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Inflammation-triggered Gli1+ stem cells engage with extracellular vesicles to prime aberrant neutrophils to exacerbate periodontal immunopathology

Cellular & Molecular Immunology volume 22, pages 371–389 (2025)Cite this article

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Abstract

Periodontitis is a prevalent and progressive detrimental disease characterized by chronic inflammation, and the immunopathological mechanisms are not yet fully understood. Mesenchymal stem cells (MSCs) play crucial roles as immunoregulators and maintain tissue homeostasis and regeneration, but their in vivo function in immunopathology and periodontal tissue deterioration is still unclear. Here, we utilized multiple transgenic mouse models to specifically mark, ablate and modulate Gli1+ cells, a critical and representative subset of MSCs in the periodontium, to explore their specific role in periodontal immunopathology. We revealed that Gli1+ cells, upon challenge with an inflammatory microenvironment, significantly induce rapid trafficking and aberrant activation of neutrophils, thus exacerbating alveolar bone destruction. Mechanistically, extracellular vesicles (EVs) released by Gli1+ cells act as crucial immune regulators in periodontal tissue, mediating the recruitment and activation of neutrophils through increased neutrophil generation of reactive oxygen species and stimulation of nuclear factor kappa-B signaling. Furthermore, we discovered that CXC motif chemokine ligand 1 (CXCL1) is exposed on the surface of EVs derived from inflammation-challenged Gli1+ cells to prime aberrant neutrophils via the CXCL1-CXC motif chemokine receptor 2 (CXCR2) axis. Importantly, specific inhibition of EV release from Gli1+ cells or pharmacological therapy with GANT61 ameliorates periodontal inflammation and alveolar bone loss. Collectively, our findings identify previously unrecognized roles of Gli1+ cells in orchestrating infiltration and promoting aberrant activation of neutrophils under inflammation, which provides pathological insights and potential therapeutic targets for periodontitis.

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Acknowledgements

This work was supported by grants from the National Key Research and Development Program of China (2022YFA1104400), the National Natural Science Foundation of China (82401201, 82370949, 82371020, 82100969, and 82100992), the Young Science and Technology Rising Star Project of Shaanxi Province (2024ZC-KJXX-122), the China Postdoctoral Science Foundation (BX20230485), the “Rapid Response” Research Projects (2023KXKT017 and 2023KXKT090), and the Shaanxi Provincial Health Research and Innovation Platform Construction Plan (2024PT-04).

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Author notes

  1. These authors contributed equally: Xin-Yue Cai, Chen-Xi Zheng, Hao Guo.

Authors and Affiliations

  1. State Key Laboratory of Oral & Maxillofacial Reconstruction and Regeneration, National Clinical Research Center for Oral Diseases, Shaanxi Key Laboratory of Stomatology, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi, 710032, China

    Xin-Yue Cai, Chen-Xi Zheng, Si-Yuan Fan, Xiao-Yao Huang, Ji Chen, Jie-Xi Liu, Yu-Ru Gao, Jia-Ning Liu, Xiao-Hui Zhang, Chao Ma, Hao Wang, Fei Fu, Peng Peng, Hao-Kun Xu, Bing-Dong Sui & Yan Jin

  2. State Key Laboratory of Oral & Maxillofacial Reconstruction and Regeneration, National Clinical Research Center for Oral Diseases, Shaanxi key Laboratory of Stomatology, Department of Preventive Dentistry, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi, 710032, China

    Xin-Yue Cai, Hao Guo, Si-Yuan Fan, Xiao-Yao Huang, An-Qi Liu, Fei Fu, Peng Peng & Kun Xuan

  3. Department of Oral Implantology, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi, 710032, China

    Ji Chen

  4. Department of Orthodontics, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi, 710032, China

    Jia-Ning Liu & Xiao-Hui Zhang

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  1. Xin-Yue Cai
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Contributions

X.Y.C., C.X.Z. and H.G. contributed equally to the experiments, data collection and analysis, and manuscript drafting. S.Y.F., X.Y.H., and J.C. contributed to the experimental performance and data collection. J.X.L., Y.R.G., A.Q.L., J.N.L. and X.H.Z. contributed to data acquisition and analysis. C.M., H.W., F.F., P.P. and H.K.X. contributed to the data analysis and interpretation. B.D.S., K.X. and Y.J. contributed to the project conception, experimental design and supervision. All the authors have read and approved the current version of the manuscript.

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Correspondence to Bing-Dong Sui, Kun Xuan or Yan Jin.

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Cai, XY., Zheng, CX., Guo, H. et al. Inflammation-triggered Gli1+ stem cells engage with extracellular vesicles to prime aberrant neutrophils to exacerbate periodontal immunopathology. Cell Mol Immunol 22, 371–389 (2025). https://doi.org/10.1038/s41423-025-01271-0

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