Effects of Gliadin on Autoimmune Responses of Central Nervous System of C57BL/6 Mice
Gliadin on Autoimmune Responses of Central Nervous System
-
Parisa Esmaeili
,
Elham Rostami
,
Arefeh Akbarijavar
,
Alireza Akbari Meyestani
,
Hamed Bashiri
,
Mohammad Ali Rezaee
,
Shohreh Fakhari
Abstract
Gluten sensitivity contributes to various degrees of neurological manifestations and neurodegenerative immunological changes. We investigated the experimental features of anti-gliadin immune responses in the central nervous system (CNS) of mice.
Female C57BL6 mice were divided into three groups. Mice immunized with complete Freund's adjuvant (CFA) or gliadin emulsified in CFA, and the control group received phosphate-buffered saline (PBS). Immunohistochemistry, hematoxylin-eosin, and Luxol fast blue staining were performed on the sections. The serum levels of interleukin (IL)-17 and interferon-gamma (IFN-γ) were measured using enzyme-linked immunosorbent assay (ELISA). Reverse transcriptase-polymerase chain reaction (RT-PCR) was used to assess the mRNA levels of chemokine (C-X-C motif) ligand-2 (CXCL-2), C-C motif chemokine ligand-2 (CCL-2), and CXCL-10.
In gliadin+CFA immunized mice, the microscopic lesions included perivascular edema, focal-microgliosis, and acute neuronal necrosis in the cortex, subcortical, Purkinje cell layer, and ventral horn of the spinal cord. While extravasation of anti-IgG antibodies and selective targeting of Purkinje cells were observed in gliadin+CFA immunized mice. A significant increase in serum IL-17 and IFN-g levels (p<0.05), as well as expression of CXCL-2, CCL-2, and CXCL-10 in mice immunized with gliadin+CFA, were monitored versus controls.
Our findings indicated that the immune responses directed against gliadin peptides might contribute to blood-brain barrier breakdown, extravasation of serum anti-IgG, gliosis, and acute neuronal necrosis in the cortex and cerebellar Purkinje cells. Anti-IgG antibodies may cause extravasation of blood-born anti-gliadin antibodies and selective targeting of Purkinje cells observed in mice immunized with peptide tryptic (pt) -gliadin in CFA.
1. Sander SD, Størdal K, Hansen TP, Andersen A-MN, Murray JA, Lillevang ST, et al. Validation of celiac disease diagnoses recorded in the Danish National Patient Register using duodenal biopsies, celiac disease-specific antibodies, and human leukocyte-antigen genotypes. Clin Epidemiol. 2016;8:789–99.
2. Caio G, Volta U, Sapone A, Leffler DA, De Giorgio R, Catassi C, et al. Celiac disease: a comprehensive current review. BMC Med. 2019;17(1):1-20.
3. Parzanese I, Qehajaj D, Patrinicola F, Aralica M, Chiriva-Internati M, Stifter S, et al. Celiac disease: From pathophysiology to treatment. World J Gastrointest Pathophysiol. 2017;8(2):27–38.
4. Yu XB, Uhde M, Green PH, Alaedini A. Autoantibodies in the extraintestinal manifestations of celiac disease. Nutrients. 2018;10(8):1123.
5. Dupont FM, Vensel WH, Tanaka CK, Hurkman WJ, Altenbach SB. Deciphering the complexities of the wheat flour proteome using quantitative two-dimensional electrophoresis, three proteases and tandem mass spectrometry. Proteome Sci. 2011;11;9:10.
6. Shimada S, Tanigawa T, Watanabe T, Nakata A, Sugimura N, Itani S, et al. Involvement of gliadin, a component of wheat gluten, in increased intestinal permeability leading to non-steroidal anti-inflammatory drug-induced small-intestinal damage. PloS one. 2019;14(2):e0211436.
7. Abazari O, Shafaei Z, Divsalar A, Eslami-Moghadam M, Ghalandari B, Saboury AA. Probing the biological evaluations of a new designed Pt (II) complex using spectroscopic and theoretical approaches: Human hemoglobin as a target. J Biomol Struct Dyn. 2016;34(5):1123-31.
8. Ahmadabadi FB, Shahbazkhani B, Tafakhori A, Khosravi A, Mashhadi MM. A genetic study of celiac disease in patients with multiple sclerosis in comparison with celiac patients and healthy controls. Govaresh. 2018;22(4):256-60.
9. Thomsen HL, Jessen EB, Passali M, Frederiksen JL. The role of gluten in multiple sclerosis: A systematic review. Mult Scler Relat Disord. 2019;27:156-63.
10. Shiri-Shahsavar MR, Mirshafiee A, Parastouei K, Ebrahimi-Kalan A, Yekaninejad S, Soleymani F, et al. A Novel Combination of Docosahexaenoic Acid, All-Trans Retinoic Acid, and 1, 25-Dihydroxyvitamin D 3 Reduces T-Bet Gene Expression, Serum Interferon Gamma, and Clinical Scores but Promotes PPARγ Gene Expression in Experimental Autoimmune Encephalomyelitis. J Mol Neurosci . 2016;60(4):498-508.
11. Torkaman M, Ghollasi M, Mohammadnia-Afrouzi M, Salimi A, Amari A. The effect of transplanted human Wharton's jelly mesenchymal stem cells treated with IFN-γ on experimental autoimmune encephalomyelitis mice. Cell Immunol. 2017;311:1-12.
12. Singh I, Nath N, Saxena N, Singh AK, Won J-S. Regulation of IL-10 and IL-17 mediated experimental autoimmune encephalomyelitis by S-nitrosoglutathione. Immunobiology. 2018;223(10):549-54.
13. Abazari O, Divsalar A, Ghobadi R. Inhibitory effects of oxali-Platin as a chemotherapeutic drug on the function and structure of bovine liver catalase. J Biomol Struct Dyn. 2020;38(2):609-15.
14. Constantinescu CS, Farooqi N, O'Brien K, Gran B. Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS). Br J Pharmacol. 2011;164(4):1079-106.
15. Pinheiro MAL, Kooij G, Mizee MR, Kamermans A, Enzmann G, Lyck R, et al. Immune cell trafficking across the barriers of the central nervous system in multiple sclerosis and stroke. Biochim BiophysActaMolBasisDis. 2016;1862(3):461-71.
16. Kuwabara T, Ishikawa F, Kondo M, Kakiuchi T. The Role of IL-17 and Related Cytokines in Inflammatory Autoimmune Diseases. Mediators Inflamm. 2017;2017:3908061.
17. Xu J, Neal LM, Ganguly A, Kolbe JL, Hargarten JC, Elsegeiny W, et al. Chemokine receptor CXCR3 is required for lethal brain pathology but not pathogen clearance during cryptococcal meningoencephalitis. Sc Adv. 2020;6(25):eaba2502.
18. Abazari O, Shafaei Z, Divsalar A, Eslami-Moghadam M, Ghalandari B, Saboury AA, et al. Interaction of the synthesized anticancer compound of the methyl-glycine 1, 10-phenanthroline platinum nitrate with human serum albumin and human hemoglobin proteins by spectroscopy methods and molecular docking. J Iran Chem Soc. 2020:1-14.
19. Kaushansky N, Bakos E, Becker-Herman S, Shachar I, Ben-Nun A. Circulating Picomolar Levels of CCL2 Downregulate Ongoing Chronic Experimental Autoimmune Encephalomyelitis by Induction of Regulatory Mechanisms. J Immunol Res. 2019;203(7):1857-66.
20. Hernandez-Lahoz C, Mauri-Capdevila G, Vega-Villar J, Rodrigo L. [Neurological disorders associated with gluten sensitivity]. Rev Neurol. 2011 1;53(5):287-300.
21. Lombardi E, Bergamo P, Maurano F, Bozzella G, Luongo D, Mazzarella G, et al. Selective inhibition of the gliadin‐specific, cell‐mediated immune response by transamidation with microbial transglutaminase. J Leukoc Biol. 2013;93(4):479-88.
22. Halon A, Donizy P, Biecek P, Rudno-Rudzinska J, Kielan W, Matkowski R. HER-2 expression in immunohistochemistry has no prognostic significance in gastric cancer patients. Sci World J. 2012;2012.
23. Wang D-W, Li D, Wang J, Zhao Y, Wang Z, Yue G, et al. Genome-wide analysis of complex wheat gliadins, the dominant carriers of celiac disease epitopes. Sci Rep. 2017;7:44609.
24. Escudié J-B, Rance B, Malamut G, Khater S, Burgun A, Cellier C, et al. A novel data-driven workflow combining literature and electronic health records to estimate comorbidities burden for a specific disease: a case study on autoimmune comorbidities in patients with celiac disease. BMC MED INFORM DECIS. 2017;17(1):140.
25. Shafaei Z, Abazari O, Divsalar A, Ghalandari B, Poursoleiman A, Saboury AA, et al. Effect of a Synthesized Amyl-Glycine1, 10-Phenanthroline Platinum Nitrate on Structure and Stability of Human Blood Carrier Protein, Albumin: Spectroscopic and Modeling Approaches. J Fluoresc. 2017;27(5):1829-38.
26. Martín ISM, Vilar EG, Yurrita LC. Can gluten contribute to degenerative and neuronal diseases? Still no evidence based results. JONNPR. 2016;1(1):3-12.
27. Palosuo K, Varjonen E, Nurkkala J, Kalkkinen N, Harvima R, Reunala T, et al. Transglutaminase-mediated cross-linking of a peptic fraction of omega-5 gliadin enhances IgE reactivity in wheat-dependent, exercise-induced anaphylaxis. J Allergy Clin Immunol. 2003;111(6):1386-92.
28. Ozuna CV, Barro F. Characterization of gluten proteins and celiac disease-related immunogenic epitopes in the Triticeae: cereal domestication and breeding contributed to decrease the content of gliadins and gluten. Mol Breed. 2018;38(3):22.
29. Petersen J, Ciacchi L, Tran MT, Loh KL, Kooy-Winkelaar Y, Croft NP, et al. T cell receptor cross-reactivity between gliadin and bacterial peptides in celiac disease. Nat Struct Mol Biol. 2020;27(1):49-61.
30. Ouahidi I, Elhamsas AEY, Bouyahyaoui Y, Mernissi FZ, Aarab L. Characterization and Stability of specific IgE to White Egg’s, Gliadin’s and Peanut’s Proteins among Children. Iran J Allergy Asthma Immunol.2010; 9(2): 97-102.
31. Musavi H, Abazari O, Barartabar Z, et al. The benefits of Vitamin D in the COVID-19 pandemic: biochemical and immunological mechanisms. Arch Physiol Biochem. 2020:1-9.
32. Kuang F, Wang BR, Zhang P, Fei LL, Jia Y, Duan XL, et al. Extravasation of blood-borne immunoglobulin G through blood-brain barrier during adrenaline-induced transient hypertension in the rat. INT J NEUROSCI. 2004;114(6):575-91.
33. Asadi A, Nezhad DY, Javazm AR, Khanicheragh P, Mashouri L, Shakeri F, et al. In vitro Effects of Curcumin on Transforming Growth Factor-β-mediated Non-Smad Signaling Pathway, Oxidative Stress, and Pro‐inflammatory Cytokines Production with Human Vascular Smooth Muscle Cells. IJAAI. 2019:1-10.
34. Michalak Z, Lebrun A, Di Miceli M, Rousset MC, Crespel A, Coubes P, et al. IgG leakage may contribute to neuronal dysfunction in drug-refractory epilepsies with blood-brain barrier disruption. J Neuropathol Exp Neurol. 2012;71(9):826-38.
35. Hadjivassiliou M, Zis P. Neurological manifestations of gluten sensitivity. Neurorheumatology. 2019:179-86.
36. Diaz-Castro J, Muriel-Neyra C, Martin-Masot R, Moreno-Fernandez J, Maldonado J, Nestares T. Oxidative stress, DNA stability and evoked inflammatory signaling in young celiac patients consuming a gluten-free diet. Eur J Nutr. 2019:1-8.
37. Zare Z, Dizaj TN, Lohrasbi A, et al. Silibinin inhibits TGF-β-induced MMP-2 and MMP-9 through Smad Signaling pathway in colorectal cancer HT-29 cells. Basic Clin Cancer Res. 2020;12(2):79-88.
38. Nanri K, Okuma M, Sato S, Yoneda M, Taguchi T, Mitoma H, et al. Prevalence of autoantibodies and the efficacy of immunotherapy for autoimmune cerebellar ataxia. Intern Med J. 2016;55(5):449-54.
39. Passali M, Josefsen K, Frederiksen JL, Antvorskov JC. Current Evidence on the Efficacy of Gluten-Free Diets in Multiple Sclerosis, Psoriasis, Type 1 Diabetes and Autoimmune Thyroid Diseases. Nutrients. 2020;12(8):2316.
40. Osipova ED, Semyachkina-Glushkovskaya OV, Morgun AV, Pisareva NV, Malinovskaya NA, Boitsova EB, et al. Gliotransmitters and cytokines in the control of blood-brain barrier permeability. Rev Neurosci. 2018;29(5):567-91.
41. Camara-Lemarroy CR, Silva C, Greenfield J, Liu W-Q, Metz LM, Yong VW. Biomarkers of intestinal barrier function in multiple sclerosis are associated with disease activity. Mult. 2019:26(11),p:1340-1350.
42. Tanuma N, Sakuma H, Sasaki A, Matsumoto Y. Chemokine expression by astrocytes plays a role in microglia/macrophage activation and subsequent neurodegeneration in secondary progressive multiple sclerosis. ACTA NEUROPATHOL. 2006;112(2):195-204.
2. Caio G, Volta U, Sapone A, Leffler DA, De Giorgio R, Catassi C, et al. Celiac disease: a comprehensive current review. BMC Med. 2019;17(1):1-20.
3. Parzanese I, Qehajaj D, Patrinicola F, Aralica M, Chiriva-Internati M, Stifter S, et al. Celiac disease: From pathophysiology to treatment. World J Gastrointest Pathophysiol. 2017;8(2):27–38.
4. Yu XB, Uhde M, Green PH, Alaedini A. Autoantibodies in the extraintestinal manifestations of celiac disease. Nutrients. 2018;10(8):1123.
5. Dupont FM, Vensel WH, Tanaka CK, Hurkman WJ, Altenbach SB. Deciphering the complexities of the wheat flour proteome using quantitative two-dimensional electrophoresis, three proteases and tandem mass spectrometry. Proteome Sci. 2011;11;9:10.
6. Shimada S, Tanigawa T, Watanabe T, Nakata A, Sugimura N, Itani S, et al. Involvement of gliadin, a component of wheat gluten, in increased intestinal permeability leading to non-steroidal anti-inflammatory drug-induced small-intestinal damage. PloS one. 2019;14(2):e0211436.
7. Abazari O, Shafaei Z, Divsalar A, Eslami-Moghadam M, Ghalandari B, Saboury AA. Probing the biological evaluations of a new designed Pt (II) complex using spectroscopic and theoretical approaches: Human hemoglobin as a target. J Biomol Struct Dyn. 2016;34(5):1123-31.
8. Ahmadabadi FB, Shahbazkhani B, Tafakhori A, Khosravi A, Mashhadi MM. A genetic study of celiac disease in patients with multiple sclerosis in comparison with celiac patients and healthy controls. Govaresh. 2018;22(4):256-60.
9. Thomsen HL, Jessen EB, Passali M, Frederiksen JL. The role of gluten in multiple sclerosis: A systematic review. Mult Scler Relat Disord. 2019;27:156-63.
10. Shiri-Shahsavar MR, Mirshafiee A, Parastouei K, Ebrahimi-Kalan A, Yekaninejad S, Soleymani F, et al. A Novel Combination of Docosahexaenoic Acid, All-Trans Retinoic Acid, and 1, 25-Dihydroxyvitamin D 3 Reduces T-Bet Gene Expression, Serum Interferon Gamma, and Clinical Scores but Promotes PPARγ Gene Expression in Experimental Autoimmune Encephalomyelitis. J Mol Neurosci . 2016;60(4):498-508.
11. Torkaman M, Ghollasi M, Mohammadnia-Afrouzi M, Salimi A, Amari A. The effect of transplanted human Wharton's jelly mesenchymal stem cells treated with IFN-γ on experimental autoimmune encephalomyelitis mice. Cell Immunol. 2017;311:1-12.
12. Singh I, Nath N, Saxena N, Singh AK, Won J-S. Regulation of IL-10 and IL-17 mediated experimental autoimmune encephalomyelitis by S-nitrosoglutathione. Immunobiology. 2018;223(10):549-54.
13. Abazari O, Divsalar A, Ghobadi R. Inhibitory effects of oxali-Platin as a chemotherapeutic drug on the function and structure of bovine liver catalase. J Biomol Struct Dyn. 2020;38(2):609-15.
14. Constantinescu CS, Farooqi N, O'Brien K, Gran B. Experimental autoimmune encephalomyelitis (EAE) as a model for multiple sclerosis (MS). Br J Pharmacol. 2011;164(4):1079-106.
15. Pinheiro MAL, Kooij G, Mizee MR, Kamermans A, Enzmann G, Lyck R, et al. Immune cell trafficking across the barriers of the central nervous system in multiple sclerosis and stroke. Biochim BiophysActaMolBasisDis. 2016;1862(3):461-71.
16. Kuwabara T, Ishikawa F, Kondo M, Kakiuchi T. The Role of IL-17 and Related Cytokines in Inflammatory Autoimmune Diseases. Mediators Inflamm. 2017;2017:3908061.
17. Xu J, Neal LM, Ganguly A, Kolbe JL, Hargarten JC, Elsegeiny W, et al. Chemokine receptor CXCR3 is required for lethal brain pathology but not pathogen clearance during cryptococcal meningoencephalitis. Sc Adv. 2020;6(25):eaba2502.
18. Abazari O, Shafaei Z, Divsalar A, Eslami-Moghadam M, Ghalandari B, Saboury AA, et al. Interaction of the synthesized anticancer compound of the methyl-glycine 1, 10-phenanthroline platinum nitrate with human serum albumin and human hemoglobin proteins by spectroscopy methods and molecular docking. J Iran Chem Soc. 2020:1-14.
19. Kaushansky N, Bakos E, Becker-Herman S, Shachar I, Ben-Nun A. Circulating Picomolar Levels of CCL2 Downregulate Ongoing Chronic Experimental Autoimmune Encephalomyelitis by Induction of Regulatory Mechanisms. J Immunol Res. 2019;203(7):1857-66.
20. Hernandez-Lahoz C, Mauri-Capdevila G, Vega-Villar J, Rodrigo L. [Neurological disorders associated with gluten sensitivity]. Rev Neurol. 2011 1;53(5):287-300.
21. Lombardi E, Bergamo P, Maurano F, Bozzella G, Luongo D, Mazzarella G, et al. Selective inhibition of the gliadin‐specific, cell‐mediated immune response by transamidation with microbial transglutaminase. J Leukoc Biol. 2013;93(4):479-88.
22. Halon A, Donizy P, Biecek P, Rudno-Rudzinska J, Kielan W, Matkowski R. HER-2 expression in immunohistochemistry has no prognostic significance in gastric cancer patients. Sci World J. 2012;2012.
23. Wang D-W, Li D, Wang J, Zhao Y, Wang Z, Yue G, et al. Genome-wide analysis of complex wheat gliadins, the dominant carriers of celiac disease epitopes. Sci Rep. 2017;7:44609.
24. Escudié J-B, Rance B, Malamut G, Khater S, Burgun A, Cellier C, et al. A novel data-driven workflow combining literature and electronic health records to estimate comorbidities burden for a specific disease: a case study on autoimmune comorbidities in patients with celiac disease. BMC MED INFORM DECIS. 2017;17(1):140.
25. Shafaei Z, Abazari O, Divsalar A, Ghalandari B, Poursoleiman A, Saboury AA, et al. Effect of a Synthesized Amyl-Glycine1, 10-Phenanthroline Platinum Nitrate on Structure and Stability of Human Blood Carrier Protein, Albumin: Spectroscopic and Modeling Approaches. J Fluoresc. 2017;27(5):1829-38.
26. Martín ISM, Vilar EG, Yurrita LC. Can gluten contribute to degenerative and neuronal diseases? Still no evidence based results. JONNPR. 2016;1(1):3-12.
27. Palosuo K, Varjonen E, Nurkkala J, Kalkkinen N, Harvima R, Reunala T, et al. Transglutaminase-mediated cross-linking of a peptic fraction of omega-5 gliadin enhances IgE reactivity in wheat-dependent, exercise-induced anaphylaxis. J Allergy Clin Immunol. 2003;111(6):1386-92.
28. Ozuna CV, Barro F. Characterization of gluten proteins and celiac disease-related immunogenic epitopes in the Triticeae: cereal domestication and breeding contributed to decrease the content of gliadins and gluten. Mol Breed. 2018;38(3):22.
29. Petersen J, Ciacchi L, Tran MT, Loh KL, Kooy-Winkelaar Y, Croft NP, et al. T cell receptor cross-reactivity between gliadin and bacterial peptides in celiac disease. Nat Struct Mol Biol. 2020;27(1):49-61.
30. Ouahidi I, Elhamsas AEY, Bouyahyaoui Y, Mernissi FZ, Aarab L. Characterization and Stability of specific IgE to White Egg’s, Gliadin’s and Peanut’s Proteins among Children. Iran J Allergy Asthma Immunol.2010; 9(2): 97-102.
31. Musavi H, Abazari O, Barartabar Z, et al. The benefits of Vitamin D in the COVID-19 pandemic: biochemical and immunological mechanisms. Arch Physiol Biochem. 2020:1-9.
32. Kuang F, Wang BR, Zhang P, Fei LL, Jia Y, Duan XL, et al. Extravasation of blood-borne immunoglobulin G through blood-brain barrier during adrenaline-induced transient hypertension in the rat. INT J NEUROSCI. 2004;114(6):575-91.
33. Asadi A, Nezhad DY, Javazm AR, Khanicheragh P, Mashouri L, Shakeri F, et al. In vitro Effects of Curcumin on Transforming Growth Factor-β-mediated Non-Smad Signaling Pathway, Oxidative Stress, and Pro‐inflammatory Cytokines Production with Human Vascular Smooth Muscle Cells. IJAAI. 2019:1-10.
34. Michalak Z, Lebrun A, Di Miceli M, Rousset MC, Crespel A, Coubes P, et al. IgG leakage may contribute to neuronal dysfunction in drug-refractory epilepsies with blood-brain barrier disruption. J Neuropathol Exp Neurol. 2012;71(9):826-38.
35. Hadjivassiliou M, Zis P. Neurological manifestations of gluten sensitivity. Neurorheumatology. 2019:179-86.
36. Diaz-Castro J, Muriel-Neyra C, Martin-Masot R, Moreno-Fernandez J, Maldonado J, Nestares T. Oxidative stress, DNA stability and evoked inflammatory signaling in young celiac patients consuming a gluten-free diet. Eur J Nutr. 2019:1-8.
37. Zare Z, Dizaj TN, Lohrasbi A, et al. Silibinin inhibits TGF-β-induced MMP-2 and MMP-9 through Smad Signaling pathway in colorectal cancer HT-29 cells. Basic Clin Cancer Res. 2020;12(2):79-88.
38. Nanri K, Okuma M, Sato S, Yoneda M, Taguchi T, Mitoma H, et al. Prevalence of autoantibodies and the efficacy of immunotherapy for autoimmune cerebellar ataxia. Intern Med J. 2016;55(5):449-54.
39. Passali M, Josefsen K, Frederiksen JL, Antvorskov JC. Current Evidence on the Efficacy of Gluten-Free Diets in Multiple Sclerosis, Psoriasis, Type 1 Diabetes and Autoimmune Thyroid Diseases. Nutrients. 2020;12(8):2316.
40. Osipova ED, Semyachkina-Glushkovskaya OV, Morgun AV, Pisareva NV, Malinovskaya NA, Boitsova EB, et al. Gliotransmitters and cytokines in the control of blood-brain barrier permeability. Rev Neurosci. 2018;29(5):567-91.
41. Camara-Lemarroy CR, Silva C, Greenfield J, Liu W-Q, Metz LM, Yong VW. Biomarkers of intestinal barrier function in multiple sclerosis are associated with disease activity. Mult. 2019:26(11),p:1340-1350.
42. Tanuma N, Sakuma H, Sasaki A, Matsumoto Y. Chemokine expression by astrocytes plays a role in microglia/macrophage activation and subsequent neurodegeneration in secondary progressive multiple sclerosis. ACTA NEUROPATHOL. 2006;112(2):195-204.
| Files | ||
| Issue | Vol 20 No 2 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v20i2.6052 | |
| Keywords | ||
| Central nervous system Gliadin Immunity Neurological disorder | ||
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How to Cite
1.
Esmaeili P, Rostami E, Akbarijavar A, Akbari Meyestani A, Bashiri H, Rezaee MA, Fakhari S. Effects of Gliadin on Autoimmune Responses of Central Nervous System of C57BL/6 Mice. Iran J Allergy Asthma Immunol. 2021;20(2):188-197.
