Viruses and Autoimmunity: A Review on the Potential Interaction and Molecular Mechanisms

Maria K Smatti, Farhan S Cyprian, Gheyath K Nasrallah, Asmaa A Al Thani, Ruba O Almishal, Hadi M Yassine, Maria K Smatti, Farhan S Cyprian, Gheyath K Nasrallah, Asmaa A Al Thani, Ruba O Almishal, Hadi M Yassine

Abstract

For a long time, viruses have been shown to modify the clinical picture of several autoimmune diseases, including type 1 diabetes (T1D), systemic lupus erythematosus (SLE), rheumatoid arthritis (RA), Sjögren's syndrome (SS), herpetic stromal keratitis (HSK), celiac disease (CD), and multiple sclerosis (MS). Best examples of viral infections that have been proposed to modulate the induction and development of autoimmune diseases are the infections with enteric viruses such as Coxsackie B virus (CVB) and rotavirus, as well as influenza A viruses (IAV), and herpesviruses. Other viruses that have been studied in this context include, measles, mumps, and rubella. Epidemiological studies in humans and experimental studies in animal have shown that viral infections can induce or protect from autoimmunopathologies depending on several factors including genetic background, host-elicited immune responses, type of virus strain, viral load, and the onset time of infection. Still, data delineating the clear mechanistic interaction between the virus and the immune system to induce autoreactivity are scarce. Available data indicate that viral-induced autoimmunity can be activated through multiple mechanisms including molecular mimicry, epitope spreading, bystander activation, and immortalization of infected B cells. Contrarily, the protective effects can be achieved via regulatory immune responses which lead to the suppression of autoimmune phenomena. Therefore, a better understanding of the immune-related molecular processes in virus-induced autoimmunity is warranted. Here we provide an overview of the current understanding of viral-induced autoimmunity and the mechanisms that are associated with this phenomenon.

Keywords: autoimmunity; molecular mechanisms; molecular mimicry; viral infections.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Mechanisms of virus-induced autoimmunity. (A) Molecular mimicry model: (1) Viruses carry epitopes structurally similar to self-epitopes. (2) Presentation of viral epitopes by antigen presenting cells (APCs) activate autoreactive T cells that bind to both, self and non-self-antigens, and induce tissue damage. (B) Bystander activation model: (1) Non-specific and over reactive antiviral immune responses lead to the liberation of self-antigens and release of inflammatory cytokines from the damaged tissue. (2) Self-antigen is taken up and presented by APCs. (3) Autoreactive T cells activated by APCs, leading to tissue destruction. (C) Epitope spreading model: (1) Persistent viral infection. (2) Continued tissue damage and release of new self-antigens. (3) Self-antigens are taken up and presented by APCs. (4) Nonspecific activation of more autoreactive T cells leading to autoimmunity.

References

    1. Ercolini A.M., Miller S.D. The role of infections in autoimmune disease. Clin. Exp. Immunol. 2009;155:1–15. doi: 10.1111/j.1365-2249.2008.03834.x.
    1. Arleevskaya M.I., Manukyan G., Inoue R., Aminov R. Editorial: Microbial and Environmental Factors in Autoimmune and Inflammatory Diseases. Front. Immunol. 2017;8:243. doi: 10.3389/fimmu.2017.00243.
    1. Lerner A., Arleevskaya M., Schmiedl A., Matthias T. Microbes and Viruses Are Bugging the Gut in Celiac Disease. Are They Friends or Foes? Front. Microbiol. 2017;8:1392. doi: 10.3389/fmicb.2017.01392.
    1. Kim B., Kaistha S.D., Rouse B.T. Viruses and autoimmunity. Autoimmunity. 2006;39:71–77. doi: 10.1080/08916930500484708.
    1. Zhao Z., Granucci F., Yeh L., Schaffer P.A., Cantor H. Molecular Mimicry by Herpes Simplex Virus-Type 1: Autoimmune Disease After Viral Infection. Science. 1998;279:1344–1347. doi: 10.1126/science.279.5355.1344.
    1. Coppieters K.T., Wiberg A., Von Herrath M.G. Viral infections and molecular mimicry in type 1 diabetes. APMIS. 2012;120:941–949. doi: 10.1111/apm.12011.
    1. 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.
    1. Croxford J., Olson J.K., Miller S.D. Epitope spreading and molecular mimicry as triggers of autoimmunity in the Theiler’s virus-induced demyelinating disease model of multiple sclerosis. Autoimmun. Rev. 2002;1:251–260. doi: 10.1016/S1568-9972(02)00080-0.
    1. Getts D.R., Chastain E.M.L., Terry R.L., Miller S.D. Virus infection, antiviral immunity, and autoimmunity. Immunol. Rev. 2013;255:197–209. doi: 10.1111/imr.12091.
    1. 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. doi: 10.1128/CMR.19.1.80-94.2006.
    1. Constantinescu C.S., Farooqi N., O’Brien K., Gran B. Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS) Br. J. Pharmacol. 2011;164:1079–1106. doi: 10.1111/j.1476-5381.2011.01302.x.
    1. Leis A.A., Szatmary G., Ross M.A., Stokic D.S. West nile virus infection and myasthenia gravis. Muscle Nerve. 2014;49:26–29. doi: 10.1002/mus.23869.
    1. 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. doi: 10.1038/nm1097-1133.
    1. Nanbo A., Inoue K., Adachi-Takasawa K., Takada K. Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt’s lymphoma. EMBO J. 2002;21:954–965. doi: 10.1093/emboj/21.5.954.
    1. Filippi C.M., von Herrath M.G. Viral trigger for type 1 diabetes: Pros and cons. Diabetes. 2008;57:2863–2871. doi: 10.2337/db07-1023.
    1. Gamble D.R., Taylor K.W. Seasonal Incidence of Diabetes Mellitus. Br. Med. J. 1969;3:631–633. doi: 10.1136/bmj.3.5671.631.
    1. Bergamin C.S., Dib S.A. Enterovirus and type 1 diabetes: What is the matter? World J. Diabetes. 2015;6:828–839. doi: 10.4239/wjd.v6.i6.828.
    1. Sarmiento L., Cubas-Dueñas I., Cabrera-Rode E. Evidence of association between type 1 diabetes and exposure to enterovirus in Cuban children and adolescents. MEDICC Rev. 2013;15:29–32. doi: 10.1590/S1555-79602013000100007.
    1. Hyoty H., Hiltunen M., Knip M., Laakkonen M., Vähäsalo P., Karjalainen J., Koskela P., Roivainen M., Leinikki P., Hovi T., et al. A Prospective Study of the Role of Coxsackie B and Other Enterovirus Infections in the Pathogenesis of IDDM. Diabetes. 1995;44:652–657. doi: 10.2337/diab.44.6.652.
    1. Kimpimäki T., Kupila A., Hämäläinen A.M., Kukko M., Kulmala P., Savola K., Simell T., Keskinen P., Ilonen J., Simell O., et al. The first signs of beta-cell autoimmunity appear in infancy in genetically susceptible children from the general population: The Finnish Type 1 Diabetes Prediction and Prevention Study. J. Clin. Endocrinol. Metab. 2001;86:4782–4788.
    1. Lönnrot M., Korpela K., Knip M., Ilonen J., Simell O., Korhonen S., Savola K., Muona P., Simell T., Koskela P., et al. 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. doi: 10.2337/diabetes.49.8.1314.
    1. 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. doi: 10.1016/j.virusres.2006.11.004.
    1. Oikarinen M., Tauriainen S., Honkanen T., Oikarinen S., Vuori K., Kaukinen K., Rantala I., Mäki M., Hyöty H. Detection of enteroviruses in the intestine of type 1 diabetic patients. Clin. Exp. Immunol. 2008;151:71–75. doi: 10.1111/j.1365-2249.2007.03529.x.
    1. Yeung W.-C.G., Rawlinson W.D., Craig M.E. Enterovirus infection and type 1 diabetes mellitus: Systematic review and meta-analysis of observational molecular studies. BMJ. 2011;342:d35. doi: 10.1136/bmj.d35.
    1. Clements G., Galbraith D., Taylor K. Coxsackie B virus infection and onset of childhood diabetes. Lancet. 1995;346:221–223. doi: 10.1016/S0140-6736(95)91270-3.
    1. Andréoletti L., Hober D., Hober-Vandenberghe C., Belaich S., Vantyghem M.-C., Lefebvre J., Wattré P., Hober-Vandenberghe C., Vantyghem M. 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. doi: 10.1002/(SICI)1096-9071(199706)52:2<121::AID-JMV1>;2-5.
    1. Andréoletti L., Hober D., Hober-Vandenberghe C., Fajardy I., Belaich S., Lambert V., Vantyghem M.C., Lefebvre J., Wattre P. Coxsackie B virus infection and beta cell autoantibodies in newly diagnosed IDDM adult patients. Clin. Diagn. Virol. 1998;9:125–133. doi: 10.1016/S0928-0197(98)00011-7.
    1. Oikarinen S., Martiskainen M., Tauriainen S., Huhtala H., Ilonen J., Veijola R., Simell O., Knip M., Hyöty H. Enterovirus RNA in blood is linked to the development of type 1 diabetes. Diabetes. 2011;60:276–279. doi: 10.2337/db10-0186.
    1. Juhela S., Hyoty H., Roivainen M., Härkönen T., Putto-Laurila A., Simell O., Ilonen J. T-cell responses to enterovirus antigens in children with type 1 diabetes. Diabetes. 2000;49:1308–1313. doi: 10.2337/diabetes.49.8.1308.
    1. Yoon J.W., Austin M., Onodera T., Notkins A.L. Isolation of a virus from the pancreas of a child with diabetic ketoacidosis. N. Engl. J. Med. 1979;300:1173–1179. doi: 10.1056/NEJM197905243002102.
    1. Dotta F., Censini S., van Halteren A.G., Marselli L., Masini M., Dionisi S., Mosca F., Boggi U., Muda A.O., Del Prato S., et al. 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. doi: 10.1073/pnas.0700442104.
    1. Pane J.A., Coulson B.S. Lessons from the mouse: Potential contribution of bystander lymphocyte activation by viruses to human type 1 diabetes. Diabetologia. 2015;58:1149–1159. doi: 10.1007/s00125-015-3562-3.
    1. Serreze D.V., Ottendorfer E.W., Ellis T.M., Gauntt C.J., Atkinson M.A. 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. doi: 10.2337/diabetes.49.5.708.
    1. Christen U., Wolfe T., Möhrle U., Hughes A.C., Rodrigo E., Green E.A., Flavell R.A., von Herrath M.G. 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. doi: 10.4049/jimmunol.166.12.7023.
    1. Kaufman D.L., Erlander M.G., Clare-Salzler M., Atkinson M.A., MacLaren N.K., Tobin A.J. Autoimmunity to two forms of glutamate decarboxylase in insulin-dependent diabetes mellitus. J. Clin. Investig. 1992;89:283–292. doi: 10.1172/JCI115573.
    1. Hou J., Said C., Franchi D., Dockstader P., Chatterjee N.K. Antibodies to Glutamic Acid Decarboxylase and P2-C Peptides in Sera from Coxsackie Virus B4-Infected Mice and IDDM Patients. Diabetes. 1994;43:1260–1266. doi: 10.2337/diab.43.10.1260.
    1. Yokota I., Shima K. GAD antibody in IDDM. Rinsho. Byori. 1998;46:331–337.
    1. Hansson S.F., Korsgren S., Pontén F., Korsgren O. Enteroviruses and the pathogenesis of type 1 diabetes revisited: Cross-reactivity of enterovirus capsid protein (VP1) antibodies with human mitochondrial proteins. J. Pathol. 2013;229:719–728. doi: 10.1002/path.4166.
    1. Casabonne D., Green J., Newton R. Coxsackie B virus serology and Type 1 diabetes mellitus: A systematic review of published case-control studies. Diabet. Med. 2004;21:507–514.
    1. Honeyman M.C., Coulson B.S., Stone N.L., Gellert S.A., Goldwater P.N., Steele C.E., Couper J.J., Tait B.D., Colman P.G., Harrison L.C. Association between rotavirus infection and pancreatic islet autoimmunity in children at risk of developing type 1 diabetes. Diabetes. 2000;49:1319–1324. doi: 10.2337/diabetes.49.8.1319.
    1. Blomqvist M., Juhela S., Erkkilä S., Korhonen S., Simell T., Kupila A., Vaarala O., Simell O., Knip M., Ilonen J. Rotavirus infections and development of diabetes-associated autoantibodies during the first 2 years of life. Clin. Exp. Immunol. 2002;128:511–515. doi: 10.1046/j.1365-2249.2002.01842.x.
    1. Pane J.A., Webster N.L., Coulson B.S. Rotavirus Activates Lymphocytes from Non-Obese Diabetic Mice by Triggering Toll-Like Receptor 7 Signaling and Interferon Production in Plasmacytoid Dendritic Cells. PLoS Pathog. 2014;10:e1003998. doi: 10.1371/journal.ppat.1003998.
    1. Graham K.L., Sanders N., Tan Y., Allison J., Kay T.W.H., Coulson B.S. Rotavirus Infection Accelerates Type 1 Diabetes in Mice with Established Insulitis. J. Virol. 2008;82:6139–6149. doi: 10.1128/JVI.00597-08.
    1. Pane J.A., Webster N.L., Graham K.L., Holloway G., Zufferey C., Coulson B.S. Rotavirus acceleration of murine type 1 diabetes is associated with a T helper 1-dependent specific serum antibody response and virus effects in regional lymph nodes. Diabetologia. 2013;56:573–582. doi: 10.1007/s00125-012-2798-4.
    1. Roman L.M., Simons L.F., Hammer R.E., Sambrook J.F., Gething M.J. The expression of influenza virus hemagglutinin in the pancreatic beta cells of transgenic mice results in autoimmune diabetes. Cell. 1990;61:383–396. doi: 10.1016/0092-8674(90)90521-F.
    1. Capua I., Mercalli A., Pizzuto M.S., Romero-Tejeda A., Kasloff S., De Battisti C., Bonfante F., Patrono L.V., Vicenzi E., Zappulli V., et al. Influenza A viruses grow in human pancreatic cells and cause pancreatitis and diabetes in an animal model. J. Virol. 2013;87:597–610. doi: 10.1128/JVI.00714-12.
    1. Likos A.M., Kelvin D.J., Cameron C.M., Rowe T., Kuehnert M.J., Norris P.J. National Heart, Lung, Blood Institute Retrovirus Epidemiology Donor Study-II (REDS-II). Influenza viremia and the potential for blood-borne transmission. Transfusion. 2007;47:1080–1088. doi: 10.1111/j.1537-2995.2007.01264.x.
    1. Oughton M., Dascal A., LaPorta D., Charest H., Afilalo M., Miller M. Evidence of viremia in 2 cases of severe pandemic influenza A H1N1/09. Diagn. Microbiol. Infect. Dis. 2011;70:213–217. doi: 10.1016/j.diagmicrobio.2010.12.013.
    1. Tan H., Wang C., Yu Y. H1N1 Influenza: The Trigger of Diabetic Ketoacidosis in a Young Woman with Ketosis-Prone Diabetes. Am. J. Med. Sci. 2012;343:180–183. doi: 10.1097/MAJ.0b013e3182376cc4.
    1. Watanabe N. Conversion to type 1 diabetes after H1N1 influenza infection: A case report. J. Diabetes. 2011;3:103. doi: 10.1111/j.1753-0407.2010.00110.x.
    1. Nenna R., Papoff P., Moretti C., Pierangeli A., Sabatino G., Costantino F., Soscia F., Cangiano G., Ferro V., Mennini M., et al. Detection of Respiratory Viruses in the 2009 Winter Season in Rome: 2009 Influenza a (H1N1) Complications in Children and Concomitant Type 1 Diabetes Onset. Int. J. Immunopathol. Pharmacol. 2011;24:651–659. doi: 10.1177/039463201102400311.
    1. Lönnrot M., Lynch K.F., Larsson H.E., Lernmark Å., Rewers M.J., Törn C., Burkhardt B.R., Briese T., Hagopian W.A., She J.X., et al. Respiratory infections are temporally associated with initiation of type 1 diabetes autoimmunity: The TEDDY study. Diabetologia. 2017;60:1931–1940. doi: 10.1007/s00125-017-4365-5.
    1. Ferreira R.C., Guo H., Coulson R.M., Smyth D.J., Pekalski M.L., Burren O.S., Cutler A.J., Doecke J.D., Flint S., McKinney E.F., et al. A Type I Interferon Transcriptional Signature Precedes Autoimmunity in Children Genetically at Risk for Type 1 Diabetes. Diabetes. 2014;63:2538–2550. doi: 10.2337/db13-1777.
    1. Xia C.Q., Peng R., Chernatynskaya A.V., Yuan L., Carter C., Valentine J., Sobel E., Atkinson M.A., Clare-Salzler M.J. Increased IFN-α-producing Plasmacytoid Dendritic Cells (pDCs) in Human Th1-mediated Type 1 Diabetes: pDCs Augment Th1 Responses through IFN-α Production1. J. Immunol. 2014;193:1024–1034. doi: 10.4049/jimmunol.1303230.
    1. Zanker D.J., Oveissi S., Tscharke D.C., Duan M., Wan S., Zhang X., Xiao K., Mifsud N.A., Gibbs J., Izzard L., et al. Influenza A Virus Infection Induces Viral and Cellular Defective Ribosomal Products Encoded by Alternative Reading Frames. J. Immunol. 2019;202:3370–3380. doi: 10.4049/jimmunol.1900070.
    1. Ahmed S.S., Volkmuth W., Duca J., Corti L., Pallaoro M., Pezzicoli A., Karle A., Rigat F., Rappuoli R., Narasimhan V., et al. Antibodies to influenza nucleoprotein cross-react with human hypocretin receptor 2. Sci. Transl. Med. 2015;7:294ra105. doi: 10.1126/scitranslmed.aab2354.
    1. Luo G., Ambati A., Lin L., Bonvalet M., Partinen M., Ji X., Maecker H.T., Mignot E.J.M. Autoimmunity to hypocretin and molecular mimicry to flu in type 1 narcolepsy. Proc. Natl. Acad. Sci. USA. 2018;115:E12323–E12332. doi: 10.1073/pnas.1818150116.
    1. Han F., Lin L., Warby S.C., Faraco J., Li J., Dong S.X., An P., Zhao L., Wang L.H., Li Q.Y., et al. Narcolepsy onset is seasonal and increased following the 2009 H1N1 pandemic in china. Ann. Neurol. 2011;70:410–417. doi: 10.1002/ana.22587.
    1. Stowe J., Andrews N., Kosky C., Dennis G., Eriksson S., Hall A., Leschziner G., Reading P., Shneerson J.M., Donegan K., et al. Risk of Narcolepsy after AS03 Adjuvanted Pandemic A/H1N1 2009 Influenza Vaccine in Adults: A Case-Coverage Study in England. Sleep. 2016;39:1051–1057. doi: 10.5665/sleep.5752.
    1. Nohynek H., Jokinen J., Partinen M., Vaarala O., Kirjavainen T., Sundman J., Himanen S.L., Hublin C., Julkunen I., Olsén P., et al. AS03 adjuvanted AH1N1 vaccine associated with an abrupt increase in the incidence of childhood narcolepsy in Finland. PLoS ONE. 2012;7:e33536. doi: 10.1371/journal.pone.0033536.
    1. Tsai T.F. MF59 Adjuvanted Seasonal and Pandemic Influenza Vaccines. Yakugaku Zasshi. 2011;131:1733–1741. doi: 10.1248/yakushi.131.1733.
    1. Update on Narcolepsy Cases Associated with Pandemrix Vaccination in 2009 in the Netherlands. [(accessed on 21 March 2019)]; Available online: .
    1. Ahmed S.S., Steinman L. Narcolepsy and influenza vaccination-induced autoimmunity. Ann. Transl. Med. 2017;5:25. doi: 10.21037/atm.2016.12.63.
    1. Virtanen J.O., Jacobson S. Viruses and multiple sclerosis. CNS Neurol. Disord. Drug Targets. 2012;11:528–544. doi: 10.2174/187152712801661220.
    1. Draborg A.H., Duus K., Houen G. Epstein-Barr Virus and Systemic Lupus Erythematosus. Clin. Dev. Immunol. 2012;2012:1–10. doi: 10.1155/2012/370516.
    1. Draborg A.H., Duus K., Houen G. Epstein-Barr Virus in Systemic Autoimmune Diseases. Clin. Dev. Immunol. 2013;2013:1–9. doi: 10.1155/2013/535738.
    1. Yu S.F., Wu H.C., Tsai W.C., Yen J.H., Chiang W., Yuo C.Y., Lu S.N., Chiang L.C., Chen C.J. Detecting Epstein-Barr virus DNA from peripheral blood mononuclear cells in adult patients with systemic lupus erythematosus in Taiwan. Med. Microbiol. Immunol. 2005;194:115–120. doi: 10.1007/s00430-004-0230-5.
    1. Moon U.Y., Park S.J., Oh S.T., Kim W.U., Park S.H., Lee S.H., Cho C.S., Kim H.Y., Lee W.K., Lee S.K. Patients with systemic lupus erythematosus have abnormally elevated Epstein–Barr virus load in blood. Arthritis Res. Ther. 2004;6:R295–R302. doi: 10.1186/ar1181.
    1. Gross A.J., Hochberg D., Rand W.M., Thorley-Lawson D.A. EBV and Systemic Lupus Erythematosus: A New Perspective. J. Immunol. 2005;174:6599–6607. doi: 10.4049/jimmunol.174.11.6599.
    1. Draborg A., Jørgensen J., Muller H., Nielsen C., Jacobsen S., Iversen L., Theander E., Nielsen L., Houen G., Duus K. Epstein–Barr virus early antigen diffuse (EBV-EA/D)-directed immunoglobulin A antibodies in systemic lupus erythematosus patients. Scand. J. Rheumatol. 2012;41:280–289. doi: 10.3109/03009742.2012.665944.
    1. Poole B.D., Scofield R.H., Harley J.B., James J.A. Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity. 2006;39:63–70. doi: 10.1080/08916930500484849.
    1. Iwakiri D., Zhou L., Samanta M., Matsumoto M., Ebihara T., Seya T., Imai S., Fujieda M., Kawa K., Takada K. Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J. Exp. Med. 2009;206:2091–2099. doi: 10.1084/jem.20081761.
    1. Sanders V.J., Waddell A.E., Felisan S.L., Li X., Conrad A.J., Tourtellotte W.W. Herpes Simplex Virus in Postmortem Multiple Sclerosis Brain Tissue. Arch. Neurol. 1996;53:125–133. doi: 10.1001/archneur.1996.00550020029012.
    1. Chucair-Elliott A.J., Conrady C., Zheng M., Kroll C.M., Lane T.E., Carr D.J.J. Microglia-induced IL-6 protects against neuronal loss following HSV-1 infection of neural progenitor cells. Glia. 2014;62:1418–1434. doi: 10.1002/glia.22689.
    1. Lünemann J.D. Epstein-Barr virus in multiple sclerosis: A continuing conundrum. Neurology. 2012;78:11–12. doi: 10.1212/WNL.0b013e318241f2b3.
    1. Verjans G.M., Remeijer L., Mooy C.M., Osterhaus A.D. Herpes simplex virus-specific T cells infiltrate the cornea of patients with herpetic stromal keratitis: No evidence for autoreactive T cells. Investig. Ophthalmol. Vis. Sci. 2000;41:2607–2612.
    1. Pak C., McArthur R., Eun H.M., Yoon J.W. Association of cytomegalovirus infection with autoimmune type 1 diabetes. Lancet. 1988;332:1–4. doi: 10.1016/S0140-6736(88)92941-8.
    1. Rickinson A.B., Young L.S., Rowe M. Influence of the Epstein-Barr virus nuclear antigen EBNA 2 on the growth phenotype of virus-transformed B cells. J. Virol. 1987;61:1310–1317.
    1. Kemppainen K.M., Lynch K.F., Liu E., Lönnrot M., Simell V., Briese T., Koletzko S., Hagopian W., Rewers M., She J.X., et al. Factors That Increase Risk of Celiac Disease Autoimmunity after a Gastrointestinal Infection in Early Life. Clin. Gastroenterol. Hepatol. 2017;15:694–702. doi: 10.1016/j.cgh.2016.10.033.
    1. Christen U., Von Herrath M.G. Infections and Autoimmunity—Good or Bad? J. Immunol. 2005;174:7481–7486. doi: 10.4049/jimmunol.174.12.7481.
    1. Plot L., Amital H., Barzilai O., Ram M., Nicola B., Shoenfeld Y. Infections May Have a Protective Role in the Etiopathogenesis of Celiac Disease. Ann. N. Y. Acad. Sci. 2009;1173:670–674. doi: 10.1111/j.1749-6632.2009.04814.x.
    1. Jansen M.A., van den Heuvel D., van der Zwet K.V., Jaddoe V.W., Hofman A., Escher J.C., Fraaij P.L., Hooijkaas H., van Zelm M.C., Moll H.A. Herpesvirus Infections and Transglutaminase Type 2 Antibody Positivity in Childhood: The Generation R Study. J. Pediatr. Gastroenterol. Nutr. 2016;63:423–430. doi: 10.1097/MPG.0000000000001163.
    1. Jansen M.A., Beth S.A., Van Den Heuvel D., Kiefte-de Jong J.C., Raat H., Jaddoe V.W., van Zelm M.C., Moll H.A. Ethnic differences in coeliac disease autoimmunity in childhood: The Generation R Study. Arch. Dis. Child. 2017;102:529–534. doi: 10.1136/archdischild-2016-311343.
    1. Caminero A., Galipeau H.J., McCarville J.L., Johnston C.W., Bernier S.P., Russell A.K., Jury J., Herran A.R., Casqueiro J., Tye-Din J.A., et al. Duodenal Bacteria from Patients With Celiac Disease and Healthy Subjects Distinctly Affect Gluten Breakdown and Immunogenicity. Gastroenterology. 2016;151:670–683. doi: 10.1053/j.gastro.2016.06.041.
    1. Zandman-Goddard G. Parasitic infection and autoimmunity. Lupus. 2009;18:1144–1148. doi: 10.1177/0961203309345735.
    1. Correale J., Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann. Neurol. 2007;61:97–108. doi: 10.1002/ana.21067.
    1. Correale J., Farez M.F. The impact of parasite infections on the course of multiple sclerosis. J. Neuroimmunol. 2011;233:6–11. doi: 10.1016/j.jneuroim.2011.01.002.
    1. Finlay C.M., Stefanska A.M., Walsh K.P., Kelly P.J., Boon L., Lavelle E.C., Walsh P.T., Mills K.H. Helminth Products Protect against Autoimmunity via Innate Type 2 Cytokines IL-5 and IL-33, Which Promote Eosinophilia. J. Immunol. 2016;196:703–714. doi: 10.4049/jimmunol.1501820.
    1. Ramondetti F., Sacco S., Comelli M., Bruno G., Falorni A., Iannilli A., d’Annunzio G., Iafusco D., Songini M., Toni S., et al. Type 1 diabetes and measles, mumps and rubella childhood infections within the Italian Insulin-dependent Diabetes Registry. Diabet. Med. 2012;29:761–766. doi: 10.1111/j.1464-5491.2011.03529.x.
    1. Vuorinen T., Nikolakaros G., Smell O., Hyypiä T., Vainionpää R. Mumps and Coxsackie B3 Virus Infection of Human Fetal Pancreatic Islet-like Cell Clusters. Pancreas. 1992;7:460–464. doi: 10.1097/00006676-199207000-00007.
    1. Numazaki K., Goldman H., Seemayer T.A., Wong I., Wainberg M.A. Infection by human cytomegalovirus and rubella virus of cultured human fetal islets of Langerhans. Vivo. 1990;4:49–54.
    1. Pinto-Díaz C.A., Rodríguez Y., Monsalve D.M., Acosta-Ampudia Y., Molano-González N., Anaya J.M., Ramírez-Santana C. Autoimmunity in Guillain-Barré syndrome associated with Zika virus infection and beyond. Autoimmun. Rev. 2017;16:327–334. doi: 10.1016/j.autrev.2017.02.002.
    1. Talib S.H., Bhattu S., Bhattu R., Deshpande S., Dahiphale D. Dengue fever triggering systemic lupus erythematosus and lupus nephritis: A case report. Int. Med Case Rep. J. 2013;6:71–75. doi: 10.2147/IMCRJ.S50708.
    1. Lucchese G., Stahl B. Peptide Sharing Between Viruses and DLX Proteins: A Potential Cross-Reactivity Pathway to Neuropsychiatric Disorders. Front. Mol. Neurosci. 2018;12:150. doi: 10.3389/fnins.2018.00150.
    1. Newcomer J.W., Farber N.B., Olney J.W. NMDA receptor function, memory, and brain aging. Dialog. Clin. Neurosci. 2000;2:219–232.
    1. Lucchese G. Understanding Neuropsychiatric Diseases, Analyzing the Peptide Sharing between Infectious Agents and the Language-Associated NMDA 2A Protein. Front. Psychol. 2016;7:60. doi: 10.3389/fpsyt.2016.00060.
    1. Kanduc D. The comparative biochemistry of viruses and humans: An evolutionary path towards autoimmunity. Biol. Chem. 2019;400:629–638. doi: 10.1515/hsz-2018-0271.
    1. Tracy S., Drescher K.M., Jackson J.D., Kim K., Kono K. Enteroviruses, type 1 diabetes and hygiene: A complex relationship. Rev. Med Virol. 2010;20:106–116. doi: 10.1002/rmv.639.
    1. Christen U., Von Herrath M.G. Do viral infections protect from or enhance type 1 diabetes and how can we tell the difference? Cell. Mol. Immunol. 2011;8:193–198. doi: 10.1038/cmi.2010.71.
    1. Sanderson N.S.R., Zimmermann M., Eilinger L., Gubser C., Schaeren-Wiemers N., Lindberg R.L.P., Dougan S.K., Ploegh H.L., Kappos L., Derfuss T. Cocapture of cognate and bystander antigens can activate autoreactive B cells. Proc. Natl. Acad. Sci. USA. 2017;114:734–739. doi: 10.1073/pnas.1614472114.
    1. Root-Bernstein R. Human Immunodeficiency Virus Proteins Mimic Human T Cell Receptors Inducing Cross-Reactive Antibodies. Int. J. Mol. Sci. 2017;18:2091. doi: 10.3390/ijms18102091.
    1. Mokhtarian F., Safavi F., Sarafraz-Yazdi E. Immunization with a peptide of Semliki Forest virus promotes remyelination in experimental autoimmune encephalomyelitis. Brain Res. 2012;1488:92–103. doi: 10.1016/j.brainres.2012.09.038.
    1. Bradshaw M.J., Pawate S., Lennon V.A., Bloch K.C., Brown K.M. Herpes simplex virus 1 encephalitis associated with voltage-gated calcium channel autoimmunity. Neurology. 2015;85:2176–2177. doi: 10.1212/WNL.0000000000002218.
    1. Cabibi D. Autoimmune hepatitis following Epstein–Barr virus infection. BMJ Case Rep. 2008;2008:bcr0620080071. doi: 10.1136/bcr.06.2008.0071.
    1. Fairweather D., Rose N.R. Coxsackievirus-induced myocarditis in mice: A model of autoimmune disease for studying immunotoxicity. Methods. 2007;41:118–122. doi: 10.1016/j.ymeth.2006.07.009.
    1. Rose N.R. Critical Cytokine Pathways to Cardiac Inflammation. J. Interf. Cytokine Res. 2011;31:705–710. doi: 10.1089/jir.2011.0057.
    1. Caselli E., D’Accolti M., Soffritti I., Zatelli M.C., Rossi R., Degli Uberti E., Di Luca D. HHV-6A in vitro infection of thyrocytes and T cells alters the expression of miRNA associated to autoimmune thyroiditis. Virol. J. 2017;14:3. doi: 10.1186/s12985-016-0672-6.
    1. Ogishi M., Yotsuyanagi H., Moriya K., Koike K. Delineation of autoantibody repertoire through differential proteogenomics in hepatitis C virus-induced cryoglobulinemia. Sci. Rep. 2016;6:29532. doi: 10.1038/srep29532.
    1. Armangue T., Leypoldt F., Málaga I., Raspall-Chaure M., Martì I., Nichter C., Pugh J., Vicente-Rasoamalala M., Lafuente-Hidalgo M., Macaya A., et al. Herpes Simplex Virus Encephalitis is a Trigger of Brain Autoimmunity. Ann. Neurol. 2014;75:317–323. doi: 10.1002/ana.24083.
    1. Kothur K., Gill D., Wong M., Mohammad S.S., Bandodkar S., Arbunckle S., Wienholt L., Dale R.C. Cerebrospinal fluid cyto-/chemokine profile during acute herpes simplex virus induced anti-N-methyl-d -aspartate receptor encephalitis and in chronic neurological sequelae. Dev. Med. Child Neurol. 2017;59:806–814. doi: 10.1111/dmcn.13431.
    1. He D., Zhang H., Xiao J., Zhang X., Xie M., Pan D., Wang M., Luo X., Bu B., Zhang M., et al. Molecular and clinical relationship between live-attenuated Japanese encephalitis vaccination and childhood onset myasthenia gravis. Ann. Neurol. 2018;84:386–400. doi: 10.1002/ana.25267.
    1. Casiraghi C., Márquez A.C., Shanina I., Horwitz M.S. Latent virus infection upregulates CD40 expression facilitating enhanced autoimmunity in a model of multiple sclerosis. Sci. Rep. 2015;5:13995. doi: 10.1038/srep13995.
    1. Nagata K., Kumata K., Nakayama Y., Satoh Y., Sugihara H., Hara S., Matsushita M., Kuwamoto S., Kato M., Murakami I., et al. Epstein–Barr Virus Lytic Reactivation Activates B Cells Polyclonally and Induces Activation-Induced Cytidine Deaminase Expression: A Mechanism Underlying Autoimmunity and Its Contribution to Graves’ Disease. Viral Immunol. 2017;30:240–249. doi: 10.1089/vim.2016.0179.
    1. Lucchese G., Kanduc D. Zika virus and autoimmunity: From microcephaly to Guillain-Barré syndrome, and beyond. Autoimmun. Rev. 2016;15:801–808. doi: 10.1016/j.autrev.2016.03.020.
    1. Janegova A., Janega P., Rychly B., Kuracinova K., Babal P. The role of Epstein-Barr virus infection in the development of autoimmune thyroid diseases. Endokrynol. Pol. 2015;66:132–136. doi: 10.5603/EP.2015.0020.
    1. Tampaki M., Koskinas J. Extrahepatic immune related manifestations in chronic hepatitis C virus infection. World J. Gastroenterol. 2014;20:12372–12380. doi: 10.3748/wjg.v20.i35.12372.
    1. Pewe L., Perlman S. Cutting edge: CD8 T cell-mediated demyelination is IFN-gamma dependent in mice infected with a neurotropic coronavirus. J. Immunol. 2002;168:1547–1551. doi: 10.4049/jimmunol.168.4.1547.
    1. Choi K.S., Jun H.S., Kim H.N., Park H.J., Eom Y.W., Noh H.L., Kwon H., Kim H.M., Yoon J.W. Role of Hck in the Pathogenesis of Encephalomyocarditis Virus-Induced Diabetes in Mice. J. Virol. 2001;75:1949–1957. doi: 10.1128/JVI.75.4.1949-1957.2001.
    1. Honkanen H., Oikarinen S., Nurminen N., Huhtala H., Lehtonen J., Ruokoranta T., Lecouturier V., Tauriainen S., Ilonen J., Veijola R., et al. Detection of enteroviruses in stools precedes islet autoimmunity by several months: Possible evidence for slowly operating mechanisms in virus-induced autoimmunity. Diabetologia. 2017;60:424–431. doi: 10.1007/s00125-016-4177-z.
    1. Chiu S., Fernandez R., Subramanian V., Sun H., DeCamp M.M., Kreisel D., Perlman H., Budinger G.R.S., Mohanakumar T., Bharat A. Lung injury combined with loss of regulatory T cells leads to de novo lung-restricted autoimmunity. J. Immunol. 2016;197:51–57. doi: 10.4049/jimmunol.1502539.
    1. Guan Y., Jakimovski D., Ramanathan M., Weinstock-Guttman B., Zivadinov R. The role of Epstein-Barr virus in multiple sclerosis: From molecular pathophysiology to in vivo imaging. Neural Regen. Res. 2019;14:373–386.
    1. Miller S.D., Katz-Levy Y., Neville K.L., VanderLugt C.L. Virus-induced autoimmunity: Epitope spreading to myelin autoepitopes in theiler’s virus infection of the central nervous system. Adv Virus Res. 2001;56:199–217.
    1. Sotelo J., Corona T. Varicella Zoster Virus and Relapsing Remitting Multiple Sclerosis. Mult. Scler. Int. 2011;2011:214763. doi: 10.1155/2011/214763.
    1. Tucker W.G., Paskauskas R.A. The MSMV hypothesis: Measles virus and multiple sclerosis, etiology and treatment. Med. Hypotheses. 2008;71:682–689. doi: 10.1016/j.mehy.2008.06.029.
    1. Vanheusden M., Broux B., Welten S.P.M., Peeters L.M., Panagioti E., Van Wijmeersch B., Somers V., Stinissen P., Arens R., Hellings N. Cytomegalovirus infection exacerbates autoimmune mediated neuroinflammation. Sci. Rep. 2017;7:663. doi: 10.1038/s41598-017-00645-3.
    1. McBride W., Gill K.R., Wiviott L. West Nile Virus infection with hearing loss. J. Infect. 2006;53:e203–e205. doi: 10.1016/j.jinf.2006.01.017.
    1. Bangham C.R.M., Araújo A., Yamano Y., Taylor G.P. HTLV-1-associated myelopathy/tropical spastic paraparesis. Nat. Rev. Dis. Prim. 2015;1:15012. doi: 10.1038/nrdp.2015.12.
    1. Zuckerman E., Keren D., Rozenbaum M., Toubi E., Slobodin G., Tamir A., Naschitz J.E., Yeshurun D., Rosner I. Hepatitis C virus-related arthritis: Characteristics and response to therapy with interferon alpha. Clin. Exp. Rheumatol. 2000;18:579–584.
    1. Bennion B.G., Ingle H., Ai T.L., Miner C.A., Platt D.J., Smith A.M., Baldridge M.T., Miner J.J. A Human Gain-of-Function STING Mutation Causes Immunodeficiency and Gammaherpesvirus-Induced Pulmonary Fibrosis in Mice. J. Virol. 2019;93:e01806-18. doi: 10.1128/JVI.01806-18.
    1. Dostál C., Newkirk M.M., Duffy K.N., Palecková A., Bosák V., Cerná M., Zd’arský E., Zvárová J. Herpes viruses in multicase families with rheumatoid arthritis and systemic lupus erythematosus. Ann. N. Y. Acad. Sci. 1997;815:334–337. doi: 10.1111/j.1749-6632.1997.tb52078.x.
    1. Pera A., Broadley I., Davies K.A., Kern F. Cytomegalovirus as a Driver of Excess Cardiovascular Mortality in Rheumatoid Arthritis: A Red Herring or a Smoking Gun? Circ. Res. 2017;120:274–277. doi: 10.1161/CIRCRESAHA.116.309982.
    1. Slight-Webb S.R., Bagavant H., Crowe S.R., James J.A. Influenza A (H1N1) Virus Infection Triggers Severe Pulmonary Inflammation in Lupus-Prone Mice following Viral Clearance. J. Autoimmun. 2015;57:66–76. doi: 10.1016/j.jaut.2014.12.003.
    1. Ramos-Casals M., Loustaud-Ratti V., De Vita S., Zeher M., Bosch J.-A., Toussirot E., Medina F., Rosas J., Anaya J.-M., Font J. Sjögren syndrome associated with hepatitis C virus: A multicenter analysis of 137 cases. Medicine. 2005;84:81–89. doi: 10.1097/01.md.0000157397.30055.c9.
    1. Deshpande S.P., Lee S., Zheng M., Song B., Knipe D., Kapp J.A., Rouse B.T. Herpes Simplex Virus-Induced Keratitis: Evaluation of the Role of Molecular Mimicry in Lesion Pathogenesis. J. Virol. 2001;75:3077–3088. doi: 10.1128/JVI.75.7.3077-3088.2001.
    1. Farooq A.V., Shukla D. Herpes Simplex Epithelial and Stromal Keratitis: An Epidemiologic Update. Surv. Ophthalmol. 2012;57:448–462. doi: 10.1016/j.survophthal.2012.01.005.
    1. Goupil B.A., Mores C.N. A Review of Chikungunya Virus-induced Arthralgia: Clinical Manifestations, Therapeutics, and Pathogenesis. Open Rheumatol. J. 2016;10:129–140. doi: 10.2174/1874312901610010129.
    1. Chen J., Zhang H., Chen P., Lin Q., Zhu X., Zhang L., Xue X. Correlation between systemic lupus erythematosus and cytomegalovirus infection detected by different methods. Clin. Rheumatol. 2015;34:691–698. doi: 10.1007/s10067-015-2868-3.
    1. Stölzel U., Schuppan D., Tillmann H.L., Manns M.P., Tannapfel A., Doss M.O., Zimmer T., Köstler E. Autoimmunity and HCV infection in porphyria cutanea tarda: A controlled study. Cell. Mol. Biol. 2002;48:43–47.
    1. Ribeiro F.M., Gomez V.E., Albuquerque E.M., Klumb E.M., Shoenfeld Y. Lupus and leprosy: Beyond the coincidence. Immunol. Res. 2015;61:160–163. doi: 10.1007/s12026-014-8596-y.
    1. Steed A.L., Stappenbeck T.S. Role of Viruses and Bacteria-Virus Interactions in Autoimmunity. Curr. Opin. Immunol. 2014;31:102–107. doi: 10.1016/j.coi.2014.10.006.
    1. Cashman K.A., Wilkinson E.R., Zeng X., Cardile A.P., Facemire P.R., Bell T.M., Bearss J.J., Shaia C.I., Schmaljohn C.S., Garry R., et al. Immune-Mediated Systemic Vasculitis as the Proposed Cause of Sudden-Onset Sensorineural Hearing Loss following Lassa Virus Exposure in Cynomolgus Macaques. MBio. 2018;9 doi: 10.1128/mBio.01896-18.
    1. Dahal S., Upadhyay S., Banjade R., Dhakal P., Khanal N., Bhatt V.R. Thrombocytopenia in Patients with Chronic Hepatitis C Virus Infection. Mediterr. J. Hematol. Infect. Dis. 2017;9:e2017019. doi: 10.4084/mjhid.2017.019.
    1. Ferri C., Colaci M., Fallahi P., Ferrari S.M., Antonelli A., Giuggioli D. Thyroid Involvement in Hepatitis C Virus-Infected Patients with/without Mixed Cryoglobulinemia. Front. Endocrinol. 2017;8:159. doi: 10.3389/fendo.2017.00159.
    1. Olsberg C., Pelka A., Miller S., Waltenbaugh C., Creighton T.M., Dal Canto M.C., Lipton H., Melvold R. Induction of Theiler’s murine encephalomyelitis virus (TMEV)-induced demyelinating disease in genetically resistant mice. Reg Immunol. 1993;5:1–10.
    1. Eizirik D.L., De Beeck A.O. Coxsackievirus and Type 1 Diabetes Mellitus: The Wolf’s Footprints. Trends Endocrinol. Metab. 2018;29:137–139. doi: 10.1016/j.tem.2017.12.002.
    1. Laitinen O.H., Honkanen H., Pakkanen O., Oikarinen S., Hankaniemi M.M., Huhtala H., Ruokoranta T., Lecouturier V., André P., Harju R., et al. Coxsackievirus B1 is associated with induction of β-cell autoimmunity that portends type 1 diabetes. Diabetes. 2014;63:446–455. doi: 10.2337/db13-0619.
    1. Stene L.C., Rewers M. Immunology in the clinic review series; focus on type 1 diabetes and viruses: The enterovirus link to type 1 diabetes: Critical review of human studies. Clin. Exp. Immunol. 2012;168:12–23. doi: 10.1111/j.1365-2249.2011.04555.x.
    1. Cacoub P., Terrier B., Saadoun D. Hepatitis C virus-induced vasculitis: Therapeutic options. Ann. Rheum. Dis. 2014;73:24–30. doi: 10.1136/annrheumdis-2013-203883.

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi