颌骨成骨细胞调控B细胞分化的效应研究

doi:10.3969/j.issn.1674-8115.2025.09.003

上海交通大学学报（医学版） ›› 2025, Vol. 45 ›› Issue (9): 1106-1115.doi: 10.3969/j.issn.1674-8115.2025.09.003

颌骨成骨细胞调控B细胞分化的效应研究

王歆雨¹, 陈芊烨², 孙计萍³, 鲁婷玮¹, 黄湘如¹, 孙思远¹, 刘媛琪¹, 潘厚文¹, 代庆刚⁴, 沈蕾³, 江凌勇¹()

^1.上海交通大学医学院附属第九人民医院口腔颅颌面科，上海交通大学口腔医学院，国家口腔医学中心，国家口腔疾病临床医学研究中心，上海市口腔医学重点实验室，上海市口腔医学研究所，上海 200011
^2.上海交通大学医学院附属第九人民医院口腔颌面-头颈肿瘤科，上海交通大学口腔医学院，国家口腔医学中心，国家口腔疾病临床医学研究中心，上海市口腔医学重点实验室，上海市口腔医学研究所，上海 200011
^3.上海交通大学基础医学院免疫学与微生物学系，上海市免疫学研究所，上海 200025
^4.上海交通大学医学院附属第九人民医院口腔第二门诊部，上海交通大学口腔医学院，国家口腔医学中心，国家口腔疾病临床医学研究中心，上海市口腔医学重点实验室，上海市口腔医学研究所，上海 200011

收稿日期:2025-02-19 接受日期:2025-04-29 出版日期:2025-09-28 发布日期:2025-09-30
通讯作者: 江凌勇，主任医师，博士；电子信箱：jianglingyong@sjtu.edu.cn。
基金资助:
上海交通大学医学院“双百人”项目(20221809);国家自然科学基金(82430032);国家自然科学基金(81870740);国家自然科学基金(82071083);国家自然科学基金(82271006);国家重点研发计划(2024YFC2510700);上海市科技创新行动计划国际科技合作项目/政府间国际科技合作项目(23410713600);上海市自然科学基金(21ZR1436900);上海市自然科学基金(22ZR1436700);上海交通大学医学院附属第九人民医院交叉研究基金(JYJC202116);上海交通大学医学院生物材料与再生医学交叉研究项目(2022LHB02)

Effect of jaw osteoblasts on B cell development via cytokine secretion

WANG Xinyu¹, CHEN Qianye², SUN Jiping³, LU Tingwei¹, HUANG Xiangru¹, SUN Siyuan¹, LIU Yuanqi¹, PAN Houwen¹, DAI Qinggang⁴, SHEN Lei³, JIANG Lingyong¹()

^1.Department of Oral and Maxillofacial Surgery, Shanghai Ninth People′s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of Stomatology, Shanghai 200011, China
^2.Department of Oral Maxillofacio-Head and Neck Oncology, Shanghai Ninth People′s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of Stomatology, Shanghai 200011, China
^3.Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Basic Medical Sciences; Shanghai Institute of Immunology, Shanghai 200025, China
^4.Department of 2nd Dental Centre, Shanghai Ninth People′s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of Stomatology, Shanghai 200011, China

Received:2025-02-19 Accepted:2025-04-29 Online:2025-09-28 Published:2025-09-30
Contact: JANG Lingyong, E-mail: jianglingyong@sjtu.edu.cn.
Supported by:
“Two-Hundred Talents” Program of Shanghai Jiao Tong University School of Medicine(20221809);National Natural Science Foundation of China(82430032);National Key Research and Development Program of China(2024YFC2510700);Shanghai Science and Technology Innovation Action Plan International Science and Technology Cooperation Program(23410713600);Natural Science Foundation of Shanghai(21ZR1436900);Cross-Disciplinary Research Fund of Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine(JYJC202116);Biomaterials and Regenerative Medicine Institute Cooperative Research Project, Shanghai Jiao Tong University School of Medicine(2022LHB02)

摘要/Abstract

摘要：

目的·探究小鼠颌骨成骨细胞对B细胞分化发育的调控效应及具体作用机制。方法·采用优化的酶消化法制备小鼠颌骨单细胞悬液，体外诱导分化为成骨细胞。通过实时荧光定量聚合酶链反应（RT-qPCR）、碱性磷酸酶（ALP）染色及茜素红S（ARS）染色验证成骨细胞的成骨潜能。通过免疫荧光染色观察小鼠颌骨组织中成骨细胞与B细胞的空间定位关系。采用流式细胞分选技术获得高纯度、高活性的造血谱系前体细胞。通过建立基于Transwell小室的共培养体系，探究不同浓度颌骨成骨细胞（5×10⁴、2.5×10⁵、5×10⁵个/孔）对B细胞分化（5×10⁴个/孔）发育的调节作用。通过流式细胞术及RT-qPCR检测不同浓度成骨细胞诱导下B细胞的活性与分化程度。利用RT-qPCR检测成骨细胞成骨分化过程中与B细胞发育相关的外分泌因子的表达情况。结果·成骨诱导后，ALP与ARS染色结果显示小鼠颌骨成骨细胞具有优越的成骨潜能。RT-qPCR结果显示成骨细胞内高表达成骨基因Runx2、Osx、Ocn和Alp。组织免疫荧光检测结果显示，小鼠颌骨组织内成骨细胞与B细胞在空间定位上紧密相邻。在体外共培养模型中，流式细胞分析结果显示，成骨细胞以浓度依赖性的方式促进B细胞分化与发育。RT-qPCR与细胞免疫荧光检测结果显示，成骨细胞上调B细胞发育关键基因Ebf1、Rag1、Il7r和Pax5（均P<0.001）。RT-qPCR结果显示，与B细胞发育密切相关的细胞因子Il7、Baff和Flt3l在成骨细胞成骨分化的过程中显著上调（均P<0.05）。结论·颌骨成骨细胞以浓度依赖性的方式促进B细胞分化与发育，成骨细胞可能通过分泌生长因子上调B细胞内分化关键基因的表达。

关键词: 颌骨成骨细胞, 骨免疫, B细胞, 免疫调节

Abstract:

Objective ·To investigate the regulatory effects and underlying mechanisms of mouse mandibular osteoblasts on B cell differentiation and development. Methods ·Single-cell suspensions from mouse mandibular bone were prepared using an optimized enzymatic digestion method and induced to differentiate into osteoblasts in vitro. Osteogenic potential was validated by real-time quantitative PCR (RT-qPCR), alkaline phosphatase (ALP) staining, and alizarin red S (ARS) staining. The spatial localization relationship between osteoblasts and B cells in mandibular tissues was examined via immunofluorescence staining. High-purity hematopoietic progenitor cells were isolated using fluorescence-activated cell sorting. A Transwell co-culture system was established to assess the regulatory effects of different osteoblast concentrations (5×10⁴, 2.5×10⁵, and 5×10⁵ cells/well) on B cell differentiation (5×10⁴ cells/well). Flow cytometry and RT-qPCR were employed to evaluate B cell viability and differentiation. Additionally, RT-qPCR was used to analyze the expression of osteoblast-secreted factors associated with B cell development during osteogenic differentiation. Results ·Mandibular osteoblasts exhibited robust osteogenic potential, as confirmed by ALP/ARS staining and high expression of osteogenic markers (Runx2, Osx, Ocn, and Alp) via RT-qPCR. Immunofluorescence revealed close spatial proximity between osteoblasts and B cells in mandibular tissues. In the co-culture system, osteoblasts promoted B cell differentiation in a concentration-dependent manner. RT-qPCR and immunofluorescence demonstrated that osteoblasts significantly upregulated key genes involved in B cell development (Ebf1, Rag1, Il7r, and Pax5; all P<0.001). Furthermore, osteoblast-derived factors (Il7, Baff, and Flt3l) were markedly elevated during osteogenic differentiation (all P<0.05). Conclusion ·Mandibular osteoblasts enhance B cell differentiation and development in a concentration-dependent manner, likely through secreting growth factors that upregulate critical B cell differentiation genes.

Key words: jaw osteoblasts, osteoimmunology, B lymphocytes, immunoregulation

中图分类号:

R329.2

王歆雨, 陈芊烨, 孙计萍, 鲁婷玮, 黄湘如, 孙思远, 刘媛琪, 潘厚文, 代庆刚, 沈蕾, 江凌勇. 颌骨成骨细胞调控B细胞分化的效应研究[J]. 上海交通大学学报（医学版）, 2025, 45(9): 1106-1115.

WANG Xinyu, CHEN Qianye, SUN Jiping, LU Tingwei, HUANG Xiangru, SUN Siyuan, LIU Yuanqi, PAN Houwen, DAI Qinggang, SHEN Lei, JIANG Lingyong. Effect of jaw osteoblasts on B cell development via cytokine secretion[J]. Journal of Shanghai Jiao Tong University (Medical Science), 2025, 45(9): 1106-1115.

图/表 8

表1 RT-qPCR引物序列

Tab 1 Primer sequence for RT-qPCR

Gene		Sequence (5'→3')
Alp	Forward	CGGGACTGGTACTCGGATAA
	Reserve	ATTCCACGTCGGTTCTGTTC
Runx2	Forward	GGCCGGGAATGATGAGAACTAC
	Reserve	GGACCGTCCACTGTCACTTT
Ocn	Forward	TCTCTCTGCTCACTCTGCTGGCC
	Reserve	TTTGTCAGACTCAGGGCCGC
Osx	Forward	CCTTCCCTCACTCATTTCCTGG
	Reserve	TGTTGCCTGGACCTGGTGAGAT
β-actin	Forward	ACCAACTGGGACGATATGGAGAAGA
	Reserve	TACGACCAGAGGCATACAGGGACAA
Ebf1	Forward	GCATCCAACGGAGTGGAAG
	Reserve	GATTTCCGCAGGTTAGAAGGC
Rag1	Forward	ACCCGATGAAATTCAACACCC
	Reserve	CTGGAACTACTGGAGACTGTTCT
Il7r	Forward	GCGGACGATCACTCCTTCTG
	Reserve	AGCCCCACATATTTGAAATTCCA
Pax5	Forward	CCATCAGGACAGGACATGGAG
	Reserve	GGCAAGTTCCACTATCCTTTGG
Il7	Forward	TTCTGCTGCCTGTCACATCA
	Reserve	CTTCAACTTGCGAGCAGCAC
Baff	Forward	CAGCGACACGCCGACTATAC
	Reserve	CCTCCAAGGCATTTCCTCTTTT
Flt3l	Forward	TGTGGCAGGGTCTAAGATGC
	Reserve	CTTCTAGGGCTATGGGACTCC

图1 小鼠颌骨成骨细胞分离、培养及鉴定Note： A. Expression of osteogenic markers after 7 and 14 d of osteogenic induction, assessed by cell staining. B. Transcriptional changes of osteogenic markers, Runx2, Osx, Ocn, and Alp, at different time points during osteogenic induction, detected by RT-qPCR (n = 9). C. Immunofluorescence showing the spatial localization of B cells and osteoblasts in alveolar bone. ①P<0.001, compared with the control group (Day 0).

Fig 1 Isolation, culture, and identification of murine jaw osteoblasts

图2 流式细胞术分选LSK细胞

Fig 2 Isolation of primary LSK cells by flow cytometry

图3 流式细胞术观察小鼠颌骨成骨细胞对B细胞分化和发育的影响Note： A. Representative flow cytometry plot showing the proportion of FVS- live cell. B. Representative flow cytometry plot showing the proportion of B220+ B cells.

Fig 3 Effects of murine jaw osteoblasts on B cell differentiation and development, assessed by flow cytometry

图4 B细胞活性及分化情况的定量分析Note： ①P<0.001, ②P=0.005, compared with the control group.

Fig 4 Quantitative analysis of B cell activity and differentiation

图5 RT-qPCR检测B细胞发育关键基因的表达Note： A‒D. Expression of Ebf1 (A), Rag1 (B), Il7r (C) and Pax5 (D) gene after osteogenic induction, measured by RT-qPCR (n=3). ①P<0.001, compared with the control group.

Fig 5 Expression of key genes involved in B cell development detected by RT-qPCR

图6 细胞免疫荧光检测B细胞中Pax5的表达Note： A. Representative immunofluorescence images showing Pax5 expression in B cells induced by different concentrations of osteoblasts. B. Quantitative analysis of the fluorescence intensity of Pax5 (n=3). ①P<0.001, compared with the control group.

Fig 6 Detection of Pax5 in B cells by cellular immunofluorescence

图7 RT-qPCR检测3种外分泌因子[Il7 (A)、 Baff (B)和 Flt3l (C)]的表达Note： ①P<0.001, compared with Day 0 (n=9).

Fig 7 Expression of three exocrine factors [Il7 (A), Baff (B), and Flt3l (C)] detected by RT-qPCR

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颌骨成骨细胞调控B细胞分化的效应研究

Effect of jaw osteoblasts on B cell development via cytokine secretion

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