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Bioactive materials from berberine-treated human bone marrow mesenchymal stem cells promote alveolar bone regeneration by regulating macrophage polarization

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Abstract

Alveolar bone regeneration has been strongly linked to macrophage polarization. M1 macrophages aggravate alveolar bone loss, whereas M2 macrophages reverse this process. Berberine (BBR), a natural alkaloid isolated and refined from Chinese medicinal plants, has shown therapeutic effects in treating metabolic disorders. In this study, we first discovered that culture supernatant (CS) collected from BBR-treated human bone marrow mesenchymal stem cells (HBMSCs) ameliorated periodontal alveolar bone loss. CS from the BBR-treated HBMSCs contained bioactive materials that suppressed the M1 polarization and induced the M2 polarization of macrophages in vivo and in vitro. To clarify the underlying mechanism, the bioactive materials were applied to different animal models. We discovered macrophage colony-stimulating factor (M-CSF), which regulates macrophage polarization and promotes bone formation, a key macromolecule in the CS. Injection of pure M-CSF attenuated experimental periodontal alveolar bone loss in rats. Colony-stimulating factor 1 receptor (CSF1R) inhibitor or anti-human M-CSF (M-CSF neutralizing antibody, Nab) abolished the therapeutic effects of the CS of BBR-treated HBMSCs. Moreover, AKT phosphorylation in macrophages was activated by the CS, and the AKT activator reversed the negative effect of the CSF1R inhibitor or Nab. These results suggest that the CS of BBR-treated HBMSCs modulates macrophage polarization via the M-CSF/AKT axis. Further studies also showed that CS of BBR-treated HBMSCs accelerated bone formation and M2 polarization in rat teeth extraction sockets. Overall, our findings established an essential role of BBR-treated HBMSCs CS and this might be the first report to show that the products of BBR-treated HBMSCs have active effects on alveolar bone regeneration.

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Acknowledgement

This work was supported by the CAMS Innovation Foundation for Medical Sciences (2016-I2M-1-011), A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (2018–87), Jiangsu Province Capability Improvement Project through Science, Technology and Education-Jiangsu Provincial Research Hospital Cultivation Unit (YJXYYJSDW4) and Jiangsu Provincial Medical Innovation Center (CXZX202227).

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Authors and Affiliations

  1. Department of Oral and Maxillofacial Surgery, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, 210029, China

    Ziyue Qin, Yifei Du, Yifeng Bian, Ruyu Wang, Haoran Wang, Fanyi Guo, Hua Yuan & Yuli Wang

  2. Jiangsu Province Key Laboratory of Oral Diseases, Nanjing Medical University, Nanjing, 210029, China

    Ziyue Qin, Yifei Du, Yifeng Bian, Ruyu Wang, Haoran Wang, Fanyi Guo, Hua Yuan, Yongchu Pan, Yuli Wang & Yan Xu

  3. Jiangsu Province Engineering Research Center of Stomatological Translational Medicine, Nanjing, 210029, China

    Ziyue Qin, Yifei Du, Yifeng Bian, Ruyu Wang, Haoran Wang, Fanyi Guo, Hua Yuan, Yongchu Pan, Yuli Wang & Yan Xu

  4. State Key Laboratory of Bioactive Substances and Function of Natural Medicine, Institute of Materia Medica, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100050, China

    Yanxing Han

  5. Gusu school, Nanjing medical university, Suzhou, 215002, China

    Yixuan Zhang

  6. Key Laboratory of Cardiovascular & Cerebrovascular Medicine, Drug Target and Drug Discovery Center, School of Pharmacy, Nanjing Medical University, Nanjing, 211166, China

    Yixuan Zhang & Feng Han

  7. Department of Orthodontics, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, 210029, China

    Yongchu Pan

  8. Department of Human Anatomy, Research Centre for Bone and Stem Cells, Key Laboratory for Aging & Disease, The State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, 211166, China

    Jianliang Jin

  9. Department of Clinical Pharmacology, School of Pharmacy, Nanjing Medical University, Nanjing Jiangsu, 211166, China

    Qigang Zhou

  10. Department of Periodontology, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, 210029, China

    Yan Xu

  11. Department of Virology, Institute of Medicinal Biotechnology, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100050, China

    Jiandong Jiang

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  1. Ziyue Qin
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Bioactive materials from berberine-treated human bone marrow mesenchymal stem cells promote alveolar bone regeneration by regulating macrophage polarization

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Qin, Z., Han, Y., Du, Y. et al. Bioactive materials from berberine-treated human bone marrow mesenchymal stem cells promote alveolar bone regeneration by regulating macrophage polarization. Sci. China Life Sci. 67, 1010–1026 (2024). https://doi.org/10.1007/s11427-023-2454-9

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