Development of gastro-food allergy model in shrimp allergen extract-induced sensitized mice promotes mast cell degranulation

Authors

  • Honey Dzikri Marhaeny Department of Pharmacy Practice, Faculty of Pharmacy, University of Airlangga, Surabaya
  • Yusuf Alif Pratama Department of Pharmacy Practice, Faculty of Pharmacy, University of Airlangga, Surabaya
  • Lutfiatur Rohmah Department of Pharmacy Practice, Faculty of Pharmacy, University of Airlangga, Surabaya
  • Salsabilla Madudari Kasatu Department of Pharmacy Practice, Faculty of Pharmacy, University of Airlangga, Surabaya
  • Andang Miatmoko Department of Pharmaceutical Science, Faculty of Pharmacy, Universitas Airlangga, Surabaya
  • Junaidi Khotib Department of Pharmacy Practice, Faculty of Pharmacy, University of Airlangga, Surabaya

DOI:

https://doi.org/10.4081/jphia.2023.2512

Keywords:

Mast cell degranulation, immune response, gastro-food allergy, shrimp allergen extract

Abstract

Background: Food allergies have become more common in the last decade. Shrimp is one of the most dominant food allergy triggers in Asian countries, including Indonesia. After ingesting allergens, B cells will produce allergen-specific Immunoglobin E (IgE). In the sensitization period, repeated allergen exposure promotes Mast Cell (MC) degranulation in intestinal tissue and releases several inflammatory mediators, thereby causing hypersensitivity reactions. Shrimp Allergen Extract (SAE) is an immunotherapy and diagnostic agent currently being developed in Indonesia. In this study, we investigated the effect of SAE administration on eliciting an MC immunological response.

Methods: Mice were divided into a non-sensitized and sensitized group. The non-sensitized group only received 1 mg of alum (i.p), whereas the sensitized group received 1 mg of alum and 100 μg of SAE on days 0, 7, and 14. Then, both groups were challenged with 400 μg SAE (p.o) on days 21, 22, and 23 following systemic allergic symptom observation.

Results: We showed that SAE was able to increase systemic allergic symptoms significantly in the sensitized mice through repeated challenge (1.33±0.21; 1.83±0.17; and 2.00±0.00), compared to non-sensitized mice (0.17±0.17). Moreover, histopathological analysis showed that the SAE administration causes an increase of MC degranulation in the ileum tissue of the sensitized mice (44.43%±0.01), compared to non-sensitized mice (35.45%±0.01)

Conclusions: This study found that SAE could induce allergic reactions in mice by influencing critical effector cells, MCs.

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References

Nowak-Wegrzyn A, Burks AW, Sampson HA. Chapter 12 – Food allergy and gastrointestinal syndromes, in: Middleton’s Allergy Essentials. Elsevier Ltd., Amsterdam, the Netherlands; 2017. 408 pp. DOI: https://doi.org/10.1016/B978-0-323-37579-5.00012-X

Abrams EM, Sicherer SH. Diagnosis and management of food allergy. Can Med Assoc J 2016;188:1087–93. DOI: https://doi.org/10.1503/cmaj.160124

Wai CY, Leung NY, Leung AS, et al. Seafood Allergy in Asia: Geographical Specificity and Beyond. Front All 2021;2:676903. DOI: https://doi.org/10.3389/falgy.2021.676903

Wang HT, Warren CM, Gupta RS, Davis CM. Prevalence and characteristics of shellfish allergy in the pediatric population of the United States. J All Clin Immunol 2020;8:1359–70.e2. DOI: https://doi.org/10.1016/j.jaip.2019.12.027

Nguyen DI, Sindher SB, Chinthrajah RS, et al. Shrimp-allergic patients in a multi-food oral immunotherapy trial. Pediatr Allergy Immunol 2022;33:e13679. DOI: https://doi.org/10.1111/pai.13679

Burks AW, Holgate ST, O’Hehir RE, et al. Middleton’s Allergy Principles and Practice, Ninth Ed. Elsevier Ltd., Amsterdam, the Netherlands; 2020. 1840 pp.

Gani MA, Nurhan AD, Maulana S, et al. Structure-based virtual screening of bioactive compounds from Indonesian medical plants against severe acute respiratory syndrome coronavirus-2. J Adv Pharmaceut Technol Res 2021;12:120-6.

Lopata AL. Food Allergy: Molecular and Clinical Practice. CRC Press: Boca Raton, USA; 2017. 392 pp. DOI: https://doi.org/10.1201/9781315120126

Lee JB. Regulation of IgE-mediated food allergy by IL-9 producing mucosal mast cells and type 2 innate lymphoid cells. Immune Network 2016;16:211–8. DOI: https://doi.org/10.4110/in.2016.16.4.211

Yu W, Freeland DMH, Nadeau KC. Food allergy: Immune mechanisms, diagnosis and immunotherapy. Nat Rev Immunol 2016;16:751–65. DOI: https://doi.org/10.1038/nri.2016.111

Satitsuksanoa P, Jansen K, Głobińska A, et al. Regulatory Immune Mechanisms in Tolerance to Food Allergy. Front Immunol 2018;9:2939. DOI: https://doi.org/10.3389/fimmu.2018.02939

Kanagaratham C, El Ansari YS, Lewis OL, et al. IgE and IgG Antibodies as Regulators of Mast Cell and Basophil Functions in Food Allergy. Front Immunol 2020;11:603050. DOI: https://doi.org/10.3389/fimmu.2020.603050

Burton OT, Darling AR, Zhou JS, et al. Direct effects of IL-4 on mast cells drive their intestinal expansion and increase susceptibility to anaphylaxis in a murine model of food allergy. Mucosal Immunol 2013;6:740-50. DOI: https://doi.org/10.1038/mi.2012.112

Reyes-Pavón D, Cervantes-García D, Bermúdez-Humarán LG, et al. Protective Effect of Glycomacropeptide on Food Allergy with Gastrointestinal Manifestations in a Rat Model through Down-Regulation of Type 2 Immune Response. Nutrients 2020;12:2942. DOI: https://doi.org/10.3390/nu12102942

Stone KD, Prussin C, Metcalfe DD. IgE, mast cells, basophils, and eosinophils. J All Clin Immunol 2010;125:S73-80. DOI: https://doi.org/10.1016/j.jaci.2009.11.017

Hogan SP, Wang YH, Strait R, et al. Food-induced anaphylaxis: Mast cells as modulators of anaphylactic severity. Sem Immunopathol 2012;34:643–53. DOI: https://doi.org/10.1007/s00281-012-0320-1

Pedrosa M, Boyano-Martínez T, García-Ara C, et al. Shellfish Allergy: A Comprehensive Review. Clin Rev All Immunol 2015;49:203–16. DOI: https://doi.org/10.1007/s12016-014-8429-8

Margaret M, Jinap S, Faizal A, et al. Allergens derived from shrimp. Immunosensor Int Food Res J 2015;22:1751–4.

Sagitaras IB. Thesis: Efektivitas Ekstrak Alergen Udang sebagai Alat Diagnostik dan Imunoterapi pada Model Mencit Alergi Gastrointestinal. Universitas Airlangga: Surabaya; 2021.

Leung A., Wong G, Tang M. Food allergy in the developing world. J All Clin Immunol 2018;14176–78.

Wai C, Leung N, Leung P, et al. Modulating Shrimp Tropomyosin-Mediated Allergy: Hypoallergen DNA Vaccines Induce Regulatory T Cells to Reduce Hypersensitivity in Mouse Model. Int J Mol Sci 2019;20:4656. DOI: https://doi.org/10.3390/ijms20184656

Fang L, Zhou F, Wu F, et al. A mouse allergic asthma model induced by shrimp tropomyosin. Int Immunopharmacol 2021;91:107289. DOI: https://doi.org/10.1016/j.intimp.2020.107289

Fu L, Peng J, Zhao S, et al. Lactic acid bacteria-specific induction of CD4+Foxp3+T cells ameliorates shrimp tropomyosin-induced allergic response in mice via suppression of mTOR signaling. Sci Rep 2017;7:1987. DOI: https://doi.org/10.1038/s41598-017-02260-8

Leung PSC, Lee YS, Tang CY, et al. Induction of shrimp tropomyosin-specific hypersensitivity in mice. Int Arch All Immunol 2008;147:305–14. DOI: https://doi.org/10.1159/000144038

Lee D, Kim H, Shin E, et al. Polysaccharide isolated from Aloe vera gel suppresses ovalbumin-induced food allergy through inhibition of Th2 immunity in mice. Biomed Pharmacother 2018;101:201–10. DOI: https://doi.org/10.1016/j.biopha.2018.02.061

Ahrens R, Osterfeld H, Wu D, et al. Intestinal mast cell levels control severity of oral antigen-induced anaphylaxis in mice. Am J Pathol 2012;180:1535–46. DOI: https://doi.org/10.1016/j.ajpath.2011.12.036

Klein O, Sagi-Eisenberg R. Anaphylactic Degranulation of Mast Cells: Focus on Compound Exocytosis. J Immunol Res 2019;2019:9542656. DOI: https://doi.org/10.1155/2019/9542656

Yang B, Li JJ, Cao JJ, et al. Polydatin attenuated food allergy via store-operated calcium channels in mast cell. World J Gastroenterol 2013;19:3980–9. DOI: https://doi.org/10.3748/wjg.v19.i25.3980

Huang M, Wang X, Xing B, et al. Critical roles of TRPV2 channels, histamine H1 and adenosine A1 receptors in the initiation of acupoint signals for acupuncture analgesia. Sci Rep 2018;8:6523. DOI: https://doi.org/10.1038/s41598-018-24654-y

Lam YF, Tong KK, Kwan KM, et al. Gastrointestinal Immune Response to the Shrimp Allergen Tropomyosin: Histological and Immunological Analysis in an Animal Model of Shrimp Tropomyosin Hypersensitivity. Int Arch Allergy Immunol 2015;167:29–40. DOI: https://doi.org/10.1159/000431228

Wai CYY, Leung NYH, Leung PSC, et al. T cell epitope immunotherapy ameliorates allergic responses in a murine model of shrimp allergy. Clin Exp All 2016;46:491–503. DOI: https://doi.org/10.1111/cea.12684

Galli SJ, Tsai M. IgE and mast cells in allergic disease. Nat Med 2012;18:693–704. DOI: https://doi.org/10.1038/nm.2755

Khotib J, Utami NW, Gani MA, et al. The change of proinflammatory cytokine tumor necrosis factor α level in the use of meloxicam in rat model of osteoarthritis. J Basic Clin Physiol Pharmacol 2019;14;30. DOI: https://doi.org/10.1515/jbcpp-2019-0331

Walker MT, Green JE, Ferrie RP, et al. Mechanism for initiation of food allergy: Dependence on skin barrier mutations and environmental allergen costimulation. J All Clin Immunol 2018;141:1711-25. DOI: https://doi.org/10.1016/j.jaci.2018.02.003

Nakamura T, Maeda S, Horiguchi K, et al. PGD2 deficiency exacerbates food antigen-induced mast cell hyperplasia. Nat Communicat 2015;10:7514. DOI: https://doi.org/10.1038/ncomms8514

Aguilera-Lizarraga J, Florens MV, Viola MF, et al. Local immune response to food antigens drives meal-induced abdominal pain. Nature 2021;590:151–6. DOI: https://doi.org/10.1038/s41586-020-03118-2

Bublin M, Breiteneder H. Developing therapies for peanut allergy. Int Arch All Immunol 2014;165:179–94. DOI: https://doi.org/10.1159/000369340

Burbank AJ, Burks W. Food specific oral immunotherapy: A potential treatment for food allergy. Exp Rev Gastroenterol Hepatol 2015;9:1147–59. DOI: https://doi.org/10.1586/17474124.2015.1065177

Schoos AMM, Bullens D, Chawes BL, et al. Immunological Outcomes of Allergen-Specific Immunotherapy in Food Allergy. Front Immunol 2020;11:1-20. DOI: https://doi.org/10.3389/fimmu.2020.568598

Pratama YA, Dinina F, Nurhan AD, et al. Effectiveness of Indonesian house dust mite allergenic extract in triggering allergic rhinitis sensitivity in a mouse model: A preliminary study. Vet World 2022;15:2333–41. DOI: https://doi.org/10.14202/vetworld.2022.2333-2341

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Published

16-03-2023

How to Cite

Marhaeny, H. D., Pratama, Y. A., Rohmah, L., Kasatu, S. M., Miatmoko, A., & Khotib, J. (2023). Development of gastro-food allergy model in shrimp allergen extract-induced sensitized mice promotes mast cell degranulation. Journal of Public Health in Africa, 14(s1). https://doi.org/10.4081/jphia.2023.2512