蓝莓提取物改善特应性皮炎的作用及机制研究

doi:10.3877/cma.j.issn.2095-1221.2026.02.002

目的

探究蓝莓提取物对特应性皮炎（AD）的改善作用，并从皮肤菌群变化、屏障功能修复及Th2型炎症改善等揭示其作用机制。

方法

采用卡泊三醇类似物MC903局部涂抹诱导小鼠AD模型，将小鼠随机分为3组（n = 6）：空白对照组（耳部涂抹无水乙醇+PBS）、模型组（涂抹MC903+PBS）及给药组（涂抹MC903+蓝莓提取物），双盲法测量第1、3、5、7、10、12和14天耳厚度，记录第14天30 min内的搔抓次数。取耳组织进行苏木精-伊红（HE）染色和表皮厚度测量。RT-qPCR检测炎症因子白细胞介素-33 （IL-33）、IL-22、胸腺基质淋巴细胞生成素（TSLP）、肿瘤坏死因子-α （TNF-α）、IL-6和IL-1β mRNA表达。采用16S rRNA测序分析蓝莓提取物对AD小鼠微生物群落的影响。采用20 μg/mL脂多糖（LPS）刺激人角质形成细胞（HaCaT）建立细胞模型，CCK-8法检测不同浓度蓝莓提取物对细胞活性的影响。Western blot检测细胞IL-33、TSLP和IL-4Rα蛋白表达。采用超高效液相色谱串联质谱（UPLC-MS/MS）对蓝莓提取物组成进行鉴定。两组间比较采用独立样本t检验，多组间比较采用单因素方差分析或重复测量方差分析，组间两两比较采用Tukey多重检验。

结果

与模型组比较，蓝莓提取物减轻AD小鼠耳肿胀，搔抓次数[（9.00 ± 0.89）比（14.67 ± 2.06）次]，表皮厚度[（37.78 ± 2.68）比（54.90 ± 10.09）μm]降低（P均< 0.05）。蓝莓提取物下调Th2型炎症因子及促炎因子mRNA表达，与模型组比较，给药组IL-33 （0.95 ± 0.18比1.36 ± 0.23）、TSLP （27.12 ± 4.73比39.09 ± 4.61）、IL-22 （1.98 ± 0.45比3.43 ± 0.36）和IL-1β mRNA表达（4.47 ± 1.44比20.26 ± 3.30）降低（P均< 0.05）。16S rRNA分析表明，蓝莓提取物可缓解微生物群落紊乱和多样性下降，抑制链球菌属、葡萄球菌属和肠杆菌属等致病菌属增殖。细胞实验中，与LPS模型组比较，80 μmol/L浓度的蓝莓提取物组IL-4Rα （1.64 ± 0.31比5.90 ± 0.24）、IL-33 （0.90 ± 0.15比4.27 ± 0.41）和TSLP蛋白表达（0.15 ± 0.07比5.61 ± 0.40）降低，IL-4Rα（2.57 ± 0.54比13.20 ± 3.43）、IL-33 （2.00 ± 0.44比5.40 ± 1.24）和TSLP mRNA表达（1.47 ± 0.06比4.04 ± 0.21）降低（P均< 0.05）。通过质谱鉴定发现，飞燕草素可能是蓝莓提取物中的核心活性成分。

结论

蓝莓提取物通过调节皮肤菌群、修复屏障功能、抑制Th2型炎症反应以及减轻HaCaT细胞炎症因子表达，改善AD小鼠模型症状，其核心活性成分可能为飞燕草素。

关键词: 特应性皮炎, 蓝莓提取物, 16S rRNA测序, 炎症反应

Objective

Exploring the ameliorative effects of blueberry extract on atopic dermatitis (AD) and elucidating its mechanisms of action through changes in skin microbiota, restoration of barrier function, and improvement of Th2-type inflammation.

Methods

The AD mouse model was induced by topical application of the vitamin D3 analog calcipotriol (MC903). Ear thickness was measured in a double-blind manner on days 1, 3, 5, 7, 10, 12, and 14, and scratching episodes within 30 minutes were recorded on day 14. Ear tissue samples were collected for hematoxylin-eosin (HE) staining and epidermal thickness measurement. The mRNA expression of inflammatory cytokines (IL-33, IL-22, TSLP, TNF-α, IL-6, and IL-1β) was detected by RT-qPCR. 16S rRNA sequencing was used to analyze the effect of blueberry extract on the microbial community in AD mice. A cellular model was established by stimulating human keratinocytes (HaCaT) with lipopolysaccharide (LPS, 20 μg/mL). The effect of different concentrations of blueberry extract on cell viability was assessed using the CCK-8 assay. Expression of IL-33, TSLP, and IL-4Rα proteins were detected by Western blot. The composition of blueberry extract was identified by ultra performance liquid chromatography tandem mass spectrometry (UPLC-MS/MS). Comparisons between two groups were performed using the independent samples t-test. Comparisons among multiple groups were conducted using either one-way ANOVA or repeated-measures ANOVA, as appropriate. Post hoc pairwise comparisons were carried out with Tukey's test.

Results

Compared with the model group, blueberry extract significantly alleviated ear swelling in AD mice, reduced scratching frequency [ (9.00 ± 0.89) vs (14.67 ± 2.06) times] and epidermal thickness [ (37.78 ± 2.68) vs (54.90 ± 10.09) μm] (all P < 0.05). Blueberry extract downregulated the expression of Th2 inflammatory cytokines and pro-inflammatory factors mRNA. Compared with the model group, the expression levels of IL-33 (0.95 ± 0.18 vs 1.36 ± 0.23), TSLP (27.12 ± 4.73 vs 39.09 ± 4.61), IL-22 (1.98 ± 0.45 vs 3.43 ± 0.36), and IL-1β (4.47 ± 1.44 vs 20.26 ± 3.30) mRNA were decreased in treatment group (P < 0.05). 16S rRNA analysis revealed that blueberry extract mitigated microbial community dysbiosis and loss of diversity, inhibiting the proliferation of pathogenic bacteria such as Streptococcus, Staphylococcus, and Enterobacter. In the cellular experiments, compared with the LPS-induced model group, treatment with 80 μmol/L blueberry extract significantly reduced the protein expression of IL-4Rα (1.64 ± 0.31 vs 5.90 ± 0.24), IL-33 (0.90 ± 0.15 vs 4.27 ± 0.41), and TSLP (0.15 ± 0.07 vs 5.61 ± 0.40), as well as the mRNA expression of IL-4Rα (2.57 ± 0.54 vs 13.20 ± 3.43), IL-33 (2.00 ± 0.44 vs 5.40 ± 1.24), and TSLP (1.47 ± 0.06 vs 4.04 ± 0.21) (all P < 0.05). Further mass spectrometry identification indicated that delphinidin might be the core active component in blueberry extract.

Conclusion

Blueberry extract significantly alleviated symptoms in the AD mouse model by modulating the skin microbiota, restoring barrier function, suppressing Th2-type inflammatory responses, and reducing inflammatory cytokine expression in HaCaT cells, with delphinidin identified as its potential core active constituent.

Key words: Atopic dermatitis, Blueberry extract, 16S rRNA sequencing, Inflammation

表1 引物序列信息

基因	种属	引物序列（5'→3'）	预期扩增长度（bp）
β-actin	Mus musculus	上游CACCCTGTGCTGCTCACC	81
		下游GAAGGTCTCAAACATGATCTGGGT
Il33	Mus musculus	上游TTCCTGTCTGTATTGAGAAACCT	122
		下游TTATTTTGCAAGGCGGGACC
Il22	Mus musculus	上游ATGAGTTTTTCCCTTATGGGGAC	124
		下游GCTGGAAGTTGGACACCTCAA
Tslp	Mus musculus	上游ACGGATGGGGCTAACTTACAA	128
		下游AGTCCTCGATTTGCTCGAACT
Tnfα	Mus musculus	上游CGAGTGACAAGCCTGTAGCCC	113
		下游CTCTTTGAGATCCATGCCGTTG
Il6	Mus musculus	上游TTCCTCTGGTCTTCTGGAGT	148
		下游TCTGTGACTCCAGCTTATCTCTTG
Il1b	Mus musculus	上游ATGCCACCTTTTGACAGTGATG	139
		下游TGATGTGCTGCTGCGAGATT
β-actin	Homo sapiens	上游TCCCTGGAGAAGAGCTACGA	136
		下游TGAAGGTAGTTTCGTGGATGC
Il4rα	Homo sapiens	上游AAACGACCCGGCAGATTTCA	88
		下游AATCCCAGACTTCAGGGTGC
Il33	Homo sapiens	上游GTGACGGTGTTGATGGTAAGAT	94
		下游AGCTCCACAGAGTGTTCCTTG
Tslp	Homo sapiens	上游TCTTGTAGCAATCGGCCACAT	96
		下游GGCGAACATTTCTTTGGCGA

表1 引物序列信息

基因	种属	引物序列（5'→3'）	预期扩增长度（bp）
β-actin	Mus musculus	上游CACCCTGTGCTGCTCACC	81
		下游GAAGGTCTCAAACATGATCTGGGT
Il33	Mus musculus	上游TTCCTGTCTGTATTGAGAAACCT	122
		下游TTATTTTGCAAGGCGGGACC
Il22	Mus musculus	上游ATGAGTTTTTCCCTTATGGGGAC	124
		下游GCTGGAAGTTGGACACCTCAA
Tslp	Mus musculus	上游ACGGATGGGGCTAACTTACAA	128
		下游AGTCCTCGATTTGCTCGAACT
Tnfα	Mus musculus	上游CGAGTGACAAGCCTGTAGCCC	113
		下游CTCTTTGAGATCCATGCCGTTG
Il6	Mus musculus	上游TTCCTCTGGTCTTCTGGAGT	148
		下游TCTGTGACTCCAGCTTATCTCTTG
Il1b	Mus musculus	上游ATGCCACCTTTTGACAGTGATG	139
		下游TGATGTGCTGCTGCGAGATT
β-actin	Homo sapiens	上游TCCCTGGAGAAGAGCTACGA	136
		下游TGAAGGTAGTTTCGTGGATGC
Il4rα	Homo sapiens	上游AAACGACCCGGCAGATTTCA	88
		下游AATCCCAGACTTCAGGGTGC
Il33	Homo sapiens	上游GTGACGGTGTTGATGGTAAGAT	94
		下游AGCTCCACAGAGTGTTCCTTG
Tslp	Homo sapiens	上游TCTTGTAGCAATCGGCCACAT	96
		下游GGCGAACATTTCTTTGGCGA

图1 特应性皮炎模型诱导及蓝莓提取物效应验证注：a图为动物实验流程；b图为蓝莓提取物对MC903诱导的小鼠耳部代表性外观（标尺4 000 μm）；c图显示不同时间点（第1、3、5、7、10、12、14天）蓝莓提取物对MC903诱导的小鼠耳部皮肤厚度的测量结果（n = 6），第0天为干预起始点（未测量）；与模型组比较，^***P < 0.001；d图为小鼠抓挠次数统计（n = 6），^***P < 0.001

图2 小鼠耳部皮肤组织HE染色及表皮厚度统计注：a图为蓝莓提取物对MC903诱导的小鼠耳部皮肤组织的HE染色代表性图像，上方为低倍图像，红色方框标示区域于下方为高倍放大图像；b图为各组间表皮厚度对比（n = 6），^***P < 0.001

图3 小鼠耳组织相关mRNA表达检测注：a图为蓝莓提取物对MC903诱导的小鼠耳部皮肤中IL-33、IL-22及TSLP的相对mRNA表达水平的影响；b图为蓝莓提取物对MC903诱导的小鼠耳部皮肤中TNF-α、IL-6、IL-1β的相对mRNA表达水平的影响；以β-actin作为内参，使用2^−∆∆Ct法计算，结果显示为相对于对照组的相对表达倍数（n = 6）；^*P < 0.05，^**P < 0.01，^***P < 0.001，ns为差异无统计学意义

图4 16S rRNA测序分析蓝莓提取物对耳组织微生物群落的影响注：a图为基于Bray-Curtis距离的PCoA分析；b图为群落Simpson多样性指数统计（n = 6），^*P < 0.05，^**P < 0.01，^***P < 0.001；c ~ d图为LEfSe分析筛选的各组显著差异群落（LDA score > 2）

图5 小鼠耳表皮属水平微生物群落丰度比较注：a图为属水平相对丰度的微生物群落热图分析；b图为属水平物种相对丰度堆叠图；c图为差异菌属（链球菌、葡萄球菌和肠杆菌）的相对丰度统计（n = 6），^*P < 0.05，^**P < 0.01

图6 HaCaT细胞活性检测注：a图为Hacat细胞在不同浓度（0.1、1、10、100、1 000 μmol/L）蓝莓提取物处理后对HaCaT细胞活力的影响（n = 3），^*P < 0.05；b图为不同浓度（10、20、40、80、160 μmol/L）蓝莓提取物对LPS刺激的HaCaT细胞活率的影响（n = 3），^*P < 0.05，^***P < 0.001

图7 Western blot检测IL-4Rα、IL-33和TSLP蛋白相对表达注：a图为Western blot检测不同浓度（40、80、160 μmol/L）蓝莓提取物处理后IL-4Rα、IL-33和TSLP蛋白表达及内参（β-actin/β-tubulin）的条带；b ~ d图为对应蛋白的相对定量比较（n = 3），^***P < 0.001

图8 RT-qPCR检测IL-4Rα、IL-33和TSLP mRNA相对表达注：a ~ c图为Hacat细胞在不同浓度（40、80、160 μmol/L）蓝莓提取物处理后IL-4Rα、IL-33、TSLP的mRNA相对表达水平的影响；以β-actin作为内参，使用2^−∆∆Ct法计算，结果显示为相对于对照组的相对表达倍数（n = 3），^*P < 0.05，^**P < 0.01，^***P < 0.001

图9 蓝莓提取物代谢物成分分析注：a图为蓝莓提取物质谱分析负离子模式总离子流图；b图为多反应检测下负离子模式代谢物检测多峰图，横坐标为代谢物检测的保留时间，纵坐标为某代谢物离子检测的离子流强度；c图为蓝莓提取物主要化合物分类及相对含量统计；d图为蓝莓提取物详细化合物亚类分布统计

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Effects and mechanisms of blueberry extract in improving atopic dermatitis

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Effects and mechanisms of blueberry extract in improving atopic dermatitis