230
Views
0
CrossRef citations to date
0
Altmetric
Review Article

The role of Epstein-Barr virus in autoimmune and autoinflammatory diseases

, , , & ORCID Icon
Received 16 Jan 2024, Accepted 11 Apr 2024, Published online: 18 Apr 2024

References

  • Afrasiabi A, Parnell GP, Fewings N, Schibeci SD, Basuki MA, Chandramohan R, Zhou Y, Taylor B, Brown DA, Swaminathan S, et al. 2019. Evidence from genome wide association studies implicates reduced control of Epstein-Barr virus infection in multiple sclerosis susceptibility. Genome Med. 11(1):26. doi:10.1186/s13073-019-0640-z.
  • Afrasiabi A, Parnell GP, Swaminathan S, Stewart GJ, Booth DR. 2020. The interaction of multiple sclerosis risk loci with Epstein-Barr virus phenotypes implicates the virus in pathogenesis. Sci Rep. 10(1):193. doi:10.1038/s41598-019-55850-z.
  • Afzal M, Nigam GB. 2018. EBV colitis with ulcerative colitis: a double whammy. BMJ Case Rep. 2018 doi:10.1136/bcr-2018-224963.
  • Alotaibi S, Kennedy J, Tellier R, Stephens D, Banwell B. 2004. Epstein-Barr virus in pediatric multiple sclerosis. JAMA. 291(15):1875–1879. doi:10.1001/jama.291.15.1875.
  • Alspaugh MA, Henle G, Lennette ET, Henle W. 1981. Elevated levels of antibodies to Epstein-Barr virus antigens in sera and synovial fluids of patients with rheumatoid arthritis. J Clin Invest. 67(4):1134–1140. doi:10.1172/jci110127.
  • Andari S, Hussein H, Fadlallah S, Jurjus AR, Shirinian M, Hashash JG, Rahal EA. 2021. Epstein-Barr Virus DNA Exacerbates Colitis Symptoms in a Mouse Model of Inflammatory Bowel Disease. Viruses. 13(7):1272. doi:10.3390/v13071272.
  • Angelini DF, Serafini B, Piras E, Severa M, Coccia EM, Rosicarelli B, Ruggieri S, Gasperini C, Buttari F, Centonze D, et al. 2013. Increased CD8+ T cell response to Epstein-Barr virus lytic antigens in the active phase of multiple sclerosis. PLoS Pathog. 9(4):e1003220. doi:10.1371/journal.ppat.1003220.
  • Ascherio A, Munger KL, Lennette ET, Spiegelman D, Hernán MA, Olek MJ, Hankinson SE, Hunter DJ. 2001. Epstein-Barr virus antibodies and risk of multiple sclerosis: a prospective study. JAMA. 286(24):3083–3088. doi:10.1001/jama.286.24.3083.
  • Ascherio A, Munger KL, Lünemann JD. 2012. The initiation and prevention of multiple sclerosis. Nat Rev Neurol. 8(11):602–612. doi:10.1038/nrneurol.2012.198.
  • Aygun D, Kuskucu MA, Sahin S, Adrovic A, Barut K, Yıldız M, Sharifova S, Midilli K, Cokugras H, Camcıoglu Y, et al. 2020. Epstein-Barr virus, cytomegalovirus and BK polyomavirus burden in juvenile systemic lupus erythematosus: correlation with clinical and laboratory indices of disease activity. Lupus. 29(10):1263–1269. doi:10.1177/0961203320940029.
  • Bachmann J, Le Thi G, Bruckner A, Kalteis AL, Schwerd T, Koletzko S, Eberhard L. 2021. Epstein-Barr virus prevalence at diagnosis and seroconversion during follow-up in pediatric inflammatory bowel disease. J Clin Med. 10(21):5187.
  • Baecklund E, Iliadou A, Askling J, Ekbom A, Backlin C, Granath F, Catrina AI, Rosenquist R, Feltelius N, Sundström C, et al. 2006. Association of chronic inflammation, not its treatment, with increased lymphoma risk in rheumatoid arthritis. Arthritis Rheum. 54(3):692–701. doi:10.1002/art.21675.
  • Balandraud N, Meynard JB, Auger I, Sovran H, Mugnier B, Reviron D, Roudier J, Roudier C. 2003. Epstein-Barr virus load in the peripheral blood of patients with rheumatoid arthritis: accurate quantification using real-time polymerase chain reaction. Arthritis Rheum. 48(5):1223–1228. doi:10.1002/art.10933.
  • Balandraud N, Roudier J. 2018. Epstein-Barr virus and rheumatoid arthritis. Joint Bone Spine. 85(2):165–170. doi:10.1016/j.jbspin.2017.04.011.
  • Banko A, Miljanovic D, Lazarevic I, Jeremic I, Despotovic A, Grk M, Cirkovic A. 2022. New evidence of significant association between EBV presence and lymphoproliferative disorders susceptibility in patients with rheumatoid arthritis: a systematic review with meta-analysis. Viruses. 14(1):115. doi:10.3390/v14010115.
  • Barcelos F, Martins C, Monteiro R, Cardigos J, Prussiani T, Sítima M, Alves N, Vaz-Patto J, Cunha-Branco J, Borrego L-M, et al. 2021. Association between EBV serological patterns and lymphocytic profile of SjS patients support a virally triggered autoimmune epithelitis. Sci Rep. 11(1):4082. doi:10.1038/s41598-021-83550-0.
  • Barr TA, Shen P, Brown S, Lampropoulou V, Roch T, Lawrie S, Fan B, O’Connor RA, Anderton SM, Bar-Or A, et al. 2012. B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J Exp Med. 209(5):1001–1010. doi:10.1084/jem.20111675.
  • Berner BR, Tary-Lehmann M, Yonkers NL, Askari AD, Lehmann PV, Anthony DD. 2005. Phenotypic and functional analysis of EBV-specific memory CD8 cells in SLE. Cell Immunol. 235(1):29–38. doi:10.1016/j.cellimm.2005.06.010.
  • Bian X, Wallstrom G, Davis A, Wang J, Park J, Throop A, Steel J, Yu X, Wasserfall C, Schatz D, et al. 2016. Immunoproteomic profiling of antiviral antibodies in new-onset type 1 diabetes using protein arrays. Diabetes. 65(1):285–296. doi:10.2337/db15-0179.
  • Bjornevik K, Cortese M, Healy BC, Kuhle J, Mina MJ, Leng Y, Elledge SJ, Niebuhr DW, Scher AI, Munger KL, et al. 2022. Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis. Science. 375(6578):296–301. doi:10.1126/science.abj8222.
  • Blaschke S, Schwarz G, Moneke D, Binder L, Müller G, Reuss-Borst M. 2000. Epstein-Barr virus infection in peripheral blood mononuclear cells, synovial fluid cells, and synovial membranes of patients with rheumatoid arthritis. J Rheumatol. 27(4):866–873.
  • Bo M, Niegowska M, Erre GL, Piras M, Longu MG, Manchia P, Manca M, Passiu G, Sechi LA. 2018. Rheumatoid arthritis patient antibodies highly recognize IL-2 in the immune response pathway involving IRF5 and EBV antigens. Sci Rep. 8(1):1789. doi:10.1038/s41598-018-19957-z.
  • Brito-Zerón P, Baldini C, Bootsma H, Bowman SJ, Jonsson R, Mariette X, Sivils K, Theander E, Tzioufas A, Ramos-Casals M, et al. 2016. Sjögren syndrome. Nat Rev Dis Primers. 2(1):16047. doi:10.1038/nrdp.2016.47.
  • Buonavoglia A, Leone P, Prete M, Solimando AG, Guastadisegno C, Lanave G, Camero M, Martella V, Lo Muzio L, and Racanelli V. 2021. Epstein-Barr virus in salivary samples from systemic lupus erythematosus patients with oral lesions. J Clin Med. 10(21):4995.
  • Burnard S, Lechner-Scott J, Scott RJ. 2017. EBV and MS: major cause, minor contribution or red-herring? Mult Scler Relat Disord. 16:24–30. doi:10.1016/j.msard.2017.06.002.
  • Calabretto M, Di Carlo D, Falasca F, Mazzuti L, Meacci A, Donato G, Greco N, Mezzatesta L, Morrone A, Turriziani O, et al. 2022. Analysis of viral nucleic acids in duodenal biopsies from adult patients with celiac disease. Eur J Gastroenterol Hepatol. 34(11):1107–1110. doi:10.1097/MEG.0000000000002404.
  • Cassaniti I, Cavagna L, Calarota SA, Adzasehoun KMG, Comolli G, Montecucco C, Baldanti F. 2019. Evaluation of EBV- and HCMV-specific T cell responses in systemic lupus erythematosus (SLE) patients using a normalized enzyme-linked immunospot (ELISPOT) assay. J Immunol Res. 2019:4236503–4236512. doi:10.1155/2019/4236503.
  • Catassi C, Verdu EF, Bai JC, Lionetti E. 2022. Coeliac disease. Lancet. 399(10344):2413–2426. doi:10.1016/S0140-6736(22)00794-2.
  • Cepok S, Rosche B, Grummel V, Vogel F, Zhou D, Sayn J, Sommer N, Hartung H-P, Hemmer B. 2005. Short-lived plasma blasts are the main B cell effector subset during the course of multiple sclerosis. Brain. 128(Pt 7):1667–1676. doi:10.1093/brain/awh486.
  • Chen T, Hudnall SD. 2006. Anatomical mapping of human herpesvirus reservoirs of infection. Mod Pathol. 19(5):726–737. doi:10.1038/modpathol.3800584.
  • Choi C, Yu Q, Deb PQ, Wang W. 2020. Rare case of EBV-induced colitis in an immunocompetent individual. BMJ Open Gastroenterol. 7(1):e000360. doi:10.1136/bmjgast-2019-000360.
  • Christen U. 2019. Pathogen infection and autoimmune disease. Clin Exp Immunol. 195(1):10–14. doi:10.1111/cei.13239.
  • Ciccocioppo R, Racca F, Paolucci S, Campanini G, Pozzi L, Betti E, Riboni R, Vanoli A, Baldanti F, Corazza GR, et al. 2015. Human cytomegalovirus and Epstein-Barr virus infection in inflammatory bowel disease: need for mucosal viral load measurement. World J Gastroenterol. 21(6):1915–1926. doi:10.3748/wjg.v21.i6.1915.
  • Ciccocioppo R, Racca F, Scudeller L, Piralla A, Formagnana P, Pozzi L, Betti E, Vanoli A, Riboni R, Kruzliak P, et al. 2016. Differential cellular localization of Epstein-Barr virus and human cytomegalovirus in the colonic mucosa of patients with active or quiescent inflammatory bowel disease. Immunol Res. 64(1):191–203. doi:10.1007/s12026-015-8737-y.
  • Corcione A, Casazza S, Ferretti E, Giunti D, Zappia E, Pistorio A, Gambini C, Mancardi GL, Uccelli A, Pistoia V, et al. 2004. Recapitulation of B cell differentiation in the central nervous system of patients with multiple sclerosis. Proc Natl Acad Sci U S A. 101(30):11064–11069. doi:10.1073/pnas.0402455101.
  • Croia C, Astorri E, Murray-Brown W, Willis A, Brokstad KA, Sutcliffe N, Piper K, Jonsson R, Tappuni AR, Pitzalis C, et al. 2014. Implication of Epstein-Barr virus infection in disease-specific autoreactive B cell activation in ectopic lymphoid structures of Sjögren’s syndrome. Arthritis Rheumatol. 66(9):2545–2557. doi:10.1002/art.38726.
  • Croia C, Serafini B, Bombardieri M, Kelly S, Humby F, Severa M, Rizzo F, Coccia EM, Migliorini P, Aloisi F, et al. 2013. Epstein-Barr virus persistence and infection of autoreactive plasma cells in synovial lymphoid structures in rheumatoid arthritis. Ann Rheum Dis. 72(9):1559–1568. doi:10.1136/annrheumdis-2012-202352.
  • de Francisco R, Castaño-García A, Martínez-González S, Pérez-Martínez I, González-Huerta AJ, Morais LR, Fernández-García MS, Jiménez S, Díaz-Coto S, Flórez-Díez P, et al. 2018. Impact of Epstein-Barr virus serological status on clinical outcomes in adult patients with inflammatory bowel disease. Aliment Pharmacol Ther. 48(7):723–730. doi:10.1111/apt.14933.
  • Decker P, Moulinet T, Pontille F, Cravat M, De Carvalho Bittencourt M, Jaussaud R. 2022. An updated review of anti-Ro52 (TRIM21) antibodies impact in connective tissue diseases clinical management. Autoimmun Rev. 21(3):103013. doi:10.1016/j.autrev.2021.103013.
  • Dimitroulia E, Pitiriga VC, Piperaki ET, Spanakis NE, Tsakris A. 2013. Inflammatory bowel disease exacerbation associated with Epstein-Barr virus infection. Dis Colon Rectum. 56(3):322–327. doi:10.1097/DCR.0b013e31827cd02c.
  • Doaty S, Agrawal H, Bauer E, Furst DE. 2016. Infection and Lupus: which Causes Which? Curr Rheumatol Rep. 18(3):13. doi:10.1007/s11926-016-0561-4.
  • Dooley MM, de Gannes SL, Fu KA, Lindsey JW. 2016. The increased antibody response to Epstein-Barr virus in multiple sclerosis is restricted to selected virus proteins. J Neuroimmunol. 299:147–151. doi:10.1016/j.jneuroim.2016.08.016.
  • Doshi A, Chataway J. 2016. Multiple sclerosis, a treatable disease. Clin Med (Lond). 16(Suppl 6):s53–s59. doi:10.7861/clinmedicine.16-6-s53.
  • Draborg AH, Duus K, Houen G. 2012. Epstein-Barr virus and systemic lupus erythematosus. Clin Dev Immunol. 2012:370516–370510. doi:10.1155/2012/370516.
  • Draborg AH, Duus K, Houen G. 2013. Epstein-Barr virus in systemic autoimmune diseases. Clin Dev Immunol. 2013:535738–535739. doi:10.1155/2013/535738.
  • Dreyfus DH, Liu Y, Ghoda LY, Chang JT. 2011. Analysis of an ankyrin-like region in Epstein Barr Virus encoded (EBV) BZLF-1 (ZEBRA) protein: implications for interactions with NF-κB and p53. Virol J. 8(1):422. doi:10.1186/1743-422X-8-422.
  • Dreyfus DH, Nagasawa M, Gelfand EW, Ghoda LY. 2005. Modulation of p53 activity by IkappaBalpha: evidence suggesting a common phylogeny between NF-kappaB and p53 transcription factors. BMC Immunol. 6(1):12. doi:10.1186/1471-2172-6-12.
  • Duddy M, Niino M, Adatia F, Hebert S, Freedman M, Atkins H, Kim HJ, Bar-Or A. 2007. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J Immunol. 178(10):6092–6099. doi:10.4049/jimmunol.178.10.6092.
  • Dunmire SK, Verghese PS, Balfour HH.Jr. 2018. Primary Epstein-Barr virus infection. J Clin Virol. 102:84–92. doi:10.1016/j.jcv.2018.03.001.
  • Emadi B, Carter M, Eswar S, Chen X, Laurynenka V, Parameswaran S, Kaufman KM, Namjou B, Kottyan LC, Weirauch M, et al. 2020. P136 Epstein-Barr virus transcription co-factors bind to many inflammatory bowel disease risk loci. Inflammatory Bowel Diseases. 26(Supplement_1):S31–S31. doi:10.1093/ibd/zaa010.077.
  • Esposito S, Bosis S, Semino M, Rigante D. 2014. Infections and systemic lupus erythematosus. Eur J Clin Microbiol Infect Dis. 33(9):1467–1475. doi:10.1007/s10096-014-2098-7.
  • Fadlallah S, Hussein H, Jallad M-A, Shehab M, Jurjus AR, Matar GM, Rahal EA. 2021. Effect of Epstein-Barr virus DNA on the incidence and severity of arthritis in a rheumatoid arthritis mouse model. Front Immunol. 12:672752. doi:10.3389/fimmu.2021.672752.
  • Fahey LM, Wilson EB, Elsaesser H, Fistonich CD, McGavern DB, Brooks DG. 2011. Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J Exp Med. 208(5):987–999. doi:10.1084/jem.20101773.
  • Fåhraeus R, Rymo L, Rhim JS, Klein G. 1990. Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature. 345(6274):447–449. doi:10.1038/345447a0.
  • Feng W-h, Cohen JI, Fischer S, Li L, Sneller M, Goldbach-Mansky R, Raab-Traub N, Delecluse H-J, Kenney SC. 2004. Reactivation of latent Epstein-Barr virus by methotrexate: a potential contributor to methotrexate-associated lymphomas. J Natl Cancer Inst. 96(22):1691–1702. doi:10.1093/jnci/djh313.
  • Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. 2002. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 3(10):944–950. doi:10.1038/ni833.
  • Finckh A, Gilbert B, Hodkinson B, Bae S-C, Thomas R, Deane KD, Alpizar-Rodriguez D, Lauper K. 2022. Global epidemiology of rheumatoid arthritis. Nat Rev Rheumatol. 18(10):591–602. doi:10.1038/s41584-022-00827-y.
  • Fugl A, Andersen CL. 2019. Epstein-Barr virus and its association with disease - a review of relevance to general practice. BMC Fam Pract. 20(1):62. doi:10.1186/s12875-019-0954-3.
  • Gehlert T, Devergne O, Niedobitek G. 2004. Epstein-Barr virus (EBV) infection and expression of the interleukin-12 family member EBV-induced gene 3 (EBI3) in chronic inflammatory bowel disease. J Med Virol. 73(3):432–438. doi:10.1002/jmv.20109.
  • Getts DR, Chastain EM, Terry RL, Miller SD. 2013. Virus infection, antiviral immunity, and autoimmunity. Immunol Rev. 255(1):197–209. doi:10.1111/imr.12091.
  • Gillespie KM. 2006. Type 1 diabetes: pathogenesis and prevention. CMAJ. 175(2):165–170. doi:10.1503/cmaj.060244.
  • Gugliesi F, Pasquero S, Griffante G, Scutera S, Albano C, Pacheco SFC, Riva G, Dell’Oste V, Biolatti M. 2021. Human Cytomegalovirus and Autoimmune Diseases: where Are We? Viruses. 13(2):260. doi:10.3390/v13020260.
  • Haas J, Bekeredjian-Ding I, Milkova M, Balint B, Schwarz A, Korporal M, Jarius S, Fritz B, Lorenz H-M, Wildemann B, et al. 2011. B cells undergo unique compartmentalized redistribution in multiple sclerosis. J Autoimmun. 37(4):289–299. doi:10.1016/j.jaut.2011.08.003.
  • Hammarskjöld ML, Simurda MC. 1992. Epstein-Barr virus latent membrane protein transactivates the human immunodeficiency virus type 1 long terminal repeat through induction of NF-kappa B activity. J Virol. 66(11):6496–6501. doi:10.1128/JVI.66.11.6496-6501.1992.
  • Hanlon P, Avenell A, Aucott L, Vickers MA. 2014. Systematic review and meta-analysis of the sero-epidemiological association between Epstein-Barr virus and systemic lupus erythematosus. Arthritis Res Ther. 16(1):R3. doi:10.1186/ar4429.
  • Hara S, Nagata K, Kumata K, Matsushita M, Kuwamoto S, Kato M, Hayashi K. 2018. Estradiol affects Epstein-Barr virus reactivation-induced thyrotropin receptor antibody and immunoglobulin production in Graves’ disease patients and healthy controls. Viral Immunol. 31(7):486–491. doi:10.1089/vim.2018.0032.
  • Harley JB, Chen X, Pujato M, Miller D, Maddox A, Forney C, Magnusen AF, Lynch A, Chetal K, Yukawa M, et al. 2018. Transcription factors operate across disease loci, with EBNA2 implicated in autoimmunity. Nat Genet. 50(5):699–707. doi:10.1038/s41588-018-0102-3.
  • Harms RZ, Ostlund KR, Cabrera MS, Edwards E, Fisher M, Sarvetnick N. 2020. Confirmation and identification of biomarkers implicating environmental triggers in the pathogenesis of type 1 diabetes. Front Immunol. 11:1922. doi:10.3389/fimmu.2020.01922.
  • Hauser SL, Waubant E, Arnold DL, Vollmer T, Antel J, Fox RJ, Bar-Or A, Panzara M, Sarkar N, Agarwal S, et al. 2008. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med. 358(7):676–688. doi:10.1056/NEJMoa0706383.
  • Hedström AK, Huang J, Brenner N, Butt J, Kockum I, Waterboer T, Olsson T, Alfredsson L. 2021. Low sun exposure acts synergistically with high Epstein-Barr nuclear antigen 1 (EBNA-1) antibody levels in multiple sclerosis etiology. Eur J Neurol. 28(12):4146–4152. doi:10.1111/ene.15082.
  • Hedström AK, Lima Bomfim I, Hillert J, Olsson T, Alfredsson L. 2015. Obesity interacts with infectious mononucleosis in risk of multiple sclerosis. Eur J Neurol. 22(3):578–e38. doi:10.1111/ene.12620.
  • Henderson S, Rowe M, Gregory C, Croom-Carter D, Wang F, Longnecker R, Kieff E, Rickinson A. 1991. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell. 65(7):1107–1115. doi:10.1016/0092-8674(91)90007-l.
  • Hong T, Parameswaran S, Donmez OA, Miller D, Forney C, Lape M, Saint Just Ribeiro M, Liang J, Edsall LE, Magnusen AF, et al. 2021. Epstein-Barr virus nuclear antigen 2 extensively rewires the human chromatin landscape at autoimmune risk loci. Genome Res. 31(12):2185–2198. doi:10.1101/gr.264705.120.
  • Hornef MW, Wagner HJ, Kruse A, Kirchner H. 1995. Cytokine production in a whole-blood assay after Epstein-Barr virus infection in vivo. Clin Diagn Lab Immunol. 2(2):209–213. doi:10.1128/cdli.2.2.209-213.1995.
  • Hosomi S, Nishida Y, Fujiwara Y. 2021. The impact of human herpesviruses in clinical practice of inflammatory bowel disease in the era of COVID-19. Microorganisms. 9(9):1870. doi:10.3390/microorganisms9091870.
  • Houen G, Trier NH. 2020. Epstein-Barr virus and systemic autoimmune diseases. Front Immunol. 11:587380. doi:10.3389/fimmu.2020.587380.
  • Hradsky O, Copova I, Zarubova K, Durilova M, Nevoral J, Maminak M, Hubacek P, Bronsky J. 2015. Seroprevalence of Epstein-Barr virus, cytomegalovirus, and polyomaviruses in children with inflammatory bowel disease. Dig Dis Sci. 60(11):3399–3407. doi:10.1007/s10620-015-3764-z.
  • Hussein HM, Rahal EA. 2019. The role of viral infections in the development of autoimmune diseases. Crit Rev Microbiol. 45(4):394–412. doi:10.1080/1040841X.2019.1614904.
  • Hyöty H, Räsänen L, Hiltunen M, Lehtinen M, Huupponen T, Leinikki P. 1991. Decreased antibody reactivity to Epstein-Barr virus capsid antigen in type 1 (insulin-dependent) diabetes mellitus. APMIS. 99(4):359–363. doi:10.1111/j.1699-0463.1991.tb05162.x.
  • Inoue H, Mishima K, Yamamoto-Yoshida S, Ushikoshi-Nakayama R, Nakagawa Y, Yamamoto K, Ryo K, Ide F, Saito I. 2012. Aryl hydrocarbon receptor-mediated induction of EBV reactivation as a risk factor for Sjögren’s syndrome. J Immunol. 188(9):4654–4662. doi:10.4049/jimmunol.1101575.
  • Ishibashi H, Imakiire S, Goto M, Nomaru R, Shibata M, Matsuoka H, Yasuda H, Yamashima T, Sakisaka H, Tanabe T, et al. 2022. Epstein-Barr virus-positive intestinal diffuse large B-cell lymphoma in a Japanese patient with celiac disease: first reported case and a literature review. Intern Med. 61(3):329–334. doi:10.2169/internalmedicine.7876-21.
  • Ishimaru N, Takagi A, Kohashi M, Yamada A, Arakaki R, Kanno J, Hayashi Y. 2009. Neonatal exposure to low-dose 2,3,7,8-tetrachlorodibenzo-p-dioxin causes autoimmunity due to the disruption of T cell tolerance. J Immunol. 182(10):6576–6586. doi:10.4049/jimmunol.0802289.
  • Izadi S, Najafizadeh SR, Nejati A, Teymoori-Rad M, Shahmahmoodi S, Golsaz Shirazi F, et al. 2021. Overall status of Epstein-Barr virus infection, IFN-a, and TLR-7/9 in patients with systemic lupus erythematous. Iran J Immunol. 18(3):230–240.
  • Izawa K, Martin E, Soudais C, Bruneau J, Boutboul D, Rodriguez R, Lenoir C, Hislop AD, Besson C, Touzot F, et al. 2017. Inherited CD70 deficiency in humans reveals a critical role for the CD70-CD27 pathway in immunity to Epstein-Barr virus infection. J Exp Med. 214(1):73–89. doi:10.1084/jem.20160784.
  • James JA, Robertson JM. 2012. Lupus and Epstein-Barr. Curr Opin Rheumatol. 24(4):383–388. doi:10.1097/BOR.0b013e3283535801.
  • Jog NR, Chakravarty EF, Guthridge JM, James JA. 2018. Epstein Barr virus interleukin 10 suppresses anti-inflammatory phenotype in human monocytes. Front Immunol. 9:2198. doi:10.3389/fimmu.2018.02198.
  • Jog NR, James JA. 2020. Epstein Barr virus and autoimmune responses in systemic lupus erythematosus. Front Immunol. 11:623944. doi:10.3389/fimmu.2020.623944.
  • Jog NR, McClain MT, Heinlen LD, Gross T, Towner R, Guthridge JM, Axtell RC, Pardo G, Harley JB, James JA. 2020. Epstein Barr virus nuclear antigen 1 (EBNA-1) peptides recognized by adult multiple sclerosis patient sera induce neurologic symptoms in a murine model. J Autoimmun. 106:102332. doi:10.1016/j.jaut.2019.102332.
  • Kato S, Shimizu H, Tomii S, Uchida H, Kawamoto A, Hibiya S, Motobayashi M, Takenaka K, Fujii T, Saito E, et al. 2021. Substantial Epstein-Barr virus reactivation in a case of severe refractory ulcerative colitis: a possible role in exacerbation. Clin J Gastroenterol. 14(2):584–588. doi:10.1007/s12328-020-01319-w.
  • Katsuyama T, Sada K-E, Yan M, Zeggar S, Hiramatsu S, Miyawaki Y, Ohashi K, Morishita M, Watanabe H, Katsuyama E, et al. 2017. Prognostic factors of methotrexate-associated lymphoproliferative disorders associated with rheumatoid arthritis and plausible application of biological agents. Mod Rheumatol. 27(5):773–777. doi:10.1080/14397595.2016.1259714.
  • Keane JT, Afrasiabi A, Schibeci SD, Swaminathan S, Parnell GP, Booth DR. 2021. The interaction of Epstein-Barr virus encoded transcription factor EBNA2 with multiple sclerosis risk loci is dependent on the risk genotype. EBioMedicine. 71:103572. doi:10.1016/j.ebiom.2021.103572.
  • Khatri B, Tessneer KL, Rasmussen A, Aghakhanian F, Reksten TR, Adler A, Alevizos I, Anaya J-M, Aqrawi LA, Baecklund E, et al. 2022. Genome-wide association study identifies Sjögren’s risk loci with functional implications in immune and glandular cells. Nat Commun. 13(1):4287. doi:10.1038/s41467-022-30773-y.
  • Kivity S, Arango MT, Ehrenfeld M, Tehori O, Shoenfeld Y, Anaya J-M, Agmon-Levin N. 2014. Infection and autoimmunity in Sjogren’s syndrome: a clinical study and comprehensive review. J Autoimmun. 51:17–22. doi:10.1016/j.jaut.2014.02.008.
  • Klatt T, Ouyang Q, Flad T, Koetter I, Buhring HJ, Kalbacher H. 2005. Expansion of peripheral CD8+ CD28- T cells in response to Epstein-Barr virus in patients with rheumatoid arthritis. J Rheumatol. 32(2):239–251.
  • Knippenberg S, Peelen E, Smolders J, Thewissen M, Menheere P, Cohen Tervaert JW, Hupperts R, Damoiseaux J. 2011. Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naïve/memory Breg ratio during a relapse but not in remission. J Neuroimmunol. 239(1-2):80–86. doi:10.1016/j.jneuroim.2011.08.019.
  • Koji H, Yazawa T, Nakabayashi K, Fujioka Y, Kamma H, Yamada A. 2016. CD8-positive T-cell lymphoproliferative disorder associated with Epstein-Barr virus-infected B-cells in a rheumatoid arthritis patient under methotrexate treatment. Mod Rheumatol. 26(2):271–275. doi:10.3109/14397595.2013.850613.
  • Kumata K, Nagata K, Matsushita M, Kuwamoto S, Kato M, Murakami I, Fukata S, Hayashi K. 2016. Thyrotropin receptor antibody (TRAb)-IgM levels are markedly higher than TRAb-IgG levels in Graves’ disease patients and controls, and TRAb-IgM production is related to Epstein-Barr virus reactivation. Viral Immunol. 29(8):459–463. doi:10.1089/vim.2016.0043.
  • Kurita D, Miyoshi H, Ichikawa A, Kato K, Imaizumi Y, Seki R, Sato K, Sasaki Y, Kawamoto K, Shimono J, et al. 2019. Methotrexate-associated lymphoproliferative disorders in patients with rheumatoid arthritis: clinicopathologic features and prognostic factors. Am J Surg Pathol. 43(7):869–884. doi:10.1097/PAS.0000000000001271.
  • Läderach F, Münz C. 2021. Epstein Barr virus exploits genetic susceptibility to increase multiple sclerosis risk. Microorganisms. 9(11):2191. doi:10.3390/microorganisms9112191.
  • Lanz TV, Brewer RC, Ho PP, Moon J-S, Jude KM, Fernandez D, Fernandes RA, Gomez AM, Nadj G-S, Bartley CM, et al. 2022. Clonally expanded B cells in multiple sclerosis bind EBV EBNA1 and GlialCAM. Nature. 603(7900):321–327. doi:10.1038/s41586-022-04432-7.
  • Lapsia S, Koganti S, Spadaro S, Rajapakse R, Chawla A, Bhaduri-McIntosh S. 2016. Anti-TNFalpha therapy for inflammatory bowel diseases is associated with Epstein-Barr virus lytic activation. J Med Virol. 88(2):312–318. doi:10.1002/jmv.24331.
  • Lenti MV, Rossi CM, Melazzini F, Gastaldi M, Bugatti S, Rotondi M, Bianchi PI, Gentile A, Chiovato L, Montecucco C, et al. 2022. Seronegative autoimmune diseases: a challenging diagnosis. Autoimmun Rev. 21(9):103143. doi:10.1016/j.autrev.2022.103143.
  • Lerner MR, Andrews NC, Miller G, Steitz JA. 1981. Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc Natl Acad Sci U S A. 78(2):805–809. doi:10.1073/pnas.78.2.805.
  • Levet S, Charvet B, Bertin A, Deschaumes A, Perron H, Hober D. 2019. Human endogenous retroviruses and type 1 diabetes. Curr Diab Rep. 19(12):141. doi:10.1007/s11892-019-1256-9.
  • Levin LI, Munger KL, O’Reilly EJ, Falk KI, Ascherio A. 2010. Primary infection with the Epstein-Barr virus and risk of multiple sclerosis. Ann Neurol. 67(6):824–830. doi:10.1002/ana.21978.
  • Li X, Chen N, You P, Peng T, Chen G, Wang J, Li J, Liu Y. 2019. The status of Epstein-Barr virus infection in intestinal mucosa of Chinese patients with inflammatory bowel disease. Digestion. 99(2):126–132. doi:10.1159/000489996.
  • Lindsey JW, deGannes SL, Pate KA, Zhao X. 2016. Antibodies specific for Epstein-Barr virus nuclear antigen-1 cross-react with human heterogeneous nuclear ribonucleoprotein L. Mol Immunol. 69:7–12. doi:10.1016/j.molimm.2015.11.007.
  • Lindsey JW. 2017. Antibodies to the Epstein-Barr virus proteins BFRF3 and BRRF2 cross-react with human proteins. J Neuroimmunol. 310:131–134. doi:10.1016/j.jneuroim.2017.07.013.
  • Liu X, Alli R, Steeves M, Nguyen P, Vogel P, Geiger TL. 2012. The T cell response to IL-10 alters cellular dynamics and paradoxically promotes central nervous system autoimmunity. J Immunol. 189(2):669–678. doi:10.4049/jimmunol.1200607.
  • Liu Y, Li Y, Li Y, Wu S, Tian X, Tang T, Sun H, He C. 2021. Clinical features of intestinal ulcers complicated by Epstein-Barr virus infection: importance of active infection. Dis Markers. 2021:6627620. doi:10.1155/2021/6627620.
  • Lomakin Y, Arapidi GP, Chernov A, Ziganshin R, Tcyganov E, Lyadova I, Butenko IO, Osetrova M, Ponomarenko N, Telegin G, et al. 2017. Exposure to the Epstein-Barr viral antigen latent membrane protein 1 induces myelin-reactive antibodies in vivo. Front Immunol. 8:777. doi:10.3389/fimmu.2017.00777.
  • Lubberts E, Koenders MI, Oppers-Walgreen B, van den Bersselaar L, Coenen-de Roo CJJ, Joosten LAB, van den Berg WB. 2004. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum. 50(2):650–659. doi:10.1002/art.20001.
  • Lucas RM, Hughes AM, Lay M-LJ, Ponsonby A-L, Dwyer DE, Taylor BV, Pender MP. 2011. Epstein-Barr virus and multiple sclerosis. J Neurol Neurosurg Psychiatry. 82(10):1142–1148. doi:10.1136/jnnp-2011-300174.
  • Magro F, Santos-Antunes J, Albuquerque A, Vilas-Boas F, Macedo GN, Nazareth N, Lopes S, Sobrinho-Simões J, Teixeira S, Dias CC, et al. 2013. Epstein-Barr virus in inflammatory bowel disease-correlation with different therapeutic regimens. Inflamm Bowel Dis. 19(8):1710–1716. doi:10.1097/MIB.0b013e318281f31c.
  • Mameli G, Poddighe L, Mei A, Uleri E, Sotgiu S, Serra C, Manetti R, Dolei A. 2012. Expression and activation by Epstein Barr virus of human endogenous retroviruses-W in blood cells and astrocytes: inference for multiple sclerosis. PLoS One. 7(9):e44991. doi:10.1371/journal.pone.0044991.
  • Márquez AC, Horwitz MS. 2015. The role of latently infected B cells in CNS autoimmunity. Front Immunol. 6:544. doi:10.3389/fimmu.2015.00544.
  • Masuoka S, Kusunoki N, Takamatsu R, Takahashi H, Tsuchiya K, Kawai S, Nanki T. 2018. Epstein-Barr virus infection and variants of Epstein-Barr nuclear antigen-1 in synovial tissues of rheumatoid arthritis. PLoS One. 13(12):e0208957. doi:10.1371/journal.pone.0208957.
  • McClain MT, Heinlen LD, Dennis GJ, Roebuck J, Harley JB, James JA. 2005. Early events in lupus humoral autoimmunity suggest initiation through molecular mimicry. Nat Med. 11(1):85–89. doi:10.1038/nm1167.
  • McDermott M, Molloy M, Buckley J, Greally J. 1989. Antibodies to Epstein-Barr viral antigens in familial rheumatoid arthritis. Ir J Med Sci. 158(8):203–205. doi:10.1007/BF02943612.
  • Middeldorp JM. 2015. Epstein-Barr Virus-Specific Humoral Immune Responses in Health and Disease. Curr Top Microbiol Immunol. 391:289–323. doi:10.1007/978-3-319-22834-1_10.
  • Miura M, Shimizu H, Saito D, Miyoshi J, Matsuura M, Kudo T, Hirayama D, Yoshida M, Arai K, Iwama I, et al. 2021. Multicenter, cross-sectional, observational study on Epstein-Barr viral infection status and thiopurine use by age group in patients with inflammatory bowel disease in Japan (EBISU study). J Gastroenterol. 56(12):1080–1091. doi:10.1007/s00535-021-01832-w.
  • Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, et al. 2012. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 142(1):46–54.e42; quiz e30. doi:10.1053/j.gastro.2011.10.001.
  • Moschen AR, Tilg H, Raine T. 2019. IL-12, IL-23 and IL-17 in IBD: immunobiology and therapeutic targeting. Nat Rev Gastroenterol Hepatol. 16(3):185–196. doi:10.1038/s41575-018-0084-8.
  • Mouat IC, Morse ZJ, Shanina I, Brown KL, Horwitz MS. 2021. Latent gammaherpesvirus exacerbates arthritis through modification of age-associated B cells. Elife. 10:e67024. doi:10.7554/eLife.67024.
  • Munroe ME, Anderson JR, Gross TF, Stunz LL, Bishop GA, James JA. 2020. Epstein-Barr functional mimicry: pathogenicity of oncogenic latent membrane protein-1 in systemic lupus erythematosus and autoimmunity. Front Immunol. 11:606936. doi:10.3389/fimmu.2020.606936.
  • Nagata K, Fukata S, Kanai K, Satoh Y, Segawa T, Kuwamoto S, Sugihara H, Kato M, Murakami I, Hayashi K, et al. 2011. The influence of Epstein-Barr virus reactivation in patients with Graves’ disease. Viral Immunol. 24(2):143–149. doi:10.1089/vim.2010.0072.
  • Nagata K, Hara S, Nakayama Y, Higaki K, Sugihara H, Kuwamoto S, Matsushita M, Kato M, Tanio S, Ishiguro K, et al. 2018. Epstein-Barr virus lytic reactivation induces IgG4 production by host B lymphocytes in Graves’ disease patients and controls: A subset of graves’ disease is an IgG4-related disease-like condition. Viral Immunol. 31(8):540–547. doi:10.1089/vim.2018.0042.
  • Nagata K, Kumata K, Nakayama Y, Satoh Y, Sugihara H, Hara S, Matsushita M, Kuwamoto S, Kato M, Murakami I, et al. 2017. 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. 30(3):240–249. doi:10.1089/vim.2016.0179.
  • Najafipoor A, Roghanian R, Zarkesh-Esfahani SH, Bouzari M, Etemadifar M. 2015. The beneficial effects of vitamin D3 on reducing antibody titers against Epstein-Barr virus in multiple sclerosis patients. Cell Immunol. 294(1):9–12. doi:10.1016/j.cellimm.2015.01.009.
  • Nakamura M, Burastero SE, Ueki Y, Larrick JW, Notkins AL, Casali P. 1988. Probing the normal and autoimmune B cell repertoire with Epstein-Barr virus. Frequency of B cells producing monoreactive high affinity autoantibodies in patients with Hashimoto’s disease and systemic lupus erythematosus. J Immunol. 141(12):4165–4172. doi:10.4049/jimmunol.141.12.4165.
  • Navone R, Lunardi C, Gerli R, Tinazzi E, Peterlana D, Bason C, Corrocher R, Puccetti A. 2005. Identification of tear lipocalin as a novel autoantigen target in Sjögren’s syndrome. J Autoimmun. 25(3):229–234. doi:10.1016/j.jaut.2005.09.021.
  • Nielsen TR, Rostgaard K, Askling J, Steffensen R, Oturai A, Jersild C, Koch-Henriksen N, Sørensen PS, Hjalgrim H. 2009. Effects of infectious mononucleosis and HLA-DRB1*15 in multiple sclerosis. Mult Scler. 15(4):431–436. doi:10.1177/1352458508100037.
  • Niiro H, Otsuka T, Abe M, Satoh H, Ogo T, Nakano T, Furukawa Y, Niho Y. 1992. Epstein-Barr virus BCRF1 gene product (viral interleukin 10) inhibits superoxide anion production by human monocytes. Lymphokine Cytokine Res. 11(5):209–214.
  • Noviello D, Mager R, Roda G, Borroni RG, Fiorino G, Vetrano S. 2021. The IL23-IL17 immune axis in the treatment of ulcerative colitis: successes, defeats, and ongoing challenges. Front Immunol. 12:611256. doi:10.3389/fimmu.2021.611256.
  • Olsson T, Barcellos LF, Alfredsson L. 2017. Interactions between genetic, lifestyle and environmental risk factors for multiple sclerosis. Nat Rev Neurol. 13(1):25–36. doi:10.1038/nrneurol.2016.187.
  • Otsuka K, Sato M, Tsunematsu T, Ishimaru N. 2022. Virus Infections Play Crucial Roles in the Pathogenesis of Sjögren’s Syndrome. Viruses. 14(7):1474. doi:10.3390/v14071474.
  • Owens GP, Ritchie AM, Burgoon MP, Williamson RA, Corboy JR, Gilden DH. 2003. Single-cell repertoire analysis demonstrates that clonal expansion is a prominent feature of the B cell response in multiple sclerosis cerebrospinal fluid. J Immunol. 171(5):2725–2733. doi:10.4049/jimmunol.171.5.2725.
  • Pakpoor J, Disanto G, Gerber JE, Dobson R, Meier UC, Giovannoni G, Ramagopalan SV. 2013. The risk of developing multiple sclerosis in individuals seronegative for Epstein-Barr virus: a meta-analysis. Mult Scler. 19(2):162–166. doi:10.1177/1352458512449682.
  • Parkkonen P, Hyoty H, Ilonen J, Reijonen H, Yla-Herttuala S, Leinikki P. 1994. Antibody reactivity to an Epstein-Barr virus BERF4-encoded epitope occurring also in Asp-57 region of HLA-DQ8 beta chain. Childhood Diabetes in Finland Study Group. Clin Exp Immunol. 95(2):287–293.
  • Pender MP. 2012. CD8+ T-Cell Deficiency, Epstein-Barr Virus Infection, Vitamin D Deficiency, and Steps to Autoimmunity: A Unifying Hypothesis. Autoimmune Dis. 2012:189096. doi:10.1155/2012/189096.
  • Perfetti V, Baldanti F, Lenti MV, Vanoli A, Biagi F, Gatti M, Riboni R, Dallera E, Paulli M, Pedrazzoli P, et al. 2016. Detection of active Epstein-Barr virus infection in duodenal mucosa of patients with refractory celiac disease. Clin Gastroenterol Hepatol. 14(8):1216–1220. doi:10.1016/j.cgh.2016.03.022.
  • Pezhouh MK, Miller JA, Sharma R, Borzik D, Eze O, Waters K, Westerhoff MA, Parian AM, Lazarev MG, Voltaggio L, et al. 2018. Refractory inflammatory bowel disease: is there a role for Epstein-Barr virus? A case-controlled study using highly sensitive Epstein-Barr virus-encoded small RNA1 in situ hybridization. Hum Pathol. 82:187–192. doi:10.1016/j.humpath.2018.08.001.
  • Pisetsky DS. 2023. Pathogenesis of autoimmune disease. Nat Rev Nephrol. 19(8):509–524. doi:10.1038/s41581-023-00720-1.
  • Pohl D, Krone B, Rostasy K, Kahler E, Brunner E, Lehnert M, Wagner H-J, Gärtner J, Hanefeld F. 2006. High seroprevalence of Epstein-Barr virus in children with multiple sclerosis. Neurology. 67(11):2063–2065. doi:10.1212/01.wnl.0000247665.94088.8d.
  • Pyzik A, Grywalska E, Matyjaszek-Matuszek B, Ludian J, Kiszczak-Bochynska E, Smolen A, et al. 2019. Does the Epstein-Barr virus play a role in the pathogenesis of Graves’ disease? Int J Mol Sci. 20(13):3145.
  • Qin B, Wang J, Yang Z, Yang M, Ma N, Huang F, Zhong R. 2015. Epidemiology of primary Sjögren’s syndrome: a systematic review and meta-analysis. Ann Rheum Dis. 74(11):1983–1989. doi:10.1136/annrheumdis-2014-205375.
  • Qin Y, Duquette P, Zhang Y, Talbot P, Poole R, Antel J. 1998. Clonal expansion and somatic hypermutation of V(H) genes of B cells from cerebrospinal fluid in multiple sclerosis. J Clin Invest. 102(5):1045–1050. doi:10.1172/JCI3568.
  • Quaglia M, Merlotti G, De Andrea M, Borgogna C, Cantaluppi V. 2021. Viral infections and systemic lupus erythematosus: new players in an old story. Viruses. 13(2):277. doi:10.3390/v13020277.
  • Radu AF, Bungau SG. 2021. Management of rheumatoid arthritis: an overview. Cells. 10(11):2857. doi:10.3390/cells10112857.
  • Ram R, Mehta M, Nguyen QT, Larma I, Boehm BO, Pociot F, Concannon P, Morahan G. 2016. Systematic evaluation of genes and genetic variants associated with type 1 diabetes susceptibility. J Immunol. 196(7):3043–3053. doi:10.4049/jimmunol.1502056.
  • Ramasamy R, Mohammed F, Meier UC. 2020. HLA DR2b-binding peptides from human endogenous retrovirus envelope, Epstein-Barr virus and brain proteins in the context of molecular mimicry in multiple sclerosis. Immunol Lett. 217:15–24. doi:10.1016/j.imlet.2019.10.017.
  • Rancan C, Schirrmann L, Hüls C, Zeidler R, Moosmann A. 2015. Latent membrane protein LMP2A impairs recognition of EBV-infected cells by CD8+ T cells. PLoS Pathog. 11(6):e1004906. doi:10.1371/journal.ppat.1004906.
  • Rasmussen NS, Draborg AH, Nielsen CT, Jacobsen S, Houen G. 2015. Antibodies to early EBV, CMV, and HHV6 antigens in systemic lupus erythematosus patients. Scand J Rheumatol. 44(2):143–149. doi:10.3109/03009742.2014.973061.
  • Richardson SJ, Horwitz MS. 2014. Is type 1 diabetes "going viral"? Diabetes. 63(7):2203–2205. doi:10.2337/db14-0510.
  • Rizzo AG, Orlando A, Gallo E, Bisanti A, Sferrazza S, Montalbano LM, Macaluso FS, Cottone M. 2017. Is Epstein-Barr virus infection associated with the pathogenesis of microscopic colitis? J Clin Virol. 97:1–3. doi:10.1016/j.jcv.2017.10.009.
  • Rolf L, Muris A-H, Mathias A, Du Pasquier R, Koneczny I, Disanto G, Kuhle J, Ramagopalan S, Damoiseaux J, Smolders J, et al. 2018. Exploring the effect of vitamin D3 supplementation on the anti-EBV antibody response in relapsing-remitting multiple sclerosis. Mult Scler. 24(10):1280–1287. doi:10.1177/1352458517722646.
  • Rose NR. 2016. Prediction and prevention of autoimmune disease in the 21st century: a review and preview. Am J Epidemiol. 183(5):403–406. doi:10.1093/aje/kwv292.
  • Ruiz-Pablos M. 2022. CD4+ Cytotoxic T cells involved in the development of EBV-associated diseases. Pathogens. 11(8):831. doi:10.3390/pathogens11080831.
  • Ryan JL, Shen Y-J, Morgan DR, Thorne LB, Kenney SC, Dominguez RL, Gulley ML. 2012. Epstein-Barr virus infection is common in inflamed gastrointestinal mucosa. Dig Dis Sci. 57(7):1887–1898. doi:10.1007/s10620-012-2116-5.
  • Salek-Ardakani S, Arrand JR, Mackett M. 2002. Epstein-Barr virus encoded interleukin-10 inhibits HLA-class I, ICAM-1, and B7 expression on human monocytes: implications for immune evasion by EBV. Virology. 304(2):342–351. doi:10.1006/viro.2002.1716.
  • Sankaran-Walters S, Ransibrahmanakul K, Grishina I, Hung J, Martinez E, Prindiville T, Dandekar S. 2011. Epstein-Barr virus replication linked to B cell proliferation in inflamed areas of colonic mucosa of patients with inflammatory bowel disease. J Clin Virol. 50(1):31–36. doi:10.1016/j.jcv.2010.09.011.
  • Sanosyan A, Daien C, Nutz A, Bollore K, Bedin A-S, Morel J, Zimmermann V, Nocturne G, Peries M, Guigue N, et al. 2019. Discrepancy of serological and molecular patterns of circulating Epstein-Barr virus reactivation in primary Sjögren’s syndrome. Front Immunol. 10:1153. doi:10.3389/fimmu.2019.01153.
  • Schmitt H, Neurath MF, Atreya R. 2021. Role of the IL23/IL17 Pathway in Crohn’s Disease. Front Immunol. 12:622934. doi:10.3389/fimmu.2021.622934.
  • Serafini B, Rosicarelli B, Franciotta D, Magliozzi R, Reynolds R, Cinque P, Andreoni L, Trivedi P, Salvetti M, Faggioni A, et al. 2007. Dysregulated Epstein-Barr virus infection in the multiple sclerosis brain. J Exp Med. 204(12):2899–2912. doi:10.1084/jem.20071030.
  • Shaffer DR, Savoldo B, Yi Z, Chow KKH, Kakarla S, Spencer DM, Dotti G, Wu M-F, Liu H, Kenney S, et al. 2011. T cells redirected against CD70 for the immunotherapy of CD70-positive malignancies. Blood. 117(16):4304–4314. doi:10.1182/blood-2010-04-278218.
  • Smatti MK, Cyprian FS, Nasrallah GK, Al Thani AA, Almishal RO, Yassine HM. 2019. Viruses and autoimmunity: a review on the potential interaction and molecular mechanisms. Viruses. 11(8):762. doi:10.3390/v11080762.
  • Smith DA, Germolec DR. 1999. Introduction to immunology and autoimmunity. Environ Health Perspect. 107 Suppl 5(Suppl 5):661–665. doi:10.1289/ehp.99107s5661.
  • Stewart JP, Rooney CM. 1992. The interleukin-10 homolog encoded by Epstein-Barr virus enhances the reactivation of virus-specific cytotoxic T cell and HLA-unrestricted killer cell responses. Virology. 191(2):773–782. doi:10.1016/0042-6822(92)90253-l.
  • Su R, Li Z, Wang Y, Liu Y, Zheng X, Gao C, et al. 2020. Imbalance between Th17 and regulatory T cells in patients with systemic lupus erythematosus combined EBV/CMV viraemia. Clin Exp Rheumatol. 38(5):864–873.
  • Szabo K, Papp G, Barath S, Gyimesi E, Szanto A, Zeher M. 2013. Follicular helper T cells may play an important role in the severity of primary Sjögren’s syndrome. Clin Immunol. 147(2):95–104. doi:10.1016/j.clim.2013.02.024.
  • Takeda T, Mizugaki Y, Matsubara L, Imai S, Koike T, Takada K. 2000. Lytic Epstein-Barr virus infection in the synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum. 43(6):1218–1225. doi:10.1002/1529-0131(200006)43:6<1218::AID-ANR4>3.0.CO;2-2.
  • Takei M, Kitamura N, Nagasawa Y, Tsuzuki H, Iwata M, Nagatsuka Y, Nakamura H, Imai K, Fujiwara S. 2022. Are viral infections key inducers of autoimmune diseases? Focus on Epstein-Barr virus. Viruses. 14(9):1900. doi:10.3390/v14091900.
  • Takeuchi M, Sato Y, Yasui H, Ozawa H, Ohno K, Takata K, Gion Y, Orita Y, Tachibana T, Itoh T, et al. 2014. Epstein-Barr virus-infected cells in IgG4-related lymphadenopathy with comparison with extranodal IgG4-related disease. Am J Surg Pathol. 38(7):946–955. doi:10.1097/PAS.0000000000000206.
  • Tamoto N, Nagata K, Hara S, Nakayama Y, Kuwamoto S, Matsushita M, Kato M, Hayashi K. 2019. Subclinical Epstein-Barr virus primary infection and lytic reactivation induce thyrotropin receptor autoantibodies. Viral Immunol. 32(9):362–369. doi:10.1089/vim.2019.0086.
  • Taussig D, Wine Y. 2021. When a virus lies in wait. Elife. 10:e71121. doi:10.7554/eLife.71121.
  • Tengvall K, Huang J, Hellström C, Kammer P, Biström M, Ayoglu B, Lima Bomfim I, Stridh P, Butt J, Brenner N, et al. 2019. Molecular mimicry between Anoctamin 2 and Epstein-Barr virus nuclear antigen 1 associates with multiple sclerosis risk. Proc Natl Acad Sci U S A. 116(34):16955–16960. doi:10.1073/pnas.1902623116.
  • Tian J, Zhang D, Yao X, Huang Y, Lu Q. 2023. Global epidemiology of systemic lupus erythematosus: a comprehensive systematic analysis and modelling study. Ann Rheum Dis. 82(3):351–356. doi:10.1136/ard-2022-223035.
  • Trier N, Izarzugaza J, Chailyan A, Marcatili P, Houen G. 2018. Human MHC-II with shared epitope motifs are optimal Epstein-Barr virus glycoprotein 42 ligands-relation to rheumatoid arthritis. Int J Mol Sci. 19(1):317. doi:10.3390/ijms19010317.
  • Trier NH, Holm BE, Heiden J, Slot O, Locht H, Lindegaard H, Svendsen A, Nielsen CT, Jacobsen S, Theander E, et al. 2018. Antibodies to a strain-specific citrullinated Epstein-Barr virus peptide diagnoses rheumatoid arthritis. Sci Rep. 8(1):3684. doi:10.1038/s41598-018-22058-6.
  • Tzartos JS, Khan G, Vossenkamper A, Cruz-Sadaba M, Lonardi S, Sefia E, Meager A, Elia A, Middeldorp JM, Clemens M, et al. 2012. Association of innate immune activation with latent Epstein-Barr virus in active MS lesions. Neurology. 78(1):15–23. doi:10.1212/WNL.0b013e31823ed057.
  • van Noort JM, Bajramovic JJ, Plomp AC, van Stipdonk MJ. 2000. Mistaken self, a novel model that links microbial infections with myelin-directed autoimmunity in multiple sclerosis. J Neuroimmunol. 105(1):46–57. doi:10.1016/s0165-5728(00)00181-8.
  • van Sechel AC, Bajramovic JJ, van Stipdonk MJ, Persoon-Deen C, Geutskens SB, van Noort JM. 1999. EBV-induced expression and HLA-DR-restricted presentation by human B cells of alpha B-crystallin, a candidate autoantigen in multiple sclerosis. Journal of Immunology. 162(1):129–135. doi:10.4049/jimmunol.162.1.129.
  • Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, Robertson N, La Rocca N, Uitdehaag B, van der Mei I, et al. 2020. Rising prevalence of multiple sclerosis worldwide: insights from the Atlas of MS, third edition. Mult Scler. 26(14):1816–1821. doi:10.1177/1352458520970841.
  • Wang L, Wang FS, Gershwin ME. 2015. Human autoimmune diseases: a comprehensive update. J Intern Med. 278(4):369–395. doi:10.1111/joim.12395.
  • Wang SC, Liao JY. 2022. Epidemiologic implication of the association between herpes simplex virus infection and the risk of type 1 diabetes mellitus: a nationwide case-control study in Taiwan. Int J Environ Res Public Health. 19(13):7832. doi:10.3390/ijerph19137832.
  • Williams H, McAulay K, Macsween KF, Gallacher NJ, Higgins CD, Harrison N, Swerdlow AJ, Crawford DH. 2005. The immune response to primary EBV infection: a role for natural killer cells. Br J Haematol. 129(2):266–274. doi:10.1111/j.1365-2141.2005.05452.x.
  • Willson TA, Kuhn BR, Jurickova I, Gerad S, Moon D, Bonkowski E, Carey R, Collins MH, Xu H, Jegga AG, et al. 2012. STAT3 genotypic variation and cellular STAT3 activation and colon leukocyte recruitment in pediatric Crohn disease. J Pediatr Gastroenterol Nutr. 55(1):32–43. doi:10.1097/MPG.0b013e318246be78.
  • Wilson MR, Arroyave CM, Miles L, Tan EM. 1977. Immune reactants in cryoproteins. Relationship to complement activation. Ann Rheum Dis. 36(6):540–548. doi:10.1136/ard.36.6.540.
  • Wood RA, Guthridge L, Thurmond E, Guthridge CJ, Kheir JM, Bourn RL, Wagner CA, Chen H, DeJager W, Macwana SR, et al. 2021. Serologic markers of Epstein-Barr virus reactivation are associated with increased disease activity, inflammation, and interferon pathway activation in patients with systemic lupus erythematosus. J Transl Autoimmun. 4:100117. doi:10.1016/j.jtauto.2021.100117.
  • Woulfe J, Gray MT, Ganesh MS, Middeldorp JM. 2016. Human serum antibodies against EBV latent membrane protein 1 cross-react with α-synuclein. Neurol Neuroimmunol Neuroinflamm. 3(4):e239. doi:10.1212/NXI.0000000000000239.
  • Wu S, He C, Tang TY, Li YQ. 2019. A review on co-existent Epstein-Barr virus-induced complications in inflammatory bowel disease. Eur J Gastroenterol Hepatol. 31(9):1085–1091. doi:10.1097/MEG.0000000000001474.
  • Wucherpfennig KW, Strominger JL. 1995. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell. 80(5):695–705. doi:10.1016/0092-8674(95)90348-8.
  • Xu W, Jiang X, Chen J, Mao Q, Zhao X, Sun X, Zhong L, Rong L. 2020. Chronic active Epstein-Barr virus infection involving gastrointestinal tract mimicking inflammatory bowel disease. BMC Gastroenterol. 20(1):257. doi:10.1186/s12876-020-01395-9.
  • Xuan J, Ji Z, Wang B, Zeng X, Chen R, He Y, Rao P, Wu P, Shi G. 2020. Serological Evidence for the Association Between Epstein-Barr Virus Infection and Sjögren’s Syndrome. Front Immunol. 11:590444. doi:10.3389/fimmu.2020.590444.
  • Yamashita K, Sato R, Fukumoto R, Ofuji Y, Nagamoto T, Kubono H, Kawamura M, Suzuki K. 2022. Epstein-Barr viral corneal stromal keratitis occurring during rheumatoid arthritis treatment: a case report. BMC Ophthalmol. 22(1):31. doi:10.1186/s12886-022-02257-6.
  • Yang J, Sundrud MS, Skepner J, Yamagata T. 2014. Targeting Th17 cells in autoimmune diseases. Trends Pharmacol Sci. 35(10):493–500. doi:10.1016/j.tips.2014.07.006.
  • Yin H, Zhao M, Wu X, Gao F, Luo Y, Ma L, Liu S, Zhang G, Chen J, Li F, et al. 2010. Hypomethylation and overexpression of CD70 (TNFSF7) in CD4+ T cells of patients with primary Sjögren’s syndrome. J Dermatol Sci. 59(3):198–203. doi:10.1016/j.jdermsci.2010.06.011.
  • Yogev N, Bedke T, Kobayashi Y, Brockmann L, Lukas D, Regen T, Croxford AL, Nikolav A, Hövelmeyer N, von Stebut E, et al. 2022. CD4(+) T-cell-derived IL-10 promotes CNS inflammation in mice by sustaining effector T cell survival. Cell Rep. 38(13):110565. doi:10.1016/j.celrep.2022.110565.
  • Yoshizaki A, Miyagaki T, DiLillo DJ, Matsushita T, Horikawa M, Kountikov EI, Spolski R, Poe JC, Leonard WJ, Tedder TF, et al. 2012. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature. 491(7423):264–268. doi:10.1038/nature11501.
  • Yu H, Nagafuchi Y, Fujio K. 2021. Clinical and immunological biomarkers for systemic lupus erythematosus. Biomolecules. 11(7):928. doi:10.3390/biom11070928.
  • Zandman-Goddard G, Shoenfeld Y. 2005. Infections and SLE. Autoimmunity. 38(7):473–485. doi:10.1080/08916930500285352.
  • Zhou H, Schmidt SCS, Jiang S, Willox B, Bernhardt K, Liang J, Johannsen EC, Kharchenko P, Gewurz BE, Kieff E, et al. 2015. Epstein-Barr virus oncoprotein super-enhancers control B cell growth. Cell Host Microbe. 17(2):205–216. doi:10.1016/j.chom.2014.12.013.
  • Zhou J-Q, Zeng L, Zhang Q, Wu X-Y, Zhang M-L, Jing X-T, Wang Y-F, Gan H-T. 2020. Clinical features of Epstein-Barr virus in the intestinal mucosa and blood of patients with inflammatory bowel disease. Saudi J Gastroenterol. 26(6):312–320. doi:10.4103/sjg.SJG_30_20.
  • Ziętara N, Łyszkiewicz M, Krueger A, Weiss S. 2014. B-cell modulation of dendritic-cell function: signals from the far side. Eur J Immunol. 44(1):23–32. doi:10.1002/eji.201344007.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.