Hyperstimulation of the immune system as a cause of autoimmune diseases
- Authors: Ryabkova V.A.1, Churilov L.P.1, Shoenfeld Y.1,2,3
-
Affiliations:
- Saint Petersburg State University
- Tel-Aviv University School of Medicine
- The First I.M. Sechenov Moscow State Medical University (Sechenov University)
- Issue: Vol 75, No 3 (2020)
- Pages: 204-213
- Section: IMMUNOLOGY: CURRENT ISSUES
- URL: https://ogarev-online.ru/vramn/article/view/125683
- DOI: https://doi.org/10.15690/vramn1276
- ID: 125683
Cite item
Full Text
Abstract
The pathogenesis of autoimmune diseases is very complex and multi-factorial. The concept of “Mosaics of Autoimmunity” was introduced to the scientific community 30 years ago by Y. Shoenfeld and D.A. Isenberg, and since then new tiles to the puzzle are continuously added. This concept specifies general pathological ideas about the multifactorial threshold model for polygenic inheritance with a threshold effect by the action of a number of external causal factors as applied to the field of autoimmunology. Among the external factors that can excessively stimulate the immune system, contributing to the development of autoimmune reactions, researchers are particularly interested in chemical substances, which are widely used in pharmacology and medicine. In this review we highlight the autoimmune dynamics — i.e. a multistep pathogenesis of autoimmune diseases and the subsequent development of lymphoma in some cases. In this context several issues are addressed — namely, genetic basis of autoimmunity; environmental immunostimulatory risk factors; gene/environmental interaction; pre-clinical autoimmunity with the presence of autoantibodies; and the mechanisms, underlying lymphomagenesis in autoimmune pathology. We believe that understanding the common model of the pathogenesis of autoimmune diseases is the first step to their successful management.
Keywords
Full Text
##article.viewOnOriginalSite##About the authors
Varvara A. Ryabkova
Saint Petersburg State University
Email: varvara-ryabkova@yandex.ru
ORCID iD: 0000-0001-6973-9901
SPIN-code: 8991-9240
Russian Federation, Saint-Petersburg
Leonid P. Churilov
Saint Petersburg State University
Email: elpach@mail.ru
ORCID iD: 0000-0001-6359-0026
SPIN-code: 8879-0875
MD, PhD, Professor
Russian Federation, Saint-PetersburgYehuda Shoenfeld
Saint Petersburg State University; Tel-Aviv University School of Medicine; The First I.M. Sechenov Moscow State Medical University (Sechenov University)
Author for correspondence.
Email: shoenfel@post.tau.ac.il
ORCID iD: 0000-0003-2802-4090
SPIN-code: 5950-3930
MD, PhD, Professor
Israel, Chaim Sheba Medical Center, The Zabludowicz Center for Autoimmune Diseases, Tel Hashomer 5265601References
- Metchnikoff E. La lutte pour l’existence entre les diverses parties de l’organisme. Rev Sci. 1892;11:324.
- Zaichik AS, Churilov LP, Utekhin VJ. Autoimmune regulation of genetically determined cell functions in health and disease. Pathophysiology. 2008;15:191–207. doi: 10.1016/J.PATHOPHYS.2008.07.002.
- Poletaev A, Boura P. The immune system, natural autoantibodies and general homeostasis in health and disease. Hippokratia. 2011;15:295–298.
- Shoenfeld Y, Isenberg DA. The mosaic of autoimmunity. Immunol Today. 1989;10:123–126. doi: 10.1016/0167-5699(89)90245-4.
- Shoenfeld Y, Isenberg D. The mosaic of autoimmunity. Holland: Elsevier; 1989.
- Perricone C, Shoenfeld Y. Mosaic of autoimmunity: the novel factors of autoimmune diseases. Academic Press; 2019.
- Kochi Y. Genetics of autoimmune diseases: perspectives from genome-wide association studies. Int Immunol. 2016;28:155–161. doi: 10.1093/intimm/dxw002.
- Yamamoto K, Okada Y. Shared genetic factors and their causality in autoimmune diseases. Ann Rheum Dis. 2019;78:1449–1451. doi: 10.1136/annrheumdis-2019-215099.
- Matzaraki V, Kumar V, Wijmenga C, Zhernakova A. The MHC locus and genetic susceptibility to autoimmune and infectious diseases. Genome Biol. 2017;18:76. doi: 10.1186/s13059-017-1207-1.
- Bodis G, Toth V, Schwarting A. Role of human leukocyte antigens (HLA) in autoimmune diseases. Rheumatol Ther. 2018;5:5–20. doi: 10.1007/s40744-018-0100-z.
- Gutierrez-Achury J, Zhernakova A, Pulit SL, Trynka G, Hunt KA, Romanos J, et al. Fine mapping in the MHC region accounts for 18% additional genetic risk for celiac disease. Nat Genet. 2015;47:577–578. doi: 10.1038/ng.3268.
- Sollid LM, Pos W, Wucherpfennig KW. Molecular mechanisms for contribution of MHC molecules to autoimmune diseases. Curr Opin Immunol. 2014;31:24–30. doi: 10.1016/j.coi.2014.08.005.
- Jonkers IH, Wijmenga C. Context-specific effects of genetic variants associated with autoimmune disease. Hum Mol Genet. 2017;26:R185–192. doi: 10.1093/hmg/ddx254.
- Gutierrez-Arcelus M, Rich SS, Raychaudhuri S. Autoimmune diseases — connecting risk alleles with molecular traits of the immune system. Nat Rev Genet. 2016;17:160–174. doi: 10.1038/nrg.2015.33.
- Zenewicz LA, Abraham C, Flavell RA, Cho JH. Unraveling the genetics of autoimmunity. Cell. 2010;140:791–797. doi: 10.1016/j.cell.2010.03.003.
- Arango M-T, Perricone C, Kivity S, Cipriano E, Ceccarelli F, Valesini G, et al. HLA-DRB1 the notorious gene in the mosaic of autoimmunity. Immunol Res. 2017;65:82–98. doi: 10.1007/s12026-016-8817-7.
- Shoenfeld Y, Ehrenfeld M, Perry O. The kaleidoscope of autoimmunity – from genes to microbiome. Clin Immunol. 2019;199:1–4. doi: 10.1016/j.clim.2018.12.003.
- Roggen EL, Corsini E, van Loveren H, Luebke R. Immunotoxicity testing: implementation of mechanistic understanding, key pathways of toxicological concern, and components of these pathways. In: Kleinjans J, ed. Toxicogenomics-Based Cell. Model., Academic Press; 2014, p. 57–65. doi: 10.1016/B978-0-12-397862-2.00004-8.
- Ercolini AM, Miller SD. The role of infections in autoimmune disease. Clin Exp Immunol 2009;155:1–15. doi: 10.1111/j.1365-2249.2008.03834.x.
- Arango M-T, Shoenfeld Y, Cervera R, Anaya J-M. Chapter 19 Infection and autoimmune diseases. In: Anaya J, Shoenfeld Y, Rojas-Villarraga A, et al., eds. Autoimmun. From Bench to Bedside, Bogota (Colombia): El Rosario University Press; 2013, p. 855.
- Toubi E, Vadasz Z. Innate immune-responses and their role in driving autoimmunity. Autoimmun Rev. 2019;18:306–311. doi: 10.1016/J.AUTREV.2018.10.005.
- Sfriso P, Ghirardello A, Botsios C, Tonon M, Zen M, Bassi N, et al. Infections and autoimmunity: the multifaceted relationship. J Leukoc Biol. 2010;87:385–395. doi: 10.1189/jlb.0709517.
- Jain A, Pasare C. Innate control of adaptive immunity: beyond the three-signal paradigm. J Immunol. 2017;198:3791–3800. doi: 10.4049/jimmunol.1602000.
- Proal AD, Albert PJ, Marshall TG. The human microbiome and autoimmunity. Curr Opin Rheumatol. 2013;25:234–240. doi: 10.1097/BOR.0b013e32835cedbf.
- Kivity S, Agmon-Levin N, Blank M, Shoenfeld Y. Infections and autoimmunity — friends or foes? Trends Immunol. 2009;30:409–414. doi: 10.1016/j.it.2009.05.005.
- Rose NR. Introduction. Infect. Autoimmun., Elsevier; 2015, p. 1–12. doi: 10.1016/B978-0-444-63269-2.09987-6.
- Rose NR. The adjuvant effect in infection and autoimmunity. Clin Rev Allergy Immunol. 2008;34:279–282. doi: 10.1007/s12016-007-8049-7.
- Perricone C, Colafrancesco S, Mazor RD, Soriano A, Agmon-Levin N, Shoenfeld Y. Autoimmune/inflammatory syndrome induced by adjuvants (ASIA) 2013: Unveiling the pathogenic, clinical and diagnostic aspects. J Autoimmun. 2013;47:1–16. doi: 10.1016/j.jaut.2013.10.004.
- Li N, Wang M, Bramble LA, Schmitz DA, Schauer JJ, Sioutas C, et al. The adjuvant effect of ambient particulate matter is closely reflected by the particulate oxidant potential. Environ Health Perspect. 2009;117:1116–1123. doi: 10.1289/ehp.0800319.
- Shelly S, Boaz M, Orbach H. Prolactin and autoimmunity. Autoimmun Rev. 2012;11:A465–470. doi: 10.1016/J.AUTREV.2011.11.009.
- Shoenfeld Y, Agmon-Levin N. “ASIA” — Autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun. 2011;36:4–8. doi: 10.1016/j.jaut.2010.07.003.
- Segal Y, Dahan S, Sharif K, Bragazzi NL, Watad A, Amital H. The value of autoimmune syndrome induced by adjuvant (ASIA) — shedding light on orphan diseases in autoimmunity. Autoimmun Rev. 2018;17:440–448. doi: 10.1016/j.autrev.2017.11.037.
- Watad A, Bragazzi NL, McGonagle D, Adawi M, Bridgewood C, Damiani G, et al. Autoimmune/inflammatory syndrome induced by adjuvants (ASIA) demonstrates distinct autoimmune and autoinflammatory disease associations according to the adjuvant subtype: Insights from an analysis of 500 cases. Clin Immunol. 2019;203:1–8. doi: 10.1016/j.clim.2019.03.007.
- Del Giudice G, Rappuoli R, Didierlaurent AM. Correlates of adjuvanticity: a review on adjuvants in licensed vaccines. Semin Immunol. 2018;39:14–21. doi: 10.1016/J.SMIM.2018.05.001.
- Pellegrino P, Clementi E, Radice S. On vaccine’s adjuvants and autoimmunity: Current evidence and future perspectives. Autoimmun Rev. 2015;14:880–888. doi: 10.1016/j.autrev.2015.05.014.
- Batista-Duharte A, Lindblad EB, Oviedo-Orta E. Progress in understanding adjuvant immunotoxicity mechanisms. Toxicol Lett. 2011;203:97–105. doi: 10.1016/j.toxlet.2011.03.001.
- Karussis D, Petrou P. The spectrum of post-vaccination inflammatory CNS demyelinating syndromes. Autoimmun Rev. 2014;13:215–224. doi: 10.1016/j.autrev.2013.10.003.
- Djurisic S, Jakobsen JC, Petersen SB, Kenfelt M, Gluud C. Aluminium adjuvants used in vaccines versus placebo or no intervention. Cochrane Database Syst Rev. 2017. doi: 10.1002/14651858.CD012805.
- Varela-Martínez E, Abendaño N, Asín J, Sistiaga-Poveda M, Pérez MM, Reina R, et al. Molecular signature of aluminum hydroxide adjuvant in ovine PBMCs by integrated mRNA and microRNA transcriptome sequencing. Front Immunol. 2018;9:2406. doi: 10.3389/fimmu.2018.02406.
- Inbar R, Weiss R, Tomljenovic L, Arango M-T, Deri Y, Shaw CA, et al. Behavioral abnormalities in female mice following administration of aluminum adjuvants and the human papillomavirus (HPV) vaccine Gardasil. Immunol Res. 2017;65:136–149. doi: 10.1007/s12026-016-8826-6.
- Exley C. Aluminium-based adjuvants should not be used as placebos in clinical trials. Vaccine. 2011;29:9289. doi: 10.1016/j.vaccine.2011.08.062.
- Levy Y, Baytner-Zamir R. Silicone and autoimmune/inflammatory syndrome induced by adjuvants (ASIA). Vaccines Autoimmun., Hoboken, NJ, USA: John Wiley & Sons, Inc; 2015, p. 79–86. doi: 10.1002/9781118663721.ch7.
- Cohen Tervaert JW, Colaris MJ, Van Der Hulst RR. Silicone breast implants and autoimmune rheumatic diseases: myth or reality. Curr Opin Rheumatol. 2017;29:348–354. doi: 10.1097/BOR.0000000000000391.
- Soriano A, Butnaru D, Shoenfeld Y. Long-term inflammatory conditions following silicone exposure: the expanding spectrum of the autoimmune/inflammatory syndrome induced by adjuvants (ASIA). Clin Exp Rheumatol. 2014;32:151–154.
- Hajdu SD, Agmon-Levin N, Shoenfeld Y. Silicone and autoimmunity. Eur J Clin Invest. 2011;41:203–211. doi: 10.1111/j.1365-2362.2010.02389.x.
- Vijaya Bhaskar TB, Ma N, Lendlein A, Roch T. The interaction of human macrophage subsets with silicone as a biomaterial. Clin Hemorheol Microcirc. 2015;61:119–133. doi: 10.3233/CH-151991.
- Miro-Mur F, Hindié M, Kandhaya-Pillai R, Tobajas V, Schwartz S, Alijotas-Reig J. Medical-grade silicone induces release of proinflammatory cytokines in peripheral blood mononuclear cells without activating T cells. J Biomed Mater Res Part B Appl Biomater. 2009;90B:510–250. doi: 10.1002/jbm.b.31312.
- Katzin WE, Centeno JA, Feng L-J, Kiley M, Mullick FG. Pathology of lymph nodes from patients with breast implants. Am J Surg Pathol. 2005;29:506–511. doi: 10.1097/01.pas.0000155145.60670.e4.
- Wolfram D, Rabensteiner E, Grundtman C, Böck G, Mayerl C, Parson W, et al. T regulatory cells and TH17 cells in peri-silicone implant capsular fibrosis. Plast Reconstr Surg 2012;129:327e–337e. doi: 10.1097/PRS.0b013e31823aeacf.
- Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng. 2005;11:1–18. doi: 10.1089/ten.2005.11.1.
- Schwarz K. A bound form of silicon in glycosaminoglycans and polyuronides. Proc Natl Acad Sci. 1973;70:1608–1612. doi: 10.1073/pnas.70.5.1608.
- Zolotykh VG, Kim AY, Shoenfeld Y, Churilov LP. Galactorrhea following silicone breast implant placement. Isr Med Assoc. J 2019;21:523.
- Gawda A, Majka G, Nowak B, Marcinkiewicz J. Air pollution, oxidative stress, and exacerbation of autoimmune diseases. Cent J Immunol. 2017;42:305–312. doi: 10.5114/ceji.2017.70975.
- Penkała M, Ogrodnik P, Rogula-Kozłowska W. Particulate matter from the road surface abrasion as a problem of non-exhaust emission control. Environments. 2018;5:9. doi: 10.3390/environments5010009.
- Yang Y, Pun VC, Sun S, Lin H, Mason TG, Qiu H. Particulate matter components and health: a literature review on exposure assessment. J Public Heal Emerg. 2018;2:14–21. doi: 10.21037/jphe.2018.03.03.
- O’Driscoll CA, Mezrich JD. The aryl hydrocarbon receptor as an immune-modulator of atmospheric particulate matter-mediated autoimmunity. Front Immunol. 2018;9:2833. doi: 10.3389/fimmu.2018.02833.
- Bernatsky S, Smargiassi A, Barnabe C, Svenson LW, Brand A, Martin R V., et al. Fine particulate air pollution and systemic autoimmune rheumatic disease in two Canadian provinces. Environ Res. 2016;146:85–91. doi: 10.1016/j.envres.2015.12.021.
- Faustini A, Renzi M, Kirchmayer U, Balducci M, Davoli M, Forastiere F. Short-term exposure to air pollution might exacerbate autoimmune diseases. Environ Epidemiol. 2018;2:e025. doi: 10.1097/EE9.0000000000000025.
- Soprun L, Akulin I, Utekhin V, Gvozdetskiy A, Churilov L. Urbanization-related factors of the incidence of Type I diabetes mellitus. Biosfera. 2019;10:282–292. doi: 10.24855/biosfera.v10i4.464.
- Zhao C-N, Xu Z, Wu G-C, Mao Y-M, Liu L-N, Qian-Wu, et al. Emerging role of air pollution in autoimmune diseases. Autoimmun Rev. 2019;18:607–614. doi: 10.1016/j.autrev.2018.12.010.
- Li N, Wang M, Bramble LA, Schmitz DA, Schauer JJ, Sioutas C, et al. The adjuvant effect of ambient particulate matter is closely reflected by the particulate oxidant potential. Environ Health Perspect. 2009;117:1116–1123. doi: 10.1289/ehp.0800319.
- Pfeffer PE, Ho TR, Mann EH, Kelly FJ, Sehlstedt M, Pourazar J, et al. Urban particulate matter stimulation of human dendritic cells enhances priming of naive CD8 T lymphocytes. Immunology. 2018;153:502–512. doi: 10.1111/imm.12852.
- Kulvinskiene I, Raudoniute J, Bagdonas E, Ciuzas D, Poliakovaite K, Stasiulaitiene I, et al. Lung alveolar tissue destruction and protein citrullination in diesel exhaust‐exposed mouse lungs. Basic Clin Pharmacol Toxicol. 2019;125:bcpt.13213. doi: 10.1111/bcpt.13213.
- Wu W, Jin Y, Carlsten C. Inflammatory health effects of indoor and outdoor particulate matter. J Allergy Clin Immunol. 2018;141:833–844. doi: 10.1016/j.jaci.2017.12.981.
- Valesini G, Gerardi MC, Iannuccelli C, Pacucci VA, Pendolino M, Shoenfeld Y. Citrullination and autoimmunity. Autoimmun Rev. 2015;14:490–497. doi: 10.1016/j.autrev.2015.01.013.
- Colasanti T, Fiorito S, Alessandri C, Serafino A, Andreola F, Barbati C, et al. Diesel exhaust particles induce autophagy and citrullination in Normal Human Bronchial Epithelial cells. Cell Death Dis. 2018;9:1073. doi: 10.1038/s41419-018-1111-y.
- Bernatsky S, Smargiassi A, Joseph L, Awadalla P, Colmegna I, Hudson M, et al. Industrial air emissions, and proximity to major industrial emitters, are associated with anti-citrullinated protein antibodies. Environ Res. 2017;157:60–63. doi: 10.1016/j.envres.2017.04.035.
- Khan S, Gerber DE. Autoimmunity, checkpoint inhibitor therapy and immune-related adverse events: a review. Semin Cancer Biol. 2019. doi: 10.1016/j.semcancer.2019.06.012.
- Toxicities associated with checkpoint inhibitor immunotherapy 2017. Available from: https://www.uptodate.com/contents/toxicities-associated-with-checkpoint-inhibitor-immunotherapy (accessed: 11.12.2019).
- Khan S, Gerber DE. Autoimmunity, checkpoint inhibitor therapy and immune-related adverse events: a review. Semin Cancer Biol. 2019. doi: 10.1016/j.semcancer.2019.06.012.
- Myers G. Immune-related adverse events of immune checkpoint inhibitors: a brief review. Curr Oncol. 2018;25. doi: 10.3747/co.25.4235.
- Albarel F, Castinetti F, Brue T. Management of endocrine disease: immune check point inhibitors-induced hypophysitis. Eur J Endocrinol. 2019;181:R107–118. doi: 10.1530/EJE-19-0169.
- Tocut M, Brenner R, Zandman-Goddard G. Autoimmune phenomena and disease in cancer patients treated with immune checkpoint inhibitors. Autoimmun Rev. 2018;17:610–616. doi: 10.1016/J.AUTREV.2018.01.010.
- Benfaremo D, Manfredi L, Luchetti MM, Gabrielli A. Musculoskeletal and rheumatic diseases induced by immune checkpoint inhibitors: a review of the literature. Curr Drug Saf. 2018;13:150–164. doi: 10.2174/1574886313666180508122332.
- Martins F, Sofiya L, Sykiotis GP, Lamine F, Maillard M, Fraga M, et al. Adverse effects of immune-checkpoint inhibitors: epidemiology, management and surveillance. Nat Rev Clin Oncol. 2019;16:563–580. doi: 10.1038/s41571-019-0218-0.
- Theofilopoulos AN, Kono DH, Baccala R. The multiple pathways to autoimmunity. Nat Immunol. 2017;18:716–724. doi: 10.1038/ni.3731.
- Khan Z, Hammer C, Guardino E, Chandler GS, Albert ML. Mechanisms of immune-related adverse events associated with immune checkpoint blockade: using germline genetics to develop a personalized approach. Genome Med. 2019;11:39. doi: 10.1186/s13073-019-0652-8.
- Kumar P, Saini S, Prabhakar BS. Cancer immunotherapy with check point inhibitor can cause autoimmune adverse events due to loss of Treg homeostasis. Semin Cancer Biol. 2019. doi: 10.1016/j.semcancer.2019.01.006.
- Harley JB, Chen X, Pujato M, Miller D, Maddox A, Forney C, et al. Transcription factors operate across disease loci, with EBNA2 implicated in autoimmunity. Nat Genet. 2018;50:699–707. doi: 10.1038/s41588-018-0102-3.
- Hasan Ali O, Berner F, Bomze D, Fässler M, Diem S, Cozzio A, et al. Human leukocyte antigen variation is associated with adverse events of checkpoint inhibitors. Eur J Cancer. 2019;107:8–14. doi: 10.1016/J.EJCA.2018.11.009.
- Whitaker JA, Ovsyannikova IG, Poland GA. Adversomics: a new paradigm for vaccine safety and design. Expert Rev Vaccines. 2015;14:935–947. doi: 10.1586/14760584.2015.1038249.
- Linnik JE, Egli A. Impact of host genetic polymorphisms on vaccine induced antibody response. Hum Vaccin Immunother. 2016;12:907–915. doi: 10.1080/21645515.2015.1119345.
- Guimarães LE, Baker B, Perricone C, Shoenfeld Y. Vaccines, adjuvants and autoimmunity. Pharmacol Res. 2015;100:190–209. doi: 10.1016/j.phrs.2015.08.003.
- Sarkanen T, Alakuijala A, Julkunen I, Partinen M. Narcolepsy associated with pandemrix vaccine. Curr Neurol Neurosci Rep. 2018;18:43. doi: 10.1007/s11910-018-0851-5.
- Pérez D, Gilburd B, Cabrera-Marante Ó, Martínez-Flores JA, Serrano M, Naranjo L, et al. Predictive autoimmunity using autoantibodies: screening for anti-nuclear antibodies. Clin Chem Lab Med. 2018;56:1771–1777. doi: 10.1515/cclm-2017-0241.
- Ma W-T, Chang C, Gershwin ME, Lian Z-X. Development of autoantibodies precedes clinical manifestations of autoimmune diseases: a comprehensive review. J Autoimmun. 2017;83:95–112. doi: 10.1016/j.jaut.2017.07.003.
- Goodnow CC. Multistep pathogenesis of autoimmune disease. Cell. 2007;130:25–35. doi: 10.1016/j.cell.2007.06.033.
- Weinstein IB. Carcinogenesis. Encycl. Cancer, Berlin, Heidelberg: Springer Berlin Heidelberg; 2008, p. 503–504. doi: 10.1007/978-3-540-47648-1_843.
- Lossos IS. Molecular pathogenesis of diffuse large B-cell lymphoma. J Clin Oncol. 2005;23:6351–6357. doi: 10.1200/JCO.2005.05.012.
- Kleinstern G, Maurer MJ, Liebow M, Habermann TM, Koff JL, Allmer C, et al. History of autoimmune conditions and lymphoma prognosis. Blood Cancer. J. 2018;8:73. doi: 10.1038/s41408-018-0105-4.
- Ekström Smedby K, Vajdic CM, Falster M, Engels EA, Martínez-Maza O, Turner J, et al. Autoimmune disorders and risk of non-Hodgkin lymphoma subtypes: a pooled analysis within the InterLymph Consortium. Blood. 2008;111:4029–3038. doi: 10.1182/blood-2007-10-119974.
- Baecklund E, Smedby KE, Sutton L-A, Askling J, Rosenquist R. Lymphoma development in patients with autoimmune and inflammatory disorders — what are the driving forces? Semin Cancer Biol. 2014;24:61–70. doi: 10.1016/j.semcancer.2013.12.001.
- Goules AV., Tzioufas AG. Lymphomagenesis in Sjögren’s syndrome: predictive biomarkers towards precision medicine. Autoimmun Rev. 2019;18:137–143. doi: 10.1016/j.autrev.2018.08.007.
- Colafrancesco S, Perricone C, Priori R, Valesini G, Shoenfeld Y. Sjögren’s syndrome: another facet of the autoimmune/inflammatory syndrome induced by adjuvants (ASIA). J Autoimmun. 2014;51:10–16. doi: 10.1016/j.jaut.2014.03.003.
- Cohen Tervaert JW. Autoinflammatory/autoimmunity syndrome induced by adjuvants (ASIA; Shoenfeld’s syndrome): a new flame. Autoimmun Rev. 2018;17:1259–1264. doi: 10.1016/j.autrev.2018.07.003.
- Bragazzi N, Watad A, Adawi M, Amital H, Aljadeff G, Shoenfeld50Y. Adjuvants and autoimmunity: why do we develop autoantibodies, autoimmune diseases and lymphomas. Isr Med Assoc J. 2017;19:403–405.
- Edward BM. Autoimmunity and lymphoma: a brief review. J Rheum Dis Treat. 2018;4. doi: 10.23937/2469-5726/1510062.
- Suarez F, Lecuit M. Infection-associated non-Hodgkin lymphomas. Clin Microbiol Infect. 2015;21:991–997. doi: 10.1016/J.CMI.2015.07.020.
- Butnaru D, Shoenfeld Y. Adjuvants and lymphoma risk as part of the ASIA spectrum. Immunol Res. 2015;61:79–89. doi: 10.1007/s12026-014-8622-0.
- Durnian JM, Stewart RMK, Tatham R, Batterbury M, Kaye SB. Cyclosporin-A associated malignancy. Clin Ophthalmol. 2007;1:421–430.
- Selmi C, Bin Gao B, Gershwin ME. The long and latent road to autoimmunity. Cell Mol Immunol. 2018;15:543–546. doi: 10.1038/s41423-018-0018-y.
- Ellis JA, Kemp AS, Ponsonby A-L. Gene-environment interaction in autoimmune disease. Expert Rev Mol Med. 2014;16:e4. doi: 10.1017/erm.2014.5.
Supplementary files
