Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interaction

Background Avian pathogenic Escherichia coli (APEC), an important extraintestinal pathogenic E. coli, causes colibacillosis, an acute and mostly systemic disease involving multiple organ lesions such as meningitis. Meningitis-causing APEC can invade the host central nervous system by crossing the bl...

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Main Authors: Peili Wang, Xia Meng, Jianji Li, Yanfei Chen, Dong Zhang, Haoran Zhong, Pengpeng Xia, Luying Cui, Guoqiang Zhu, Heng Wang
Format: Article
Language:English
Published: PeerJ Inc. 2020-05-01
Series:PeerJ
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Online Access:https://peerj.com/articles/9172.pdf
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author Peili Wang
Xia Meng
Jianji Li
Yanfei Chen
Dong Zhang
Haoran Zhong
Pengpeng Xia
Luying Cui
Guoqiang Zhu
Heng Wang
author_facet Peili Wang
Xia Meng
Jianji Li
Yanfei Chen
Dong Zhang
Haoran Zhong
Pengpeng Xia
Luying Cui
Guoqiang Zhu
Heng Wang
author_sort Peili Wang
collection DOAJ
description Background Avian pathogenic Escherichia coli (APEC), an important extraintestinal pathogenic E. coli, causes colibacillosis, an acute and mostly systemic disease involving multiple organ lesions such as meningitis. Meningitis-causing APEC can invade the host central nervous system by crossing the blood–brain barrier (BBB), which is a critical step in the development of meningitis. However, the bacteria-host interaction mechanism in this process remains unclear. Methods In this study, we examined E. coli and bEnd.3 cells transcriptomes during infection and mock infection to investigate the global transcriptional changes in both organisms using RNA sequencing approach. Results When APEC infected the bEnd.3 cells, several significant changes in the expression of genes related to cell junctional complexes, extracellular matrix degradation, actin cytoskeleton rearrangement, immune activation and the inflammatory response in bEnd.3 cells were observed as compared to the mock infection group. Thus, the immune activation of bEnd.3 cells indicated that APEC infection activated host defenses. Furthermore, APEC may exploit cell junction degradation to invade the BBB. In addition, amino acid metabolism and energy metabolism related genes were downregulated and the protein export pathway related genes were upregulated in APEC cultured with bEnd.3 cells, compared to that in control. Thus, APEC may encounter starvation and express virulence factors during incubation with bEnd.3 cells. Conclusion This study provides a comprehensive overview of transcriptomic changes that occur during APEC infection of bEnd.3 cells, and offers insights into the bacterial invasion strategies and the subsequent host defense mechanism.
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spelling doaj.art-86e32304d5b94488a2bd3500f29026332023-12-03T10:34:17ZengPeerJ Inc.PeerJ2167-83592020-05-018e917210.7717/peerj.9172Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interactionPeili Wang0Xia Meng1Jianji Li2Yanfei Chen3Dong Zhang4Haoran Zhong5Pengpeng Xia6Luying Cui7Guoqiang Zhu8Heng Wang9College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaBackground Avian pathogenic Escherichia coli (APEC), an important extraintestinal pathogenic E. coli, causes colibacillosis, an acute and mostly systemic disease involving multiple organ lesions such as meningitis. Meningitis-causing APEC can invade the host central nervous system by crossing the blood–brain barrier (BBB), which is a critical step in the development of meningitis. However, the bacteria-host interaction mechanism in this process remains unclear. Methods In this study, we examined E. coli and bEnd.3 cells transcriptomes during infection and mock infection to investigate the global transcriptional changes in both organisms using RNA sequencing approach. Results When APEC infected the bEnd.3 cells, several significant changes in the expression of genes related to cell junctional complexes, extracellular matrix degradation, actin cytoskeleton rearrangement, immune activation and the inflammatory response in bEnd.3 cells were observed as compared to the mock infection group. Thus, the immune activation of bEnd.3 cells indicated that APEC infection activated host defenses. Furthermore, APEC may exploit cell junction degradation to invade the BBB. In addition, amino acid metabolism and energy metabolism related genes were downregulated and the protein export pathway related genes were upregulated in APEC cultured with bEnd.3 cells, compared to that in control. Thus, APEC may encounter starvation and express virulence factors during incubation with bEnd.3 cells. Conclusion This study provides a comprehensive overview of transcriptomic changes that occur during APEC infection of bEnd.3 cells, and offers insights into the bacterial invasion strategies and the subsequent host defense mechanism.https://peerj.com/articles/9172.pdfDual RNA-seqHost–pathogen interactionsMeningitisAPECbEnd.3 cells
spellingShingle Peili Wang
Xia Meng
Jianji Li
Yanfei Chen
Dong Zhang
Haoran Zhong
Pengpeng Xia
Luying Cui
Guoqiang Zhu
Heng Wang
Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interaction
PeerJ
Dual RNA-seq
Host–pathogen interactions
Meningitis
APEC
bEnd.3 cells
title Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interaction
title_full Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interaction
title_fullStr Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interaction
title_full_unstemmed Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interaction
title_short Transcriptome profiling of avian pathogenic Escherichia coli and the mouse microvascular endothelial cell line bEnd.3 during interaction
title_sort transcriptome profiling of avian pathogenic escherichia coli and the mouse microvascular endothelial cell line bend 3 during interaction
topic Dual RNA-seq
Host–pathogen interactions
Meningitis
APEC
bEnd.3 cells
url https://peerj.com/articles/9172.pdf
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