Integrative network pharmacology and experimental validation to decipher the anti-angiogenic mechanisms of Xuandan Sanjie decotion (玄丹散结汤) in adenomyosis

doi:10.19852/j.cnki.jtcm.20260514.001

Journal of Traditional Chinese Medicine ›› 2026, Vol. 46 ›› Issue (5): 1218-1229.DOI: 10.19852/j.cnki.jtcm.20260514.001

• Original Articles • Previous Articles Next Articles

Integrative network pharmacology and experimental validation to decipher the anti-angiogenic mechanisms of Xuandan Sanjie decotion (玄丹散结汤) in adenomyosis

GAN Lin¹^,², ZHOU Fangfang¹, QIU Yingying³, HUANG Meihua¹, LI Zhenli¹(), GUI Tao¹()

¹ Department of Obstetrics and Gynecology, Affiliated Hospital of Integrated Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing 210028, China
² Department of Gynecology, Affiliated Jiangning Hospital of Chinese Medicine, China Pharmaceutical University, Nanjing 211100, China
³ Department of Gynecology, Affiliated Xuzhou Municipal Hospital of Xuzhou Medical University, Xuzhou 221112, China

Received:2025-05-22 Accepted:2026-02-09 Online:2026-10-15 Published:2026-05-14
Contact: GUI Tao, Department of Obstetrics and Gynecology, Affiliated Hospital of Integrated Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing 210028, China. guitao@jsatcm.com; LI Zhenli, Department of Obstetrics and Gynecology, Affiliated Hospital of Integrated Traditional Chinese and Western Medicine, Nanjing University of Chinese Medicine, Nanjing 210028, China. lizhenli79@163.com,Telephone: +86-25-85630285
About author:
GAN Lin and ZHOU Fangfang are co-first authors and contributed equally to this work
Supported by:
National Natural Science Foundation of China: To Explore the Effect and Mechanism of Yiqi Sanjie Decoction in Relieving Pain of Adenomyosis Based on the Nerve Growth Factor/Extracellular Regulated Protein Kinases pathway(81403321);Science and Technology Project of Jiangsu Provincial Administration of Traditional Chinese Medicine: Study on the Mechanism of Xuandan Sanjie Decoction Regulating the Estradiol/G-protein Coupled Estrogen Receptor 1 /Hypoxia Inducible Factor-1α Pathway of Endometrial Mesenchymal Stem Cells to Inhibit Angiogenesis in Uterine Adenomyosis(MS2023039);Science and Technology Project of Jiangsu Provincial Administration of Traditional Chinese Medicine: Study on the Mechanism of the Formula of Tonifying Kidney and Activating Blood Circulation and Dissipating Blood Stasis in Regulating Macrophage Polarization and Improving Endometrial Receptivity Based on the miRNA-103a-3p/Dual Specificity Protein Phosphatase 2/Extracellular Regulated Protein Kinases Axis(MS2023079);Science and Technology Project of Jiangsu Provincial Administration of Traditional Chinese Medicine: Based on the Study of Inducing Macrophage Polarization by Endometrial Mesenchymal Stem Cells, Exploring the Mechanism of the "Supplement Kidney and Activate Blood, Dispel Stasis" Formula in Inhibiting the Invasion and Migration of Endometrium in Uterine Adenomyosis(ZD202419);Nanjing Jiangning District Science and Technology Benefit People Plan Project: In vitro Mechanism of Xuandan Sanjie Decoction Inhibiting Adenomyosis Angiogenesis through the Estradiol/Hypoxia Inducible Factor-1α Pathway(2024003S);Jiangsu Chinese Medicine Society: Mechanistic Study of Xuandan Sanjie Decoction in the Treatment of Adenomyosis via Inhibiting Transferrin Receptor Protein 1-mediated Ferroptosis(CYTF2024025);Research Project Funding from Affiliated Jiangning Hospital of Chinese Medicine, China Pharmaceutical University: Xuandan Sanjie Decoction Suppresses Adenomyosis by Modulating Ferroptosis through Transferrin Receptor/Nuclear Receptor Coactivator 4-mediated Ferritinophagy(YJZD2025001);Science and Technology Program of Xuzhou: Research and Development of Intervention Technology for Embryo Implantation Disorders in Adenomyosis Based on a 3D Endometrium-Embryo Co-culture Platform(KC25074)

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Abstract

Abstract:

OBJECTIVE: To investigate the mechanisms by which Xuandan Sanjie decoction (玄丹散结汤, XSD) inhibits angiogenesis in adenomyosis (AM), using both AM-derived primary endometrial stromal cells (ESCs) and a mouse model.

METHODS: Core components and targets of XSD for AM treatment were predicted using multiple databases. Gene ontology and kyoto encyclopedia of genes and genomes pathway analyses were used to elucidate the potential mechanisms. Ultra-high-performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS) was applied to identify chemical constituents of XSD. A cobalt (II) chloride (CoCl₂)-induced hypoxia-mimicking ESC model and an AM mouse model were established to experimentally validate the anti-angiogenic effects of XSD.

RESULTS: According to bioinformatics analysis, hypoxia signaling and angiogenesis are crucial for AM progression. Twenty chemical constituents of the 106 compounds identified from the Traditional Chinese Medicine systems pharmacology database and analysis platform database were validated by UHPLC-MS/MS. Network pharmacology identified protein kinase B alpha, epidermal growth factor receptor, hypoxia inducible factor-1α (HIF-1α), and estrogen receptor 1 (ESR1) as core targets. According to in vitro and in vivo experiments, XSD exhibits anti-angiogenic properties through ESR1/G protein-coupled estrogen receptor (GPER)-mediated HIF-1α signaling.

CONCLUSION: Our study confirms that XSD inhibits angiogenesis in AM viaESR1/GPER-mediated HIF-1α signaling. These findings elucidate the molecular mechanisms underlying XSD's therapeutic effects for abnormal uterine bleeding associated with adenomyosis, offering new therapeutic strategies for this condition.

Key words: network pharmacology, endometrial stromal cells, adenomyosis, angiogenesis, Xuandan Sanjie decoction

GAN Lin, ZHOU Fangfang, QIU Yingying, HUANG Meihua, LI Zhenli, GUI Tao. Integrative network pharmacology and experimental validation to decipher the anti-angiogenic mechanisms of Xuandan Sanjie decotion (玄丹散结汤) in adenomyosis[J]. Journal of Traditional Chinese Medicine, 2026, 46(5): 1218-1229.

Figures/Tables 5

Figure 1 Identification of chemical constituents in XSD by UHPLC-MS/MS A: A1: XSD in ESI positive mode; A2: XSD in ESI negative mode. The red numbers in the mass spectrum represent 20 identified compounds. 1: kaempferol; 2: coumaric acid; 3: sclareol; 4: nicotinic acid; 5: palmatine; 6: allocryptopine; 7: acetophenone; 8: boldine; 9: camphor; 10: linderane; 11: apigenin; 12: kaempferol; 13: azelaic acid; 14: naringenin; 15: isoimperatorin; 16: coumaric acid; 17: caffeic acid; 18: cirsimaritin; 19: vanillic acid; 20: quercetin; B: metabolite class composition ring diagram; C: sankey diagram illustrating relationships between the ingredients and source herbs in XSD. XSD: Xuandan Sanjie decoction; UHPLC-MS/MS: ultra-high performance liquid chromatography coupled with tandem mass spectrometry; ESI: electrospray ionization.

Table 1 Characterization of compounds of XSD by UPLC-MS/MS

No.	Compound	Formula	mzmed	ms2Adduct	Relative content	Class
1	Kaempferol	C15H10O6	287.055	[M+H]+	3860556.051	Flavonoids
2	Coumaric acid	C9H8O3	147.043	[M+H-H2O]+	42418783.33	Phenylpropanoids
3	sclareol	C20H36O2	326.305	[M+NH4]+	31763629.87	Terpenoids
4	Nicotinic acid	C6H5NO2	124.039	[M+H]	87096072.94	Alkaloid
5	Palmatine	C21H22NO4	352.153	[M]+	1414855.134	Alkaloid
6	Allocryptopine	C21H23NO5	370.165	[M+H]	20554792.16	Alkaloid
7	Acetophenone	C8H8O	121.064	[M+H]	4027023.846	Phenols
8	Boldine	C19H21NO4	328.153	[M+H]+	4970057868	Alkaloid
9	Camphor	C10H16O	153.127	[M+H]	1193613.001	Terpenoids
10	Linderane	C15H16O4	261.111	[M+H]	103593915.9	Terpenoids
11	Apigenin	C15H10O5	269.045	[M-H]-	2469278.777	Flavonoids
12	Kaempferol	C15H10O6	285.042	[M-H]-	3370501.518	Flavonoids
13	Azelaic acid	C9H16O4	187.097	[M-H]-	6112865.346	Aliphatic acyl
14	Naringenin	C15H12O5	271.060	[M-H]	7626711.301	Flavonoids
15	isoimperatorin	C16H14O4	269.082	[M-H]-	11272505.7	Phenylpropanoids
16	Coumaric acid	C9H8O3	163.039	[M-H]-	12214940.45	Phenylpropanoids
17	Caffeic acid	C9H8O4	179.034	[M-H]-	42289183.19	Phenylpropanoids
18	cirsimaritin	C17H14O6	313.071	[M-H]-	55540661.17	Flavonoids
19	Vanillic acid	C8H8O4	167.034	[M-H]-	67417507.56	Cinnamic acid derivatives
20	Quercetin	C15H10O7	301.037	[M-H]-	3860556.051	Flavonoids

Figure 2 XSD inhibits angiogenesis by modulating VEGF and MMP9 secretion in vitro A: VEGF levels in ESC supernatants after 24 h of treatment; B: MMP9 levels in ESC supernatants after 24 h of treatment; C: C1-C7: tube formation assays of HUVECs treated with conditioned media from each group (× 40); C8-C14: representative images of endothelial tube formation analyzed by AngioTool; D: migration assays of HUVECs treated with conditioned media (× 100); E: invasion assays of HUVECs treated with conditioned media (× 100). C1, C8, D1, E1: Control group; C2, C9, D2, E2: E2 group; C3, C10, D3, E3: Vehicle group; C4, C11, D4, E4: Low dose XSD group; C5, C12, D5, E5: Middle dose XSD group; C6, C13, D6, E6: High dose XSD group; C7, C14, D7, E7: Mifepristone group. Control: ESCs treated with 200 μM CoCl2. E2: ESCs treated with 10 nM E2. Vehicle: ESCs treated with blank. XSD-L: ESCs treated with 2.5% (v/v) XSD-containing serum. XSD-M: ESCs treated with 5% (v/v) XSD-containing serum. XSD-H: ESCs treated with 10% (v/v) XSD-containing serum. Mifepristone: ESCs treated with 10 μM mifepristone. VEGF: vascular endothelial growth factor; MMP9: matrix metalloproteinase-9; ESCs: endometrial stromal cells; E2: Estrogen; XSD: Xuandan Sanjie decoction; ANOVA: analysis of variance. ANOVA tests were used among these groups. Data were presented as mean ± standard deviation (n = 3). Compared with the Control group, aP < 0.05; compared with the Vehicle group, bP > 0.05, cP < 0.05, dP < 0.01.

Figure 3 XSD regulates VEGF and MMP9 expression via ESR1/GPER-HIF-1α pathways A: qPCR analysis of HIF-1α mRNA in ESCs after 24 h; B: qPCR analysis of VEGF mRNA after 24 h; C: Western blot of ESR1 and HIF-1α at 24 h; D: VEGF levels in ESC supernatants (24 h); E: early (1 h) expression of HIF-1α mRNA; F: early (1 h) expression of VEGF mRNA; G: Western blot of GPER and HIF-1α at 1 h post-stimulation; H: VEGF secretion after 1 h assessed by ELISA. Group definitions: Control: 200 μM CoCl2; E2: 10 nM E2 under hypoxia; Vehicle: blank serum under hypoxia + E2; XSD: 10% (v/v) XSD serum under hypoxia + E2; Giredestrant: 10 nM Giredestrant under hypoxia + E2; G15: 100 nM G15 under hypoxia + E2. qPCR: quantitative reverse transcription polymerase chain reaction; ESCs: endometrial stromal cells; VEGF: vascular endothelial growth factor; MMP9: matrix metalloproteinase-9; CoCl2: cobalt (II) chloride; ESR1: estrogen receptor 1; HIF-1α: hypoxia inducible factor-1α; ELISA: enzyme-linked immunosorbent assay; GPER: G protein-coupled estrogen receptor; PI3K: phosphatidylinositol 3-kinase; p-PI3K: phospho-PI3K; AKT: protein kinase B; p-AKT: phospho-AKT; ERK: extracellular signal-regulated kinase; p-ERK: phospho-ERK; XSD: Xuandan Sanjie decoction; ANOVA: analysis of variance. ANOVA tests were used among these groups. Data were presented as mean ± standard deviation (n = 3). Compared with the Control group, aP < 0.05; compared with the Vehicle group, bP < 0.05; compared with the XSD group, cP > 0.05.

Figure 4 XSD inhibits angiogenesis in vivo in AM through ESR1/GPER-HIF-1α signaling A: VEGF levels in ectopic lesions from all groups (ELISA); B: MMP9 levels in ectopic lesions from all groups (ELISA); C: uterus index comparison; D: number of AM nodules; E: HE staining of uterine tissues (× 10); F: pathology scoring; G: immunohistochemistry staining of GPER, ESR1, HIF-1α, and CD31 (× 200); E1, G1, G7, G13, G19: Control group; E2, G2, G8, G14, G20: Model group; E3, G3, G9, G15, G21: Vehicle group; E4, G4, G10, G16, G22: Positive group; E5, G5, G11, G17, G23: XSD-L group; E6, G6, G12, G18, G24: XSD-H group. H: H-score quantification of GPER. I: H-score quantification of ESR1. J: H-score quantification of HIF-1α. Group definitions: Control: untreated mice; Model: saline (0.2 mL/d); Vehicle: distilled water (0.2 mL/d); Positive control (Mifepristone): 3.25 mg/kg bw; XSD-L: low dose (5.2 g/kg bw) XSD; XSD-H: high dose (10.4 g/kg bw) XSD. ESR1: estrogen receptor 1; GPER: G protein-coupled estrogen receptor; HIF-1α: hypoxia inducible factor-1α; VEGF: vascular endothelial growth factor; MMP9: matrix metalloproteinase-9; HE: hematoxylin and eosin; ELISA: enzyme-linked immunosorbent assay; AM: adenomyosis; XSD: Xuandan Sanjie decoction; ANOVA: analysis of variance. Statistical analysis was carried out using ANOVA tests among these groups. Data were presented as mean ± standard deviation (n = 8). Compared with the Control group, aP < 0.05; compared with the Model group, bP > 0.05, cP < 0.01, dP < 0.05.

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Integrative network pharmacology and experimental validation to decipher the anti-angiogenic mechanisms of Xuandan Sanjie decotion (玄丹散结汤) in adenomyosis

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