Effect of improved Yupingfeng powder prescription (玉屏风散加味) on interleukin-33/suppression of tumorigenicity 2 pathway in mice with ovalbumins-induced allergic rhinitis

doi:10.19852/j.cnki.jtcm.2025.06.004

Journal of Traditional Chinese Medicine ›› 2025, Vol. 45 ›› Issue (6): 1215-1227.DOI: 10.19852/j.cnki.jtcm.2025.06.004

• Original Articles • Previous Articles Next Articles

Effect of improved Yupingfeng powder prescription (玉屏风散加味) on interleukin-33/suppression of tumorigenicity 2 pathway in mice with ovalbumins-induced allergic rhinitis

LEI Xiaochun¹, LIU Cuizhen¹, LIN Xiujuan¹, XIE Xiangyu¹, KE Wei¹, QIU Zhenwen², TANG Hongmei², HUANG Yushen³, ZHANG Lijuan⁴, HUANG Baoyuan², WAN Xin¹^,²(), LI Detang²^,⁵()

1 The First Clinical Medical School of Guangzhou University of Chinese Medicine, Guangzhou 510405, China
2 Department of Pharmacy, the First Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou 510405, China
3 Lingnan Medical Research Center, the First Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou 510405, China
4 Department of otorhinolaryngology, the First Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou 510405, China
5 Department of Pharmacy, Chongqing Hospital of the First Affiliated Hospital of Guangzhou University of Chinese Medicine (Chongqing Beibei Hospital of Traditional Chinese Medicine), Chongqing 400700, China

Received:2024-11-22 Accepted:2025-04-11 Online:2025-12-15 Published:2025-11-24
Contact: Prof. WAN Xin, Department of Pharmacy, The First Clinical Medical School of Guangzhou University of Chinese Medicine, Guangzhou 510405, China, wanxin145@163.com, Telephone: + 86-19928311931;
Prof. LI Detang, Department of Pharmacy, Chongqing Hospital of the First Affiliated Hospital of Guangzhou University of Chinese Medicine (Chongqing Beibei Hospital of Traditional Chinese Medicine), Chongqing 400700, China, lidetang2002@163.com
Supported by:
Exploring the Mechanism of Improved Yupingfeng Powder in Treating Allergic Rhinitis Based on the Nucleotide-Binding Oligomerization Domain, Leucine-rich Repeat and Pyrin Domain-containing Protein 3/Interleukin-33-Mediated Activation Pathway of Pulmonary Group 2 Innate Lymphoid Cells in Airway Epithelial Cells(82374526);Mechanism of Shikonin in Treating Acute Lung Injury Through Regulating M1 Macrophage Polarization via Adenosine 5'-monophosphate-Activated Protein Kinase/Dynamin-Related Protein 1-mediated Mitochondrial Dynamics(2024A04J4334);Exemplary Study on Process Optimization and Quality Standard Enhancement of Hospital Preparations Such as Gangmei Qingyan Mixture(2023A03J0299);Anti-Allergic Mechanism of Improved Yupingfeng Powder in Alleviating Nasal Mucosal Inflammation in Allergic Rhinitis via Interleukin-33/Suppression of Tumorigenicity 2-Regulated Group 2 Innate Lymphoid Cells Suppression(202201020457);Elite Talent Program of the First Affiliated Hospital of Guangzhou University of Chinese Medicine by 2023 Years and Guangdong Province Lingnan Characteristic Hospital Preparation Transformation Engineering Technology Research Center(2023A170)

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Abstract

Abstract:

OBJECTIVE: To identify the main active ingredients of Improved Yupingfeng Powder prescription (IYPFP, 玉屏风散加味) and investigate its anti-inflammatory effects and underlying mechanisms in ovalbumins (OVA)-induced allergic rhinitis (AR) in mice.

METHODS: Bagg Albino/substrain mice were sensitized with OVA emulsified in aluminum hydroxide adjuvant, followed by intranasal challenge to establish AR models. Treatment groups received IYPFP (1.5 or 4.5 g/kg) via daily gavage for 14 d. The nasal mucosa tissues were collected for pathological observation. The expression of OVA-specific immunoglobulin E (IgE), histamine, and interleukin-33 (IL-33) was detected by enzyme-linked immunosorbent assay. IL-5, IL-13, IL-33, suppression of tumorigenicity 2 (ST2), tumor necrosis factor-α (TNF-α) and interferon-γ (IFN-γ) in the nasal mucosa and lung were detected by quantitative polymerase chain reaction and Western blot. High performance liquid chromatography and ultra-high performance liquid chromatography quadrupole exactive orbitrap mass spectrometry were used to detect the chemical fingerprints of IYPFP, and the chemical compositions of plasma from rats treated with IYPFP at 0.5, 1, 1.5, 2, 3, 4 and 6 h, respectively. Virtual screening of bioactive compounds was conducted through molecular docking targeting IL-33/ST2 pathway proteins.

RESULTS: Eight chemical compounds of IYPFP were accurately identified, they are prim-O-glucosylcimifugin (peak 2), calycosin-7-O-β-D-glucoside (peak 4), cimifugin (peak 5), 5-O-methylvisammioside (peak 6), sec-O-glucosylhamaudol (peak 12), calycosin (peak 15), formononetin (peak 19), and magnolin (peak 21). Compared with the OVA model group, IYPFP alleviated the nasal symptoms, improved nasal mucosal injury and downregulated the levels of OVA-specific IgE, histamine and IL-33. Additionally, IYPFP reduced the levels of IL-5, IL-13, TNF-α, IL-33, and ST2 in the lungs, but upregulated IFN-γ. Molecular docking confirmed that eight representative compounds of IYPFP had good binding properties with IL-5, IL-13, IFN-γ, histamine, IL-33 and ST2, and were able to inhibit the activation of the IL33/ST2 inflammatory pathway.

CONCLUSION: This study demonstrates that IYPFP ameliorates AR by modulating IL-33/ST2 pathway which provides a theoretical basis for the clinical treatment of patients with AR.

Key words: rhinitis, allergic, inflammation, ovalbumin, IL-33/ST2 pathway, molecular docking simulation, improved Yupingfeng powder prescription

LEI Xiaochun, LIU Cuizhen, LIN Xiujuan, XIE Xiangyu, KE Wei, QIU Zhenwen, TANG Hongmei, HUANG Yushen, ZHANG Lijuan, HUANG Baoyuan, WAN Xin, LI Detang. Effect of improved Yupingfeng powder prescription (玉屏风散加味) on interleukin-33/suppression of tumorigenicity 2 pathway in mice with ovalbumins-induced allergic rhinitis[J]. Journal of Traditional Chinese Medicine, 2025, 45(6): 1215-1227.

Figures/Tables 8

Figure 1 Chemical profiling of IYPFP: plasma component identification by UPLC-Q-exactive orbitrap-MS/MS and quality evaluation through HPLC fingerprinting and content analysis A: establishment of high-performance liquid chromatogram and identification of 8 chemical components in IYPFP and chemical structure and formulae of 8 chemical ingredients; B: the eight major chemical compounds of IYPFP: prim-O-glucosylcimifugin (peak 2), calycosin-7-O-β-D-glucoside (peak 4), cimifugin (peak 5), 5-O-methylvisammioside (peak 6), sec-O-glucosylhamaudol (peak 12), calycosin (peak 15), formononetin (peak 19), and magnolin (peak 21). IYPFP: improved Yupingfeng Powder prescription; UPLC-Q-Exactive Orbitrap-MS/MS: ultra high performance liquid chromatography quadrupole exactive orbitrap mass spectrometry; HPLC: high performance liquid chromatography.

Table 1 IYPFP decoction Results of similarity evaluation and analysis of 10 batches of samples

	S1	S2	S3	S4	S5	S6	S7	S8	S9	S10
S1	1	0.970	0.978	0.965	0.982	0.982	0.983	0.990	0.992	0.988
S2	0.970	1	0.931	0.920	0.950	0.944	0.966	0.964	0.974	0.969
S3	0.978	0.931	1	0.988	0.992	0.994	0.978	0.973	0.976	0.986
S4	0.965	0.920	0.988	1	0.975	0.986	0.977	0.953	0.958	0.977
S5	0.982	0.950	0.992	0.975	1	0.997	0.982	0.976	0.984	0.991
S6	0.982	0.944	0.994	0.986	0.997	1	0.986	0.974	0.981	0.991
S7	0.983	0.966	0.978	0.977	0.982	0.986	1	0.969	0.978	0.991
S8	0.990	0.964	0.973	0.953	0.976	0.974	0.969	1	0.996	0.984
S9	0.992	0.974	0.976	0.958	0.984	0.981	0.978	0.996	1	0.988
S10	0.988	0.969	0.986	0.977	0.991	0.991	0.991	0.984	0.988	1
Similarity results	0.993	0.968	0.991	0.981	0.994	0.995	0.991	0.989	0.993	0.997

Table 2 Concentration of IYPFP of eight major chemical compositions ($\bar{x}$ ± s, n = 3)

Chemical constituents	Molecular formula	Linear range	Concentration (μg/mL)
Prim-O-glucosylcimifugin	C₂₂H₂₈O₁₁	y=2299.0x-4.6027	12.123±0.358
Cimifugin	C₁₆H₁₈O₆	y=3952.2x-6.781	3.857±0.102
Sec-O-Glucosylhamaudol	C₂₁H₂₆O₁₀	y=2113.5x-4.8354	3.809±0.034
5-O-Methylvisammioside	C₂₂H₂₈O₁₀	y=2469.8x-5.2983	11.137±0.079
Calycosin-7-O-β-D-glucoside	C₂₂H₂₂O₁₀	y=3262.4x-3.2236	5.372±0.046
Calycosin	C₂₂H₂₂O₁₀	y=5330.7x-9.1153	1.313±0.052
Formononetin	C₁₆H₁₂O₄	y=7421.5x-10.649	0.288±0.014
Magnolin	C₂₃H₂₈O₇	y=2893.5x-5.7248	2.068±0.041

Figure 2 Comparison of the nasal mucosa tissues pathology of mice in each group A: HE staining of nasal mucosa tissues from mice (A1: × 2, scale bar = 1000 μm; A2-A6: × 100, scale bar = 20 μm); B: statistical analysis results of thickness of nasal mucosa; C: HE staining of nasal mucosa tissues from mice (C1: × 2, scale bar = 1000 μm; C2-C6: × 40, scale bar = 50 μm); D: statistical analysis results of goblet cells in nasal mucosa. A1: observation of nasal mucosa thickness; C1: observation of goblet cells; A2, C2: blank control group; A3, C3: OVA model group; A4, C4: OVA + DEX group; A5, C5: OVA + 1.5 g/kg IYPFP group; A6, C6: OVA + 4.5 g/kg IYPFP group; Control group: injected with 200 μL saline on days 0, 7 and 14 and administered 20 μL saline per nostril daily from days 22 to 28; Model group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28; DEX group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28, then intraperitoneally administered with 200 μL saline containing 0.5 mg Dex daily from day 15 to 28; IYPFP 1.5 g/kg group and IYPFP 4.5 g/kg group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28, then intragastrically administered 200 μL of IYPFP at 1.5 or 4.5 g/kg daily from day 15 to 28. Control: blank control group; Model: OVA model group; DEX: OVA + DEX group; IYPFP 1.5 g/kg: OVA + 1.5 g/kg IYPFP group; IYPFP 4.5 g/kg: OVA+4.5 g/kg IYPFP group. Differences in means between groups were examined using one-way analysis of variance, with the Dunnett’s T3 test used for the data in this table. Data were presented as mean ± standard deviation (n = 3). Compared with the Control group, aP < 0.01; compared with the Model group, bP < 0.01, cP < 0.05.

Table 3 The expression of OVA-specific IgE, histamine and IL-33 in serum was detected by ELISA ($\bar{x}$ ± s)

Group	n	IgE	Histamine	IL-33
Control	3	16.02±0.21	12.73±0.27	99.46±6.00
Model	3	18.01±0.45^a	15.14±0.52^a	152.55±5.23^a
DEX	3	14.27±0.33^b	12.05±0.21^b	127.87±3.18^b
IYPFP 1.5 g/kg	3	15.48±0.29^b	13.16±0.31^b	133.28±1.48^b
IYPFP 4.5 g/kg	3	14.76±0.55^b	12.84±0.78^b	119.90±5.47^b

Figure 3 real-time PCR analysis to evaluate the expression of IFN-γ, IL-5, IL-13 and TNF-α mRNA in lung tissue A: IFN-γ mRNA level in lung; B: IL-5 mRNA level in lung; C: IL-13 mRNA level in lung; D: TNF-α mRNA level in lung; E: the ratio of IL-5 to IFN-g produced by the individual variations in T-cell is expressed as Th2/Th1; F: the ratio of IL-13 to IFN-γ produced by the individual variations in T-cell is expressed as Th2/Th1. Control group: injected with 200 μL saline on days 0, 7 and 14 and administered 20 μL saline per nostril daily from days 22 to 28; Model group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28; DEX group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28, then intraperitoneally administered with 200 μL saline containing 0.5 mg Dex daily from day 15 to 28; IYPFP 1.5 g/kg group and IYPFP 4.5 g/kg group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28, then intragastrically administered 200 μL of IYPFP at 1.5 or 4.5 g/kg daily from day 15 to 28. Control: blank control group; Model: OVA model group; DEX: OVA + DEX group; IYPFP 1.5 g/kg: OVA + 1.5 g/kg IYPFP group; IYPFP 4.5 g/kg: OVA + 4.5 g/kg IYPFP group. IFN-γ: interferon γ; IL-5: interleukin-5; IL-13: interleukin-13; TNF-α: tumor necrosis factor-α; OVA: ovalbumin; DEX: dexamethasone; IYPFP: improved Yupingfeng powder prescription. The 2-△△CT method was used to analyse relative gene expression. All data are expressed as mean ± standard deviation (n = 6). Differences in means between groups were examined using one-way analysis of variance, with the Dunnett’s T3 test used for the data in this table. Compared with the Control group, aP < 0.01, cP < 0.05; compared with the Model group, bP < 0.01, dP < 0.05.

Figure 4 influence of IYPFP on the IL-33/ST2 signaling pathway and Th1/Th2 cytokines A-B: all pictures were stained by immunohistochemical method to observe the expression of the IL-33 and ST2 protein in nasal mucosa. The brown color was positive (× 63, scale bar = 20 μm); C: the average density value of IL33 proteins in nasal mucosa (n = 3); D: the average density value of ST2 proteins in nasal mucosa (n = 3); E: real-time PCR analysis to evaluate the mRNA expression of IL-33 in the lung tissues (n = 6); F: real-time PCR analysis to evaluate the mRNA expression of ST2 in the lung tissues (n = 6); G: Western blot analysis for expression of IL-33 and ST2 in the lung tissues in each group of mice. The graph showed relative density was calculated using β-actin as a control. All data are expressed as mean ± standard deviation (n = 3); H: protein expression of IL-33 in lung tissues of mice; I: protein expression of ST2 in lung tissues of mice; A1, B1: blank Control group; A2, B2: OVA model group; A3, B3: OVA + DEX group; A4, B4: OVA + 1.5 g/kg IYPFP group; A5, B5: OVA + 4.5 g/kg IYPFP group. Control group: injected with 200 μL saline on days 0, 7 and 14 and administered 20 μL saline per nostril daily from days 22 to 28; Model group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28; DEX group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28, then intraperitoneally administered with 200 μL saline containing 0.5 mg Dex daily from day 15 to 28; IYPFP 1.5 g/kg group and IYPFP 4.5 g/kg group: injected of 200 μL of saline containing 50 μg of OVA and 2 mg of aluminium hydroxide on days 0, 7 and 14, and challenged intranasally with 20 μL saline containing 25 mg/mL OVA per nostril daily from days 22 to 28, then intragastrically administered 200 μL of IYPFP at 1.5 or 4.5 g/kg daily from day 15 to 28. IL-33: interleukin-33; ST2: suppression of tumorigenicity 2; OVA: ovalbumin; DEX: dexamethasone; IYPFP: Improved Yupingfeng Powder Prescription. The 2-△△CT method was used to analyse relative gene expression. Differences in means between groups were examined using one-way analysis of variance, with the Dunnett’s T3 test used for the data in this table. Compared with the Control group, aP < 0.01, dP < 0.05; compared with the Model group, bP < 0.01, cP < 0.05.

Table 4 Binding energies between the key ingredients of IYPFP and the target gene

Compound	IL-33	ST2	IL-5	IL-13	IFN-γ	Histamine	Total
Prim-O-glucosylcimifugin	－4.88	－4.49	－4.31	－3.67	－3.70	－4.79	－25.84
Calycosin-7-O-β-D-glucoside	－7.09	－8.26	－7.50	－6.42	－7.27	－8.16	－44.70
Cimifugin	－6.18	－6.15	－5.74	－5.62	－6.70	－7.99	－38.38
5-O-methylvisammioside	－5.62	－7.25	－6.08	－5.98	－6.84	－7.91	－39.68
sec-O-Glucosylhamaudol	－6.30	－8.05	－6.77	－6.47	－6.44	－7.57	－41.60
Calycosin	－6.24	－8.12	－6.64	－6.29	－6.74	－7.83	－41.86
formononetin	－6.00	－7.93	－6.59	－5.56	－6.49	－7.77	－40.34
Magnolin	－6.64	－7.43	－6.82	－6.31	－7.16	－8.89	－43.25
Total	－48.95	－57.68	－50.45	－46.32	－51.34	－60.91

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Effect of improved Yupingfeng powder prescription (玉屏风散加味) on interleukin-33/suppression of tumorigenicity 2 pathway in mice with ovalbumins-induced allergic rhinitis

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