Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2018

Open Access 01-12-2018 | Research article

Shuang-Huang-Lian prevents basophilic granulocyte activation to suppress Th2 immunity

Authors: Qiaoling Fei, Yixin Han, Ruijuan Qi, Yuan Gao, Lei Fang, Rui Hou, Runlan Cai, Yun Qi

Published in: BMC Complementary Medicine and Therapies | Issue 1/2018

Login to get access

Abstract

Background

Basophilic granulocytes (BGs) not only initiate the induction of Th2 cell differentiation, but also amplify the ongoing Th2 response. Shuang-Huang-Lian (SHL) is clinically used for relieving type I hypersensitivity by continuous treatment for several weeks.

Methods

ELISA, flow cytometry, magnetic activated cell sorting, isoelectric precipitation, hybridoma technique, transfection and luciferase reporter assay were used in this study. The statistical analysis was performed using a one-way ANOVA.

Results

Our recently published study demonstrated that SHL exerted a remarkable effect on mast cell stabilization. Herein, we sought to elucidate the effect of SHL on shrimp tropomyosin (ST)-induced Th2 immunity and its underlying mechanisms. The obtained data showed that continuous treatment with SHL significantly suppressed ST-stimulated Th2-cytokines release and IgE synthesis. A mechanistic study indicated that SHL not only reduced BG early IL-4 release before ST-specific IgE (sIgE) production, but also inhibited BG activation in the presence of sIgE, including suppressing CD200R surface expression and decreasing IL-4 production. Moreover, SHL markedly decreased the cytosolic Ca2+ (Ca2+[c]) level and inhibited the nuclear factor of activated T cells (NFAT) activation in RBL-2H3 cells.

Conclusions

Collectively, SHL potently reduces ST-induced Th2 immunity by inhibiting the BG Ca2+-NFAT pathway and, thus, suppressing the early IL-4 release before sIgE synthesis and inhibiting BG activation in the presence of sIgE. This study provides the pharmacological basis for the clinical use of SHL to relieve type I hypersensitivity by a successive dose regimen.
Appendix
Available only for authorised users
Literature
2.
go back to reference HÄGGQVIST B, HULTMAN P. Effects of deviating the Th2-response in murine mercury-induced autoimmunity towards a Th1-response. Clin Exp Immunol. 2003;134:202–9.CrossRefPubMedPubMedCentral HÄGGQVIST B, HULTMAN P. Effects of deviating the Th2-response in murine mercury-induced autoimmunity towards a Th1-response. Clin Exp Immunol. 2003;134:202–9.CrossRefPubMedPubMedCentral
3.
go back to reference Maggi E, Parronchi P, Manetti R, Simonelli C, Piccinni MP, Rugiu FS, De Carli M, Ricci M, Romagnani S. Reciprocal regulatory effects of IFN-gamma and IL-4 on the in vitro development of human Th1 and Th2 clones. J Immunol. 1992;148:2142–7.PubMed Maggi E, Parronchi P, Manetti R, Simonelli C, Piccinni MP, Rugiu FS, De Carli M, Ricci M, Romagnani S. Reciprocal regulatory effects of IFN-gamma and IL-4 on the in vitro development of human Th1 and Th2 clones. J Immunol. 1992;148:2142–7.PubMed
5.
go back to reference Rogge L, Barberis-Maino L, Biffi M, Passini N, Presky DH, Gubler U, Sinigaglia F. Selective expression of an interleukin-12 receptor component by human T helper 1 cells. J Exp Med. 1997;185:825–31.CrossRefPubMedPubMedCentral Rogge L, Barberis-Maino L, Biffi M, Passini N, Presky DH, Gubler U, Sinigaglia F. Selective expression of an interleukin-12 receptor component by human T helper 1 cells. J Exp Med. 1997;185:825–31.CrossRefPubMedPubMedCentral
6.
go back to reference Nakanishi K. Basophils are potent antigen-presenting cells that selectively induce Th2 cells. Eur J Immunol. 2010;40:1836–42.CrossRefPubMed Nakanishi K. Basophils are potent antigen-presenting cells that selectively induce Th2 cells. Eur J Immunol. 2010;40:1836–42.CrossRefPubMed
7.
go back to reference Otsuka A, Nakajima S, Kubo M, Egawa G, Honda T, Kitoh A, Nomura T, Hanakawa S, Sagita-Moniaga C, Kim B, Matsuoka S, Watanabe T, Miyachi Y, Kabashima K. Basophils are required for the induction of Th2 immunity to haptens and peptide antigens. Nat Commun. 2013;4:1739.CrossRefPubMed Otsuka A, Nakajima S, Kubo M, Egawa G, Honda T, Kitoh A, Nomura T, Hanakawa S, Sagita-Moniaga C, Kim B, Matsuoka S, Watanabe T, Miyachi Y, Kabashima K. Basophils are required for the induction of Th2 immunity to haptens and peptide antigens. Nat Commun. 2013;4:1739.CrossRefPubMed
8.
go back to reference Perrigoue JG, Saenz SA, Siracusa MC, Allenspach EJ, Taylor BC, Giacomin PR, Nair MG, Du Y, Zaph C, van Rooijen N, Comeau MR, Pearce EJ, Laufer TM, Artis D. MHC class II-dependent basophil-CD4+ T cell interactions promote T (H) 2 cytokine-dependent immunity. Nat Immunol. 2009;10:697–705.CrossRefPubMedPubMedCentral Perrigoue JG, Saenz SA, Siracusa MC, Allenspach EJ, Taylor BC, Giacomin PR, Nair MG, Du Y, Zaph C, van Rooijen N, Comeau MR, Pearce EJ, Laufer TM, Artis D. MHC class II-dependent basophil-CD4+ T cell interactions promote T (H) 2 cytokine-dependent immunity. Nat Immunol. 2009;10:697–705.CrossRefPubMedPubMedCentral
9.
go back to reference Sokol CL, Chu NQ, Yu S, Nish SA, Laufer TM, Medzhitov R. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat Immunol. 2009;10:713–20.CrossRefPubMedPubMedCentral Sokol CL, Chu NQ, Yu S, Nish SA, Laufer TM, Medzhitov R. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat Immunol. 2009;10:713–20.CrossRefPubMedPubMedCentral
10.
go back to reference Yoshimoto T, Yasuda K, Tanaka H, Nakahira M, Imai Y, Fujimori Y, Nakanishi K. Basophils contribute to T (H) 2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat Immunol. 2009;10:706–12.CrossRefPubMed Yoshimoto T, Yasuda K, Tanaka H, Nakahira M, Imai Y, Fujimori Y, Nakanishi K. Basophils contribute to T (H) 2-IgE responses in vivo via IL-4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat Immunol. 2009;10:706–12.CrossRefPubMed
11.
13.
go back to reference State Pharmacopoeia Committee. Chinese pharmacopoeia (Vol. 1). Beijing: Chemical Industry Press; 2010. p. 846–8. State Pharmacopoeia Committee. Chinese pharmacopoeia (Vol. 1). Beijing: Chemical Industry Press; 2010. p. 846–8.
14.
go back to reference Fang L, Gao Y, Liu F, Hou R, Cai RL, Qi Y. Shuang-huang-lian attenuates lipopolysaccharide-induced acute lung injury in mice involving anti-inflammatory and antioxidative activities. Evid Based Complement Alternat Med. 2015;2015:283939.PubMedPubMedCentral Fang L, Gao Y, Liu F, Hou R, Cai RL, Qi Y. Shuang-huang-lian attenuates lipopolysaccharide-induced acute lung injury in mice involving anti-inflammatory and antioxidative activities. Evid Based Complement Alternat Med. 2015;2015:283939.PubMedPubMedCentral
15.
go back to reference Gao Y, Fang L, Cai R, Zong C, Chen X, Lu J, Qi Y. Shuang-Huang-Lian exerts anti-inflammatory and anti-oxidative activities in lipopolysaccharide-stimulated murine alveolar macrophages. Phytomedicine. 2014;21:461–9.CrossRefPubMed Gao Y, Fang L, Cai R, Zong C, Chen X, Lu J, Qi Y. Shuang-Huang-Lian exerts anti-inflammatory and anti-oxidative activities in lipopolysaccharide-stimulated murine alveolar macrophages. Phytomedicine. 2014;21:461–9.CrossRefPubMed
16.
go back to reference Gao Y, Hou R, Fei Q, Fang L, Han Y, Cai R, Peng C, Qi Y. The three-herb formula Shuang-Huang-Lian stabilizes mast cells through activation of mitochondrial calcium uniporter. Sci Rep. 2017;7:38736.CrossRefPubMedPubMedCentral Gao Y, Hou R, Fei Q, Fang L, Han Y, Cai R, Peng C, Qi Y. The three-herb formula Shuang-Huang-Lian stabilizes mast cells through activation of mitochondrial calcium uniporter. Sci Rep. 2017;7:38736.CrossRefPubMedPubMedCentral
17.
go back to reference Chen HS, Huang QM. Shuang-Huang-Lian powder-injection for the treatment of bronchial asthma (30 cases). Guangxi J Tradit Chin Med. 1998;21:16. Chen HS, Huang QM. Shuang-Huang-Lian powder-injection for the treatment of bronchial asthma (30 cases). Guangxi J Tradit Chin Med. 1998;21:16.
18.
go back to reference Dong YH, Sun ZY, Chu AH. Clinical analysis of the adjuvant therapy of Shuang Huang Lian on infantile asthma through aerosol inhalation (54 cases). J Conval Rehab. 1997;12:1997. Dong YH, Sun ZY, Chu AH. Clinical analysis of the adjuvant therapy of Shuang Huang Lian on infantile asthma through aerosol inhalation (54 cases). J Conval Rehab. 1997;12:1997.
19.
go back to reference Li XM, Schofield BH, Huang CK, Kleiner GI, Sampson HA. A murine model of IgE-mediated cow's milk hypersensitivity. J Allergy Clin Immunol. 1999;103:206–14.CrossRefPubMed Li XM, Schofield BH, Huang CK, Kleiner GI, Sampson HA. A murine model of IgE-mediated cow's milk hypersensitivity. J Allergy Clin Immunol. 1999;103:206–14.CrossRefPubMed
20.
go back to reference Abril-Gil M, Massot-Cladera M, Pérez-Cano FJ, Castellote C, Franch A, Castell M. A diet enriched with cocoa prevents IgE synthesis in a rat allergy model. Pharmacol Res. 2012;65:603–8.CrossRefPubMed Abril-Gil M, Massot-Cladera M, Pérez-Cano FJ, Castellote C, Franch A, Castell M. A diet enriched with cocoa prevents IgE synthesis in a rat allergy model. Pharmacol Res. 2012;65:603–8.CrossRefPubMed
21.
go back to reference Banerjee S, Medina-Fatimi A, Nichols R, Tendler D, Michetti M, Simon J, Kelly CP, Monath TP, Michetti P. Safety and efficacy of low dose Escherichia Coli enterotoxin adjuvant for urease based oral immunisation against helicobacter pylori in healthy volunteers. Gut. 2002;51:634–40.CrossRefPubMedPubMedCentral Banerjee S, Medina-Fatimi A, Nichols R, Tendler D, Michetti M, Simon J, Kelly CP, Monath TP, Michetti P. Safety and efficacy of low dose Escherichia Coli enterotoxin adjuvant for urease based oral immunisation against helicobacter pylori in healthy volunteers. Gut. 2002;51:634–40.CrossRefPubMedPubMedCentral
22.
go back to reference Torrero MN, Larson D, Hübner MP, Mitre E. CD200R surface expression as a marker of murine basophil activation. Clin Exp Allergy. 2009;39:361–9.CrossRefPubMed Torrero MN, Larson D, Hübner MP, Mitre E. CD200R surface expression as a marker of murine basophil activation. Clin Exp Allergy. 2009;39:361–9.CrossRefPubMed
23.
24.
go back to reference Li F, Li HQ. The study of Lonicera extract from water solution on ovalbumin -induced allergic mice model. J Chongqing Med Univ. 2004;29:288–91. Li F, Li HQ. The study of Lonicera extract from water solution on ovalbumin -induced allergic mice model. J Chongqing Med Univ. 2004;29:288–91.
25.
go back to reference Shin HS, Bae MJ, Jung SY, Shon DH. Preventive effects of skullcap (Scutellaria Baicalensis) extract in a mouse model of food allergy. J Ethnopharmacol. 2014;153:667–73.CrossRefPubMed Shin HS, Bae MJ, Jung SY, Shon DH. Preventive effects of skullcap (Scutellaria Baicalensis) extract in a mouse model of food allergy. J Ethnopharmacol. 2014;153:667–73.CrossRefPubMed
26.
go back to reference Sung YY, Lee AY, Kim HK. Forsythia Suspensa fruit extracts and the constituent matairesinol confer anti-allergic effects in an allergic dermatitis mouse model. J Ethnopharmacol. 2016;187:49–56.CrossRefPubMed Sung YY, Lee AY, Kim HK. Forsythia Suspensa fruit extracts and the constituent matairesinol confer anti-allergic effects in an allergic dermatitis mouse model. J Ethnopharmacol. 2016;187:49–56.CrossRefPubMed
27.
go back to reference Shin HS, Bae MJ, Choi DW, Shon DH. Skullcap (Scutellaria Baicalensis) extract and its active compound, wogonin, inhibit ovalbumin-induced Th2-mediated response. Molecules. 2014;19:2536–45.CrossRefPubMed Shin HS, Bae MJ, Choi DW, Shon DH. Skullcap (Scutellaria Baicalensis) extract and its active compound, wogonin, inhibit ovalbumin-induced Th2-mediated response. Molecules. 2014;19:2536–45.CrossRefPubMed
28.
30.
go back to reference Tsujimura Y, Obata K, Mukai K, Shindou H, Yoshida M, Nishikado H, Kawano Y, Minegishi Y, Shimizu T, Karasuyama H. Basophils play a pivotal role in immunoglobulin-G-mediated but not immunoglobulin-E-mediated systemic anaphylaxis. Immunity. 2008;28:581–9.CrossRefPubMed Tsujimura Y, Obata K, Mukai K, Shindou H, Yoshida M, Nishikado H, Kawano Y, Minegishi Y, Shimizu T, Karasuyama H. Basophils play a pivotal role in immunoglobulin-G-mediated but not immunoglobulin-E-mediated systemic anaphylaxis. Immunity. 2008;28:581–9.CrossRefPubMed
Metadata
Title
Shuang-Huang-Lian prevents basophilic granulocyte activation to suppress Th2 immunity
Authors
Qiaoling Fei
Yixin Han
Ruijuan Qi
Yuan Gao
Lei Fang
Rui Hou
Runlan Cai
Yun Qi
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2018
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-017-2071-y

Other articles of this Issue 1/2018

BMC Complementary Medicine and Therapies 1/2018 Go to the issue