Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> Meningitis
<i>Streptococcus</i> <i>suis</i> is a zoonotic agent causing meningitis in pigs and humans. Neutrophils, as the first line of defense against <i>S. suis</i> infections, release neutrophil extracellular traps (NETs) to entrap pathogens. In this study, we investigat...
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MDPI AG
2020-07-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/21/15/5289 |
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| author | Marita Meurer Sophie Öhlmann Marta C. Bonilla Peter Valentin-Weigand Andreas Beineke Isabel Hennig-Pauka Christian Schwerk Horst Schroten Christoph G. Baums Maren von Köckritz-Blickwede Nicole de Buhr |
| author_facet | Marita Meurer Sophie Öhlmann Marta C. Bonilla Peter Valentin-Weigand Andreas Beineke Isabel Hennig-Pauka Christian Schwerk Horst Schroten Christoph G. Baums Maren von Köckritz-Blickwede Nicole de Buhr |
| author_sort | Marita Meurer |
| collection | DOAJ |
| description | <i>Streptococcus</i> <i>suis</i> is a zoonotic agent causing meningitis in pigs and humans. Neutrophils, as the first line of defense against <i>S. suis</i> infections, release neutrophil extracellular traps (NETs) to entrap pathogens. In this study, we investigated the role of the secreted nuclease A of <i>S. suis</i> (SsnA) as a NET-evasion factor in vivo and in vitro. Piglets were intranasally infected with <i>S. suis </i>strain<i> </i>10 or an isogenic <i>ssnA</i> mutant. DNase and NET-formation were analyzed in cerebrospinal fluid (CSF) and brain tissue. Animals infected with <i>S. suis </i>strain 10 or S. suis 10ΔssnA showed the presence of NETs in CSF and developed similar clinical signs. Therefore, SsnA does not seem to be a crucial virulence factor that contributes to the development of meningitis in pigs. Importantly, DNase activity was detectable in the CSF of both infection groups, indicating that host nucleases, in contrast to bacterial nuclease SsnA, may play a major role during the onset of meningitis. The effect of DNase 1 on neutrophil functions was further analyzed in a 3D-cell culture model of the porcine blood–CSF barrier. We found that DNase 1 partially contributes to enhanced killing of <i>S. suis</i> by neutrophils, especially when plasma is present. In summary, host nucleases may partially contribute to efficient innate immune response in the CSF. |
| first_indexed | 2024-03-10T18:12:44Z |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T18:12:44Z |
| publishDate | 2020-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-1e27c94b73d748099a05a8312aea0c9a2023-11-20T07:58:08ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-07-012115528910.3390/ijms21155289Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> MeningitisMarita Meurer0Sophie Öhlmann1Marta C. Bonilla2Peter Valentin-Weigand3Andreas Beineke4Isabel Hennig-Pauka5Christian Schwerk6Horst Schroten7Christoph G. Baums8Maren von Köckritz-Blickwede9Nicole de Buhr10Department of Physiological Chemistry, University of Veterinary Medicine Hannover, 30559 Hannover, GermanyCentre for Infectious Diseases, Institute of Bacteriology and Mycology, Faculty of Veterinary Medicine, University Leipzig, 04103 Leipzig, GermanyDepartment of Physiological Chemistry, University of Veterinary Medicine Hannover, 30559 Hannover, GermanyDepartment of Infectious Diseases, Institute for Microbiology, University of Veterinary Medicine Hannover, 30173 Hannover, GermanyDepartment of Pathology, University of Veterinary Medicine Hannover, 30559 Hannover, GermanyField Station for Epidemiology Bakum, University of Veterinary Medicine Hannover, 49456 Bakum, GermanyDepartment of Pediatrics, Pediatric Infectious Diseases, Medical Faculty Mannheim, Heidelberg University, 68167 Mannheim, GermanyDepartment of Pediatrics, Pediatric Infectious Diseases, Medical Faculty Mannheim, Heidelberg University, 68167 Mannheim, GermanyCentre for Infectious Diseases, Institute of Bacteriology and Mycology, Faculty of Veterinary Medicine, University Leipzig, 04103 Leipzig, GermanyDepartment of Physiological Chemistry, University of Veterinary Medicine Hannover, 30559 Hannover, GermanyDepartment of Physiological Chemistry, University of Veterinary Medicine Hannover, 30559 Hannover, Germany<i>Streptococcus</i> <i>suis</i> is a zoonotic agent causing meningitis in pigs and humans. Neutrophils, as the first line of defense against <i>S. suis</i> infections, release neutrophil extracellular traps (NETs) to entrap pathogens. In this study, we investigated the role of the secreted nuclease A of <i>S. suis</i> (SsnA) as a NET-evasion factor in vivo and in vitro. Piglets were intranasally infected with <i>S. suis </i>strain<i> </i>10 or an isogenic <i>ssnA</i> mutant. DNase and NET-formation were analyzed in cerebrospinal fluid (CSF) and brain tissue. Animals infected with <i>S. suis </i>strain 10 or S. suis 10ΔssnA showed the presence of NETs in CSF and developed similar clinical signs. Therefore, SsnA does not seem to be a crucial virulence factor that contributes to the development of meningitis in pigs. Importantly, DNase activity was detectable in the CSF of both infection groups, indicating that host nucleases, in contrast to bacterial nuclease SsnA, may play a major role during the onset of meningitis. The effect of DNase 1 on neutrophil functions was further analyzed in a 3D-cell culture model of the porcine blood–CSF barrier. We found that DNase 1 partially contributes to enhanced killing of <i>S. suis</i> by neutrophils, especially when plasma is present. In summary, host nucleases may partially contribute to efficient innate immune response in the CSF.https://www.mdpi.com/1422-0067/21/15/5289Streptococcus suismeningitisDNaseneutrophilsNETspathogenesis |
| spellingShingle | Marita Meurer Sophie Öhlmann Marta C. Bonilla Peter Valentin-Weigand Andreas Beineke Isabel Hennig-Pauka Christian Schwerk Horst Schroten Christoph G. Baums Maren von Köckritz-Blickwede Nicole de Buhr Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> Meningitis International Journal of Molecular Sciences Streptococcus suis meningitis DNase neutrophils NETs pathogenesis |
| title | Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> Meningitis |
| title_full | Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> Meningitis |
| title_fullStr | Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> Meningitis |
| title_full_unstemmed | Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> Meningitis |
| title_short | Role of Bacterial and Host DNases on Host-Pathogen Interaction during <i>Streptococcus suis</i> Meningitis |
| title_sort | role of bacterial and host dnases on host pathogen interaction during i streptococcus suis i meningitis |
| topic | Streptococcus suis meningitis DNase neutrophils NETs pathogenesis |
| url | https://www.mdpi.com/1422-0067/21/15/5289 |
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