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Transcriptome Profiling of miRNA-mRNA Interactions and Associated Mechanisms in Chemotherapy-Induced Neuropathic Pain

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Abstract

Chemotherapy-induced neuropathic pain (CINP) is a dose-limiting adverse event affecting 40% of chemotherapy patients. MiRNA-mRNA interaction plays an important role in various processes. However, detailed profiling of miRNA-mRNA interactions in CINP remains unclear. Here, a rat-based CINP model was established using paclitaxel, followed by nociceptive behavioral tests related to mechanical allodynia, thermal hyperalgesia, and cold allodynia. The landscape of miRNA-mRNA interaction in the spinal dorsal horn was investigated through mRNA transcriptomics and small RNA sequencing. Under CINP condition, 86 differentially expressed mRNAs and 56 miRNAs were identified. Gene Set Enrichment Analysis (GSEA), Gene Ontology (GO), and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses indicated the activity of Odorant binding, postsynaptic specialization and synaptic density, extracellular matrix, mitochondrial matrix, retrograde endocannabinoid signaling, and GTPase activity. Protein–protein interaction (PPI), networks of circRNA-miRNA-mRNA, lncRNA-miRNA-mRNA, and TF-genes were demonstrated. We next explored the immune infiltration microenvironment and found a higher infiltration abundance of Th17 and a lower abundance of MDSC in CINP. RT-qPCR and dual-luciferase assays were used to verify the sequencing results, and single-cell analysis based on the SekSeeq database was conducted. Combined with bioinformatics analyses and experimental validations, Mpz, a protein-coding gene specifically expressed in Schwann cells, was found critical in maintaining CINP under miRNA regulation. Therefore, these data highlight the expression patterns of miRNA-mRNA, and the underlying mechanism in the spinal dorsal horn under CINP condition, and Mpz may serve as a promising therapeutic target for patients with CINP.

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Data Availability

Code and data that support the findings of this study are available from the corresponding author upon reasonable request.

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Funding

This study was supported by the National Natural Science Foundation of China (81870878, 8217102207, 82101348), and Guangdong Basic and Applied Basic Research Foundation (2019B151502010, 2022B1515120026, 2020A1515110087).

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Author notes

  1. Xiaohua Yang, Xiqiang Huang, and Weicheng Lu contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Oncology in Southern China, Department of Anesthesiology, Sun Yat-sen University Cancer Center, Guangzhou, 510060, Guangdong, China

    Xiaohua Yang, Weicheng Lu, Fang Yan, Yaqi Ye, Xiaole Tang, Weian Zeng, Jingxiu Huang & Jingdun Xie

  2. Department of Anesthesiology, Zhongshan People’s Hospital, Zhongshan, 528400, Guangdong, China

    Xiqiang Huang

  3. Department of Human Anatomy and Physiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510060, Guangdong, China

    Linjie Wang

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  4. Fang Yan
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  9. Jingxiu Huang
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Contributions

XJD and HJX conceived the study. YXH, HXQ, and LWC performed bioinformatics and statistical data analyses. YXH and YF constructed the CINP models and collected the tissues. YXH, LWC, YYQ, WLJ, and TXL performed the experiments. ZWA helped perform the analysis with constructive discussions. YXH, HXQ, and LWC wrote the manuscript. All the authors approved the manuscript.

Corresponding authors

Correspondence to Jingxiu Huang or Jingdun Xie.

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Ethics Approval and Consent to Participate

All experimental animal procedures were approved by Sun Yat-sen University Cancer Center Animal Care and Use Committee and conformed to the National Institutes of Health guidelines on the care and ethical treatment of animals.

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All the authors read and approved the publication of this manuscript.

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The authors declare no competing interests.

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Yang, X., Huang, X., Lu, W. et al. Transcriptome Profiling of miRNA-mRNA Interactions and Associated Mechanisms in Chemotherapy-Induced Neuropathic Pain. Mol Neurobiol 60, 5672–5690 (2023). https://doi.org/10.1007/s12035-023-03398-5

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