多房棘球蚴感染小鼠腹膜腔免疫细胞迁移及其功能变化

doi:10.12140/j.issn.1000-7423.2025.01.012

中国寄生虫学与寄生虫病杂志 ›› 2025, Vol. 43 ›› Issue (1): 76-83.doi: 10.12140/j.issn.1000-7423.2025.01.012

多房棘球蚴感染小鼠腹膜腔免疫细胞迁移及其功能变化

邓冰清¹^,²(), 阿迪莱·多力坤¹^,², 李寅时¹^,², 阿比旦·艾尼瓦尔¹^,², 孙胜¹^,², 肖雯颖¹^,², 葛聪蕙¹^,², 唐娜¹^,², 姜涛³, 王慧¹^,², 张传山¹^,², 李静¹^,⁴^,⁵^,^*()

1 新疆医科大学基础医学院，新疆乌鲁木齐 830054
2 新疆医科大学第一附属医院临床医学研究院，新疆乌鲁木齐 830054
3 新疆医科大学实验动物中心，新疆乌鲁木齐 830011
4 新疆地区高发疾病研究教育部重点实验室（新疆医科大学），新疆乌鲁木齐 830054
5 中国疾病预防控制中心寄生虫病预防控制所（国家热带病研究中心），国家卫生健康委员会寄生虫病原与媒介生物学重点实验室（中国疾病预防控制中心寄生虫病预防控制所），上海 200025

收稿日期:2024-10-21 修回日期:2025-01-24 出版日期:2025-02-28 发布日期:2025-03-26
通讯作者: *李静，女，博士，教授，从事寄生虫感染与免疫研究。E-mai：lijing0527@163.com
作者简介:邓冰清，女，硕士研究生，从事寄生虫感染与免疫研究。E-mail：Bingqingdeng@163.com
基金资助:
新疆维吾尔自治区自然科学基金(2022D01E51);新疆维吾尔自治区自然科学基金(2022D01D60);国家自然科学基金(82302561);国家自然科学基金(82372279);国家自然科学基金(82160396);新疆地区高发疾病研究教育部重点实验室开放课题资助项目(2023B03);省部共建中亚高发病成因与防治国家重点实验室开放课题资助项目(SKL-HIDCA-2024-25);国家卫健委寄生虫病原与媒介生物学重点实验室开放课题资助项目(NHCKFKT2022-05)

Immune cell migration and its functional changes in the peritoneal cavity of mice infected with Echinococcus multilocular

DENG Bingqing¹^,²(), ADILAI Duolikun¹^,², LI Yinshi¹^,², ABIDAN Ainiwaer¹^,², SUN Sheng¹^,², XIAO Wenying¹^,², GE Conghui¹^,², TANG Na¹^,², JIANG Tao³, WANG Hui¹^,², ZHANG Chuanshan¹^,², LI Jing¹^,⁴^,⁵^,^*()

1 College of Basic Medical, Xinjiang Medical University, Urumqi 830054, Xinjiang, China
2 Clinical Medicine Research Institute, the First Afilicated Hospital of Xinjiang Medical University, Urumqi 830054, Xinjiang, China
3 Xinjiang Medical University Laboratory Animal Center, Urumqi 830011, Xinjiang, China
4 Key Laboratory of High Incidence Disease Research in Xingjiang (Xinjiang Medical University), Ministry of Education, Urumqi 830054, Xinjiang, China
5 National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research); NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), Shanghai 200025, China

Received:2024-10-21 Revised:2025-01-24 Online:2025-02-28 Published:2025-03-26
Contact: *E-mail: lijing0527@163.com
Supported by:
Natural Science Foundation of Xinjiang Uyghur Autonomous Region(2022D01E51);Natural Science Foundation of Xinjiang Uyghur Autonomous Region(2022D01D60);National Natural Science Foundation of China(82302561);National Natural Science Foundation of China(82372279);National Natural Science Foundation of China(82160396);Funding of Open Subjects in the Key Laboratory of the Ministry of Education for the Study of Highly Prevalent Diseases in the Xinjiang Region(2023B03);Provincial-Ministerial Joint Establishment of State Key Laboratory of Causes and Prevention of High Morbidity in Central Asia(SKL-HIDCA-2024-25);Open Topic Funding Program of the Key Laboratory of Parasitic Pathogen and Vector Biology of the National Health Commission of China(NHCKFKT2022-05)

摘要/Abstract

摘要：

目的了解多房棘球蚴感染小鼠腹膜腔免疫细胞迁移及分化的变化，探讨其发挥免疫功能的机制。方法裂解增强绿色荧光蛋白（EGFP）小鼠脾组织，分离EGFP示踪免疫细胞。C57BL/6J小鼠腹腔注射2.5 × 10⁷个示踪免疫细胞，5 d后经肝门静脉穿刺接种3 000个多房棘球蚴原头节。感染19周后，取感染小鼠肝、脾组织，冷冻切片后4,6-二脒基-2-苯基吲哚（DAPI）染色，免疫荧光观察示踪免疫细胞的分布。分离感染小鼠外周血、肝、脾和腹膜腔免疫细胞，流式细胞术检测EGFP示踪免疫细胞在不同组织的迁移分布和细胞分型，以及细胞因子γ干扰素（IFN-γ）、肿瘤坏死因子-α（TNF-α）、白细胞介素4（IL-4）的分泌情况。结果免疫荧光结果显示，EGFP示踪细胞主要迁移至小鼠脾组织。肝组织中各型示踪淋巴细胞占比从高到低依次为CD8⁺ T细胞（79.63 ± 5.00）%、CD4⁺ T细胞（7.08 ± 4.00）%、B细胞（2.01 ± 1.00）%（F = 396.20，P < 0.01）；脾组织中各型淋巴细胞占比从高到低依次为CD8⁺ T细胞（73.97 ± 3.56）%、CD4⁺ T细胞（11.92 ± 5.02）%、B细胞（3.86 ± 0.32）%（F = 349.00，P < 0.01）；腹膜腔中各型淋巴细胞占比从高到低依次为CD8⁺ T细胞（45.27 ± 4.53）%、CD4⁺ T细胞（34.60 ± 8.00）%、B细胞（15.03 ± 6.38）%（F = 16.90，P < 0.05）。肝、脾、腹膜腔中的示踪CD4⁺ T细胞数量分别为2 700 ± 3 120、14 407 ± 11 958、3 376 ± 1 481，示踪CD8⁺ T细胞数量分别为26 407 ± 22 190、109 179 ± 92 692、4 245 ± 798，示踪B细胞数量分别为698 ± 719、5 794 ± 4 971、1 476 ± 840，3种示踪淋巴细胞均主要分布在脾组织中（F = 2.51、3.03、2.62，均P > 0.05）。肝组织中各型髓系细胞占比从高到低依次为树突状细胞（3.94 ± 1.33）%、单核细胞（3.79 ± 1.80）%、巨噬细胞（3.13 ± 1.85）%、嗜酸粒细胞（2.40 ± 1.81）%、骨髓来源抑制性细胞（0.76 ± 0.17）%、中性粒细胞（0.67 ± 0.04）%（F = 3.21，P < 0.05）；脾组织中各型髓系细胞占比从高到低依次为树突状细胞（1.86 ± 0.89）%、单核细胞（0.41 ± 0.09）%、巨噬细胞（0.23 ± 0.03）%、中性粒细胞和骨髓来源抑制性细胞[均（0.13 ± 0.14）%]、嗜酸粒细胞（0.04 ± 0.04）%（F = 42.70，P < 0.01）；外周血中组织中各型髓系细胞占比从高到低依次为树突状细胞（0.37 ± 0.28）%、单核细胞（0.22 ± 0.27）%、巨噬细胞（0.22 ± 0.21）%、中性粒细胞和骨髓来源抑制性细胞[均（0.17 ± 0.08）%]、嗜酸粒细胞（0.05 ± 0.08）%（F = 0.92，P > 0.05）。肝组织的示踪CD4⁺ T细胞中，分泌IFN-γ、TNF-α、IL-4的细胞分别占（41.17 ± 19.92）%、（30.70 ± 3.35）%、（2.78 ± 4.81）%（F = 8.22，P < 0.05）；示踪CD8⁺ T细胞中，分泌IFN-γ、TNF-α、IL-4的细胞分别占（64.17 ± 3.17）%、（24.85 ± 15.66）%、（5.67 ± 6.35）%（F = 27.08，P < 0.01）。脾组织的示踪CD4⁺ T细胞中，分泌IFN-γ、TNF-α、IL-4的细胞分别占（52.43 ± 19.43）%、（27.67 ± 18.99）%、（4.77 ± 2.23）%（F = 6.88，P < 0.05）；示踪CD8⁺ T细胞中，分泌TNF-α、IFN-γ、IL-4的细胞分别占（40.53 ± 17.79）%、（38.97 ± 18.04）%、（3.23 ± 3.09）%（F = 6.15，P < 0.05）。腹膜腔的示踪CD4⁺ T细胞中，分泌IFN-γ、TNF-α、IL-4的细胞分别占（64.33 ± 6.82）%、（46.43 ± 13.44）%、（4.03 ± 3.51）%（F = 36.04，P < 0.01）；示踪CD8⁺ T细胞中，分泌IFN-γ、TNF-α、IL-4的细胞分别占（53.57 ± 19.17）%、（21.47 ± 8.54）%、（6.13 ± 8.63）%（F = 10.24，P < 0.05）。结论多房棘球蚴感染小鼠腹膜腔内免疫细胞主要迁移至脾组织，细胞类型以CD8⁺ T细胞和树突状细胞为主。T细胞主要分泌IFN-γ，呈Th1型免疫应答。

关键词: 多房棘球蚴病, 腹膜腔, 免疫细胞, 迁移, CD8⁺ T细胞

Abstract:

Objective To understand the changes in the migration and differentiation of immune cells in the peritoneal cavity of mice infected with Echinococcus multilocularis, and to explore the mechanism of immune function. Methods Spleen tissues of enhanced green fluorescent protein (EGFP) mice were lysed to isolate EGFP-labeled immune cells. C57BL/6J mice were intraperitoneally injected with 2.5 × 10⁷ traced immune cells. Five days later, 3 000 protoscoleces of E. multilocularis were inoculated via the hepatic portal vein. After 19 weeks of infection, the liver and spleen tissues of the infected mice were collected. After frozen sectioning, the sections were stained with 4,6-diamidino-2-phenylindole (DAPI), and immunofluorescence was used to observe the distribution of the traced immune cells. Immune cells from peripheral blood, liver, spleen and peritoneal cavity of infected mice were isolated, and the migration distribution and cell typing of EGFP-labeled immune cells in different tissues were detected by flow cytometry, as well as the secretion of cytokines interferon-γ (IFN-γ), tumor necrosis factor-α (TNF-α) and interleukin-4 (IL-4). Results The immunofluorescence results showed that the EGFP-traced cells mainly migrated to the spleen tissue of the mice. In the liver tissue, the proportions of various types of traced lymphocytes from high to low were as follows: CD8⁺ T cells (79.63 ± 5.00)%, CD4⁺ T cells (7.08 ± 4.00)%, and B cells (2.01 ± 1.00)% (F = 396.20, P < 0.01). In the spleen tissue, the proportions of various types of lymphocytes from high to low were as follows: CD8⁺ T cells (73.97 ± 3.56)%, CD4⁺ T cells (11.92 ± 5.02)% and B cells (3.86 ± 0.32)% (F = 349.00, P < 0.01). In the peritoneal cavity, the proportions of various types of lymphocytes from high to low were as follows: CD8⁺ T cells (45.27 ± 4.53)%, CD4⁺ T cells (34.60 ± 8.00)% and B cells (15.03 ± 6.38)% (F = 16.90, P < 0.05). The numbers of traced CD4⁺ T cells in the liver, spleen, and peritoneal cavity were 2 700 ± 3 120, 14 407 ± 11 958 and 3 376 ± 1 481 respectively. The numbers of traced CD8⁺ T cells were 26 407 ± 22 190, 109 179 ± 92 692 and 4 245 ± 798 respectively. The numbers of traced B cells were 698 ± 719, 5 794 ± 4 971 and 1 476 ± 840 respectively. All three types of traced lymphocytes were mainly distributed in the spleen tissue (F = 2.51, 3.03, 2.62, all P > 0.05). In the liver tissue, the proportions of various types of myeloid cells from high to low were as follows: dendritic cells (3.94 ± 1.33)%, monocytes (3.79 ± 1.80)%, macrophages (3.13 ± 1.85)%, eosinophils (2.40 ± 1.81)%, myeloid-derived suppressor cells (0.76 ± 0.17)% and neutrophils (0.67 ± 0.04)% (F = 3.21, P < 0.05). In the spleen tissue, the proportions of various types of myeloid cells from high to low were as follows: dendritic cells (1.86 ± 0.89)%, monocytes (0.41 ± 0.09)%, macrophages (0.23 ± 0.03)%, neutrophils and myeloid-derived suppressor cells [both (0.13 ± 0.14)%], and eosinophils (0.04 ± 0.04)% (F = 42.70, P < 0.01). In the peripheral blood, the proportions of various types of myeloid cells from high to low were as follows: dendritic cells (0.37 ± 0.28)%, monocytes (0.22 ± 0.27)%, macrophages (0.22 ± 0.21)%, neutrophils and myeloid-derived suppressor cells [both (0.17 ± 0.08)%], and eosinophils (0.05 ± 0.08)% (F = 0.92, P > 0.05). Among the traced CD4⁺ T cells in the liver tissue, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (41.17 ± 19.92)%, (30.70 ± 3.35)%, and (2.78 ± 4.81)% respectively (F = 8.22, P < 0.05). Among the traced CD8⁺ T cells, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (64.17 ± 3.17)%, (24.85 ± 15.66)%, and (5.67 ± 6.35)% respectively (F = 27.08, P < 0.01). Among the traced CD4⁺ T cells in the spleen tissue, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (52.43 ± 19.43)%, (27.67 ± 18.99)%, and (4.77 ± 2.23)% respectively (F = 6.88, P < 0.05). Among the traced CD8⁺ T cells, the cells secreting TNF-α, IFN-γ, and IL-4 accounted for (40.53 ± 17.79)%, (38.97 ± 18.04)%, and (3.23 ± 3.09)% respectively (F = 6.15, P < 0.05). Among the traced CD4⁺ T cells in the peritoneal cavity, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (64.33 ± 6.82)%, (46.43 ± 13.44)%, and (4.03 ± 3.51)% respectively (F = 36.04, P < 0.01). Among the traced CD8⁺ T cells, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (53.57 ± 19.17)%, (21.47 ± 8.54)%, and (6.13 ± 8.63)% respectively (F = 10.24, P < 0.05). Conclusion Immune cells in the peritoneal cavity of E. multilocularis infected mice mainly migrate to the spleen tissue, and the cell types are mainly CD8⁺ T cells and dendritic cells. T cells mainly secreted IFN-γ, which showed Th1 immune response.

Key words: Alveolar echinococcoisis, Peritoneal cavity, Immume cell, Migration, CD8⁺ T cell

中图分类号:

R532.32

邓冰清, 阿迪莱·多力坤, 李寅时, 阿比旦·艾尼瓦尔, 孙胜, 肖雯颖, 葛聪蕙, 唐娜, 姜涛, 王慧, 张传山, 李静. 多房棘球蚴感染小鼠腹膜腔免疫细胞迁移及其功能变化[J]. 中国寄生虫学与寄生虫病杂志, 2025, 43(1): 76-83.

DENG Bingqing, ADILAI Duolikun, LI Yinshi, ABIDAN Ainiwaer, SUN Sheng, XIAO Wenying, GE Conghui, TANG Na, JIANG Tao, WANG Hui, ZHANG Chuanshan, LI Jing. Immune cell migration and its functional changes in the peritoneal cavity of mice infected with Echinococcus multilocular[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2025, 43(1): 76-83.

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多房棘球蚴感染小鼠腹膜腔免疫细胞迁移及其功能变化

Immune cell migration and its functional changes in the peritoneal cavity of mice infected with Echinococcus multilocular

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