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E. coli LPS/TLR4/NF-κB Signaling Pathway Regulates Th17/Treg Balance Mediating Inflammatory Responses in Oral Lichen Planus

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Abstract

Oral lichen planus (OLP) is a chronic inflammatory autoimmune disease mediated by T cells. The imbalance of microflora has potential impacts on the onset and development of OLP, but the mechanism is still unclear. Here, we investigated the effects of Escherichia coli (E. coli) lipopolysaccharide (LPS) simulating the microbial enrichment state of OLP on T cell immune functions in vitro. Effect of E. coli LPS on the viability of T cell using CCK8 assay. After E. coli LPS pretreatment, the expression of the toll-like receptor 4 (TLR4), nuclear factor-kappa B p65 (NF-κB p65), cytokines, retinoic acid-related orphan receptor γt (RORγt), and forkhead box p3 (Foxp3) in the peripheral blood of OLP patients and normal controls (NC) were assessed using quantitative RT-PCR (qRT-PCR), western blot, and enzyme-linked immunosorbent assay (ELISA). Finally, Th17 and Treg cells were detected by flow cytometry. We found that the TLR4/NF-κB pathway was activated and the expression of interleukin (IL)-6 and IL-17 was increased in both groups after E. coli LPS stimulation. CC chemokine ligand (CCL)20 and CC chemokine receptor (CCR)4 expression was increased in OLP after E. coli LPS treatment, while no difference was found in CCR6 and CCL17 expression of both groups. Moreover, E. coli LPS treatment enhanced the proportion of Th17 cells, Th17/Treg ratio, and RORγt/Foxp3 ratio in OLP. In conclusion, E. coli LPS regulated Th17/Treg balance to mediate the inflammatory responses of OLP through the TLR4/NF-κB pathway in vitro, indicating that oral microbiota dysbiosis affected the chronic inflammatory state of OLP.

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DATA AVAILABILITY

The datasets that support the findings of this study are available from the corresponding author upon reasonable request.

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ACKNOWLEDGEMENTS

The authors would like to acknowledge the Core Facility of the First Affiliated Hospital of Nanjing Medical University for technical support in flow cytometry experiments.

Funding

This project was supported by the National Natural Science Foundation of China (81970941), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD, 2018–87), and the Critical Research and Development Project of Jiangsu Province (Grant Nos. BE2021723).

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  1. Mengna Zhang and Linglin Wang contributed equally to this work.

Authors and Affiliations

  1. Department of Oral Mucosal Diseases, The Affiliated Stomatological Hospital of Nanjing Medical University, Nanjing, China

    Mengna Zhang, Linglin Wang, Chenyu Zhou, Jia Wang, Juehua Cheng & Yuan Fan

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

    Mengna Zhang, Chenyu Zhou, Jia Wang, Juehua Cheng & Yuan Fan

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

    Mengna Zhang, Chenyu Zhou, Jia Wang, Juehua Cheng & Yuan Fan

  4. Affiliated Changzhou Children’s Hospital of Nantong University, Changzhou, China

    Linglin Wang

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Contributions

All authors contributed to the study conception and design. Material preparation and data collection were performed by Mengna Zhang and Linglin Wang. Data analyses were performed by Mengna Zhang, Linglin Wang, Chenyu Zhou, Jia Wang, and Juehua Cheng. The first draft of the manuscript was written by Mengna Zhang. YuanFan designed the experiments and reviewed the manuscript, and all the authors read and approved the final manuscript.

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Correspondence to Yuan Fan.

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This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Nanjing Medical University (No. 2019–281).

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Zhang, M., Wang, L., Zhou, C. et al. E. coli LPS/TLR4/NF-κB Signaling Pathway Regulates Th17/Treg Balance Mediating Inflammatory Responses in Oral Lichen Planus. Inflammation 46, 1077–1090 (2023). https://doi.org/10.1007/s10753-023-01793-7

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