirus replication. J Immunol 2003;170:4731-4737. (Pubitemid 36519981)
75. Frisancho-Kiss S, Davis SE, Nyland JF, Frisancho JA, Cihakova D, Barrett MA, Rose NR, Fairweather D: Cutting edge: cross-regulation by TLR4 and T cell Ig mucin-3 determines sex differences in inflammatory heart disease. J Immunol 2007;178:6710-6714. (Pubitemid 46847392)
76. Richer MJ, Fang D, Shanina I, Horwitz MS: Toll-like receptor 4-induced cytokine production circumvents protection conferred by TGF-beta in coxsackievirus-mediated autoimmune myocarditis. Clin Immunol 2006;121:339-349. (Pubitemid 44738716)
77. Devaraj S, Dasu MR, Rockwood J, Winter W, Griffen SC, Jialal I: Increased toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with type 1 diabetes: further evidence of a proinflammatory state. J Clin Endocrinol Metab 2008;93:578-583. (Pubitemid 351240834)
78. Vallois D, Grimm CH, Avner P, Boitard C, Rogner UC: The type 1 diabetes locus Idd6 controls TLR1 expression. J Immunol 2007;179:3896-3903.
79. Kim HS, Han MS, Chung KW, Kim S, Kim E, Kim MJ, Jang E, Lee HA, Youn J, Akira S, Lee MS: Toll-like receptor 2 senses beta-cell death and contributes to the initiation of autoimmune diabetes. Immunity 2007;27:321-333. (Pubitemid 47284922)
80. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV: Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008;455:1109-1113.
81. Wong FS, Hu C, Zhang L, Du W, Alexopoulou L, Flavell RA, Wen L: The role of Toll-like receptors 3 and 9 in the development of autoimmune diabetes in NOD mice. Ann NY Acad Sci 2008;1150:146-148.
82. Guberski DL, Thomas VA, Shek WR, Like AA, Handler ES, Rossini AA, Wallace JE, Welsh RM: Induction of type I diabetes by Kilham's rat virus in diabetes-resistant BB/Wor rats. Science 1991;254:1010-1013.
83. Brown DW, Welsh RM, Like AA: Infection of peripancreatic lymph nodes but not islets precedes Kilham rat virus-induced diabetes in BB/Wor rats. J Virol 1993;67:5873-5878.
84. Zipris D, Lien E, Nair A, Xie JX, Greiner DL, Mordes JP, Rossini AA: TLR9-signaling pathways are involved in Kilham rat virus-induced autoimmune diabetes in the biobreeding diabetes-resistant rat. J Immunol 2007;178:693-701. (Pubitemid 46095141)
85. Zipris D, Lien E, Xie JX, Greiner DL, Mordes JP, Rossini AA: TLR activation synergizes with Kilham rat virus infection to induce diabetes in BBDR rats. J Immunol 2005;174:131-142. (Pubitemid 40007399)
86. Athanassopoulos P, Vaessen LM, Maat AP, Balk AH, Weimar W, Bogers AJ: Peripheral blood dendritic cells in human end-stage heart failure and the early post-transplant period: evidence for systemic Th1 immune responses. Eur J Cardiothorac Surg 2004;25:619-626. (Pubitemid 38376079)
87. Smith SC, Allen PM: Expression of myosinclass II major histocompatibility complexes in the normal myocardium occurs before induction of autoimmune myocarditis. Proc Natl Acad Sci USA 1992;89:9131-9135.
88. Donermeyer DL, Beisel KW, Allen PM, Smith SC: 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.
89. Eriksson U, Ricci R, Hunziker L, Kurrer MO, Oudit GY, Watts TH, Sonderegger I, Bachmaier K, Kopf M, Penninger JM: Dendritic cell-induced autoimmune heart failure requires cooperation between adaptive and innate immunity. Nat Med 2003;9:1484-1490. (Pubitemid 38004775)
90. Weinzierl AO, Szalay G, Wolburg H, Sauter M, Rammensee HG, Kandolf R, Stevanovic S, Klingel K: Effective chemokine secretion by dendritic cells and expansion of cross-presenting CD4-/CD8+ dendritic cells define a protective phenotype in the mouse model of coxsackievirus myocarditis. J Virol 2008;82:8149-8160.
91. Martinez FO, Sica A, Mantovani A, Locati M: Macrophage activation and polarization. Front Biosci 2008;13:453-461.
92. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ: The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007;204:3037-3047. (Pubitemid 350179569)
93. 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. (Pubitemid 351671534)
94. Horwitz MS, Knudsen M, Ilic A, Fine C, Sarvetnick N: Transforming growth factor-beta inhibits coxsackievirus-mediated autoimmune myocarditis. Viral Immunol 2006;19:722-733. (Pubitemid 46068065)
95. Ellis JE, Ansari AA, Fett JD, Carraway RD, Randall HW, Mosunjac MI, Sundstrom JB: Inhibition of progenitor dendritic cell maturation by plasma from patients with peripartum cardiomyopathy: role in pregnancy-associated heart disease. Clin Dev Immunol 2005;12:265-273.
96. Shinomiya M, Nadano S, Shinomiya H, Onji M: In situ characterization of dendritic cells occurring in the islets of nonobese diabetic mice during the development of insulitis. Pancreas 2000;20:290-296.
97. Jun HS, Yoon CS, Zbytnuik L, van Rooijen N, Yoon JW: The role of macrophages in T cell-mediated autoimmune diabetes in nonobese diabetic mice. J Exp Med 1999;189:347-358. (Pubitemid 29063256)
98. Martin AP, Rankin S, Pitchford S, Charo IF, Furtado GC, Lira SA: Increased expression of CCL2 in insulin-producing cells of transgenic mice promotes mobilization of myeloid cells from the bone marrow, marked insulitis, and diabetes. Diabetes 2008;57:3025-3033.
99. Walker LS: Natural Treg in autoimmune diabetes: all present and correct? Expert Opin Biol Ther 2008;8:1691-1703.
100. Anderson AC, Chandwaskar R, Lee DH, Kuchroo VK: Cutting edge: the Idd3 genetic interval determines regulatory T cell function through CD11b+CD11c- APC. J Immunol 2008;181:7449-7452.
101. Richer MJ, Straka N, Fang D, Shanina I, Horwitz MS: Regulatory T-cells protect from type 1 diabetes after induction by coxsackievirus infection in the context of transforming growth factor-beta. Diabetes 2008;57:1302-1311.
102. Weber MS, Prod'homme T, Youssef S, Dunn SE, Rundle CD, Lee L, Patarroyo JC, Stuve O, Sobel RA, Steinman L, Zamvil SS: Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat Med 2007;13:935-943.
103. Horwitz MS, 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. (Pubitemid 30398795)
104. 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.
105. Fuse K, Kodama M, Hanawa H, Okura Y, Ito M, Shiono T, Maruyama S, Hirono S, Kato K, Watanabe K, Aizawa Y: Enhanced expression and production of monocyte chemoattractant protein-1 in myocarditis. Clin Exp Immunol 2001;124:346-352. (Pubitemid 32701693)
106. Shen Y, Xu W, Chu YW, Wang Y, Liu QS, Xiong SD: Coxsackievirus group B type 3 infection upregulates expression of monocyte chemoattractant protein 1 in cardiac myocytes, which leads to enhanced migration of mononuclear cells in viral myocarditis. J Virol 2004;78:12548-12556. (Pubitemid 39458773)
107. Cook DN, Beck MA, Coffman TM, Kirby SL, Sheridan JF, Pragnell IB, Smithies O: Requirement of MIP-1 alpha for an inflammatory response to viral infection. Science 1995;269:1583-1585.
108. Kanda T, Takahashi T: Interleukin-6 and cardiovascular diseases. Jpn Heart J 2004;45:183-193.
109. Kanda T, McManus JE, Nagai R, Imai S, Suzuki T, Yang D, McManus BM, Kobayashi I: Modification of viral myocarditis in mice by interleukin-6. Circ Res 1996;78:848-856. (Pubitemid 26131369)
110. 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. J Mol Cell Cardiol 2001;33:1627-1635. (Pubitemid 32844221)
111. Serreze DV, Wasserfall C, Ottendorfer EW, Stalvey M, Pierce MA, Gauntt C, O'Donnell B, Flanagan JB, Campbell-Thompson M, Ellis TM, Atkinson MA: Diabetes acceleration or prevention by a coxsackievirus B4 infection: critical requirements for both interleukin- 4 and gamma interferon. J Virol 2005;79:1045-1052. (Pubitemid 40053888)
112. Christen U, Wolfe T, Mohrle U, Hughes AC, Rodrigo E, Green EA, Flavell RA, von Herrath MG: A dual role for TNF-alpha in type 1 diabetes: islet-specific expression abrogates the ongoing autoimmune process when induced late but not early during pathogenesis. J Immunol 2001;166:7023-7032. (Pubitemid 32525571)
113. Huber SA, 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. (Pubitemid 35176195)
114. Fairweather D, Frisancho-Kiss S, Njoku DB, Nyland JF, Kaya Z, Yusung SA, Davis SE, Frisancho JA, Barrett MA, Rose NR: Complement receptor 1 and 2 deficiency increases coxsackievirus B3-induced myocarditis, dilated cardiomyopathy, and heart failure by increasing macrophages, IL-1- beta, and immune complex deposition in the heart. J Immunol 2006;176:3516-3524. (Pubitemid 43363999)
115. Rodacki M, Milech A, de Oliveira JE: NK cells and type 1 diabetes. Clin Dev Immunol 2006;13:101-107.
116. Novak J, Griseri T, Beaudoin L, Lehuen A: Regulation of type 1 diabetes by NKT cells. Int Rev Immunol 2007;26:49-72. (Pubitemid 46512166)
117. Barrat FJ, Coffman RL: Development of TLR inhibitors for the treatment of autoimmune diseases. Immunol Rev 2008;223:271-283. (Pubitemid 351986175)