芪黄健脾滋肾颗粒通过AIM2/Blimp-1/Bcl-6轴抑制B细胞分化改善MRL/lpr小鼠肾损害

doi:10.12122/j.issn.1673-4254.2025.11.02

南方医科大学学报 ›› 2025, Vol. 45 ›› Issue (11): 2297-2308.doi: 10.12122/j.issn.1673-4254.2025.11.02

芪黄健脾滋肾颗粒通过AIM2/Blimp-1/Bcl-6轴抑制B细胞分化改善MRL/lpr小鼠肾损害

程丽丽¹(), 汤忠富¹, 李明¹^,², 陈君洁³, 尚双双¹, 刘思娣¹, 黄传兵¹^,²()

^1.安徽中医药大学第一附属医院风湿科，安徽合肥 230012
^2.新安医学与中医药现代化研究所，安徽合肥 230031
^3.安徽中医药大学中医学院，安徽合肥 230031

收稿日期:2025-06-13 出版日期:2025-11-20 发布日期:2025-11-28
通讯作者: 黄传兵 E-mail:3265544980@qq.com;chuanbinh@163.com
作者简介:程丽丽，在读博士研究生，医师，E-mail: 3265544980@qq.com
基金资助:
国家自然科学基金(82574970);安徽省临床医学研究转化专项项目(202304295107020114);安徽省临床医学研究转化专项项目(202304295107020115);大健康研究院新安医学与中医药现代化研究所专项(2023CXMMTCM015);大健康研究院新安医学与中医药现代化研究所专项(2023CXMMTCM004);安徽省研究生质量工程研究生创新创业实践项目(2024cxcysj121);安徽省高等学校科学重点研究项目(2024AH050957)

Qihuang Jianpi Zishen Granules improves renal damage in MRL/lpr mice by inhibiting B cell differentiation via the AIM2/Blimp-1/Bcl-6 axis

Lili CHENG¹(), Zhongfu TANG¹, Ming LI¹^,², Junjie CHEN³, Shuangshuang SHANG¹, Sidi LIU¹, Chuanbing HUANG¹^,²()

^1.Department of Rheumatology, First Affiliated Hospital of Anhui University of Chinese Medicine, Hefei 230012, China
^2.Institute of Xin'an Medicine and Modernization of Traditional Chinese Medicine, Hefei 230031, China
^3.School of Traditional Chinese Medicine, Anhui University of Chinese Medicine, Hefei 230031, China

Received:2025-06-13 Online:2025-11-20 Published:2025-11-28
Contact: Chuanbing HUANG E-mail:3265544980@qq.com;chuanbinh@163.com
Supported by:
National Natural Science Foundation of China(82574970)

摘要/Abstract

摘要：

目的分析芪黄健脾滋肾颗粒（QJZ）抑制MRL/lpr 小鼠肾B细胞分化的疗效并探讨其潜在机制。方法 30只8周龄雌性MRL/lpr小鼠随机分为5组：模型组、QJZ组、泼尼松（Pred）组、QJZ+Pred组、黑素瘤缺乏因子2（AIM2）抑制剂组，6只/组，8周龄雌性C57BL/6小鼠为正常组，各组按相应方法连续处理8周。采用生化仪检测尿液尿总蛋白/尿肌酐（TPCR）、尿白蛋白/尿肌酐（ACR）及血清中肌酐（Scr）、尿素氮（BUN）水平；组织病理学染色（HE、Masson、过碘酸-雪夫）观察小鼠肾脏病理结构的变化；电镜观察肾脏超微结构变化；酶联免疫吸附测定抗dsDNA、细胞因子、趋化因子的变化；免疫组化观察肾脏中补体C3、C4沉积情况；免疫荧光观察肾脏中AIM2、CD19、CD27、CD138表达情况；流式细胞术分析脾脏 B 淋巴细胞亚群的变化，Western blotting检测B淋巴细胞诱导成熟蛋白1（Blimp-1）/B细胞淋巴瘤6蛋白（Bcl-6）信号轴的影响。结果 QJZ改善了MRL/lpr小鼠的Cr、BUN、TPCR、ACR水平（P<0.05），并改善肾脏的病理变化，降低抗双链DNA抗体（ds-DNA）、B细胞活化因子（BAFF）、白细胞介素（IL）-21、CXC 趋化因子受体（CXCR）-12、CXCR-19、C3、C4表达，提高IL-10水平（P<0.05）；Western blotting结果显示QJZ降低B细胞关键转录蛋白Blimp-1、X-box结合蛋白1（XBP-1）的表达，升高Bcl-6、配对盒5（PAX5）的表达（P<0.05）；流式细胞术结果显示QJZ影响B细胞的分化，免疫荧光结果显示QJZ 可降低AIM2、CD27、CD138、CD69的表达。AIM2抑制可降低B细胞关键转录蛋白Blimp-1、XBP-1的表达，升高Bcl-6、PAX5的表达（P<0.05），抑制B细胞的分化，减少IgG生成，减少C3、C4的沉积，改善肾脏的病理变化。结论 QJZ可能通过抑制AIM2/Blimp-1/Bcl-6信号通路影响B细胞分化抑制系统性红斑狼疮肾损害。

关键词: 芪黄健脾滋肾颗粒, 系统性红斑狼疮, 肾损害, B细胞, AIM2/Blimp-1/Bcl-6

Abstract:

Objective To investigate the efficacy of Qihuang Jianpi Zishen Granules (QJZ) for inhibiting renal B cell differentiation in MRL/lpr mice and explore its underlying mechanism. Methods Thirty 8-week-old female MRL/lpr mice were randomly divided into model group, QJZ group, prednisone (Pred) group, QJZ+Pred group, and AIM2 inhibitor group (n=6), with 6 8-week-old female C57BL/6 mice as the normal control group. After treatments with normal saline, QJZ, Pred, or AIM2 inhibitor for 8 weeks, the mice were examined for urinary total protein-to-creatinine ratio (TPCR) and albumin-to-creatinine ratio (ACR), serum creatinine (Cr) and blood urea nitrogen (BUN) levels, and renal histopathology (with HE, Masson, and PAS staining) and ultrastructural changes (with electron microscopy). ELISA, immunohistochemistry, immunofluorescence staining and flow cytometry were used to detect blood levels of anti-dsDNA antibodies, cytokines and chemokines, renal deposition of complement components C3 and C4, renal expressions of AIM2, CD19, CD27 and CD138, and changes in splenic B lymphocyte subsets. The effect of QJZ on the AIM2/Blimp-1/Bcl-6 signaling axis was examined using Western blotting. Results QJZ treatment significantly improved Cr, BUN, TPCR and ACR in MRL/lpr mice, ameliorated renal pathologies, reduced the expressions of ds-DNA, BAFF, IL-21, CXCL12, CXCL13, C3 and C4, and increased IL-10 levels. QJZ significantly downregulated renal expressions of the key B-cell transcription factors Blimp-1 and XBP-1, upregulated Bcl-6 and PAX5 expressions, inhibited B-cell differentiation, and lowered the expressions of AIM2, CD27, CD138 and CD69. Inhibition of AIM2 similarly reduced renal Blimp-1 and XBP-1 expressions, increased Bcl-6 and PAX5 levels, suppressed B-cell differentiation, decreased IgG production, reduced C3 and C4 deposition, and alleviated renal pathology in MRL/lpr mice. Conclusion QJZ inhibits B cell differentiation and alleviates renal damage in systemic lupus erythematosus possibly by suppressing the AIM2/Blimp-1/Bcl-6 signaling pathway.

Key words: Qihuang Jianpi Zishen Granules, systemic lupus erythematosus, renal damage, B cells, AIM2/Blimp-1/Bcl-6

程丽丽, 汤忠富, 李明, 陈君洁, 尚双双, 刘思娣, 黄传兵. 芪黄健脾滋肾颗粒通过AIM2/Blimp-1/Bcl-6轴抑制B细胞分化改善MRL/lpr小鼠肾损害[J]. 南方医科大学学报, 2025, 45(11): 2297-2308.

Lili CHENG, Zhongfu TANG, Ming LI, Junjie CHEN, Shuangshuang SHANG, Sidi LIU, Chuanbing HUANG. Qihuang Jianpi Zishen Granules improves renal damage in MRL/lpr mice by inhibiting B cell differentiation via the AIM2/Blimp-1/Bcl-6 axis[J]. Journal of Southern Medical University, 2025, 45(11): 2297-2308.

图/表 10

图1 各组MRL/lpr小鼠肾功能的比较

Fig.1 Comparison of renal function among different groups of MRL/lpr mice. A: Expression levels of ACR in MRL/lpr mice in each group. B: Expression levels of TPCR in each group. C: Expression levels of Scr in each group. D: Expression levels of BUN in each group. *P<0.05, **P<0.01.

图2 各组MRL/lpr小鼠ds-DNA抗体、细胞因子、趋化因子水平的比较

Fig.2 Comparison of ds-DNA antibody, cytokine and chemokine levels in MRL/lpr mice in each group. A: Levels of ds-DNA in each group. B: Levels of IL-10 in each group. C: Levels of BAFF in each group. D: Levels of IL-21 in each group. E: Levels of CXCR-12 in each group. F: Levels of CXCR-19 in each group. **P<0.01.

图3 QJZ对MRL/lpr狼疮鼠肾脏病理的影响

Fig.3 Effect of QJZ on renal pathology in MRL/lpr lupus mice. A: Results of HE, PAS and Masson staining of the kidneys in each group (Scale bar=50 μm). B: Comparison of pathological AI scores of the kidneys in each group. C: Comparison of pathological CI scores of the kidneys in each group. *P<0.05, **P<0.01.

图4 各组小鼠肾小球透射电镜下超微结构的比较

Fig.4 Comparison of ultrastructural changes in renal glomeruli in each group under transmission electron microscopy (Scale bar=2 μm).

图5 各组MRL/lpr小鼠肾脏中C3、C4沉积水平的比较

Fig.5 Comparison of C3 and C4 deposition levels in the kidneys of MRL/lpr mice among the groups. A: Immunohistochemistry for detecting expressions of C3 and C4 in the kidneys in each group (×100). B: Average fluorescence intensity of C3 in the kidneys in each group. C: Average fluorescence intensity of C4 in each group. *P<0.05, **P<0.01.

图6 各组B细胞分化关键转录蛋白表达水平比较

Fig.6 Comparison of expression levels of key transcriptional proteins involved in B-cell differentiation in each group. A: Relative protein expression levels of Blimp-1 in each group. B: Relative protein expression levels of Bcl-6 in each group. C: Relative protein expression levels of XBP-1 in each group. D: Relative protein expression levels of PAX-5 in each group. E: Protein bands in Western blotting in each group. **P<0.01.

图7 各组MRL/lpr 小鼠脾脏组织脾脏指数的比较

Fig.7 Spleen index of the spleen tissues in each group of MRL/lpr mice. *P<0.05, **P<0.01.

图8 各组MRL/lpr小鼠B细胞的比较

Fig.8 Percentages of B cells in each group of MRL/lpr mice.

图9 各组MRL/lpr 小鼠肾组织CD19、CD138、IgG、AIM2表达的比较

Fig.9 Expression levels of CD19, CD138, IgG and AIM2 in the renal tissues of MRL/lpr mice in each group (Immunofluorescence staining; Scale bar=50 μm). A: CD19 expression levels in each group. B: CD138 expression levels in each group. C: IgG expression levels in each group. D: AIM2 expression levels in each group.

图10 AIM2抑制剂对MRL/lpr狼疮鼠肾损害的影响

Fig.10 Effect of AIM2 inhibitor on renal damage in MRL/lpr mice. A: Relative protein expression levels of Blimp-1 in each group. B: Relative protein expression levels of Bcl-6 in each group. C: Relative protein expression levels of PAX-5 in each group. D: Relative protein expression levels of XBP-1 in each group. E: Western blotting bands in each group. F: Results of HE, Masson, and PAS staining in each group (×200). G: Expression of IgG in each group (×200). H: Level of B cells in each group. I: Expression of C3 and C4 in each group (×200). **P<0.01.

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芪黄健脾滋肾颗粒通过AIM2/Blimp-1/Bcl-6轴抑制B细胞分化改善MRL/lpr小鼠肾损害

Qihuang Jianpi Zishen Granules improves renal damage in MRL/lpr mice by inhibiting B cell differentiation via the AIM2/Blimp-1/Bcl-6 axis

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[3]	李云飞, 庞利君, 束龙武, 李明, 黄传兵. 芪黄健脾滋肾颗粒可改善小鼠系统性红斑狼疮血小板减少：基于Ca²⁺/CaMKK2/AMPK/mTOR信号通路介导的自噬[J]. 南方医科大学学报, 2024, 44(12): 2327-2334.
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