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M2 macrophage-derived exosomes carry miR-142-3p to restore the differentiation balance of irradiated BMMSCs by targeting TGF-β1

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Abstract

Radiotherapy is essential to cancer treatment, while it inevitably injures surrounding normal tissues, and bone tissue is one of the most common sites prone to irradiation. Bone marrow mesenchymal stem cells (BMMSCs) are sensitive to irradiation and the irradiated dysfunction of BMMSCs may be closely related to irradiation-induced bone damage. Macropahges play important role in regulating stem cell function, bone metabolic balance and irradiation response, but the effects of macrophages on irradiated BMMSCs are still unclear. This study aimed to investigate the role of macrophages and macrophage-derived exosomes in restoring irradiated BMMSCs function. The effects of macrophage conditioned medium (CM) and macrophage-derived exosomes on osteogenic and fibrogenic differentiation capacities of irradiated BMMSCs were detected. The key microribonucleic acids (miRNAs) and targeted proteins in exosomes were also determined. The results showed that irradiation significantly inhibited the proliferation of BMMSCs, and caused differentiation imbalance of BMMSCs, with decreased osteogenic differentiation and increased fibrogenic differentiation. M2 macrophage-derived exosomes (M2D-exos) inhibited the fibrogenic differentiation and promoted the osteogenic differentiation of irradiated BMMSCs. We identified that miR-142-3p was significantly overexpressed in M2D-exos and irradiated BMMSCs treated with M2D-exos. After inhibition of miR-142-3p in M2 macrophage, the effects of M2D-exos on irradiated BMMSCs differentiation were eliminated. Furthermore, transforming growth factor beta 1 (TGF-β1), as a direct target of miR-142-3p, was significantly decreased in irradiated BMMSCs treated with M2D-exos. This study indicated that M2D-exos could carry miR-142-3p to restore the differentiation balance of irradiated BMMSCs by targeting TGF-β1. These findings pave a new way for promising and cell-free method to treat irradiation-induced bone damage.

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Data availability

The data that support the findings of this study are available from the corresponding author, LT, as well as CZ, upon reasonable request.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (81903249) and Shaanxi Provincial Natural Science Basic Research Program project (2022JZ-50).

Funding

This work was supported by the National Natural Science Foundation of China (81903249) and Shaanxi Provincial Natural Science Basic Research Program project (2022JZ-50).

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  1. Chong Huang and Lu Zhao have contributed equally as first authors of this manuscript.

Authors and Affiliations

  1. Key Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, 229 Taibai North Road, 710069, Xi’an, People’s Republic of China

    Chong Huang

  2. State Key Laboratory of Military Stomatology, National Clinical Research Center for Oral Diseases, Shaanxi Clinical Research Center for Oral Diseases, Department of Oral and Maxillofacial Surgery, School of Stomatology, The Fourth Military Medical University, 145 West Changle Road, Xi’an, 710032, People’s Republic of China

    Lu Zhao, Zihao Tang, Li Jing, Kai Guo, Lei Tian & Chunlin Zong

  3. School of Stomatology, Jiamusi University, 522 Hongqi Street, Jiamusi, 154000, People’s Republic of China

    Yun Xiao

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Contributions

All authors contributed to the general study conception and design. The material preparation and data collection were performed by CH, LZ, YX, ZT, LJ and KG. The data analysis and visualization were performed by Chong Huang, Lu Zhao, and CZ. The first draft of the manuscript was written by CH and LZ. The manuscript was revised by LT and CZ. All authors commented on previous versions of the manuscript, gave valuable suggestions for corrections, and approved the final manuscript. LT and CZ supervised the research project.

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Correspondence to Lei Tian or Chunlin Zong.

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All animal research protocols in this study were approved by the Welfare and Ethics Committee of Laboratory Animal Center of the Fourth Military Medical University (Approval number: IACUC-20210971).

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Huang, C., Zhao, L., Xiao, Y. et al. M2 macrophage-derived exosomes carry miR-142-3p to restore the differentiation balance of irradiated BMMSCs by targeting TGF-β1. Mol Cell Biochem 479, 993–1010 (2024). https://doi.org/10.1007/s11010-023-04775-3

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