Sesamin attenuates mast cell-mediated allergic responses by suppressing the activation of p38 and nuclear factor-κB

Li,Liang  Chang; Piao,Hong  Mei; Zheng,Ming  Yu; Lin,Zhen  Hua; Li,Guangzhao; Yan,Guang  Hai

doi:10.3892/mmr.2015.4546

Sesamin attenuates mast cell-mediated allergic responses by suppressing the activation of p38 and nuclear factor-κB

Authors:
- Liang Chang Li
- Hong Mei Piao
- Ming Yu Zheng
- Zhen Hua Lin
- Guangzhao Li
- Guang Hai Yan
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Affiliations: Department of Anatomy, Histology and Embryology, Yanbian University Medical College, Yanji, Jilin 133002, P.R. China, Department of Respiratory Medicine, Yanbian University, Yanji, Jilin 133002, P.R. China, College of Pharmacy, Yanbian University, Yanji, Jilin 133002, P.R. China, Department of Pathology, Yanbian University School of Basic Medical Sciences, Yanji, Jilin 133000, P.R. China
Published online on: November 11, 2015 https://doi.org/10.3892/mmr.2015.4546
Pages: 536-542

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Abstract

Establishing therapeutic agents for the treatment of allergic diseases is an important focus of human health research. Sesamin, a lignan in sesame oil, exhibits a diverse range of pharmacological properties. However, to the best of our knowledge, the effect of sesamin on mast cell‑mediated allergic responses has not yet been investigated. Thus, the aim of the present study was to investigate the effect of sesamin on mast cell‑mediated allergic responses and the underlying mechanisms by which it produces this effect. In rats, oral administration of sesamin inhibited passive cutaneous anaphylaxis. Sesamin exposure attenuated immunoglobulin E‑induced histamine release from rat peritoneal mast cells, which was indicated to be mediated by the modulation of intracellular calcium. In human mast cells, sesamin reduced the stimulatory effects of phorbol 12‑myristate 13‑acetate and calcium ionophore A23187 on the production and secretion of pro‑inflammatory cytokines, including tumor necrosis factor‑α and interleukin‑6. The inhibitory effect of sesamin on pro‑inflammatory cytokine production was dependent on nuclear factor κ‑light‑chain‑enhancer of activated B cells (NF‑κB) and p38 mitogen‑activated protein kinase (MAPK). The present study demonstrates that sesamin inhibits mast cell‑derived inflammatory allergic reactions by blocking histamine release, and pro‑inflammatory cytokine production and secretion. In addition, the findings indicate that the effect of sesamin is mediated by its effect on p38 MAPK/NF‑κB signaling. Furthermore, the in vivo and in vitro anti‑allergic effects of sesamin reported in the present study suggest that it is a promising therapeutic agent for the treatment of inflammatory allergic diseases.

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1	Galli SJ, Borregaard N and Wynn TA: Phenotypic and functional plasticity of cells of innate immunity: Macrophages, mast cells and neutrophils. Nat Immunol. 12:1035–1044. 2011. View Article : Google Scholar : PubMed/NCBI
2	Kumar V and Sharma A: Mast cells: Emerging sentinel innate immune cells with diverse role in immunity. Mol Immunol. 48:14–25. 2010. View Article : Google Scholar : PubMed/NCBI
3	Kalesnikoff J and Galli SJ: New developments in mast cell biology. Nat Immunol. 9:1215–1223. 2008. View Article : Google Scholar : PubMed/NCBI
4	Beaven MA, Rogers J, Moore JP, Hesketh TR, Smith GA and Metcalfe JC: The mechanism of the calcium signal and correlation with histamine release in 2H3 cells. J Biol Chem. 259:7129–7136. 1984.PubMed/NCBI
5	Beaven MA and Metzger H: Signal transduction by Fc receptors: The Fc epsilon RI case. Immunol Today. 14:222–226. 1993. View Article : Google Scholar : PubMed/NCBI
6	Plaut M, Pierce JH, Watson CJ, Hanley-Hyde J, Nordan RP and Paul WE: Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature. 339:64–67. 1989. View Article : Google Scholar : PubMed/NCBI
7	Nasirullah and Latha RB: Storage stability of sunflower oil with added natural antioxidant concentrate from sesame seed oil. J Oleo Sci. 58:453–459. 2009. View Article : Google Scholar : PubMed/NCBI
8	Jeng KC, Hou RC, Wang JC and Ping LI: Sesamin inhibits lipopolysaccharide-induced cytokine production by suppression of p38 mitogen-activated protein kinase and nuclear factor-kappaB. Immunol Lett. 97:101–106. 2005. View Article : Google Scholar : PubMed/NCBI
9	Periasamy S, Hsu DZ, Chandrasekaran VR and Liu MY: Sesame oil accelerates healing of 2,4,6-trinitrobenzenesulfonic acid-induced acute colitis by attenuating inflammation and fibrosis. J Parenter and Enteral Nutr. 37:674–682. 2013. View Article : Google Scholar
10	Hsieh CC, Kuo CH, Kuo HF, Chen YS, Wang SL, Chao D, Lee MS and Hung CH: Sesamin suppresses macrophage-derived chemokine expression in human monocytes via epigenetic regulation. Food Funct. 5:2494–500. 2014. View Article : Google Scholar : PubMed/NCBI
11	Choi YH and Yan GH: Ellagic Acid attenuates immunoglobulin E-mediated allergic response in mast cells. Biol Pharm Bull. 32:1118–1121. 2009. View Article : Google Scholar : PubMed/NCBI
12	Choi YH and Yan GH: Pycnogenol inhibits immunoglobulin E-mediated allergic response in mast cells. Phytother Res. 23:1691–1695. 2009. View Article : Google Scholar : PubMed/NCBI
13	Hachisuka H, Nomura H, Sakamoto F, Mori O, Okubo K and Sasai Y: Effect of antianaphylactic agents on substance-P induced histamine release from rat peritoneal mast cells. Arch Dermatol Res. 280:158–162. 1988. View Article : Google Scholar : PubMed/NCBI
14	Yoshimura T, Hamaguchi E, Usami E, Nakashima K, Kawaguchi M, Suzuki N, Okamoto Y, Nakao T and Yamazaki F: Increased in vitro release of interferon-gamma from ampicillin-stimulated peripheral blood mononuclear cells in Stevens-Johnson syndrome. Biol Pharm Bull. 27:929–931. 2004. View Article : Google Scholar : PubMed/NCBI
15	Harvima RJ, Harvima IT and Fraki JE: Optimization of histamine radio enzyme assay with purified histamine-N-methyltransferase. Clin Chim Acta. 171:247–256. 1988. View Article : Google Scholar : PubMed/NCBI
16	Choi YH, Yan GH, Chai OH, Lim JM, Sung SY, Zhang X, Kim JH, Choi SH, Lee MS, Han EH, et al: Inhibition of anaphylaxis like reaction and mast cell activation by water extract from the fruiting body of Phellinus linteus. Biol Pharm Bull. 29:1360–1365. 2006. View Article : Google Scholar : PubMed/NCBI
17	Nunomura S, Kitanaka S and Ra C: 3-O-(2,3-dimethylbutanoyl)-13-O-decanoylingenol from Euphorbia kansui suppresses IgE-mediated mast cell activation. Biol Pharm Bull. 29:286–290. 2006. View Article : Google Scholar : PubMed/NCBI
18	Choi YH and Yan GH: Anti-allergic effects of scoparone on mast cell-mediated allergy model. Phytomedicine. 16:1089–1094. 2009. View Article : Google Scholar : PubMed/NCBI
19	McCloskey MA and Zhang L: Potentiation of Fcepsilon receptor I-activated Ca(2⁺) current (I(CRAC)) by cholera toxin: Possible mediation by ADP ribosylation factor. J Cell Biol. 148:137–146. 2000. View Article : Google Scholar : PubMed/NCBI
20	Sillaber C, Bevec D, Butterfield JH, Heppner C, Valenta R, Scheiner O, Kraft D, Lechner K, Bettelheim P and Valent P: Tumor necrosis factor alpha and interleukin-1 beta mRNA expression in HMC-1 cells: Differential regulation of gene product expression by recombinant interleukin-4. Exp Hematol. 21:1271–1275. 1993.PubMed/NCBI
21	Takeishi Y, Huang Q, Abe J, Che W, Lee JD, Kawakatsu H, Hoit BD, Berk BC and Walsh RA: Activation of mitogen-activated protein kinases and p90 ribosomal S6 kinase in failing human hearts with dilated cardiomyopathy. Cardiovasc Res. 53:131–137. 2002. View Article : Google Scholar
22	Siebenlist U, Franzoso G and Brown K: Structure, regulation and function of NF kappa B. Annu Rev Cell Biol. 10:405–455. 1994. View Article : Google Scholar
23	Liu SF and Malik AB: NF-kappa B activation as a pathological mechanism of septic shock and inflammation. Am J Physiol Lung Cell Mol Physiol. 290:L622–L645. 2006. View Article : Google Scholar : PubMed/NCBI
24	Doggrell SA: NF-kappa B–a target in the inflammation of bone destruction. Expert Opin Ther Targets. 9:191–193. 2005. View Article : Google Scholar : PubMed/NCBI
25	Kemp SF and Lockey RF: Anaphylaxis: A review of causes and mechanisms. J Allergy Clin Immunol. 110:341–348. 2002. View Article : Google Scholar : PubMed/NCBI
26	Dvorak AM: Mast cell-derived mediators of enhanced microvascular permeability, vascular permeability factor/vascular endothelial growth factor, histamine, and serotonin, cause leakage of macromolecules through a new endothelial cell permeability organelle, the vesiculo-vacuolar organelle. Chem Immunol Allergy. 85:185–204. 2005. View Article : Google Scholar
27	Rattmann YD, Pereira CR, Cury Y, Gremski W, Marques MC and da Silva-Santos JE: Vascular permeability and vasodilation induced by the Loxosceles intermedia venom in rats: involvement of mast cell degranulation, histamine and 5-HT receptors. Toxicon. 51:363–372. 2008. View Article : Google Scholar
28	Neel NF, Creasy BM, Rankin JN, Pierce EM, McCoy ME, Daner RH, Fowler JA, Daniel JC and Lantz CS: Absence of interleukin-3 does not affect the severity of local and systemic anaphylaxis but does enhance eosinophil infiltration in a mouse model of allergic peritonitis. Immunol Lett. 95:37–44. 2004. View Article : Google Scholar : PubMed/NCBI
29	Kabu K, Yamasaki S, Kamimura D, Ito Y, Hasegawa A, Sato E, Kitamura H, Nishida K and Hirano T: Zinc is required for Fc epsilon RI-mediated mast cell activation. J Immunol. 177:1296–1305. 2006. View Article : Google Scholar : PubMed/NCBI
30	Nishida K, Yamasaki S, Ito Y, Kabu K, Hattori K, Tezuka T, Nishizumi H, Kitamura D, Goitsuka R, Geha RS, et al: Fc{epsilon} RI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J Cell Biol. 170:115–126. 2005. View Article : Google Scholar : PubMed/NCBI
31	Tshori S and Razin E: Editorial: Mast cell degranulation and calcium entry–the Fyn-calcium store connection. J Leukoc Biol. 88:837–838. 2010. View Article : Google Scholar : PubMed/NCBI
32	Chakravarty N and Yu WJ: Role of intracellular calcium in histamine release from rat mast cells. Agents and Actions. 14:386–391. 1984. View Article : Google Scholar : PubMed/NCBI
33	Shumilina E, Lam RS, Wolbing F, Matzner N, Zemtsova IM, Sobiesiak M, Mahmud H, Sausbier U, Biedermann T, Ruth P, et al: Blunted IgE-mediated activation of mast cells in mice lacking the Ca2⁺-activated K⁺ channel KCa3.1. J Immunol. 180:8040–8047. 2008. View Article : Google Scholar : PubMed/NCBI
34	Möller A, Henz BM, Grutzkau A, Lippert U, Aragane Y, Schwarz T and Kruger-Krasagakes S: Comparative cytokine gene expression: Regulation and release by human mast cells. Immunology. 93:289–295. 1998. View Article : Google Scholar : PubMed/NCBI
35	Thomas PS: Tumour necrosis factor-alpha: The role of this multifunctional cytokine in asthma. Immunol Cell Biol. 79:132–140. 2001. View Article : Google Scholar : PubMed/NCBI
36	Hu ZQ, Zhao WH and Shimamura T: Regulation of mast cell development by inflammatory factors. Curr Med Chem. 14:3044–3050. 2007. View Article : Google Scholar
37	Mican JA, Arora N, Burd PR and Metcalfe DD: Passive cutaneous anaphylaxis in mouse skin is associated with local accumulation of interleukin-6 mRNA and immunoreactive interleukin-6 protein. J Allergy Clin Immunol. 90:815–824. 1992. View Article : Google Scholar : PubMed/NCBI
38	Arbabi S and Maier RV: Mitogen-activated protein kinases. Crit Care Med. 30(Suppl): S74–S79. 2002. View Article : Google Scholar : PubMed/NCBI
39	Ashwell JD: The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nat Rev Immunol. 6:532–540. 2006. View Article : Google Scholar : PubMed/NCBI
40	Manthey CL, Wang SW, Kinney SD and Yao Z: SB202190, a selective inhibitor of p38 mitogen-activated protein kinase, is a powerful regulator of LPS-induced mRNAs in monocytes. J Leukoc Biol. 64:409–417. 1998.PubMed/NCBI
41	Jeong HJ, Koo HN, Na HJ, Kim MS, Hong SH, Eom JW, Kim KS, Shin TY and Kim HM: Inhibition of TNF-alpha and IL-6 production by Aucubin through blockade of NF-kappaB activation RBL-2H3 mast cells. Cytokine. 18:252–259. 2002. View Article : Google Scholar : PubMed/NCBI
42	Klemm S and Ruland J: Inflammatory signal transduction from the Fc epsilon RI to NF-kappa B. Immunobiology. 211:815–820. 2006. View Article : Google Scholar : PubMed/NCBI