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Prevotella histicola Prevented Particle-Induced Osteolysis via Gut Microbiota-Dependent Modulation of Inflammation in Ti-Treated Mice

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Abstract

Wear particles generated from total joint replacements induce chronic osteolysis mediated by inflammatory upregulation, which leads to implant failure. Recent studies have suggested an important role of the gut microbiota in modulating the host’s metabolism and immune system, leading to alterations in bone mass. Following gavage with P. histicola, micro-CT and HE staining revealed that osteolysis was significantly reduced in titanium (Ti)-treated mice. Immunofluorescence analysis revealed an increased macrophage (M)1/M2 ratio in the guts of Ti-treated mice, which decreased when P. histicola was added. P. histicola was also found to upregulate the tight junction proteins ZO-1, occludin, claudin-1, and MUC2 in the gut, reduce the levels of inflammatory factors IL-1β, IL-6, IL-8, and TNF-α, primarily in the ileum and colon, and decrease the expression of IL-1β and TNF-α and increase the level of IL-10 in the serum and cranium. Furthermore, P. histicola treatment resulted in a significant downregulation of CTX-1, RANKL, and RANKL/OPG. These findings demonstrate that P. histicola significantly mitigates osteolysis in Ti-treated mice by improving intestinal microbiota that repairs intestinal leakage and reduces systemic and local inflammation which in turn inhibits RANKL expression for bone resorption. P. histicola treatment may thus be therapeutically beneficial for particle-induced osteolysis.

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Data Availability

The original contributions presented in the study are publicly available. This data can be found here: https://www.jianguoyun.com/p/DYtOBHgQh8LpCRizwN8EIAA.

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Funding

This work was supported by the Basic Public Welfare Research Project of Zhejiang Natural Science Foundation of China (LGF19H070004), and the Wenzhou Science and Technology Bureau (Y20210418).

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Authors and Affiliations

  1. Clinical Research Unit, The Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical University, Wenzhou, 325000, Zhejiang, China

    Furong Huang & Ting Li

  2. Key Laboratory of Intelligent Critical Care and Life Support Research of Zhejiang Province, Wenzhou, 325000, China

    Furong Huang & Hao Pan

  3. Department of Orthopaedics, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, 325000, China

    Hao Pan, Zenglin Tan, Lei Chen & Yangbo Liu

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  1. Furong Huang
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  2. Hao Pan
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  6. Yangbo Liu
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Contributions

YL was responsible for the study concept and design. FH and HP collected the data. ZT analyzed and interpreted the data. LC and TL drafted the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yangbo Liu.

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The original contributions presented in the study are publicly available. This data can be found here: https://www.jianguoyun.com/p/DYtOBHgQh8LpCRizwN8EIAA

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Huang, F., Pan, H., Tan, Z. et al. Prevotella histicola Prevented Particle-Induced Osteolysis via Gut Microbiota-Dependent Modulation of Inflammation in Ti-Treated Mice. Probiotics & Antimicro. Prot. 16, 383–393 (2024). https://doi.org/10.1007/s12602-023-10057-7

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