益气滋肾方通过抑制PI3K/Akt/NF-κB通路改善小鼠慢性阻塞性肺疾病的炎症反应

doi:10.12122/j.issn.1673-4254.2025.07.07

南方医科大学学报 ›› 2025, Vol. 45 ›› Issue (7): 1409-1422.doi: 10.12122/j.issn.1673-4254.2025.07.07

益气滋肾方通过抑制PI3K/Akt/NF-κB通路改善小鼠慢性阻塞性肺疾病的炎症反应

王立明¹^,²(), 陈宏睿¹^,², 杜燕¹^,², 赵鹏¹^,²^,³, 王玉洁¹^,², 田燕歌¹^,²^,³, 刘新光¹^,²^,³(), 李建生¹^,²^,³

^1.河南中医药大学呼吸疾病中医药防治省部共建协同创新中心//河南省中医药防治呼吸病重点实验室，河南郑州 450046
^2.河南中医药大学中医药科学院，河南郑州 450046
^3.河南中医药大学第一附属医院呼吸科，河南郑州 450046

收稿日期:2025-03-24 出版日期:2025-07-20 发布日期:2025-07-17
通讯作者: 刘新光 E-mail:15956982550@163.com;xgliu2016@126.com
作者简介:王立明，硕士，E-mail: 15956982550@163.com
基金资助:
国家重点研发计划中医药现代化重点专项2023年度“揭榜挂帅”项目(2023YFC3502605);国家自然科学基金(82274274);中华中医药学会青年人才托举工程(2023-QNRC2-B05);河南省高校创新人才支持项目(25HASTIT060);河南省科技研发计划联合基金（优势学科培育类）项目(222301420020)

Yiqi Zishen Formula ameliorates inflammation in mice with chronic obstructive pulmonary disease by inhibiting the PI3K/Akt/NF-κB signaling pathway

Liming WANG¹^,²(), Hongrui CHEN¹^,², Yan DU¹^,², Peng ZHAO¹^,²^,³, Yujie WANG¹^,², Yange TIAN¹^,²^,³, Xinguang LIU¹^,²^,³(), Jiansheng LI¹^,²^,³

^1.Collaborative Innovation Center for Chinese Medicine and Respiratory Diseases Co-constructed by Henan Province and State Ministry of Education, Henan Key Laboratory of Chinese Medicine for Respiratory Disease, Henan University of Chinese Medicine, Zhengzhou 450046, China
^2.Academy of Chinese Medical Sciences, Henan University of Chinese Medicine, Zhengzhou 450046, China
^3.Department of Respiratory Medicine, First Affiliated Hospital of Henan University of Chinese Medicine, Zhengzhou 450046, China

Received:2025-03-24 Online:2025-07-20 Published:2025-07-17
Contact: Xinguang LIU E-mail:15956982550@163.com;xgliu2016@126.com
Supported by:
National Natural Science Foundation of China(82274274)

摘要/Abstract

摘要：

目的明确益气滋肾方（YZF）的化学成分和入血成分，并阐明YZF改善慢性阻塞性肺疾病（COPD）炎症的整合作用机制与药效物质。方法通过超高效液相色谱串联四极杆轨道离子阱质谱（UHPLC-Q-Extractive-Orbitrap MS）鉴定YZF化学成分和入血成分。基于YZF入血成分构建YZF改善COPD的成分-疾病靶点网络，并进行富集分析筛选关键通路与作用靶标。通过香烟烟雾诱导构建小鼠COPD模型评价YZF抗炎作用及验证网络药理学富集到相关通路中关键蛋白的表达情况。50只C57BL/6J雄鼠随机分为对照组、模型组、YZF高、低剂量组和N-乙酰半胱氨酸组，10只/组。采用全身体积描记系统检测肺功能；HE染色法观察各组小鼠肺病理并进行肺泡和气道评估；ELISA法检测小鼠肺泡灌洗液中炎症因子IL-1β、IL-6、TNF-α含量；采用免疫组化法检测肺组织PI3K、Akt、p-Akt、p65和p-p65的表达水平。结果从YZF中共鉴定出156种化学成分，包括26种黄酮及黄酮苷类、27种生物碱类、11种皂苷类等成分；从含药血清样本中鉴定出43种原型入血成分。网络药理学分析获得YZF成分704个靶点和COPD 1199个疾病靶点；整合分析成分-疾病靶点后发现YZF缓解COPD可能与PI3K-Akt等信号通路相关；动物实验表明YZF可增加COPD模型小鼠的平均肺泡数和呼气峰流速（P<0.05）；降低COPD模型小鼠的肺泡平均线性截距和支气管壁厚度和肺系数以及肺泡灌洗液的IL-1β、IL-6、TNF-α含量（P<0.01），并能够抑制肺组织PI3K、Akt、p-Akt、p65和p-p65蛋白的表达（P<0.01）。结论 YZF能有效改善COPD症状，缓解COPD炎症，机制可能与其通过多成分-多靶点作用抑制PI3K/Akt/NF-κB通路相关。

关键词: 益气滋肾方, 慢性阻塞性肺疾病, 入血成分, 网络药理学, 炎症

Abstract:

Objective To investigate pharmacologically active components of Yiqi Zishen Formula (YZF) and their mechanisms for alleviating airway inflammation in mice with chronic obstructive pulmonary disease (COPD). Methods Ultra-high-performance liquid chromatography coupled with quadrupole-orbitrap mass spectrometry was employed to characterize the chemical components in YZF and YZF-medicated rat serum. A compound-disease target network was constructed based on serum components of YZF to screen the key pathways and targets using enrichment analysis. A mouse model of cigarette smoke-induced COPD was used to evaluate the anti-inflammatory effect of YZF and validate the expression of key proteins in network pharmacology-enriched pathways. Fifty male C57BL/6J mice were randomized equally into control group, COPD model group, high- and low-dose YZF treatment groups, and N-acetylcysteine treatment group. Pulmonary function of the mice was assessed using whole-body plethysmography, and lung histopathology, alveolar structure, and airway remodeling were analyzed using HE staining. The levels of IL-1β, IL-6, and TNF‑α in bronchoalveolar lavage fluid (BALF) were determined with ELISA, and pulmonary expressions of PI3K, Akt, phosphorylated Akt (p-Akt), p65, and phosphorylated p65 (p-p65) were detected using immunohistochemistry. Results We identified a total of 156 chemical components (including 26 flavonoids or flavonoid glycosides, 27 alkaloids, and 11 saponins) in YZF and 43 prototype components in medicated rat serum. Network pharmacology revealed 704 YZF-related targets and 1199 COPD-associated targets. Integrated analysis suggested that the anti-COPD effects of YZF were associated with the PI3K-Akt signaling pathway. In mouse models of COPD, YZF treatment significantly increased mean alveolar number and peak expiratory flow (P<0.05), reduced mean linear intercept, bronchial wall thickness, lung coefficient, and BALF cytokine levels, and suppressed the expressions of PI3K, Akt, p-Akt, p65, and p-p65 in the lung tissues. Conclusion YZF alleviates COPD symptoms and airway inflammation in mice possibly by inhibiting the PI3K/Akt/NF‑κB pathway through its multiple components that interact with multiple targets.

Key words: Yiqi Zishen Formula, chronic obstructive pulmonary disease, serum-absorbed components, network pharmacology, inflammation

王立明, 陈宏睿, 杜燕, 赵鹏, 王玉洁, 田燕歌, 刘新光, 李建生. 益气滋肾方通过抑制PI3K/Akt/NF-κB通路改善小鼠慢性阻塞性肺疾病的炎症反应[J]. 南方医科大学学报, 2025, 45(7): 1409-1422.

Liming WANG, Hongrui CHEN, Yan DU, Peng ZHAO, Yujie WANG, Yange TIAN, Xinguang LIU, Jiansheng LI. Yiqi Zishen Formula ameliorates inflammation in mice with chronic obstructive pulmonary disease by inhibiting the PI3K/Akt/NF-κB signaling pathway[J]. Journal of Southern Medical University, 2025, 45(7): 1409-1422.

图/表 10

参考文献 34

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NO.	Compound	Retention time (min)	Formula	MS/MS	Error (ppm)
1	Synephrine	1.6	C₉H₁₃NO₂	150.0917	1.20
2	Histidinyl-asparagine	1.62	C₁₀H₁₃N₄O₃	192.0785; 120.0650; 103.0390	-5.53
3	Fructose-phenylalanine	1.62	C₁₅H₂₁NO₇	310.1298; 292.1188	-1.52
4	Chlorogenic acid	12.03	C₁₆H₁₈O₉	163.0389; 145.0285; 135.0439; 117.0336	-6.19
5	p-Coumaric acid O-glycoside (a)	12.69	C₁₅H₁₆O₈	163.0390	1.24
6	Schizonepetoside A	12.72	C₁₆H₂₆O₇	169.1223	-1.71
7	Neostemonine or its isomer (a)	13.15	C₁₈H₂₅NO₄	246.1492	0.50
8	Croomine	13.19	C₁₈H₂₇NO₄	248.1645	-1.09
9	Neostemonine or its isomer (b)	13.43	C₁₈H₂₅NO₄	246.1491	0.50
10	Verticine-N-Oxide	14.55	C₂₇H₄₅NO₄	430.3311	-1.44
11	Diosmetin-6-C-glucoside	15.06	C₂₂H₂₂O₁₁	445.1081; 397.0879; 367.0805	-1.22
12	Verticinone-N-Oxide or its isomer (a)	15.51	C₂₇H₄₃NO₄	428.3118; 410.3059	-1.60
13	Verticinone-N-Oxide or its isomer (b)	15.83	C₂₇H₄₃NO₄	428.3174; 410.3051	-1.60
14	Stemoninine or its isomer (a)	16.78	C₂₂H₃₁NO₅	372.2172; 316.0912	-2.08
15	Stemoninine or its isomer (b)	17.4	C₂₂H₃₁NO₅	372.2175; 316.0909	-3.26
16	Peimisine	17.75	C₂₇H₄₁O₃N	410.3039	-1.85
17	Meranzin	18	C₁₅H₁₆O₄	189.0547	-0.53
18	Peimine	19.18	C₂₇H₄₅O₃N	414.3372	-0.33
19	TuberostemonineK/Neotuberostemonine	19.73	C₂₂H₃₃NO₄	358.2334; 348.2545; 302.2115; 250.1802	0.21
20	Peiminine	21.25	C₂₇H₄₃NO₃	412.3218; 396.2900	-0.91
21	Peimine isomer	23.46	C₂₇H₄₅O₃N	414.3374	-0.75
22	Gomisin R	23.74	C₂₂H₂₄O₇	383.1506;	-1.28
23	Dihydrocapsaicin	23.76	C₁₈H₂₉NO₃	290.2121;262.2171; 192.1391;136.0762;122.0602	-0.90
24	Peiminine isomer	23.97	C₂₇H₄₃NO₃	412.3222	-2.26
25	Hapepunine	24.31	C₂₈H₄₇NO₂	412.3602	-1.44
26	Fritillarizine/Puqiedinone	24.4	C₂₇H₄₃NO₂	396.3281	-1.08
27	Gentrogenin or its isomer (a)	25.1	C₂₇H₄₀O₄	411.2920	5.86
28	Gomisin S	25.2	C₂₃H₃₀O₇	401.1963; 369.1695	-1.18
29	Gentrogenin or its isomer (b)	25.44	C₂₇H₄₀O₄	411.2888	-3.86
30	Methyl eugenol	26.14	C₁₁H₁₄O₂	151.0752; 116.0011	0.16
31	Schisandrol A	26.43	C₂₄H₃₂O₇	415.2115; 400.1886; 384.1931; 369.1700; 338.1512	-1.69
32	Nobiletin	26.65	C₂₁H₂₂O₈	388.1158; 373.0921; 358.0685; 355.0820; 327.0869; 211.0245	-3.12
33	Schisanhenol or its isomer (a)	28.39	C₂₃H₃₀O₆	388.1881; 371.1856; 340.1665; 325.1430	-2.42
34	Schisantherin A	28.85	C₃₀H₃₂O₉	415.1725; 268.9779; 91.0565	-6.24
35	Schisanhenol or its isomer (b)	28.87	C₂₃H₃₀O₆	388.1876; 371.1868; 340.1668; 325.1438	-2.42
36	(-)-Gomisin L2	28.87	C₂₂H₂₆O₆	371.1465	-1.69
37	9-Tetradecenoic acid	29.8	C₁₄H₂₆O₂	209.1927	-1.06
38	Schisandrin A	30.09	C₂₄H₃₂O₆	402.2043; 386.2090; 371.1852; 347.1491; 316.1307; 301.1073	-1.23
39	Schisandrin B	30.88	C₂₃H₂₈O₆	386.1725; 370.1776; 355.1534; 300.0990; 285.0758	-1.31
40	Wuweizisu C	31.53	C₂₂H₂₄O₆	285.0756; 257.0808; 227.0703; 212.0466	3.93
41	Gondoic acid or its isomer (a)	32.83	C₂₀H₃₈O₂	265.2524; 247.2425	-0.57
42	Gondoic acid or its isomer (b)	33.96	C₂₀H₃₈O₂	293.2838	-1.94
43	Gondoic acid or its isomer (c)	34.48	C₂₀H₃₈O₂	293.2824	-3.41

NO.	Compound	Retention time (min)	Formula	MS/MS	Error (ppm)
1	Synephrine	1.6	C₉H₁₃NO₂	150.0917	1.20
2	Histidinyl-asparagine	1.62	C₁₀H₁₃N₄O₃	192.0785; 120.0650; 103.0390	-5.53
3	Fructose-phenylalanine	1.62	C₁₅H₂₁NO₇	310.1298; 292.1188	-1.52
4	Chlorogenic acid	12.03	C₁₆H₁₈O₉	163.0389; 145.0285; 135.0439; 117.0336	-6.19
5	p-Coumaric acid O-glycoside (a)	12.69	C₁₅H₁₆O₈	163.0390	1.24
6	Schizonepetoside A	12.72	C₁₆H₂₆O₇	169.1223	-1.71
7	Neostemonine or its isomer (a)	13.15	C₁₈H₂₅NO₄	246.1492	0.50
8	Croomine	13.19	C₁₈H₂₇NO₄	248.1645	-1.09
9	Neostemonine or its isomer (b)	13.43	C₁₈H₂₅NO₄	246.1491	0.50
10	Verticine-N-Oxide	14.55	C₂₇H₄₅NO₄	430.3311	-1.44
11	Diosmetin-6-C-glucoside	15.06	C₂₂H₂₂O₁₁	445.1081; 397.0879; 367.0805	-1.22
12	Verticinone-N-Oxide or its isomer (a)	15.51	C₂₇H₄₃NO₄	428.3118; 410.3059	-1.60
13	Verticinone-N-Oxide or its isomer (b)	15.83	C₂₇H₄₃NO₄	428.3174; 410.3051	-1.60
14	Stemoninine or its isomer (a)	16.78	C₂₂H₃₁NO₅	372.2172; 316.0912	-2.08
15	Stemoninine or its isomer (b)	17.4	C₂₂H₃₁NO₅	372.2175; 316.0909	-3.26
16	Peimisine	17.75	C₂₇H₄₁O₃N	410.3039	-1.85
17	Meranzin	18	C₁₅H₁₆O₄	189.0547	-0.53
18	Peimine	19.18	C₂₇H₄₅O₃N	414.3372	-0.33
19	TuberostemonineK/Neotuberostemonine	19.73	C₂₂H₃₃NO₄	358.2334; 348.2545; 302.2115; 250.1802	0.21
20	Peiminine	21.25	C₂₇H₄₃NO₃	412.3218; 396.2900	-0.91
21	Peimine isomer	23.46	C₂₇H₄₅O₃N	414.3374	-0.75
22	Gomisin R	23.74	C₂₂H₂₄O₇	383.1506;	-1.28
23	Dihydrocapsaicin	23.76	C₁₈H₂₉NO₃	290.2121;262.2171; 192.1391;136.0762;122.0602	-0.90
24	Peiminine isomer	23.97	C₂₇H₄₃NO₃	412.3222	-2.26
25	Hapepunine	24.31	C₂₈H₄₇NO₂	412.3602	-1.44
26	Fritillarizine/Puqiedinone	24.4	C₂₇H₄₃NO₂	396.3281	-1.08
27	Gentrogenin or its isomer (a)	25.1	C₂₇H₄₀O₄	411.2920	5.86
28	Gomisin S	25.2	C₂₃H₃₀O₇	401.1963; 369.1695	-1.18
29	Gentrogenin or its isomer (b)	25.44	C₂₇H₄₀O₄	411.2888	-3.86
30	Methyl eugenol	26.14	C₁₁H₁₄O₂	151.0752; 116.0011	0.16
31	Schisandrol A	26.43	C₂₄H₃₂O₇	415.2115; 400.1886; 384.1931; 369.1700; 338.1512	-1.69
32	Nobiletin	26.65	C₂₁H₂₂O₈	388.1158; 373.0921; 358.0685; 355.0820; 327.0869; 211.0245	-3.12
33	Schisanhenol or its isomer (a)	28.39	C₂₃H₃₀O₆	388.1881; 371.1856; 340.1665; 325.1430	-2.42
34	Schisantherin A	28.85	C₃₀H₃₂O₉	415.1725; 268.9779; 91.0565	-6.24
35	Schisanhenol or its isomer (b)	28.87	C₂₃H₃₀O₆	388.1876; 371.1868; 340.1668; 325.1438	-2.42
36	(-)-Gomisin L2	28.87	C₂₂H₂₆O₆	371.1465	-1.69
37	9-Tetradecenoic acid	29.8	C₁₄H₂₆O₂	209.1927	-1.06
38	Schisandrin A	30.09	C₂₄H₃₂O₆	402.2043; 386.2090; 371.1852; 347.1491; 316.1307; 301.1073	-1.23
39	Schisandrin B	30.88	C₂₃H₂₈O₆	386.1725; 370.1776; 355.1534; 300.0990; 285.0758	-1.31
40	Wuweizisu C	31.53	C₂₂H₂₄O₆	285.0756; 257.0808; 227.0703; 212.0466	3.93
41	Gondoic acid or its isomer (a)	32.83	C₂₀H₃₈O₂	265.2524; 247.2425	-0.57
42	Gondoic acid or its isomer (b)	33.96	C₂₀H₃₈O₂	293.2838	-1.94
43	Gondoic acid or its isomer (c)	34.48	C₂₀H₃₈O₂	293.2824	-3.41

Ingredient	Degree	Closeness centrality	Betweenness centrality
Gomisin S	46	0.4087	0.1222
Schisandrin A	45	0.4026	0.1143
(-)-Gomisin L2	44	0.4011	0.1029
Wuweizisu C	38	0.3923	0.0869
Schisantherin A	35	0.3894	0.0765
Dihydrocapsaicin	34	0.3894	0.1012
Schisandrol A	34	0.3881	0.0748
Gentrogenin	33	0.3759	0.0782
9-Tetradecenoic acid	32	0.3881	0.0940
Hapepunine	31	0.3853	0.0848

Ingredient	Degree	Closeness centrality	Betweenness centrality
Gomisin S	46	0.4087	0.1222
Schisandrin A	45	0.4026	0.1143
(-)-Gomisin L2	44	0.4011	0.1029
Wuweizisu C	38	0.3923	0.0869
Schisantherin A	35	0.3894	0.0765
Dihydrocapsaicin	34	0.3894	0.1012
Schisandrol A	34	0.3881	0.0748
Gentrogenin	33	0.3759	0.0782
9-Tetradecenoic acid	32	0.3881	0.0940
Hapepunine	31	0.3853	0.0848

益气滋肾方通过抑制PI3K/Akt/NF-κB通路改善小鼠慢性阻塞性肺疾病的炎症反应

Yiqi Zishen Formula ameliorates inflammation in mice with chronic obstructive pulmonary disease by inhibiting the PI3K/Akt/NF-κB signaling pathway

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