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Erschienen in: Immunologic Research 1/2017

14.07.2016 | Environment and Autoimmunity

Adjuvants- and vaccines-induced autoimmunity: animal models

verfasst von: Jiram Torres Ruiz, Luis Luján, Miri Blank, Yehuda Shoenfeld

Erschienen in: Immunologic Research | Ausgabe 1/2017

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Abstract

The emergence of autoimmunity after vaccination has been described in many case reports and series. Everyday there is more evidence that this relationship is more than casual. In humans, adjuvants can induce non-specific constitutional, musculoskeletal or neurological clinical manifestations and in certain cases can lead to the appearance or acceleration of an autoimmune disease in a subject with genetic susceptibility. The fact that vaccines and adjuvants can trigger a pathogenic autoimmune response is corroborated by animal models. The use of animal models has enabled the study of the effects of application of adjuvants in a homogeneous population with certain genetic backgrounds. In some cases, adjuvants may trigger generalized autoimmune response, resulting in multiple auto-antibodies, but sometimes they can reproduce human autoimmune diseases including rheumatoid arthritis, systemic lupus erythematosus, Sjögren syndrome, autoimmune thyroiditis and antiphospholipid syndrome and may provide insights about the potential adverse effects of adjuvants. Likewise, they give information about the clinical, immunological and histologic characteristics of autoimmune diseases in many organs, especially secondary lymphoid tissue. Through the description of the physiopathological characteristics of autoimmune diseases reproduced in animal models, new treatment targets can be described and maybe in the future, we will be able to recognize some high-risk population in whom the avoidance of certain adjuvants can reduce the incidence of autoimmune diseases, which typically results in high morbidity and mortality in young people. Herein, we describe the main animal models that can reproduce human autoimmune diseases with emphasis in how they are similar to human conditions.
Literatur
2.
Zurück zum Zitat Ahmed SS, Schur PH, Macdonald NE, Steinman L, Narcolepsy. A(H1N1) pandemic influenza, and pandemic influenza vaccinations: what is known and unknown about the neurological disorder, the role for autoimmunity, and vaccine adjuvants. J Autoimmun. 2014;50:1–11.CrossRefPubMed Ahmed SS, Schur PH, Macdonald NE, Steinman L, Narcolepsy. A(H1N1) pandemic influenza, and pandemic influenza vaccinations: what is known and unknown about the neurological disorder, the role for autoimmunity, and vaccine adjuvants. J Autoimmun. 2014;50:1–11.CrossRefPubMed
3.
Zurück zum Zitat Fournie GJ, Mas M, Cautain B, et al. Induction of autoimmunity through bystander effects. Lessons from immunological disorders induced by heavy metals. J Autoimmun. 2001;16(3):319–26.CrossRefPubMed Fournie GJ, Mas M, Cautain B, et al. Induction of autoimmunity through bystander effects. Lessons from immunological disorders induced by heavy metals. J Autoimmun. 2001;16(3):319–26.CrossRefPubMed
4.
Zurück zum Zitat Guimaraes LE, Baker B, Perricone C, Shoenfeld Y. Vaccines, adjuvants and autoimmunity. Pharmacol Res. 2015;100:190–209.CrossRefPubMed Guimaraes LE, Baker B, Perricone C, Shoenfeld Y. Vaccines, adjuvants and autoimmunity. Pharmacol Res. 2015;100:190–209.CrossRefPubMed
5.
Zurück zum Zitat Cruz-Tapias P, Agmon-Levin N, Israeli E, Anaya JM, Shoenfeld Y. Autoimmune (auto-inflammatory) syndrome induced by adjuvants (ASIA)—animal models as a proof of concept. Curr Med Chem. 2013;20:4030–6.CrossRefPubMed Cruz-Tapias P, Agmon-Levin N, Israeli E, Anaya JM, Shoenfeld Y. Autoimmune (auto-inflammatory) syndrome induced by adjuvants (ASIA)—animal models as a proof of concept. Curr Med Chem. 2013;20:4030–6.CrossRefPubMed
6.
Zurück zum Zitat Whitehouse M. Oily adjuvants and autoimmunity: Now time for reconsideration? Lupus. 2012;21:217–22.CrossRefPubMed Whitehouse M. Oily adjuvants and autoimmunity: Now time for reconsideration? Lupus. 2012;21:217–22.CrossRefPubMed
7.
Zurück zum Zitat Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol. 2004;82:9. Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol. 2004;82:9.
8.
Zurück zum Zitat Hoffmann MH, Tuncel J, Skriner K, et al. The rheumatoid arthritis-associated autoantigen hnRNP-A2 (RA33) is a major stimulator of autoimmunity in rats with pristane-induced arthritis. J Immunol. 2007;179(11):7568–76.CrossRefPubMed Hoffmann MH, Tuncel J, Skriner K, et al. The rheumatoid arthritis-associated autoantigen hnRNP-A2 (RA33) is a major stimulator of autoimmunity in rats with pristane-induced arthritis. J Immunol. 2007;179(11):7568–76.CrossRefPubMed
9.
Zurück zum Zitat Platica M, Bojko C, Steiner G, Hollander VP. Effect of subcutaneously administered 2,6,10,14-tetramethylpentadecane on plasmacytoma growth. Cancer Res. 1980;40:2229–33.PubMed Platica M, Bojko C, Steiner G, Hollander VP. Effect of subcutaneously administered 2,6,10,14-tetramethylpentadecane on plasmacytoma growth. Cancer Res. 1980;40:2229–33.PubMed
10.
Zurück zum Zitat Bizjak M, Selmi C, Praprotnik S, et al. Silicone implants and lymphoma: the role of inflammation. J Autoimmun. 2015;65:64–73.CrossRefPubMed Bizjak M, Selmi C, Praprotnik S, et al. Silicone implants and lymphoma: the role of inflammation. J Autoimmun. 2015;65:64–73.CrossRefPubMed
11.
Zurück zum Zitat Israeli E, Agmon-Levin N, Blank M, Shoenfeld Y. Macrophagic myofaciitis a vaccine (alum) autoimmune-related disease. Clin Rev Allergy Immunol. 2011;41(2):163–8.CrossRefPubMed Israeli E, Agmon-Levin N, Blank M, Shoenfeld Y. Macrophagic myofaciitis a vaccine (alum) autoimmune-related disease. Clin Rev Allergy Immunol. 2011;41(2):163–8.CrossRefPubMed
12.
Zurück zum Zitat Favoino E, Favia EI, Digiglio L, Racanelli V, Shoenfeld Y, Perosa F. Effects of adjuvants for human use in systemic lupus erythematosus (SLE)-prone (New Zealand black/New Zealand white) F1 mice. Clin Exp Immunol. 2012;175:32–40.CrossRef Favoino E, Favia EI, Digiglio L, Racanelli V, Shoenfeld Y, Perosa F. Effects of adjuvants for human use in systemic lupus erythematosus (SLE)-prone (New Zealand black/New Zealand white) F1 mice. Clin Exp Immunol. 2012;175:32–40.CrossRef
13.
Zurück zum Zitat Soldevilla HF, Briones SFR, Navarra SV. Systemic lupus erythematosus following HPV immunization or infection? Lupus. 2012;21:4.CrossRef Soldevilla HF, Briones SFR, Navarra SV. Systemic lupus erythematosus following HPV immunization or infection? Lupus. 2012;21:4.CrossRef
14.
Zurück zum Zitat Agmon-Levin N, Arango MT, Kivity S, et al. Immunization with hepatitis B vaccine accelerates SLE-like disease in a murine model. J Autoimmun. 2014;54:21–32.CrossRefPubMed Agmon-Levin N, Arango MT, Kivity S, et al. Immunization with hepatitis B vaccine accelerates SLE-like disease in a murine model. J Autoimmun. 2014;54:21–32.CrossRefPubMed
15.
Zurück zum Zitat Holmdahl R, Lorentzen JC, Lu S, et al. Arthritis induced in rats with non-immunogenic adjuvants as models for rheumatoid arthritis. Immunol Rev. 2001;184:19.CrossRef Holmdahl R, Lorentzen JC, Lu S, et al. Arthritis induced in rats with non-immunogenic adjuvants as models for rheumatoid arthritis. Immunol Rev. 2001;184:19.CrossRef
16.
Zurück zum Zitat Salemo S, D’Amelio R. Could autoimmunity be induced by vaccination? Int Rev Immunol. 2010;29:247–69.CrossRef Salemo S, D’Amelio R. Could autoimmunity be induced by vaccination? Int Rev Immunol. 2010;29:247–69.CrossRef
17.
Zurück zum Zitat Stratton KR, Howe CJ, Johnston RB Jr. Adverse events associated with childhood vaccines other than pertussis and rubella. Summary of a report from the Institute of Medicine. JAMA. 1994;271(20):1602–5.CrossRefPubMed Stratton KR, Howe CJ, Johnston RB Jr. Adverse events associated with childhood vaccines other than pertussis and rubella. Summary of a report from the Institute of Medicine. JAMA. 1994;271(20):1602–5.CrossRefPubMed
18.
19.
Zurück zum Zitat Ropper AH, Victor M. Influenza vaccination and the Guillain–Barré syndrome. N Engl J Med. 1998;339(25):1845–6.CrossRefPubMed Ropper AH, Victor M. Influenza vaccination and the Guillain–Barré syndrome. N Engl J Med. 1998;339(25):1845–6.CrossRefPubMed
20.
Zurück zum Zitat Tishler M, Shoenfeld Y. Vaccination may be associated with autoimmune diseases. Isr Med Assoc J. 2004;6(7):430–2.PubMed Tishler M, Shoenfeld Y. Vaccination may be associated with autoimmune diseases. Isr Med Assoc J. 2004;6(7):430–2.PubMed
21.
Zurück zum Zitat Praprotnik S, Sodin-Semrl S, Tomsic M, Shoenfeld Y. The curiously suspicious: infectious disease may ameliorate an ongoing autoimmune destruction in systemic lupus erythematosus patients. J Autoimmun. 2008;30(1–2):37–41.CrossRefPubMed Praprotnik S, Sodin-Semrl S, Tomsic M, Shoenfeld Y. The curiously suspicious: infectious disease may ameliorate an ongoing autoimmune destruction in systemic lupus erythematosus patients. J Autoimmun. 2008;30(1–2):37–41.CrossRefPubMed
22.
Zurück zum Zitat Shoenfeld Y, Agmon-Levin N. ASIA Autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun. 2011;36(1):4–8.CrossRefPubMed Shoenfeld Y, Agmon-Levin N. ASIA Autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun. 2011;36(1):4–8.CrossRefPubMed
23.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
24.
Zurück zum Zitat Hall SW, Cooke A. Autoimmunity and inflammation: murine models and translational studies. Mamm Genome. 2011;22(7–8):377–89.CrossRefPubMed Hall SW, Cooke A. Autoimmunity and inflammation: murine models and translational studies. Mamm Genome. 2011;22(7–8):377–89.CrossRefPubMed
25.
Zurück zum Zitat Rose NR. The adjuvant effect in infection and autoimmunity. Clin Rev Allergy Immunol. 2008;34(3):279–82.CrossRefPubMed Rose NR. The adjuvant effect in infection and autoimmunity. Clin Rev Allergy Immunol. 2008;34(3):279–82.CrossRefPubMed
26.
Zurück zum Zitat Vladutiu AO, Rose N. Autoimmune murine thyroiditis relation to histocompatibility (H-2) type. Science. 1971;174(4014):1137–9.CrossRefPubMed Vladutiu AO, Rose N. Autoimmune murine thyroiditis relation to histocompatibility (H-2) type. Science. 1971;174(4014):1137–9.CrossRefPubMed
27.
Zurück zum Zitat Lujan L, Pérez M, Salazar E, et al. Autoimmune/autoinflammatory syndrome induced by adjuvants (ASIA syndrome) in commercial sheep. Immunol Res. 2013;56(2–3):317–24.CrossRefPubMed Lujan L, Pérez M, Salazar E, et al. Autoimmune/autoinflammatory syndrome induced by adjuvants (ASIA syndrome) in commercial sheep. Immunol Res. 2013;56(2–3):317–24.CrossRefPubMed
28.
Zurück zum Zitat Wester L, Olofsson P, Ibrahim SM, Holmdahl R. Chronicity of pristane-induced arthritis in rats is controlled by genes on chromosome 14. J Autoimmun. 2003;21(4):305–13.CrossRefPubMed Wester L, Olofsson P, Ibrahim SM, Holmdahl R. Chronicity of pristane-induced arthritis in rats is controlled by genes on chromosome 14. J Autoimmun. 2003;21(4):305–13.CrossRefPubMed
29.
Zurück zum Zitat Holm BC, Lorentzen JC, Bucht A. Adjuvant oil induces waves of arthritogenic lymph node cells prior to arthritis onset. Clin Exp Immunol. 2004;137(1):59–64.CrossRefPubMedPubMedCentral Holm BC, Lorentzen JC, Bucht A. Adjuvant oil induces waves of arthritogenic lymph node cells prior to arthritis onset. Clin Exp Immunol. 2004;137(1):59–64.CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Wester L, Koczan D, Holmberg J, et al. Differential gene expression in pristane-induced arthritis susceptible DA versus resistant E3 rats. Arthritis Res Ther. 2003;5(6):R361–72.CrossRefPubMedPubMedCentral Wester L, Koczan D, Holmberg J, et al. Differential gene expression in pristane-induced arthritis susceptible DA versus resistant E3 rats. Arthritis Res Ther. 2003;5(6):R361–72.CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Vingsbo C, Sahlstrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R. Pristane-induced arthritis in rats a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. Am J Pathol. 1996;149(5):9. Vingsbo C, Sahlstrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R. Pristane-induced arthritis in rats a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. Am J Pathol. 1996;149(5):9.
32.
Zurück zum Zitat Reeves WH, Lee PY, Weinstein JS, Satoh M, Lu L. Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol. 2009;30(9):455–64.CrossRefPubMedPubMedCentral Reeves WH, Lee PY, Weinstein JS, Satoh M, Lu L. Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol. 2009;30(9):455–64.CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat De Franco M, Peters LC, Correa MA, et al. Pristane-induced arthritis loci interact with the Slc11a1 gene to determine susceptibility in mice selected for high inflammation. PLoS ONE. 2014;9(2):e88302.CrossRefPubMedPubMedCentral De Franco M, Peters LC, Correa MA, et al. Pristane-induced arthritis loci interact with the Slc11a1 gene to determine susceptibility in mice selected for high inflammation. PLoS ONE. 2014;9(2):e88302.CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Barker RN, Easterfield AJ, Allen RF, Wells AD, Elson CJ, Thompson SJ. B- and T-cell autoantigens in pristane-induced arthritis. Immunology. 1996;89:6.CrossRef Barker RN, Easterfield AJ, Allen RF, Wells AD, Elson CJ, Thompson SJ. B- and T-cell autoantigens in pristane-induced arthritis. Immunology. 1996;89:6.CrossRef
35.
Zurück zum Zitat Holmberg J, Tuncel J, Yamada H, Lu S, Olofsson P, Holmdahl R. Pristane, a Non-antigenic adjuvant, induces MHC class II-restricted, arthritogenic T cells in the rat. J Immunol. 2006;176(2):1172–9.CrossRefPubMed Holmberg J, Tuncel J, Yamada H, Lu S, Olofsson P, Holmdahl R. Pristane, a Non-antigenic adjuvant, induces MHC class II-restricted, arthritogenic T cells in the rat. J Immunol. 2006;176(2):1172–9.CrossRefPubMed
36.
Zurück zum Zitat Morgan R, Wu B, Song Z, Wooley PH. Immune reactivity to connective tissue antigens in pristane induced arthritis. J Rheumatol. 2004;31:10. Morgan R, Wu B, Song Z, Wooley PH. Immune reactivity to connective tissue antigens in pristane induced arthritis. J Rheumatol. 2004;31:10.
37.
Zurück zum Zitat Zhu W, Jiang C, Xu J, et al. Pristane primed rat T cells enhance TLR3 expression of fibroblast-like synoviocytes via TNF-alpha initiated p38 MAPK and NF-kappaB pathways. Clin Immunol. 2015;156(2):141–53.CrossRefPubMed Zhu W, Jiang C, Xu J, et al. Pristane primed rat T cells enhance TLR3 expression of fibroblast-like synoviocytes via TNF-alpha initiated p38 MAPK and NF-kappaB pathways. Clin Immunol. 2015;156(2):141–53.CrossRefPubMed
38.
Zurück zum Zitat Vingsbo C, Sahistrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R. Avridine-induced arthritis in rats; a T cell-dependent chronic disease influenced both by MHC genes and by non-MHC genes. Clin Exp Immunol. 1995;99(3):359–63.CrossRefPubMedPubMedCentral Vingsbo C, Sahistrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R. Avridine-induced arthritis in rats; a T cell-dependent chronic disease influenced both by MHC genes and by non-MHC genes. Clin Exp Immunol. 1995;99(3):359–63.CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Kaibara N, Hotokebuchi T, Takagishi K, et al. Pathogenic difference between collagen arthritis and adjuvant arthritis. J Exp Med. 1984;159:9.CrossRef Kaibara N, Hotokebuchi T, Takagishi K, et al. Pathogenic difference between collagen arthritis and adjuvant arthritis. J Exp Med. 1984;159:9.CrossRef
40.
Zurück zum Zitat Ratkay LG, Zhang L, Tonzetich J, Waterfield JD. Complete Freund’s adjuvant induces an earlier and more severe arthritis in MRL-ipr mice. J Immunol. 1993;151(1):5081–7.PubMed Ratkay LG, Zhang L, Tonzetich J, Waterfield JD. Complete Freund’s adjuvant induces an earlier and more severe arthritis in MRL-ipr mice. J Immunol. 1993;151(1):5081–7.PubMed
41.
42.
Zurück zum Zitat Svelander L, Müssener A, Erlandsson-Harris H, Kleinau S. Polyclonal Thl cells transfer oil-induced arthritis. Immunology. 1994;91(2):260–5.CrossRef Svelander L, Müssener A, Erlandsson-Harris H, Kleinau S. Polyclonal Thl cells transfer oil-induced arthritis. Immunology. 1994;91(2):260–5.CrossRef
43.
Zurück zum Zitat Lorentzen JC, Glaser A, Jacobsson L, et al. Identification of rat susceptibility loci for adjuvant-oil-induced arthritis. Proc Natl Acad Sci USA. 1998;95:5.CrossRef Lorentzen JC, Glaser A, Jacobsson L, et al. Identification of rat susceptibility loci for adjuvant-oil-induced arthritis. Proc Natl Acad Sci USA. 1998;95:5.CrossRef
44.
Zurück zum Zitat Holm BC, Xu HW, Jacobsson L, Larsson A, Luthman H, Lorentzen J. Rats made congenic for Oia3 on chromosome 10 become susceptible to squalene-induced arthritis. Hum Mol Gen. 2001;10(6):565–72.CrossRefPubMed Holm BC, Xu HW, Jacobsson L, Larsson A, Luthman H, Lorentzen J. Rats made congenic for Oia3 on chromosome 10 become susceptible to squalene-induced arthritis. Hum Mol Gen. 2001;10(6):565–72.CrossRefPubMed
45.
Zurück zum Zitat Carlson BC, Jansson AM, Larsson A, Bucht A, Lorentzen JC. The endogenous adjuvant squalene can induce a chronic T-cell-mediated arthritis in rats. Am J Pathol. 2000;156:2057–65.CrossRefPubMedPubMedCentral Carlson BC, Jansson AM, Larsson A, Bucht A, Lorentzen JC. The endogenous adjuvant squalene can induce a chronic T-cell-mediated arthritis in rats. Am J Pathol. 2000;156:2057–65.CrossRefPubMedPubMedCentral
46.
Zurück zum Zitat Satoh M, Richards HB, Shaheen VM, et al. Widespread susceptibility among inbred mouse strains to the induction of lupus autoantibodies by pristane. Clin Exp Immunol. 2000;121:399–405.CrossRefPubMedPubMedCentral Satoh M, Richards HB, Shaheen VM, et al. Widespread susceptibility among inbred mouse strains to the induction of lupus autoantibodies by pristane. Clin Exp Immunol. 2000;121:399–405.CrossRefPubMedPubMedCentral
47.
Zurück zum Zitat Richards HB, Satoh M, Shaw M, Libert C, Poli V, Reeves WH. Interleukin 6 dependence of anti-DNA antibody production: evidence for two pathways of autoantibody formation in pristane-induced lupus. J Exp Med. 1998;188(5):6.CrossRef Richards HB, Satoh M, Shaw M, Libert C, Poli V, Reeves WH. Interleukin 6 dependence of anti-DNA antibody production: evidence for two pathways of autoantibody formation in pristane-induced lupus. J Exp Med. 1998;188(5):6.CrossRef
48.
Zurück zum Zitat Satoh M, Kumar A, Kanwar YS, Reeves WH. Anti-nuclear antibody production and immune-complex glomerulonephritis in BALB/c mice treated with pristane. Proc Natl Acad Sci USA. 1995;92(24):10934–8.CrossRefPubMedPubMedCentral Satoh M, Kumar A, Kanwar YS, Reeves WH. Anti-nuclear antibody production and immune-complex glomerulonephritis in BALB/c mice treated with pristane. Proc Natl Acad Sci USA. 1995;92(24):10934–8.CrossRefPubMedPubMedCentral
49.
Zurück zum Zitat Feng D, Yang L, Bi X, Stone RC, Patel P, Barnes BJ. Protection of Irf5-deficient mice from pristane-induced lupus involves altered cytokine production and class switching. Eur J Immunol. 2012;42(6):1477–87.CrossRefPubMedPubMedCentral Feng D, Yang L, Bi X, Stone RC, Patel P, Barnes BJ. Protection of Irf5-deficient mice from pristane-induced lupus involves altered cytokine production and class switching. Eur J Immunol. 2012;42(6):1477–87.CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Richards HB, Satoh M, Jennette JC, Okano T, Kanwar YS, Reeves WH. Disparate T cell requirements of two subsets of lupus-specific autoantibodies in pristane-treated mice. Clin Exp Immunol. 1999;115(3):547–53.CrossRefPubMedPubMedCentral Richards HB, Satoh M, Jennette JC, Okano T, Kanwar YS, Reeves WH. Disparate T cell requirements of two subsets of lupus-specific autoantibodies in pristane-treated mice. Clin Exp Immunol. 1999;115(3):547–53.CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Perry D, Sang A, Yin Y, Zheng YY, Morel L. Murine models of systemic lupus erythematosus. J Biomed Biotechnol. 2011;2011:1–19.CrossRef Perry D, Sang A, Yin Y, Zheng YY, Morel L. Murine models of systemic lupus erythematosus. J Biomed Biotechnol. 2011;2011:1–19.CrossRef
52.
Zurück zum Zitat Summers SA, Odobasic D, Khouri MB, et al. Endogenous interleukin (IL)-17A promotes pristane-induced systemic autoimmunity and lupus nephritis induced by pristane. Clin Exp Immunol. 2014;176:342–50.CrossRef Summers SA, Odobasic D, Khouri MB, et al. Endogenous interleukin (IL)-17A promotes pristane-induced systemic autoimmunity and lupus nephritis induced by pristane. Clin Exp Immunol. 2014;176:342–50.CrossRef
53.
Zurück zum Zitat Clynes R, Calvani N, Croker PB, Richards HB. Modulation of the immune response in pristane-induced lupus by expression of activation and inhibitory Fc receptors. Clin Exp Immunol. 2005;141:230–7.CrossRefPubMedPubMedCentral Clynes R, Calvani N, Croker PB, Richards HB. Modulation of the immune response in pristane-induced lupus by expression of activation and inhibitory Fc receptors. Clin Exp Immunol. 2005;141:230–7.CrossRefPubMedPubMedCentral
54.
Zurück zum Zitat Bagavant H, Nandula SR, Kaplonek P, Rybakowska PD, Deshmukh US. Alum, an aluminium based adjuvant, induces Sjögren’s syndrome-like disorder in mice. Clin Exp Rheumatol. 2014;32(2):251–5.PubMedPubMedCentral Bagavant H, Nandula SR, Kaplonek P, Rybakowska PD, Deshmukh US. Alum, an aluminium based adjuvant, induces Sjögren’s syndrome-like disorder in mice. Clin Exp Rheumatol. 2014;32(2):251–5.PubMedPubMedCentral
55.
Zurück zum Zitat Kong YC, Audibert F, Giraldo AA, Rose NR, Chedid L. Effects of natural or synthetic microbial adjuvants on induction of autoimmune thyroiditis. Infect Immun. 1985;49:40–5.PubMedPubMedCentral Kong YC, Audibert F, Giraldo AA, Rose NR, Chedid L. Effects of natural or synthetic microbial adjuvants on induction of autoimmune thyroiditis. Infect Immun. 1985;49:40–5.PubMedPubMedCentral
56.
Zurück zum Zitat Blank M, Krause I, Fridkin M, et al. Bacterial induction of autoantibodies to β2-glycoprotein-I accounts for the infectious etiology of antiphospholipid syndrome. J Clin Invest. 2002;109(6):797–804.CrossRefPubMedPubMedCentral Blank M, Krause I, Fridkin M, et al. Bacterial induction of autoantibodies to β2-glycoprotein-I accounts for the infectious etiology of antiphospholipid syndrome. J Clin Invest. 2002;109(6):797–804.CrossRefPubMedPubMedCentral
57.
Zurück zum Zitat Zivkovic I, Stojanovic M, Petrusic V, Inic-Kanada A, Dimitrijevic L. Induction of APS after TTd hyper-immunization has a different outcome in BALB/c and C57BL/6 mice. Am J Reprod Immunol. 2011;65(5):492–502.CrossRefPubMed Zivkovic I, Stojanovic M, Petrusic V, Inic-Kanada A, Dimitrijevic L. Induction of APS after TTd hyper-immunization has a different outcome in BALB/c and C57BL/6 mice. Am J Reprod Immunol. 2011;65(5):492–502.CrossRefPubMed
58.
Zurück zum Zitat Petrusic V, Zivkovic I, Muhandes L, Dimitrijevic R, Stojanovic M, Dimitrijevic L. Infection-induced autoantibodies and pregnancy related pathology: an animal model. Reprod Fertil Dev. 2014;26(4):578–86.CrossRefPubMed Petrusic V, Zivkovic I, Muhandes L, Dimitrijevic R, Stojanovic M, Dimitrijevic L. Infection-induced autoantibodies and pregnancy related pathology: an animal model. Reprod Fertil Dev. 2014;26(4):578–86.CrossRefPubMed
59.
Zurück zum Zitat Petrusic V, Todorovic N, Zivkovic I, et al. Autoantibody response and pregnancy-related pathology induced by combined LPS and tetanus toxoid hyperimmunization in BALB/c and C57BL/6 mice. Autoimmunity. 2015;48(2):87–99.CrossRefPubMed Petrusic V, Todorovic N, Zivkovic I, et al. Autoantibody response and pregnancy-related pathology induced by combined LPS and tetanus toxoid hyperimmunization in BALB/c and C57BL/6 mice. Autoimmunity. 2015;48(2):87–99.CrossRefPubMed
60.
Zurück zum Zitat Koppang EO, Bjerkas I, Haugarvoll E, et al. Vaccination-induced systemic autoimmunity in farmed Atlantic salmon. J Immunol. 2008;181(7):4807–14.CrossRefPubMed Koppang EO, Bjerkas I, Haugarvoll E, et al. Vaccination-induced systemic autoimmunity in farmed Atlantic salmon. J Immunol. 2008;181(7):4807–14.CrossRefPubMed
Metadaten
Titel
Adjuvants- and vaccines-induced autoimmunity: animal models
verfasst von
Jiram Torres Ruiz
Luis Luján
Miri Blank
Yehuda Shoenfeld
Publikationsdatum
14.07.2016
Verlag
Springer US
Erschienen in
Immunologic Research / Ausgabe 1/2017
Print ISSN: 0257-277X
Elektronische ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-016-8819-5

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