Boeravinone B ameliorates allergic nasal inflammation by modulating the GATA-3/T-bet signaling pathway in a mouse model of allergic rhinitis

Abstract

Objective: To evaluate the anti-allergic effect of boeravinone B against ovalbumin-induced allergic rhinitis in mice and explore its possible mechanism. Methods: For the induction of allergic rhinitis, mice were intraperitoneally sensitized and intranasally challenged with ovalbumin, as well as orally received various concentrations of boeravinone B. Nasal mucosal inflammation, and the levels of nitric oxide, β-hexosaminidase, IFN-γ, LTC-4, myeloperoxidase, Nrf2, HO-1, GATA-3, ROR-γ, T-bet, antioxidant parameters, and allergen-specific cytokines were assessed. Results: Boeravinone B markedly reduced ovalbumin-induced increase in the number of episodes of nasal sneezing, rubbing, and discharge, as well as the levels of IgE, IgG1, and β-hexosaminidase (P<0.05). It also significantly reduced differential cell count, myeloperoxidase, oxide-nitrosative stress, and the levels of IL-1β, IL-4, IL-5, IL-6, IL-13, IL-17, tumor necrosis factor-α, GATA-3, and ROR-γ while enhancing the level of T-bet. Conclusions: Boeravinone B is a potential therapeutic agent for allergic rhinitis by modulating various inflammatory mediators and immune responses.

Keywords

Allergic reaction / Boeravinone B / Oxidative stress / Inflammation / Ovalbumin

Conflict of interest statement

The authors declare that there is no conflict of interest.

Funding

The study received no extramural funding.

Data availability statement

The data supporting the findings of this study are available from the corresponding authors upon request.

Authors’ contributions

BY performed the experimental study. JZW designed the work, drafted the article, and reviewed the article. Both authors approved the final version of the published paper.

References

[1] Wang J, Liu X, Liu Z, Ge Y, He S. Protective effect of Ellipticine in ovalbumin (OVA)-induced murine model of allergic rhinitis via dual inhibition of COX-2 and NF-κB. Isr J Plant Sci 2021; 53(9): 79-89.

[2] Kamm GL, Hagmeyer KO. Allergic-type reactions to corticosteroids. Ann Pharmacother 1999; 33(4): 451-460.

[3] Polito V, Barbacki A, Isabwe G. Type I allergic reaction to rituximab upon first lifetime exposure: A case report. Allergy Asthma Clin Immunol 2020; 16(1): 56.

[4] Wei L, Ren D, Zhao G, Zhao L. Protective effect of corynoline in a murine allergic rhinitis model via inhibition of caspase-1/NF-κB. Arch Pharm (Weinheim) 2021; 354(2). doi: 10.1002/ardp.202000231.

[5] Bae CH, Kim J, Nam W, Kim H, Kim J, Nam B, et al. Fermented red ginseng alleviates ovalbumin-induced inflammation in mice by suppressing interleukin-4 and immunoglobulin E expression. J Med Food 2021; 24(6): 569-576.

[6] Van Nguyen T, Piao CH, Fan YJ, Shin DU, Kim SY, Song HJ. Anti-allergic rhinitis activity of α-lipoic acid via balancing Th17/Treg expression and enhancing Nrf2/HO-1 pathway signaling. Sci Rep 2020; 10(1): 12528. doi: 10.1038/s41598-020-69234-1.

[7] Li K, Chen Y, Jiang R, Chen D, Wang H, Xiong W, et al. Protective effects of astragaloside IV against ovalbumin-induced allergic rhinitis are mediated by T-box protein expressed in T cells/GATA-3 and forkhead box protein 3/retinoic acid-related orphan nuclear receptor γt. Mol Med Rep 2017; 16(2): 1207-1215.

[8] Chen S, Chen G, Shu S, Xu Y, Ma X. Metabolomics analysis of baicalin on ovalbumin-sensitized allergic rhinitis rats. R Soc Open Sci 2019; 6(2). doi: 10.1098/rsos.181081.

[9] Ohno T, Morita H, Arae K, Matsumoto K, Nakae S. Interleukin-33 in allergy. Allergy Eur J Allergy Clin Immunol 2012; 67(10): 1203-1214.

[10] Makrinioti H, Toussaint M, Jackson DJ, Walton RP, Johnston SL. Role of interleukin 33 in respiratory allergy and asthma. Lancet Respir Med 2014; 2(3): 226-237.

[11] Nakae S, Morita H, Ohno T, Arae K, Matsumoto K, Saito H. Role of interleukin-33 in innate-type immune cells in allergy. Allergol Int 2013; 62(1): 13-20.

[12] Shi YN, Su JZ, Wang J, Geng JQ. Myricetin alleviates ovalbumin-induced allergic rhinitis in mice by regulating Th1/Th2 balance. Asian Pac J Trop Biomed 2023; 13(7): 306-314.

[13] Bui TT, Fan Y, Piao CH, Nguyen TV, Shin D, Jung SY, et al. Piper nigrum extract improves OVA-induced nasal epithelial barrier dysfunction via activating Nrf2/HO-1 signaling. Cell Immunol 2020; 351. doi: 10.1016/j.cellimm.2019.104035.

[14] Jung HW, Jung JK, Park YK. Antiallergic effect of Ostericum koreanum root extract on ovalbumin-induced allergic rhinitis mouse model and mast cells. Asian Pac J Allergy Immunol 2011; 29(4): 338-348.

[15] Lee JE. Hizikia fusiformis ameliorates allergic inflammation in an OVA-induced allergic rhinitis mouse model. J Allergy Clin Immunol 2019; 143(2). doi: 10.1016/j.jaci.2018.12.900.

[16] Şahin A, Sakat MS, Kılıç K, Aktan B, Yildirim S, Kandemir FM, et al. The protective effect of naringenin against ovalbumin-induced allergic rhinitis in rats. Eur Arch Otorhinolaryngol 2021; 278(12): 4839-4846.

[17] Jena S, Kumar G, Singh D, Sethi A. Herbs used in dentistry: Need of the new era. J Prim Care Dent Oral Heal 2021; 2(1): 11.

[18] Kozlov V, Lavrenova G, Savlevich E, Bazarkina K. Evidence-based phytotherapy in allergic rhinitis. Clin Phytosci 2018; 4(1): 12-23.

[19] Piao CH, Fan YJ, Van Nguyen T, Song CH, Chai OH. Mangiferin alleviates ovalbumin-induced allergic rhinitis via Nrf2/HO-1/NF-κB signaling pathways. Int J Mol Sci 2020; 21(10). doi: 10.3390/ijms21103415.

[20] Liu T, Xu J, Wu Y, Li X, Ding D, Ma D, et al. Beneficial effects of baicalein on a model of allergic rhinitis. Acta Pharm 2020; 70(1): 35-47.

[21] Wang Z, Xiao S, Huang J, Liu S, Xue M, Lu F. Chemoprotective effect of boeravinone B against dmba/croton oil induced skin cancer via reduction of inflammation. J Oleo Sci 2021; 70(7): 955-964.

[22] Zhou C, Ou W, Xu Q, Lin L, Xu F, Chen R, et al. Chemoprotective effect of boeravinone B against 1,2-dimethyl hydrazine induced colorectal cancer in rats via suppression of oxidative stress and inflammatory reaction. J Gastrointest Oncol 2022; 13(4): 1832-1841.

[23] Liu Y, Wang F, Zhang D, Li Z. Anti-Inflammatory and immunomodulatory effects of hesperidin against the ovalbumin-induced allergic rhinitis in mice. Int J Pharmacol 2022; 18(5): 1026-1037.

[24] Wang J, Kandhare A, Mukherjee-Kandhare A, Bodhankar S. Chrysin ameliorates ovalbumin-induced allergic response in allergic rhinitis: Potential role of GATA-3, T-box protein expressed in T cells, nuclear factor-kappa B, and nuclear factor erythroid 2-related factor 2. Pharmacogn Mag 2020; 16(70): 335-344.

[25] Nishikimi M, Appaji Rao N, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 1972; 46(2): 849-854.

[26] Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med 1963; 61: 882-888.

[27] Romagnani S. Cytokines and chemoattractants in allergic inflammation. Mol Immunol 2002; 38(12-13): 881-885.

[28] Possa SS, Leick EA, Prado CM, Martins MA, Tibério IFLC. Eosinophilic inflammation in allergic asthma. Front Pharmacol 2013; 4. doi: 10.3389/fphar.2013.00046.

[29] Sim CS, Lee JH, Kim SH, Han MW, Kim Y, Oh I, et al. Oxidative stress in schoolchildren with allergic rhinitis: Propensity score matching case-control study. Ann Allergy Asthma Immunol 2015; 115(5): 391-395.

[30] Fang S, Li X, Wei X, Zhang YU, Ma Z, Wei Y, et al. Beneficial effects of hydrogen gas inhalation a murine model of allergic rhinitis. Exp Ther Med 2018; 16(6): 5178-5184.

[31] Pandhare RB, Sangameswaran B, Mohite PB, Khanage SG. Anti-hyperglycaemic and lipid lowering potential of Adenanthera pavonina Linn. in streptozotocin induced diabetic rats. Orient Pharm Exp Med 2012; 12(3): 197-203.

[32] Chen F, He D, Yan B. Apigenin attenuates allergic responses of ovalbumin-induced allergic rhinitis through modulation of Th1/Th2 responses in experimental mice. Dose Response 2020; 18(1). doi: 10.1177/1559325820904799.

[33] Walanj S, Walanj A, Mohan V, Thakurdesai PA. Efficacy and safety of the topical use of intranasal cinnamon bark extract in seasonal allergic rhinitis patients: A double-blind placebo-controlled pilot study. J Herb Med 2014; 4(1): 37-47.

[34] Zhang YL, Shin HJ, Lee JH, Lee J. Antiallergic effect of Hizikia fusiformis in an ovalbumin-induced allergic rhinitis mouse model. Clin Exp Otorhinolaryngol 2019; 12(2): 196-205.

[35] Carr VMM, Robinson AM, Kern RC. Tissue-specific effects of allergic rhinitis in mouse nasal epithelia. Chem Senses 2012; 37(7): 655-668.

[36] Bui TT, Piao CH, Hyeon E, Fan Y, Choi DW, Jung SY, et al. Preventive effect of Bupleurum chinense on nasal inflammation via suppressing T helper type 2, eosinophil and mast cell activation. Am J Chin Med 2019; 47(2): 405-421.

[37] Li J, Wang B, Luo Y, Zhang Q, Bian Y, Wang R. Resveratrol-mediated SIRT1 activation attenuates ovalbumin-induced allergic rhinitis in mice. Mol Immunol 2020; 122: 156-162.

[38] Nam SY, Kim HM, Jeong HJ. The potential protective role of taurine against experimental allergic inflammation. Life Sci 2017; 184: 18-24.