TLR3 is required for survival following Coxsackievirus B3 infection by driving T lymphocyte activation and polarization: The role of dendritic cells

PLoS ONE

Volumn 12, Issue 10, 2017, Pages

  Sesti Costa, Renata ^a   Françozo, Marcela Cristina Santiago ^a,b   Silva, Grace Kelly ^a   Proenca Modena, José Luiz ^c   Silva, João Santana ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^c UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 23; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR; CYTOKINE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; AUTOPHAGY; BONE MARROW DERIVED DENDRITIC CELL; COCULTURE; CONTROLLED STUDY; COXSACKIE VIRUS INFECTION; COXSACKIEVIRUS B3; CROSS PRESENTATION; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE ASSOCIATION; GENE EXPRESSION PROFILING; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; MYOCARDITIS; NONHUMAN; PANCREATITIS; PHAGOCYTOSIS; POLARIZATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH17 CELL; UPREGULATION; VIRUS REPLICATION; ADOPTIVE TRANSFER; ANIMAL; CD4+ T LYMPHOCYTE; ENTEROVIRUS B; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY;

ADOPTIVE TRANSFER; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; COXSACKIEVIRUS INFECTIONS; CYTOKINES; DENDRITIC CELLS; ENTEROVIRUS B, HUMAN; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; TOLL-LIKE RECEPTOR 3;

EID: 85030463658     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0185819     Document Type: Article

References (62)

1. Cooper LT Jr. Myocarditis. The New England journal of medicine. 2009; 360(15):1526–38. https://doi.org/10.1056/NEJMra0800028 PMID: 19357408.
2. Gupta S, Markham DW, Drazner MH, Mammen PP. Fulminant myocarditis. Nature clinical practice Cardiovascular medicine. 2008; 5(11):693–706. https://doi.org/10.1038/ncpcardio1331 PMID: 18797433.
3. Huber S, Ramsingh AI. Coxsackievirus-induced pancreatitis. Viral immunology. 2004; 17(3):358–69. https://doi.org/10.1089/vim.2004.17.358 PMID: 15357902.
4. Whitton JL, Cornell CT, Feuer R. Host and virus determinants of picornavirus pathogenesis and tropism. Nature reviews Microbiology. 2005; 3(10):765–76. https://doi.org/10.1038/nrmicro1284 PMID: 16205710.
5. Leonard EG. Viral myocarditis. The Pediatric infectious disease journal. 2004; 23(7):665–6. PMID: 15247607.
6. World Health Organization. Enterovirus non-polio. http://wwwwhoint/mediacentre/factsheets/fs174/en/printhtml
7. Pankuweit S, Klingel K. Viral myocarditis: from experimental models to molecular diagnosis in patients. Heart failure reviews. 2013; 18(6):683–702. https://doi.org/10.1007/s10741-012-9357-4 PMID: 23070541.
8. Rosamond W, Flegal K, Furie K, Go A, Greenlund K, Haase N, et al. Heart disease and stroke statistics - 2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2008; 117(4):e25–146. https://doi.org/10.1161/CIRCULATIONAHA.107.187998 PMID: 18086926.
9. Kandolf R, Sauter M, Aepinus C, Schnorr JJ, Selinka HC, Klingel K. Mechanisms and consequences of enterovirus persistence in cardiac myocytes and cells of the immune system. Virus research. 1999; 62 (2):149–58. PMID: 10507324.
10. Klingel K, Hohenadl C, Canu A, Albrecht M, Seemann M, Mall G, et al. Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proceedings of the National Academy of Sciences of the United States of America. 1992; 89(1):314–8. PMID: 1309611; PubMed Central PMCID: PMC48227.
11. Weinzierl AO, Szalay G, Wolburg H, Sauter M, Rammensee HG, Kandolf R, et al. 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. Journal of virology. 2008; 82 (16):8149–60. https://doi.org/10.1128/JVI.00047-08 PMID: 18550677; PubMed Central PMCID: PMC2519575.
12. Huber SA, Sartini D. Roles of tumor necrosis factor alpha (TNF-alpha) and the p55 TNF receptor in CD1d induction and coxsackievirus B3-induced myocarditis. Journal of virology. 2005; 79(5):2659–65. https://doi.org/10.1128/JVI.79.5.2659-2665.2005 PMID: 15708985; PubMed Central PMCID: PMC548425.
13. Kemball CC, Harkins S, Whitmire JK, Flynn CT, Feuer R, Whitton JL. Coxsackievirus B3 inhibits antigen presentation in vivo, exerting a profound and selective effect on the MHC class I pathway. PLoS pathogens. 2009; 5(10):e1000618. https://doi.org/10.1371/journal.ppat.1000618 PMID: 19834548; PubMed Central PMCID: PMC2757675.
14. Li K, Xu W, Guo Q, Jiang Z, Wang P, Yue Y, et al. Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circulation research. 2009; 105(4):353–64. https://doi.org/10.1161/CIRCRESAHA.109.195230 PMID: 19608981.
15. Fairweather D, Frisancho-Kiss S, Yusung SA, Barrett MA, Davis SE, Steele RA, et al. IL-12 protects against coxsackievirus B3-induced myocarditis by increasing IFN-gamma and macrophage and neutro-phil populations in the heart. Journal of immunology. 2005; 174(1):261–9. PMID: 15611248.
16. Yuan J, Cao AL, Yu M, Lin QW, Yu X, Zhang JH, et al. Th17 cells facilitate the humoral immune response in patients with acute viral myocarditis. Journal of clinical immunology. 2010; 30(2):226–34. https://doi.org/10.1007/s10875-009-9355-z PMID: 20012175.
17. Yuan J, Yu M, Lin QW, Cao AL, Yu X, Dong JH, et al. Th17 cells contribute to viral replication in coxsackievirus B3-induced acute viral myocarditis. Journal of immunology. 2010; 185(7):4004–10. https://doi.org/10.4049/jimmunol.1001718 PMID: 20802148.
18. Cihakova D, Barin JG, Afanasyeva M, Kimura M, Fairweather D, Berg M, et al. Interleukin-13 protects against experimental autoimmune myocarditis by regulating macrophage differentiation. The American journal of pathology. 2008; 172(5):1195–208. https://doi.org/10.2353/ajpath.2008.070207 PMID: 18403598; PubMed Central PMCID: PMC2329830.
19. Frisancho-Kiss S, Coronado MJ, Frisancho JA, Lau VM, Rose NR, Klein SL, et al. Gonadectomy of male BALB/c mice increases Tim-3(+) alternatively activated M2 macrophages, Tim-3(+) T cells, Th2 cells and Treg in the heart during acute coxsackievirus-induced myocarditis. Brain, behavior, and immunity. 2009; 23(5):649–57. https://doi.org/10.1016/j.bbi.2008.12.002 PMID: 19126426; PubMed Central PMCID: PMC3148833.
20. Abston ED, Coronado MJ, Bucek A, Onyimba JA, Brandt JE, Frisancho JA, et al. TLR3 deficiency induces chronic inflammatory cardiomyopathy in resistant mice following coxsackievirus B3 infection: role for IL-4. American journal of physiology Regulatory, integrative and comparative physiology. 2013; 304(4):R267–77. https://doi.org/10.1152/ajpregu.00516.2011 PMID: 23255589; PubMed Central PMCID: PMC3567355.
21. Huber SA, Feldman AM, Sartini D. Coxsackievirus B3 induces T regulatory cells, which inhibit cardiomyopathy in tumor necrosis factor-alpha transgenic mice. Circulation research. 2006; 99(10):1109–16. https://doi.org/10.1161/01.RES.0000249405.13536.49 PMID: 17038643.
22. Shi Y, Fukuoka M, Li G, Liu Y, Chen M, Konviser M, et al. Regulatory T cells protect mice against coxsackievirus-induced myocarditis through the transforming growth factor beta-coxsackie-adenovirus receptor pathway. Circulation. 2010; 121(24):2624–34. https://doi.org/10.1161/CIRCULATIONAHA.109.893248 PMID: 20530002.
23. Sesti-Costa R, Silva GK, Proenca-Modena JL, Carlos D, Silva ML, Alves-Filho JC, et al. The IL-33/ST2 pathway controls coxsackievirus B5-induced experimental pancreatitis. Journal of immunology. 2013; 191(1):283–92. https://doi.org/10.4049/jimmunol.1202806 PMID: 23733876.
24. Wilkins C, Gale M Jr. Recognition of viruses by cytoplasmic sensors. Current opinion in immunology. 2010; 22(1):41–7. https://doi.org/10.1016/j.coi.2009.12.003 PMID: 20061127; PubMed Central PMCID: PMC3172156.
25. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature immunology. 2010; 11(5):373–84. https://doi.org/10.1038/ni.1863 PMID: 20404851.
26. Lee HK, Lund JM, Ramanathan B, Mizushima N, Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science. 2007; 315(5817):1398–401. https://doi.org/10.1126/science. 1136880 PMID: 17272685.
27. Fuse K, Chan G, Liu Y, Gudgeon P, Husain M, Chen M, et al. 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(15):2276–85. https://doi.org/10.1161/CIRCULATIONAHA.105.536433 PMID: 16216974.
28. Abston ED, Coronado MJ, Bucek A, Bedja D, Shin J, Kim JB, et al. Th2 regulation of viral myocarditis in mice: different roles for TLR3 versus TRIF in progression to chronic disease. Clinical & developmental immunology. 2012; 2012:129486. https://doi.org/10.1155/2012/129486 PMID: 22013485; PubMed Central PMCID: PMC3195533.
29. Riad A, Westermann D, Zietsch C, Savvatis K, Becher PM, Bereswill S, et al. TRIF is a critical survival factor in viral cardiomyopathy. Journal of immunology. 2011; 186(4):2561–70. https://doi.org/10.4049/jimmunol.1002029 PMID: 21239721.
30. Yamamoto M, Sato S, Mori K, Hoshino K, Takeuchi O, Takeda K, et al. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. Journal of immunology. 2002; 169(12):6668–72. PMID: 12471095.
31. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 2001; 413(6857):732–8. https://doi.org/10.1038/35099560 PMID: 11607032.
32. Gorbea C, Makar KA, Pauschinger M, Pratt G, Bersola JL, Varela J, et al. A role for Toll-like receptor 3 variants in host susceptibility to enteroviral myocarditis and dilated cardiomyopathy. The Journal of biological chemistry. 2010; 285(30):23208–23. https://doi.org/10.1074/jbc.M109.047464 PMID: 20472559; PubMed Central PMCID: PMC2906314.
33. 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(1):e4127. https://doi.org/10.1371/journal.pone.0004127 PMID: 19122812; PubMed Central PMCID: PMC2606033.
34. Lee HK, Iwasaki A. Innate control of adaptive immunity: dendritic cells and beyond. Seminars in immunology. 2007; 19(1):48–55. https://doi.org/10.1016/j.smim.2006.12.001 PMID: 17276695.
35. Chen P, Chen R, Yang Y, Yu Y, Xie Y, Zou Y, et al. Coxsackievirus B3 infection promotes generation of myeloid dendritic cells from bone marrow and accumulation in the myocardium. International immuno-pharmacology. 2009; 9(11):1304–12. https://doi.org/10.1016/j.intimp.2009.07.014 PMID: 19664723.
36. Rahnefeld A, Ebstein F, Albrecht N, Opitz E, Kuckelkorn U, Stangl K, et al. Antigen-presentation capacity of dendritic cells is impaired in ongoing enterovirus myocarditis. European journal of immunology. 2011; 41(9):2774–81. https://doi.org/10.1002/eji.201041039 PMID: 21630249.
37. Negishi H, Osawa T, Ogami K, Ouyang X, Sakaguchi S, Koshiba R, et al. A critical link between Toll-like receptor 3 and type II interferon signaling pathways in antiviral innate immunity. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(51):20446–51. https://doi.org/10.1073/pnas.0810372105 PMID: 19074283; PubMed Central PMCID: PMC2629334.
38. Kemball CC, Flynn CT, Hosking MP, Botten J, Whitton JL. Wild-type coxsackievirus infection dramatically alters the abundance, heterogeneity, and immunostimulatory capacity of conventional dendritic cells in vivo. Virology. 2012; 429(1):74–90. https://doi.org/10.1016/j.virol.2012.04.005 PMID: 22551767; PubMed Central PMCID: PMC3358485.
39. Gauntt C, Huber S. Coxsackievirus experimental heart diseases. Frontiers in bioscience: a journal and virtual library. 2003; 8:e23–35. PMID: 12456330.
40. Tracy S, Hofling K, Pirruccello S, Lane PH, Reyna SM, Gauntt CJ. Group B coxsackievirus myocarditis and pancreatitis: connection between viral virulence phenotypes in mice. Journal of medical virology. 2000; 62(1):70–81. PMID: 10935991.
41. Yanagawa B, Spiller OB, Proctor DG, Choy J, Luo H, Zhang HM, et al. Soluble recombinant coxsackievirus and adenovirus receptor abrogates coxsackievirus b3-mediated pancreatitis and myocarditis in mice. The Journal of infectious diseases. 2004; 189(8):1431–9. https://doi.org/10.1086/382598 PMID: 15073680.
42. Schulz O, Diebold SS, Chen M, Naslund TI, Nolte MA, Alexopoulou L, et al. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature. 2005; 433(7028):887–92. https://doi.org/10.1038/nature03326 PMID: 15711573.
43. Lee J, Tian Y, Chan ST, Kim JY, Cho C, Ou JH. TNF-alpha Induced by Hepatitis C Virus via TLR7 and TLR8 in Hepatocytes Supports Interferon Signaling via an Autocrine Mechanism. PLoS pathogens. 2015; 11(5):e1004937. https://doi.org/10.1371/journal.ppat.1004937 PMID: 26023919; PubMed Central PMCID: PMC4449221.
44. Kaya Z, Dohmen KM, Wang Y, Schlichting J, Afanasyeva M, Leuschner F, et al. Cutting edge: a critical role for IL-10 in induction of nasal tolerance in experimental autoimmune myocarditis. Journal of immunology. 2002; 168(4):1552–6. PMID: 11823481.
45. McGeachy MJ, Cua DJ. Th17 cell differentiation: the long and winding road. Immunity. 2008; 28 (4):445–53. https://doi.org/10.1016/j.immuni.2008.03.001 PMID: 18400187.
46. Longhi MP, Trumpfheller C, Idoyaga J, Caskey M, Matos I, Kluger C, et al. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. The Journal of experimental medicine. 2009; 206(7):1589–602. https://doi.org/10.1084/jem.20090247 PMID: 19564349; PubMed Central PMCID: PMC2715098.
47. Fairweather D, Frisancho-Kiss S, Yusung SA, Barrett MA, Davis SE, Gatewood SJ, et al. Interferon-gamma protects against chronic viral myocarditis by reducing mast cell degranulation, fibrosis, and the profibrotic cytokines transforming growth factor-beta 1, interleukin-1 beta, and interleukin-4 in the heart. The American journal of pathology. 2004; 165(6):1883–94. PMID: 15579433; PubMed Central PMCID: PMC1618717.
48. Klingel K, Schnorr JJ, Sauter M, Szalay G, Kandolf R. beta2-microglobulin-associated regulation of interferon-gamma and virus-specific immunoglobulin G confer resistance against the development of chronic coxsackievirus myocarditis. The American journal of pathology. 2003; 162(5):1709–20. PMID: 12707055; PubMed Central PMCID: PMC1851178.
49. 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. Virology journal. 2011; 8:17. https://doi.org/10.1186/1743-422X-8-17 PMID: 21235788; PubMed Central PMCID: PMC3032710.
50. Xie Y, Chen R, Zhang X, Chen P, Liu X, Xie Y, et al. The role of Th17 cells and regulatory T cells in Coxsackievirus B3-induced myocarditis. Virology. 2011; 421(1):78–84. https://doi.org/10.1016/j.virol.2011.09.006 PMID: 21993400.
51. Edelmann KH, Richardson-Burns S, Alexopoulou L, Tyler KL, Flavell RA, Oldstone MB. Does Toll-like receptor 3 play a biological role in virus infections? Virology. 2004; 322(2):231–8. https://doi.org/10.1016/j.virol.2004.01.033 PMID: 15110521.
52. Le Goffic R, Balloy V, Lagranderie M, Alexopoulou L, Escriou N, Flavell R, et al. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS pathogens. 2006; 2(6):e53. https://doi.org/10.1371/journal.ppat.0020053 PMID: 16789835; PubMed Central PMCID: PMC1475659.
53. Menager P, Roux P, Megret F, Bourgeois JP, Le Sourd AM, Danckaert A, et al. Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS pathogens. 2009; 5(2): e1000315. https://doi.org/10.1371/journal.ppat.1000315 PMID: 19247444; PubMed Central PMCID: PMC2642728.
54. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nature medicine. 2004; 10(12):1366–73. https://doi.org/10.1038/nm1140 PMID: 15558055.
55. Hardarson HS, Baker JS, Yang Z, Purevjav E, Huang CH, Alexopoulou L, et al. Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury. American journal of physiology Heart and circulatory physiology. 2007; 292(1):H251–8. https://doi.org/10.1152/ajpheart.00398.2006 PMID: 16936008.
56. Oshiumi H, Okamoto M, Fujii K, Kawanishi T, Matsumoto M, Koike S, et al. The TLR3/TICAM-1 pathway is mandatory for innate immune responses to poliovirus infection. Journal of immunology. 2011; 187(10):5320–7. https://doi.org/10.4049/jimmunol.1101503 PMID: 21998457.
57. McCall KD, Thuma JR, Courreges MC, Benencia F, James CB, Malgor R, et al. Toll-like receptor 3 is critical for coxsackievirus B4-induced type 1 diabetes in female NOD mice. Endocrinology. 2015; 156 (2):453–61. https://doi.org/10.1210/en.2013-2006 PMID: 25422874; PubMed Central PMCID: PMC4298321.
58. O’Neill LA. When signaling pathways collide: positive and negative regulation of toll-like receptor signal transduction. Immunity. 2008; 29(1):12–20. https://doi.org/10.1016/j.immuni.2008.06.004 PMID: 18631453.
59. Swiecki M, Colonna M. The multifaceted biology of plasmacytoid dendritic cells. Nature reviews Immunology. 2015; 15(8):471–85. https://doi.org/10.1038/nri3865 PMID: 26160613; PubMed Central PMCID: PMC4808588.
60. Edelson BT, Kc W, Juang R, Kohyama M, Benoit LA, Klekotka PA, et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. The Journal of experimental medicine. 2010; 207(4):823–36. https://doi.org/10.1084/jem.20091627 PMID: 20351058; PubMed Central PMCID: PMC2856032.
61. Proietto AI, O’Keeffe M, Gartlan K, Wright MD, Shortman K, Wu L, et al. Differential production of inflammatory chemokines by murine dendritic cell subsets. Immunobiology. 2004; 209(1–2):163–72. https://doi.org/10.1016/j.imbio.2004.03.002 PMID: 15481150.
62. Szeles L, Meissner F, Dunand-Sauthier I, Thelemann C, Hersch M, Singovski S, et al. TLR3-Mediated CD8+ Dendritic Cell Activation Is Coupled with Establishment of a Cell-Intrinsic Antiviral State. Journal of immunology. 2015; 195(3):1025–33. https://doi.org/10.4049/jimmunol.1402033 PMID: 26101320.