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Cerebrospinal Fluid Pressure Reduction Induces Glia-Mediated Retinal Inflammation and Leads to Retinal Ganglion Cell Injury in Rats

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Abstract

Low intracranial pressure (LICP)–induced translaminar cribrosa pressure difference (TLCPD) elevation has been proven as a risk factor in glaucomatous neurodegeneration, whereas the underlying retinal immune features of LICP-induced retinal ganglion cells (RGC) injury remain elusive. Here, we identified the retinal immune characteristics of LICP rats, and minocycline (Mino) treatment was utilized to analyze its inhibitory role in glia-mediated retinal inflammation of LICP rats. The results showed that retrograde axonal transport was decreased in LICP rats without significant RGC loss, indicating the RGC injury was at an early stage before the morphological loss. The activation of retinal microglia and astrocytes with morphologic and M1 or A1-marker alternations was detected in TLCPD elevation rats, the activation level is more dramatic in HIOP rats than in the LICP rats (P<0.05). Besides, we detected reduced retinal tight junction protein expressions, accompanied by specific imbalance patterns of T lymphocytes in the retina of both LICP and HIOP rats (P<0.05). Further Mino treatment showed an effective inhibitory role in glia-driven inflammatory responses in LICP rats, including improving retrograde axonal transport, inhibiting retinal glial activation and proinflammatory subtype polarization, and alleviating the blood-retina barrier compromise. This study identified the glia-mediated retinal inflammation features triggered by LICP stimulus, and Mino application exhibited an effective role in the inhibition of retinal glia-mediated inflammation in LICP-induced TLCPD elevation rats.

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Data Availability

The datasets generated during and/or analyzed during the current study are not publicly available due to the confidentiality of original data but are available from the corresponding author on reasonable request.

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Acknowledgements

The contributions from every author in this study are greatly appreciated.

Funding

This work was supported by National Natural Science Foundation of China (81730027, 82130029), Beijing Postdoctoral Research Foundation (2021), and Beijing Natural Science Foundation (L212036).

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Author notes

  1. Ningli Wang and Jingxue Zhang contributed equally as the corresponding author.

Authors and Affiliations

  1. Beijing Institute of Ophthalmology, Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, Beijing Ophthalmology & Visual Sciences Key Laboratory, Beijing, 100730, China

    Ying Cheng, Danting Lin, Shen Wu, Qian Liu, Xuejing Yan, Tianmin Ren, Jingxue Zhang & Ningli Wang

  2. Department of Ophthalmology, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, 710061, China

    Ying Cheng

  3. Beijing Institute of Brain Disorders, Collaborative Innovation Center for Brain Disorders, Capital Medical University, Beijing, 100069, China

    Jingxue Zhang & Ningli Wang

  4. Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Capital Medical University, Beijing, 100069, China

    Jingxue Zhang & Ningli Wang

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Contributions

Ying Cheng designed and conducted the experiments and data analysis, and wrote the paper. Danting Lin and Shen Wu conducted the experiments. Qian Liu and Xuejing Yan helped design the experiments. Tianmin Ren helped analyze the data. Jingxue Zhang and Ningli Wang revised the paper and provided the materials. All authors contributed to the manuscript revision, read, and approved the submitted version.

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Cheng, Y., Lin, D., Wu, S. et al. Cerebrospinal Fluid Pressure Reduction Induces Glia-Mediated Retinal Inflammation and Leads to Retinal Ganglion Cell Injury in Rats. Mol Neurobiol 60, 5770–5788 (2023). https://doi.org/10.1007/s12035-023-03430-8

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