Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injury

Background Neurogenic bladder (NB) following suprasacral spinal cord injury (SSCI) is an interstitial disease with the structural remodeling of bladder tissue and matrix over-deposition. Circular RNAs (circRNAs) are involved in fibrotic disease development through their post-transcriptional regulato...

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Main Authors: Jimeng Ruan, Xin Cui, Hao Yan, Chunsong Jia, Tongwen Ou, Zhenhua Shang
Format: Article
Language:English
Published: PeerJ Inc. 2023-09-01
Series:PeerJ
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Online Access:https://peerj.com/articles/16042.pdf
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author Jimeng Ruan
Xin Cui
Hao Yan
Chunsong Jia
Tongwen Ou
Zhenhua Shang
author_facet Jimeng Ruan
Xin Cui
Hao Yan
Chunsong Jia
Tongwen Ou
Zhenhua Shang
author_sort Jimeng Ruan
collection DOAJ
description Background Neurogenic bladder (NB) following suprasacral spinal cord injury (SSCI) is an interstitial disease with the structural remodeling of bladder tissue and matrix over-deposition. Circular RNAs (circRNAs) are involved in fibrotic disease development through their post-transcriptional regulatory functions. This study aimed to use transcriptome high-throughput sequencing to investigate the process of NB and bladder fibrosis after SSCI. Methods Spinal cord transection at the T10–T11 level was used to construct the SSCI model in rats (10–week–old female Wistar rats, weighing 200 ± 20 g). The bladders were collected without (sham group) and with (SSCI 1–3 groups) NB status. Morphological examination was conducted to assess the extent of bladder fibrosis. Additionally, RNA sequencing was utilized to determine mRNAs and circRNAs expression patterns. The dynamic changes of differentially expressed mRNAs (DEMs) and circRNAs (DECs) in different periods of SSCI were further analyzed. Results Bladder weight, smooth muscle cell hypertrophy, and extracellular matrix gradually increased after SSCI. Compared with the sham group, 3,255 DEMs and 1,339 DECs, 3,449 DEMs and 1,324 DECs, 884 DEMs, and 1,151 DECs were detected in the SSCI 1–3 groups, respectively. Specifically, circRNA3621, circRNA0617, circRNA0586, and circRNA4426 were significant DECs common to SSCI 1–3 groups compared with the sham group. Moreover, Gene Ontology (GO) enrichment suggested that inflammatory and chronic inflammatory responses were the key events in NB progression following SSCI. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways enrichment associated with the “Chemokine signaling pathway”, the “IL-17 signaling pathway”, and the “TGF-beta signaling pathway” suggests their potential involvement in regulating biological processes. The circRNA–miRNA–mRNA interaction networks of DECs revealed rno-circ-2239 (micu2) as the largest node, indicating that the rno-circ-2239–miRNA–mRNA–mediated network may play a critical role in the pathogenesis of SSCI-induced NB. Conclusions This study offers a comprehensive outlook on the possible roles of DEMs and DECs in bladder fibrosis and NB progression following SSCI. These findings have the potential to serve as novel biomarkers and therapeutic targets.
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spelling doaj.art-7fab534edf024955bdc6a47d9d9a86682023-12-02T23:38:22ZengPeerJ Inc.PeerJ2167-83592023-09-0111e1604210.7717/peerj.16042Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injuryJimeng RuanXin CuiHao YanChunsong JiaTongwen OuZhenhua ShangBackground Neurogenic bladder (NB) following suprasacral spinal cord injury (SSCI) is an interstitial disease with the structural remodeling of bladder tissue and matrix over-deposition. Circular RNAs (circRNAs) are involved in fibrotic disease development through their post-transcriptional regulatory functions. This study aimed to use transcriptome high-throughput sequencing to investigate the process of NB and bladder fibrosis after SSCI. Methods Spinal cord transection at the T10–T11 level was used to construct the SSCI model in rats (10–week–old female Wistar rats, weighing 200 ± 20 g). The bladders were collected without (sham group) and with (SSCI 1–3 groups) NB status. Morphological examination was conducted to assess the extent of bladder fibrosis. Additionally, RNA sequencing was utilized to determine mRNAs and circRNAs expression patterns. The dynamic changes of differentially expressed mRNAs (DEMs) and circRNAs (DECs) in different periods of SSCI were further analyzed. Results Bladder weight, smooth muscle cell hypertrophy, and extracellular matrix gradually increased after SSCI. Compared with the sham group, 3,255 DEMs and 1,339 DECs, 3,449 DEMs and 1,324 DECs, 884 DEMs, and 1,151 DECs were detected in the SSCI 1–3 groups, respectively. Specifically, circRNA3621, circRNA0617, circRNA0586, and circRNA4426 were significant DECs common to SSCI 1–3 groups compared with the sham group. Moreover, Gene Ontology (GO) enrichment suggested that inflammatory and chronic inflammatory responses were the key events in NB progression following SSCI. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways enrichment associated with the “Chemokine signaling pathway”, the “IL-17 signaling pathway”, and the “TGF-beta signaling pathway” suggests their potential involvement in regulating biological processes. The circRNA–miRNA–mRNA interaction networks of DECs revealed rno-circ-2239 (micu2) as the largest node, indicating that the rno-circ-2239–miRNA–mRNA–mediated network may play a critical role in the pathogenesis of SSCI-induced NB. Conclusions This study offers a comprehensive outlook on the possible roles of DEMs and DECs in bladder fibrosis and NB progression following SSCI. These findings have the potential to serve as novel biomarkers and therapeutic targets.https://peerj.com/articles/16042.pdfSuprasacral spinal cord injuryNeurogenic bladderBladder fibrosiscircRNAsTranscriptome high-throughput sequencingCo-expression network
spellingShingle Jimeng Ruan
Xin Cui
Hao Yan
Chunsong Jia
Tongwen Ou
Zhenhua Shang
Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injury
PeerJ
Suprasacral spinal cord injury
Neurogenic bladder
Bladder fibrosis
circRNAs
Transcriptome high-throughput sequencing
Co-expression network
title Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injury
title_full Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injury
title_fullStr Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injury
title_full_unstemmed Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injury
title_short Expression profiles of circular RNAs and interaction networks of competing endogenous RNAs in neurogenic bladder of rats following suprasacral spinal cord injury
title_sort expression profiles of circular rnas and interaction networks of competing endogenous rnas in neurogenic bladder of rats following suprasacral spinal cord injury
topic Suprasacral spinal cord injury
Neurogenic bladder
Bladder fibrosis
circRNAs
Transcriptome high-throughput sequencing
Co-expression network
url https://peerj.com/articles/16042.pdf
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