变应原诱导常年性变应性鼻炎患者血液中CCR3+粒细胞亚群活化

doi:10.12122/j.issn.1673-4254.2026.02.16

南方医科大学学报 ›› 2026, Vol. 46 ›› Issue (2): 385-393.doi: 10.12122/j.issn.1673-4254.2026.02.16

• • 上一篇

变应原诱导常年性变应性鼻炎患者血液中CCR3⁺粒细胞亚群活化

王秋丽¹(), 胥伟华¹, 谷芳秋², 王思勤³, 何韶衡², 王君灵²^,³()

^1.上海中医药大学附属普陀医院耳鼻咽喉科，上海 200062
^2.锦州医科大学附属第一医院变态反应与临床免疫研究中心，辽宁锦州 121001
^3.郑州大学人民医院河南省人民医院过敏反应科，河南郑州 450003

收稿日期:2025-08-03 出版日期:2026-02-20 发布日期:2026-03-10
通讯作者: 王君灵 E-mail:18841609323@163.com;wangjuneling@163.com
作者简介:王秋丽，医师，硕士，E-mail: 18841609323@163.com
基金资助:
国家自然科学基金(81471592);河南省重点研发与推广专项(232102311022);河南省博士后科研项目(HN2022097);辽宁省自然科学基金(2019-ZD-0801);辽宁省自然科学基金(LJKZ0796)

Allergens induce activation of blood CCR3⁺ granulocyte subsets in patients with perennial allergic rhinitis

Qiuli WANG¹(), Weihua XU¹, Fangqiu GU², Siqin WANG³, Shaoheng HE², Junling WANG²^,³()

^1.Department of Otolaryngology, Putuo Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai 200062, China
^2.Allergy and Clinical Immunology Research Centre, the First Affiliated Hospital of Jinzhou Medical University, Jinzhou 121001, China
^3.Department of Allergy, Henan Provincial People's Hospital, Zhengzhou University People's Hospital, Zhengzhou 450003, China.

Received:2025-08-03 Online:2026-02-20 Published:2026-03-10
Contact: Junling WANG E-mail:18841609323@163.com;wangjuneling@163.com
Supported by:
National Natural Science Foundation of China(81471592)

摘要/Abstract

摘要：

目的探讨变应原对变应性鼻炎（AR）患者血液CCR3⁺粒细胞亚型活化的影响。方法流式细胞术检测变应原对AR患者血液粒细胞群CCR3⁺CD203c^-嗜酸性粒细胞和CCR3⁺CD203c⁺嗜碱性粒细胞活化分子CD63和CD203c表达水平的影响。多重免疫荧光分析和ELISA技术分别检测志愿者血浆IL-25和TSLP的水平，并分析其与嗜酸性粒细胞和嗜碱性粒细胞数量的相关性。转录组测序AR患者血液CD16^-粒细胞，并富集分析其差异表达基因的功能和潜在机制。结果 AR患者CCR3⁺粒细胞中嗜酸性粒细胞和嗜碱性粒细胞的比例增加（P<0.005），变应原诱导嗜碱性粒细胞的比例增加（P<0.005）。季节性AR（sAR）和常年性AR（pAR）而非皮肤点刺试验阴性的AR（nAR）患者血液粒细胞群中嗜酸性粒细胞CD63的平均荧光强度表达水平增强（P<0.005），变应原诱导pAR患者嗜酸性粒细胞和嗜碱性粒细胞CD63和CD203c平均荧光强度的表达水平增强（P<0.005）。AR患者升高的血浆IL-25和TSLP水平与增加的嗜酸性粒细胞和嗜碱性粒细胞的数量相关（均P<0.005）。皮肤点刺试验阳性AR患者CD16^-粒细胞差异表达的3999个基因在蛋白合成、能量代谢和免疫功能等方面发生了潜在变化，内吞作用、吞噬体和碳代谢等通路可能参与上述变化。结论本研究深化了对血液粒细胞群中CCR3⁺嗜酸性粒细胞和嗜碱性粒细胞参与皮肤点刺试验阳性AR发病机制的理解，揭示了AR治疗的潜在靶点。

关键词: 变应原, 变应性鼻炎, 嗜酸性粒细胞, 嗜碱性粒细胞, 活化

Abstract:

Objective To explore the effects of allergens on activation of blood CCR3⁺ granulocyte subtypes in patients with allergic rhinitis (AR). Methods Flow cytometry was used to examine the effects of allergens on CD63 and CD203c expressions on CCR3⁺CD203c^- eosinophils and CCR3⁺CD203c⁺ basophils of AR patients. Plasma levels of IL-25 and TSLP of the patients were detected with multiplex immunoassay and ELISA, respectively, and their correlations with eosinophils and basophils were analyzed. RNA-sequencing of blood CD16^- granulocytes from AR patients was performed, and enrichment analysis was used to explore the functions and potential mechanisms of the differentially expressed genes. Results The percentages of eosinophils and basophils in CCR3⁺ granulocytes increased significantly in AR patients (P<0.005), and exposure to allergens further upregulated the percentage of basophils (P<0.005). CD63 expression was significantly increased in patients with seasonal AR (sAR) and perennial AR (pAR) (P<0.005) but not in AR patients negative for skin prick test (nAR). Allergen exposures enhanced the expressions of CD63 and CD203c on eosinophils and basophils in pAR patients (P<0.005). Elevated plasma IL-25 and TSLP levels in AR patients were associated with increased eosinophil and basophil counts (P<0.005). The 3999 differentially expressed genes in CD16^- granulocytes from AR patients positive for skin prick test (SPT⁺) were involved in protein synthesis, energy metabolism and immune function and in endocytosis, phagosome and carbon metabolism pathways. Conclusion The findings in this study enrich the understanding of the roles of CCR3⁺ eosinophils and basophils in the pathogenesis of SPT⁺AR and reveal potential therapeutic targets for AR.

Key words: allergen, allergic rhinitis, basophils, eosinophil, activation

王秋丽, 胥伟华, 谷芳秋, 王思勤, 何韶衡, 王君灵. 变应原诱导常年性变应性鼻炎患者血液中CCR3⁺粒细胞亚群活化[J]. 南方医科大学学报, 2026, 46(2): 385-393.

Qiuli WANG, Weihua XU, Fangqiu GU, Siqin WANG, Shaoheng HE, Junling WANG. Allergens induce activation of blood CCR3⁺ granulocyte subsets in patients with perennial allergic rhinitis[J]. Journal of Southern Medical University, 2026, 46(2): 385-393.

图/表 8

表1 志愿者的基本信息

Tab.1 Basic information of volunteers

Population	Positive allergen	Sample size (n)	Age (year)	Medical history (year)	Onset age (year)
HC	——	30	34.5 (23.8-42.0)	——	——
nAR	——	14	35.5 (18.0-42.3)	3.0 (2.0-6.3)	30.5 (15.3-34.5)
sAR	ASE	16	32.0 (24.5-39.8)	4.0 (3.0-10.0)	26.5 (13.3-30.8)
pAR	ASE+DPE+Others	24	26.0 (19-44.5)	3.5 (2.0-10.0)	19.0 (14.0-38.8)
	DPE+Cockroach+Others	1	9.0 (9.0-9.0)	6.0 (6.0-6.0)	3.0 (3.0-3.0)
	Cockroach+Others	4	38.5 (14.0-48.0)	4.0 (1.3-12.8)	34.0 (12.8-35.8)
In total		29	28.0 (18.5-44.0)	4.0 (2.0-10.0)	20.0 (11.5-35.5)
——: not applicable; Age, medical history and onset age were expressed as Median (P₂₅-P₇₅). HC: Healthy control; nAR: AR with negative skin prick test; sAR: Seasonal AR with positive skin prick test; pAR: Perennial AR with positive skin prick test.

图1 AR患者血液粒细胞群中嗜酸性粒细胞、嗜碱性粒细胞的比例

Fig.1 Ratios of eosinophils and basophils in blood granulocytes of AR patients. A: Flow cytometry gating strategy for human blood granulocytes. B, C: Representative flow cytometry graphs of CCR3+ cells (B), CCR3+CD203c- eosinophils and CCR3+CD203c+ basophils (C) in granulocytes. D-F: Statistical graphs of the expression ratios of CCR3+ cells (D), eosinophils (E), basophils (F) in granulocytes. *P<0.05 vs HC, #P<0.05 vs nAR Medium, △P<0.05 vs sAR Medium, ¶P<0.05 vs pAR Medium.

图2 变应原对AR患者血液粒细胞群中嗜酸性粒细胞CD63和嗜碱性粒细胞CD203c MFI表达水平的影响

Fig.2 Effects of allergens on MFI expression levels of CD63 on eosinophils and CD203c on basophils in blood granulocytes of AR patients. A, B: Flow cytometry for analyzing MFI expression levels of CD63 on eosinophils (A) and CD203c on basophils (B) in granulocytes. C, D: Statistical graph of the MFI expression levels of CD63on eosinophils (C) and CD203c on basophils (D). *P<0.05 vs HC, #P<0.05 vs nAR Medium, △P<0.05 vs sAR Medium, ¶P<0.05 vs pAR Medium.

图3 AR患者血浆IL-25和TSLP的水平

Fig.3 Plasma levels of IL-25 (A) and TSLP (B) in AR patients. *P<0.05 vs HC.

图4 AR患者血液粒细胞群嗜酸性粒细胞和嗜碱性粒细胞的数量

Fig.4 Eosinophil (A) and basophil (B) counts in blood granulocytes of AR patients. *P<0.05 vs HC.

表2 细胞因子水平与嗜酸性粒细胞和嗜碱性粒细胞数量间Spearman's秩相关系数（R）

Tab.2 Spearman's rank correlation coefficient (R) between cytokine levels and eosinophil and basophil counts in granulocytes

Group	Compound	IL-25	TSLP	Eosinophil	Basophil
HC	IL-25	——	-0.343	0.165	-0.056
HC	TSLP	-0.343	——	-0.401	-0.231
nAR	IL-25	——	0.741^⁋	0.587^⁋	0.630^⁋
nAR	TSLP	0.741^⁋	——	0.582^⁋	0.669^⁋
sAR	IL-25	——	0.577^⁋	0.802^⁋	0.895^⁋
sAR	TSLP	0.577^⁋	——	0.590^⁋	0.537^⁋
pAR	IL-25	——	0.772^⁋	0.880^⁋	0.601^⁋
pAR	TSLP	0.772^⁋	——	0.666^⁋	0.429^⁋
——: not applicable;^⁋P<0.05.

图5 转录组测序AR患者血液CD16-粒细胞

Fig.5 RNA-seq analysis of blood CD16- granulocytes of AR patients. A, B: Volcano plot (A) and cluster heatmap (B) of differential expression genes. C, D: GO (C) and KEGG (D) enrichment diagramsof differential expression genes.

表3 转录组分析CD16- 粒细胞中CCR3、CD203c和CD63 mRNA的表达水平

Tab.3 RNA-seq analysis of the expression levels of CCR3, ENPP3 and CD63 mRNA in CD16- granulocytes

Protein name	Gene number	Gene name	log₂ fold change (AR vs HC)
CCR3	ENSG00000183625	CCR3	2.55**
CD203c	ENSG00000154269	ENPP3	-0.44
CD63	ENSG00000135404	CD63	2.34**
**P<0.01vs HC.

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变应原诱导常年性变应性鼻炎患者血液中CCR3⁺粒细胞亚群活化

Allergens induce activation of blood CCR3⁺ granulocyte subsets in patients with perennial allergic rhinitis

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变应原诱导常年性变应性鼻炎患者血液中CCR3+粒细胞亚群活化

Allergens induce activation of blood CCR3+ granulocyte subsets in patients with perennial allergic rhinitis

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变应原诱导常年性变应性鼻炎患者血液中CCR3⁺粒细胞亚群活化

Allergens induce activation of blood CCR3⁺ granulocyte subsets in patients with perennial allergic rhinitis