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Dynamics of global gene expression and chromatin accessibility of the peripheral nervous system in animal models of persistent pain

View ORCID ProfileKimberly E. Stephens, Weiqiang Zhou, Zachary Renfro, Zhicheng Ji, Hongkai Ji, Yun Guan, Sean D. Taverna
doi: https://doi.org/10.1101/2021.01.27.427793
Kimberly E. Stephens
1Department of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas
2Arkansas Children’s Research Institute, Little Rock, Arkansas
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  • ORCID record for Kimberly E. Stephens
  • For correspondence: kestephens@uams.edu staverna@jhmi.edu yguan1@jhmi.edu
Weiqiang Zhou
3Department of Biostatistics, School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Zachary Renfro
1Department of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas
2Arkansas Children’s Research Institute, Little Rock, Arkansas
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Zhicheng Ji
4Department of Biostatistics and Bioinformatics, Duke University, Durham, North Carolina
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Hongkai Ji
3Department of Biostatistics, School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Yun Guan
5Department of Anesthesia and Critical Care Medicine, School of Medicine, Johns Hopkins University, Baltimore, Maryland
6Department of Neurological Surgery, School of Medicine, Johns Hopkins University, Baltimore, Maryland
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  • For correspondence: kestephens@uams.edu staverna@jhmi.edu yguan1@jhmi.edu
Sean D. Taverna
7Department of Pharmacology and Molecular Sciences, School of Medicine, Johns Hopkins University, Baltimore, Maryland
8Center for Epigenetics, Johns Hopkins University, Baltimore, Maryland
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  • For correspondence: kestephens@uams.edu staverna@jhmi.edu yguan1@jhmi.edu
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Abstract

Efforts to understand genetic variability involved in an individual’s susceptibility to chronic pain support a role for upstream regulation by epigenetic mechanisms. To examine the transcriptomic and epigenetic basis of chronic pain that resides in the peripheral nervous system, we used RNA-seq and ATAC-seq of the rat dorsal root ganglion (DRG) to identify novel molecular pathways associated with pain hypersensitivity in two well-studied persistent pain models induced by Chronic Constriction Injury (CCI) of the sciatic nerve and intra-plantar injection of Complete Freund’s Adjuvant (CFA) in rats. Our RNA-seq studies identify a variety of biological process related to synapse organization, membrane potential, transmembrane transport, and ion binding. Interestingly, genes that encode transcriptional regulators were disproportionately downregulated in both models. Our ATAC-seq data provide a comprehensive map of chromatin accessibility changes in the DRG. A total of 1123 regions showed changes in chromatin accessibility in one or both models when compared to the naïve and 31 shared differentially accessible regions (DAR)s. Functional annotation of the DARs identified disparate molecular functions enriched for each pain model which suggests that chromatin structure may be altered differently following sciatic nerve injury and hind paw inflammation. Motif analysis identified 17 DNA sequences known to bind transcription factors in the CCI DARs and 33 in the CFA DARs. Two motifs were significantly enriched in both models. Our improved understanding of the changes in chromatin accessibility that occur in chronic pain states may identify regulatory genomic elements that play essential roles in modulating gene expression in the DRG.

Summary Shared transcriptomic and epigenetic changes in two animal models improves our understanding of how chromatin structural changes alter DRG gene expression under persistent pain conditions.

Competing Interest Statement

The authors have declared no competing interest.

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Posted January 28, 2021.
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Dynamics of global gene expression and chromatin accessibility of the peripheral nervous system in animal models of persistent pain
Kimberly E. Stephens, Weiqiang Zhou, Zachary Renfro, Zhicheng Ji, Hongkai Ji, Yun Guan, Sean D. Taverna
bioRxiv 2021.01.27.427793; doi: https://doi.org/10.1101/2021.01.27.427793
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Dynamics of global gene expression and chromatin accessibility of the peripheral nervous system in animal models of persistent pain
Kimberly E. Stephens, Weiqiang Zhou, Zachary Renfro, Zhicheng Ji, Hongkai Ji, Yun Guan, Sean D. Taverna
bioRxiv 2021.01.27.427793; doi: https://doi.org/10.1101/2021.01.27.427793

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