RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model
Avian pathogenic <i>Escherichia coli</i> (APEC) is an important member of extraintestinal pathogenic <i>Escherichia coli</i> (ExPEC). It shares similar pathogenic strategies with neonatal meningitis <i>E. coli</i> (NMEC) and may threaten human health due to its po...
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MDPI AG
2022-12-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/24/15532 |
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| author | Xia Meng Yanfei Chen Peili Wang Mengping He Yuxing Shi Yuxin Lai Guoqiang Zhu Heng Wang |
| author_facet | Xia Meng Yanfei Chen Peili Wang Mengping He Yuxing Shi Yuxin Lai Guoqiang Zhu Heng Wang |
| author_sort | Xia Meng |
| collection | DOAJ |
| description | Avian pathogenic <i>Escherichia coli</i> (APEC) is an important member of extraintestinal pathogenic <i>Escherichia coli</i> (ExPEC). It shares similar pathogenic strategies with neonatal meningitis <i>E. coli</i> (NMEC) and may threaten human health due to its potential zoonosis. RyhB is a small non-coding RNA that regulates iron homeostasis in <i>E. coli</i>. However, it is unclear whether RyhB regulates meningitis occurrence. To investigate the function of RyhB in the development of meningitis, we constructed the deletion mutant APEC XM∆<i>ryhB</i> and the complemented mutant APEC XM∆<i>ryhB</i>/p<i>ryhB</i>, established a mouse meningitis model and evaluated the role of RyhB in virulence of APEC. The results showed that the deletion of <i>ryhB</i> decreased biofilm formation, adhesion to the brain microvascular endothelial cell line bEnd.3 and serum resistance. RNA-seq data showed that the expression of multiple virulence-related genes changed in the <i>ryhB</i> deletion mutant in the presence of duck serum. Deletion of <i>ryhB</i> reduced the clinical symptoms of mice, such as opisthotonus, diarrhea and neurological signs, when challenged with APEC. Compared with the mice infected with the wild-type APEC, fewer histopathological lesions were observed in the brain of mice infected with the <i>ryhB</i> deletion mutant APEC XM∆<i>ryhB</i>. The bacterial loads in the tissues and the relative expression of cytokines (<i>IL-1β</i>, <i>IL-6</i>, and <i>TNF-α</i>) in the brain significantly decreased when challenged with the APEC XM∆<i>ryhB</i>. The expressions of tight junction proteins (claudin-5, occludin and ZO-1) were not reduced in the brain of mice infected with APEC XM∆<i>ryhB</i>; that is, the blood-brain barrier permeability of mice was not significantly damaged. In conclusion, RyhB contributes to the pathogenicity of APEC XM in the meningitis-causing process by promoting biofilm formation, adhesion to endothelial cells, serum resistance and virulence-related genes expression. |
| first_indexed | 2024-03-09T16:20:32Z |
| format | Article |
| id | doaj.art-405782f01c284b10859bbcd399ed8d8a |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T16:20:32Z |
| publishDate | 2022-12-01 |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-405782f01c284b10859bbcd399ed8d8a2023-11-24T15:23:09ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-12-0123241553210.3390/ijms232415532RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse ModelXia Meng0Yanfei Chen1Peili Wang2Mengping He3Yuxing Shi4Yuxin Lai5Guoqiang Zhu6Heng Wang7Jiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaJiangsu Co-Innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, ChinaAvian pathogenic <i>Escherichia coli</i> (APEC) is an important member of extraintestinal pathogenic <i>Escherichia coli</i> (ExPEC). It shares similar pathogenic strategies with neonatal meningitis <i>E. coli</i> (NMEC) and may threaten human health due to its potential zoonosis. RyhB is a small non-coding RNA that regulates iron homeostasis in <i>E. coli</i>. However, it is unclear whether RyhB regulates meningitis occurrence. To investigate the function of RyhB in the development of meningitis, we constructed the deletion mutant APEC XM∆<i>ryhB</i> and the complemented mutant APEC XM∆<i>ryhB</i>/p<i>ryhB</i>, established a mouse meningitis model and evaluated the role of RyhB in virulence of APEC. The results showed that the deletion of <i>ryhB</i> decreased biofilm formation, adhesion to the brain microvascular endothelial cell line bEnd.3 and serum resistance. RNA-seq data showed that the expression of multiple virulence-related genes changed in the <i>ryhB</i> deletion mutant in the presence of duck serum. Deletion of <i>ryhB</i> reduced the clinical symptoms of mice, such as opisthotonus, diarrhea and neurological signs, when challenged with APEC. Compared with the mice infected with the wild-type APEC, fewer histopathological lesions were observed in the brain of mice infected with the <i>ryhB</i> deletion mutant APEC XM∆<i>ryhB</i>. The bacterial loads in the tissues and the relative expression of cytokines (<i>IL-1β</i>, <i>IL-6</i>, and <i>TNF-α</i>) in the brain significantly decreased when challenged with the APEC XM∆<i>ryhB</i>. The expressions of tight junction proteins (claudin-5, occludin and ZO-1) were not reduced in the brain of mice infected with APEC XM∆<i>ryhB</i>; that is, the blood-brain barrier permeability of mice was not significantly damaged. In conclusion, RyhB contributes to the pathogenicity of APEC XM in the meningitis-causing process by promoting biofilm formation, adhesion to endothelial cells, serum resistance and virulence-related genes expression.https://www.mdpi.com/1422-0067/23/24/15532RyhBvirulence regulationAPECmeningitis development |
| spellingShingle | Xia Meng Yanfei Chen Peili Wang Mengping He Yuxing Shi Yuxin Lai Guoqiang Zhu Heng Wang RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model International Journal of Molecular Sciences RyhB virulence regulation APEC meningitis development |
| title | RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model |
| title_full | RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model |
| title_fullStr | RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model |
| title_full_unstemmed | RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model |
| title_short | RyhB in Avian Pathogenic <i>Escherichia coli</i> Regulates the Expression of Virulence-Related Genes and Contributes to Meningitis Development in a Mouse Model |
| title_sort | ryhb in avian pathogenic i escherichia coli i regulates the expression of virulence related genes and contributes to meningitis development in a mouse model |
| topic | RyhB virulence regulation APEC meningitis development |
| url | https://www.mdpi.com/1422-0067/23/24/15532 |
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