Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infection
Abstract Escherichia coli is the most common gram-negative pathogenic bacterium causing meningitis. It penetrates the blood–brain barrier (BBB) and activates nuclear factor kappa B (NF-κB) signaling, which are vital events leading to the development of meningitis. Long non-coding RNAs (lncRNAs) have...
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| Format: | Article |
| Language: | English |
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BMC
2022-01-01
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| Series: | Molecular Brain |
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| Online Access: | https://doi.org/10.1186/s13041-021-00890-8 |
| _version_ | 1818750234313883648 |
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| author | Bojie Xu Ruicheng Yang Bo Yang Liang Li Jiaqi Chen Jiyang Fu Xinyi Qu Dong Huo Chen Tan Huanchun Chen Zhong Peng Xiangru Wang |
| author_facet | Bojie Xu Ruicheng Yang Bo Yang Liang Li Jiaqi Chen Jiyang Fu Xinyi Qu Dong Huo Chen Tan Huanchun Chen Zhong Peng Xiangru Wang |
| author_sort | Bojie Xu |
| collection | DOAJ |
| description | Abstract Escherichia coli is the most common gram-negative pathogenic bacterium causing meningitis. It penetrates the blood–brain barrier (BBB) and activates nuclear factor kappa B (NF-κB) signaling, which are vital events leading to the development of meningitis. Long non-coding RNAs (lncRNAs) have been implicated in regulating neuroinflammatory signaling, and our previous study showed that E. coli can induce differential expression of lncRNAs, including lncC11orf54-1, in human brain microvascular endothelial cells (hBMECs). The hBMECs constitute the structural and functional basis for the BBB, however, it is unclear whether lncRNAs are involved in the regulation of inflammatory responses of hBMECs during meningitic E. coli infection. In this study, we characterized an abundantly expressed lncRNA, lncC11orf54-1, which was degraded by translocated coilin to produce mgU2-19 and mgU2-30 in hBMECs during E. coli infection. Functionally, lncC11orf54-1-originated non-coding RNA mgU2-30 interacted with interleukin-1 receptor-associated kinase 1 (IRAK1) to induce its oligomerization and autophosphorylation, thus promoting the activation of NF-κB signaling and facilitating the production of pro-inflammatory cytokines. In summary, our study uncovers the involvement of lncC11orf54-1 in IRAK1–NF-κB signaling, and it functions as a positive regulator of inflammatory responses in meningitic E. coli-induced neuroinflammation, which may be a valuable therapeutic and diagnostic target for bacterial meningitis. |
| first_indexed | 2024-12-18T04:16:26Z |
| format | Article |
| id | doaj.art-2bd6c34b73994166a48505dedb2903dd |
| institution | Directory Open Access Journal |
| issn | 1756-6606 |
| language | English |
| last_indexed | 2024-12-18T04:16:26Z |
| publishDate | 2022-01-01 |
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| series | Molecular Brain |
| spelling | doaj.art-2bd6c34b73994166a48505dedb2903dd2022-12-21T21:21:21ZengBMCMolecular Brain1756-66062022-01-0115111610.1186/s13041-021-00890-8Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infectionBojie Xu0Ruicheng Yang1Bo Yang2Liang Li3Jiaqi Chen4Jiyang Fu5Xinyi Qu6Dong Huo7Chen Tan8Huanchun Chen9Zhong Peng10Xiangru Wang11State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityAbstract Escherichia coli is the most common gram-negative pathogenic bacterium causing meningitis. It penetrates the blood–brain barrier (BBB) and activates nuclear factor kappa B (NF-κB) signaling, which are vital events leading to the development of meningitis. Long non-coding RNAs (lncRNAs) have been implicated in regulating neuroinflammatory signaling, and our previous study showed that E. coli can induce differential expression of lncRNAs, including lncC11orf54-1, in human brain microvascular endothelial cells (hBMECs). The hBMECs constitute the structural and functional basis for the BBB, however, it is unclear whether lncRNAs are involved in the regulation of inflammatory responses of hBMECs during meningitic E. coli infection. In this study, we characterized an abundantly expressed lncRNA, lncC11orf54-1, which was degraded by translocated coilin to produce mgU2-19 and mgU2-30 in hBMECs during E. coli infection. Functionally, lncC11orf54-1-originated non-coding RNA mgU2-30 interacted with interleukin-1 receptor-associated kinase 1 (IRAK1) to induce its oligomerization and autophosphorylation, thus promoting the activation of NF-κB signaling and facilitating the production of pro-inflammatory cytokines. In summary, our study uncovers the involvement of lncC11orf54-1 in IRAK1–NF-κB signaling, and it functions as a positive regulator of inflammatory responses in meningitic E. coli-induced neuroinflammation, which may be a valuable therapeutic and diagnostic target for bacterial meningitis.https://doi.org/10.1186/s13041-021-00890-8LncC11orf54-1NeuroinflammationBrain microvascular endothelial cellsNF-κB signalingMeningitic Escherichia coliBlood–brain barrier |
| spellingShingle | Bojie Xu Ruicheng Yang Bo Yang Liang Li Jiaqi Chen Jiyang Fu Xinyi Qu Dong Huo Chen Tan Huanchun Chen Zhong Peng Xiangru Wang Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infection Molecular Brain LncC11orf54-1 Neuroinflammation Brain microvascular endothelial cells NF-κB signaling Meningitic Escherichia coli Blood–brain barrier |
| title | Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infection |
| title_full | Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infection |
| title_fullStr | Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infection |
| title_full_unstemmed | Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infection |
| title_short | Long non-coding RNA lncC11orf54-1 modulates neuroinflammatory responses by activating NF-κB signaling during meningitic Escherichia coli infection |
| title_sort | long non coding rna lncc11orf54 1 modulates neuroinflammatory responses by activating nf κb signaling during meningitic escherichia coli infection |
| topic | LncC11orf54-1 Neuroinflammation Brain microvascular endothelial cells NF-κB signaling Meningitic Escherichia coli Blood–brain barrier |
| url | https://doi.org/10.1186/s13041-021-00890-8 |
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