MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1

Abstract Spinal cord injury (SCI) is a debilitating condition characterized by significant sensory, motor, and autonomic dysfunctions, leading to severe physical, psychological, and financial burdens. The current therapeutic approaches for SCI show limited effectiveness, highlighting the urgent need...

Full description

Saved in:
Bibliographic Details
Main Authors: Huandong Liu, Chong Liang, Hongfei Liu, Ping Liang, Huilin Cheng
Format: Article
Language:English
Published: BMC 2024-11-01
Series:European Journal of Medical Research
Subjects:
Online Access:https://doi.org/10.1186/s40001-024-02133-7
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846158677003730944
author Huandong Liu
Chong Liang
Hongfei Liu
Ping Liang
Huilin Cheng
author_facet Huandong Liu
Chong Liang
Hongfei Liu
Ping Liang
Huilin Cheng
author_sort Huandong Liu
collection DOAJ
description Abstract Spinal cord injury (SCI) is a debilitating condition characterized by significant sensory, motor, and autonomic dysfunctions, leading to severe physical, psychological, and financial burdens. The current therapeutic approaches for SCI show limited effectiveness, highlighting the urgent need for innovative treatments. MicroRNAs (miRNAs) like miR-10b-5p are known to play pivotal roles in gene expression regulation and have been implicated in various neurodegenerative diseases, including SCI. Polypyrimidine tract binding protein 1 (PTBP1) has also been associated with neural injury responses and recovery. This study aims to explore the interaction between miR-10b-5p and PTBP1 in the context of SCI, hypothesizing that miR-10b-5p regulates PTBP1 to influence SCI pathogenesis and recovery using a rat model of SCI and lipopolysaccharide (LPS)-induced PC12 cells. Reverse transcription-quantitative polymerase chain reaction (RT-qPCR) was performed to measure miR-10b-5p levels, revealing its low expression in SCI rats. We then assessed neurological function, histopathological changes, and spinal cord water content. We found that administering the agomiR-10b-5p significantly improved neurological function and decreased the spinal cord water content and normal motor neuron loss in SCI rats. Additionally, we explored the functions of miR-10b-5p in LPS-treated PC12 cells. Our results showed that miR-10b-5p repressed LPS-stimulated apoptosis, inflammation, and oxidative stress in PC12 cells. PTBP1 was predicted as a potential target gene of miR-10b-5p using the TargetScan database. Pulldown and luciferase reporter assays further demonstrated that miR-10b-5p binds to the 3’ untranslated region (UTR) of PTBP1. RT-qPCR revealed that miR-10b-5p negatively modulated PTBP1 expression both in vivo and in vitro. Furthermore, rescue assays indicated that miR-10b-5p alleviated SCI in rats and LPS-triggered injury in PC12 cells by downregulating PTBP1. We also investigated the regulation of miR-10b-5p and PTBP1 on the transforming growth factor-beta 1 (TGF-β1)/small mother against decapentaplegic (Smad3) pathway. We found that miR-10b-5p targeted PTBP1 to repress TGF-β1 decay and facilitated TGF-β1/Smad3 pathway activation. In conclusion, our results demonstrate that miR-10b-5p alleviates SCI by repressing TGF-β1 decay and inducing TGF-β1/Smad3 pathway activation through PTBP1 downregulation. This study provides novel insights into potential targeted therapy plans for SCI.
format Article
id doaj-art-8b531b84a6934e8daf02877e89591381
institution Kabale University
issn 2047-783X
language English
publishDate 2024-11-01
publisher BMC
record_format Article
series European Journal of Medical Research
spelling doaj-art-8b531b84a6934e8daf02877e895913812024-11-24T12:16:17ZengBMCEuropean Journal of Medical Research2047-783X2024-11-0129111410.1186/s40001-024-02133-7MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1Huandong Liu0Chong Liang1Hongfei Liu2Ping Liang3Huilin Cheng4Department of Neurosurgery, School of Medicine, Zhongda Hospital, Southeast UniversityDepartment of Neurosurgery, Jinling Hospital, Nanjing University School of MedicineDepartment of Encephalopathy, Nanjing Hospital of Chinese Medicine Affiliated to Nanjing University of Chinese MedicineDepartment of Neurosurgery, School of Medicine, Zhongda Hospital, Southeast UniversityDepartment of Neurosurgery, School of Medicine, Zhongda Hospital, Southeast UniversityAbstract Spinal cord injury (SCI) is a debilitating condition characterized by significant sensory, motor, and autonomic dysfunctions, leading to severe physical, psychological, and financial burdens. The current therapeutic approaches for SCI show limited effectiveness, highlighting the urgent need for innovative treatments. MicroRNAs (miRNAs) like miR-10b-5p are known to play pivotal roles in gene expression regulation and have been implicated in various neurodegenerative diseases, including SCI. Polypyrimidine tract binding protein 1 (PTBP1) has also been associated with neural injury responses and recovery. This study aims to explore the interaction between miR-10b-5p and PTBP1 in the context of SCI, hypothesizing that miR-10b-5p regulates PTBP1 to influence SCI pathogenesis and recovery using a rat model of SCI and lipopolysaccharide (LPS)-induced PC12 cells. Reverse transcription-quantitative polymerase chain reaction (RT-qPCR) was performed to measure miR-10b-5p levels, revealing its low expression in SCI rats. We then assessed neurological function, histopathological changes, and spinal cord water content. We found that administering the agomiR-10b-5p significantly improved neurological function and decreased the spinal cord water content and normal motor neuron loss in SCI rats. Additionally, we explored the functions of miR-10b-5p in LPS-treated PC12 cells. Our results showed that miR-10b-5p repressed LPS-stimulated apoptosis, inflammation, and oxidative stress in PC12 cells. PTBP1 was predicted as a potential target gene of miR-10b-5p using the TargetScan database. Pulldown and luciferase reporter assays further demonstrated that miR-10b-5p binds to the 3’ untranslated region (UTR) of PTBP1. RT-qPCR revealed that miR-10b-5p negatively modulated PTBP1 expression both in vivo and in vitro. Furthermore, rescue assays indicated that miR-10b-5p alleviated SCI in rats and LPS-triggered injury in PC12 cells by downregulating PTBP1. We also investigated the regulation of miR-10b-5p and PTBP1 on the transforming growth factor-beta 1 (TGF-β1)/small mother against decapentaplegic (Smad3) pathway. We found that miR-10b-5p targeted PTBP1 to repress TGF-β1 decay and facilitated TGF-β1/Smad3 pathway activation. In conclusion, our results demonstrate that miR-10b-5p alleviates SCI by repressing TGF-β1 decay and inducing TGF-β1/Smad3 pathway activation through PTBP1 downregulation. This study provides novel insights into potential targeted therapy plans for SCI.https://doi.org/10.1186/s40001-024-02133-7Spinal cord injuryMicroRNAsMolecular targeted therapy
spellingShingle Huandong Liu
Chong Liang
Hongfei Liu
Ping Liang
Huilin Cheng
MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1
European Journal of Medical Research
Spinal cord injury
MicroRNAs
Molecular targeted therapy
title MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1
title_full MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1
title_fullStr MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1
title_full_unstemmed MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1
title_short MiR-10b-5p attenuates spinal cord injury and alleviates LPS-induced PC12 cells injury by inhibiting TGF-β1 decay and activating TGF-β1/Smad3 pathway through PTBP1
title_sort mir 10b 5p attenuates spinal cord injury and alleviates lps induced pc12 cells injury by inhibiting tgf β1 decay and activating tgf β1 smad3 pathway through ptbp1
topic Spinal cord injury
MicroRNAs
Molecular targeted therapy
url https://doi.org/10.1186/s40001-024-02133-7
work_keys_str_mv AT huandongliu mir10b5pattenuatesspinalcordinjuryandalleviateslpsinducedpc12cellsinjurybyinhibitingtgfb1decayandactivatingtgfb1smad3pathwaythroughptbp1
AT chongliang mir10b5pattenuatesspinalcordinjuryandalleviateslpsinducedpc12cellsinjurybyinhibitingtgfb1decayandactivatingtgfb1smad3pathwaythroughptbp1
AT hongfeiliu mir10b5pattenuatesspinalcordinjuryandalleviateslpsinducedpc12cellsinjurybyinhibitingtgfb1decayandactivatingtgfb1smad3pathwaythroughptbp1
AT pingliang mir10b5pattenuatesspinalcordinjuryandalleviateslpsinducedpc12cellsinjurybyinhibitingtgfb1decayandactivatingtgfb1smad3pathwaythroughptbp1
AT huilincheng mir10b5pattenuatesspinalcordinjuryandalleviateslpsinducedpc12cellsinjurybyinhibitingtgfb1decayandactivatingtgfb1smad3pathwaythroughptbp1