Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgia
Trigeminal neuropathic pain (TNP) induces mechanical allodynia and hyperalgesia, which are known to alter gene expression in injured dorsal root ganglia primary sensory neurons. Non-coding RNAs (ncRNAs) have been linked to TNP. However, the functional mechanism underlying TNP and the expression prof...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Pharmacology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphar.2023.1230633/full |
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| author | Xiaona Cui Xiaona Cui Xiaona Cui Bo Qin Chaoyun Xia Chaoyun Xia Hong Li Hong Li Zhiye Li Zhisong Li Abdul Nasir Abdul Nasir Qian Bai Qian Bai |
| author_facet | Xiaona Cui Xiaona Cui Xiaona Cui Bo Qin Chaoyun Xia Chaoyun Xia Hong Li Hong Li Zhiye Li Zhisong Li Abdul Nasir Abdul Nasir Qian Bai Qian Bai |
| author_sort | Xiaona Cui |
| collection | DOAJ |
| description | Trigeminal neuropathic pain (TNP) induces mechanical allodynia and hyperalgesia, which are known to alter gene expression in injured dorsal root ganglia primary sensory neurons. Non-coding RNAs (ncRNAs) have been linked to TNP. However, the functional mechanism underlying TNP and the expression profile of ncRNAs in the trigeminal ganglion (TG) and trigeminal subnucleus caudalis (Sp5C) are still unknown. We used RNA sequencing and bioinformatics analysis to examine the TG and Sp5C transcriptomes after infraorbital nerve chronic constrictive injury (IoN-CCI). The robust changes in the gene expression of lncRNAs, circRNAs, and mRNAs were observed within the TG and Sp5C from mice that underwent IoN-CCI and the sham-operated mice (day 7). In total, 111,003 lncRNAs were found in TG and 107,157 in Sp5C; 369 lncRNAs were differentially expressed in TG, and 279 lncRNAs were differentially expressed in Sp5C. In addition, 13,216 circRNAs in TG and 21,658 circRNAs in Sp5C were identified, with 1,155 circRNAs and 2,097 circRNAs differentially expressed in TG and Sp5C, respectively. Furthermore, 5,205 DE mRNAs in TG and 3,934 DE mRNAs in Sp5C were differentially expressed between IoN-CCI and sham groups. The study revealed a high correlation of pain-related differentially expressed genes in the TG and Sp5C to anxiety, depression, inflammation, neuroinflammation, and apoptosis. Gene Ontology analysis revealed that binding-related molecular functions and membrane-related cell components were significantly enriched. Kyoto Encyclopedia of Genes and Genomes analysis shows the most significant enrichments in neurogenesis, nervous system development, neuron differentiation, adrenergic signaling, cAMP signaling, MAPK signaling, and PI3K-Akt signaling pathways. Furthermore, protein–protein interaction analysis showed that hub genes were implicated in neuropeptide signaling pathways. Functional analysis of DE ncRNA-targeting genes was mostly enriched with nociception-related signaling pathways underpinning TNP. Our findings suggest that ncRNAs are involved in TNP development and open new avenues for research and treatment. |
| first_indexed | 2024-03-11T21:16:56Z |
| format | Article |
| id | doaj.art-75870854c2574bc3a24a175a5efa9f73 |
| institution | Directory Open Access Journal |
| issn | 1663-9812 |
| language | English |
| last_indexed | 2024-03-11T21:16:56Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Pharmacology |
| spelling | doaj.art-75870854c2574bc3a24a175a5efa9f732023-09-28T16:25:16ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122023-09-011410.3389/fphar.2023.12306331230633Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgiaXiaona Cui0Xiaona Cui1Xiaona Cui2Bo Qin3Chaoyun Xia4Chaoyun Xia5Hong Li6Hong Li7Zhiye Li8Zhisong Li9Abdul Nasir10Abdul Nasir11Qian Bai12Qian Bai13Medical Research Center, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anesthesiology and Perioperative Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anesthesiology, International Peace Maternity & Child Health Hospital, Shanghai Jiaotong University, School of Medicine, Shanghai, ChinaTranslational Medical Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaMedical Research Center, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anesthesiology and Perioperative Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaMedical Research Center, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anesthesiology and Perioperative Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Pharmacy, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anesthesiology and Perioperative Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaMedical Research Center, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anesthesiology and Perioperative Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaMedical Research Center, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anesthesiology and Perioperative Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaTrigeminal neuropathic pain (TNP) induces mechanical allodynia and hyperalgesia, which are known to alter gene expression in injured dorsal root ganglia primary sensory neurons. Non-coding RNAs (ncRNAs) have been linked to TNP. However, the functional mechanism underlying TNP and the expression profile of ncRNAs in the trigeminal ganglion (TG) and trigeminal subnucleus caudalis (Sp5C) are still unknown. We used RNA sequencing and bioinformatics analysis to examine the TG and Sp5C transcriptomes after infraorbital nerve chronic constrictive injury (IoN-CCI). The robust changes in the gene expression of lncRNAs, circRNAs, and mRNAs were observed within the TG and Sp5C from mice that underwent IoN-CCI and the sham-operated mice (day 7). In total, 111,003 lncRNAs were found in TG and 107,157 in Sp5C; 369 lncRNAs were differentially expressed in TG, and 279 lncRNAs were differentially expressed in Sp5C. In addition, 13,216 circRNAs in TG and 21,658 circRNAs in Sp5C were identified, with 1,155 circRNAs and 2,097 circRNAs differentially expressed in TG and Sp5C, respectively. Furthermore, 5,205 DE mRNAs in TG and 3,934 DE mRNAs in Sp5C were differentially expressed between IoN-CCI and sham groups. The study revealed a high correlation of pain-related differentially expressed genes in the TG and Sp5C to anxiety, depression, inflammation, neuroinflammation, and apoptosis. Gene Ontology analysis revealed that binding-related molecular functions and membrane-related cell components were significantly enriched. Kyoto Encyclopedia of Genes and Genomes analysis shows the most significant enrichments in neurogenesis, nervous system development, neuron differentiation, adrenergic signaling, cAMP signaling, MAPK signaling, and PI3K-Akt signaling pathways. Furthermore, protein–protein interaction analysis showed that hub genes were implicated in neuropeptide signaling pathways. Functional analysis of DE ncRNA-targeting genes was mostly enriched with nociception-related signaling pathways underpinning TNP. Our findings suggest that ncRNAs are involved in TNP development and open new avenues for research and treatment.https://www.frontiersin.org/articles/10.3389/fphar.2023.1230633/fullneuropathic painallodyniahyperalgesiadifferentially expressed genesRNA sequencingnon-coding RNAs |
| spellingShingle | Xiaona Cui Xiaona Cui Xiaona Cui Bo Qin Chaoyun Xia Chaoyun Xia Hong Li Hong Li Zhiye Li Zhisong Li Abdul Nasir Abdul Nasir Qian Bai Qian Bai Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgia Frontiers in Pharmacology neuropathic pain allodynia hyperalgesia differentially expressed genes RNA sequencing non-coding RNAs |
| title | Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgia |
| title_full | Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgia |
| title_fullStr | Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgia |
| title_full_unstemmed | Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgia |
| title_short | Transcriptome-wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury-induced trigeminal neuralgia |
| title_sort | transcriptome wide analysis of trigeminal ganglion and subnucleus caudalis in a mouse model of chronic constriction injury induced trigeminal neuralgia |
| topic | neuropathic pain allodynia hyperalgesia differentially expressed genes RNA sequencing non-coding RNAs |
| url | https://www.frontiersin.org/articles/10.3389/fphar.2023.1230633/full |
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