Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to Cypriniviruses
The zebrafish (<i>Danio rerio</i>) represents an increasingly important model organism in virology. We evaluated its utility in the study of economically important viruses from the genus <i>Cyprinivirus</i> (anguillid herpesvirus 1, cyprinid herpesvirus 2 and cyprinid herpesv...
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-03-01
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| Series: | Viruses |
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| Online Access: | https://www.mdpi.com/1999-4915/15/3/768 |
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| author | Cindy Streiff Bo He Léa Morvan Haiyan Zhang Natacha Delrez Mickael Fourrier Isabelle Manfroid Nicolás M. Suárez Stéphane Betoulle Andrew J. Davison Owen Donohoe Alain Vanderplasschen |
| author_facet | Cindy Streiff Bo He Léa Morvan Haiyan Zhang Natacha Delrez Mickael Fourrier Isabelle Manfroid Nicolás M. Suárez Stéphane Betoulle Andrew J. Davison Owen Donohoe Alain Vanderplasschen |
| author_sort | Cindy Streiff |
| collection | DOAJ |
| description | The zebrafish (<i>Danio rerio</i>) represents an increasingly important model organism in virology. We evaluated its utility in the study of economically important viruses from the genus <i>Cyprinivirus</i> (anguillid herpesvirus 1, cyprinid herpesvirus 2 and cyprinid herpesvirus 3 (CyHV-3)). This revealed that zebrafish larvae were not susceptible to these viruses after immersion in contaminated water, but that infections could be established using artificial infection models in vitro (zebrafish cell lines) and in vivo (microinjection of larvae). However, infections were transient, with rapid viral clearance associated with apoptosis-like death of infected cells. Transcriptomic analysis of CyHV-3-infected larvae revealed upregulation of interferon-stimulated genes, in particular those encoding nucleic acid sensors, mediators of programmed cell death and related genes. It was notable that uncharacterized non-coding RNA genes and retrotransposons were also among those most upregulated. CRISPR/Cas9 knockout of the zebrafish gene encoding protein kinase R (PKR) and a related gene encoding a protein kinase containing Z-DNA binding domains (PKZ) had no impact on CyHV-3 clearance in larvae. Our study strongly supports the importance of innate immunity-virus interactions in the adaptation of cypriniviruses to their natural hosts. It also highlights the potential of the CyHV-3-zebrafish model, versus the CyHV-3-carp model, for study of these interactions. |
| first_indexed | 2024-03-11T05:45:35Z |
| format | Article |
| id | doaj.art-3ce5b9f996374279943b6162ea7e8f42 |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-11T05:45:35Z |
| publishDate | 2023-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-3ce5b9f996374279943b6162ea7e8f422023-11-17T14:24:04ZengMDPI AGViruses1999-49152023-03-0115376810.3390/v15030768Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to CyprinivirusesCindy Streiff0Bo He1Léa Morvan2Haiyan Zhang3Natacha Delrez4Mickael Fourrier5Isabelle Manfroid6Nicolás M. Suárez7Stéphane Betoulle8Andrew J. Davison9Owen Donohoe10Alain Vanderplasschen11Immunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumImmunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumImmunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumImmunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumImmunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumImmunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumZebrafish Development and Disease Models Laboratory, GIGA-Molecular Biology of Diseases, University of Liège, B-4000 Liège, BelgiumMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UKUMR-I 02 Stress Environnementaux et BIOsurveillance des Milieux Aquatiques (SEBIO), UFR Sciences Exactes et Naturelles, Université de Reims Champagne-Ardenne, CEDEX 2, 51687 Reims, FranceMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UKImmunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumImmunology–Vaccinology, Department of Infectious and Parasitic Diseases, Fundamental and Applied Research for Animals & Health (FARAH), Faculty of Veterinary Medicine, University of Liège, B-4000 Liège, BelgiumThe zebrafish (<i>Danio rerio</i>) represents an increasingly important model organism in virology. We evaluated its utility in the study of economically important viruses from the genus <i>Cyprinivirus</i> (anguillid herpesvirus 1, cyprinid herpesvirus 2 and cyprinid herpesvirus 3 (CyHV-3)). This revealed that zebrafish larvae were not susceptible to these viruses after immersion in contaminated water, but that infections could be established using artificial infection models in vitro (zebrafish cell lines) and in vivo (microinjection of larvae). However, infections were transient, with rapid viral clearance associated with apoptosis-like death of infected cells. Transcriptomic analysis of CyHV-3-infected larvae revealed upregulation of interferon-stimulated genes, in particular those encoding nucleic acid sensors, mediators of programmed cell death and related genes. It was notable that uncharacterized non-coding RNA genes and retrotransposons were also among those most upregulated. CRISPR/Cas9 knockout of the zebrafish gene encoding protein kinase R (PKR) and a related gene encoding a protein kinase containing Z-DNA binding domains (PKZ) had no impact on CyHV-3 clearance in larvae. Our study strongly supports the importance of innate immunity-virus interactions in the adaptation of cypriniviruses to their natural hosts. It also highlights the potential of the CyHV-3-zebrafish model, versus the CyHV-3-carp model, for study of these interactions.https://www.mdpi.com/1999-4915/15/3/768anguillid herpesvirus 1cyprinid herpesvirus 2cyprinid herpesvirus 3alloherpesviruscypriniviruszebrafish |
| spellingShingle | Cindy Streiff Bo He Léa Morvan Haiyan Zhang Natacha Delrez Mickael Fourrier Isabelle Manfroid Nicolás M. Suárez Stéphane Betoulle Andrew J. Davison Owen Donohoe Alain Vanderplasschen Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to Cypriniviruses Viruses anguillid herpesvirus 1 cyprinid herpesvirus 2 cyprinid herpesvirus 3 alloherpesvirus cyprinivirus zebrafish |
| title | Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to Cypriniviruses |
| title_full | Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to Cypriniviruses |
| title_fullStr | Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to Cypriniviruses |
| title_full_unstemmed | Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to Cypriniviruses |
| title_short | Susceptibility and Permissivity of Zebrafish (<i>Danio rerio</i>) Larvae to Cypriniviruses |
| title_sort | susceptibility and permissivity of zebrafish i danio rerio i larvae to cypriniviruses |
| topic | anguillid herpesvirus 1 cyprinid herpesvirus 2 cyprinid herpesvirus 3 alloherpesvirus cyprinivirus zebrafish |
| url | https://www.mdpi.com/1999-4915/15/3/768 |
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