Impact of virus-induced gill disease caused by carp edema virus (CEV) on the immunological status of fish
Final Report Abstract
Viral gill diseases seriously affect fish health and have a high negative impact on aquaculture, mainly because of the multifunctional involvement of gills in fish physiology. In the project entitled “Impact of virus-induced gill disease caused by carp edema virus (CEV) on the immunological status of fish (CARPCEV)” funded by DFG and NCN in the frame of the BEETHOVEN LIFE 1 program, we studied the carp edema virus (CEV), a fish-infecting poxvirus which affects predominantly the gills of common carp (Cyprinus carpio) and induces a severe gill disease known as koi sleepy disease (KSD) causing severe mortality. Our goal was to determine whether differential stress responses, stress sensitivities, and immune responses might affect the outcome of KSD in carp strains (koi and Amur Sazan - AS). Second, we tested whether severe immunosuppression induced during KSD could impact susceptibility to secondary infections and the general immunological status of survivors during and after CEV infection. Additional research was conducted using cyprinid herpesvirus 3 (CyHV-3), spring viremia of carp virus (SVCV), and tilapia lake virus (TiLV) models to compare effects, better understand viral gill diseases, and search for solutions to the threat posed by CEV. We demonstrated that carp from the KSD-resistant AS strain and the susceptible Koi strain have similar total capacities to respond to stress. However, there were differences in the course of infection depending on the strain and temperature. Importantly, CEV infection activates the stress response, increasing serum cortisol and glucose levels, with a stronger effect at 18°C. CEV exhibits immunomodulatory properties by affecting the adaptive response of carp. Stress induced by CEV infection causes distinct changes in the gill and intestinal microbiomes, initiating secondary infections. CEV can also interact with other viral pathogens, exploiting them. For example, coinfection of fish with CEV and KHV or CEV and SVCV resulted in higher levels of CEV in the gills than infection with these viruses alone. Using OMICS (transcriptome, proteome, phosphoproteome, metabolome, and lipidome), we demonstrated the clear effects of infection, indicating pathological processes that lead to disease development and stress. Further, the detrimental effects of CEV on carp brains and testes have been demonstrated, explaining the detrimental effects on behavior and possible detrimental effects on reproductive success. Despite its strong immunomodulatory effects, CEV does not affect the efficacy of vaccines against other viruses, such as CyHV-3, and therefore does not influence vaccination success. Finally, it is important to note that carp that are naturally immunized show increased resistance to reinfection with CEV, which provides good prospects for developing a CEV vaccine. The project resulted in the publication of 14 peer-reviewed articles presenting original research results, as well as synthesizing existing and obtained knowledge in the form of reviews. By better understanding the interactions between the common carp and CEV and relating them to current knowledge about gill diseases in fish, we also identified avenues that could lead to the mitigation of disease burdens in the future, ensuring the better welfare of fish in aquaculture.
Publications
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Feeling dizzy – brain as a secondary site of koi sleepy disease related pathology. Virtual 20th International Conference on Diseases of Fish and Shellfish, 20-23 September 2021
Adamek M. Orzechowska U. Zawisza M. Rakus K. Chadzińska M. Jung-Schroers V. Teitge F. Piackova V. Gela D. Kocour M. & Steinhagen D.
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It is everywhere—A survey on the presence of carp edema virus in carp populations in Germany. Transboundary and Emerging Diseases, 69(4), 2227-2241.
Adamek, Mikolaj; Heling, Max; Bauer, Julia; Teitge, Felix; Bergmann, Sven M.; Kleingeld, Dirk Willem; Welzel, Alice; Scuda, Nelly; Bachmann, Johannes; Louis, Carola Sauter; Böttcher, Kerstin; Bräuer, Grit; Steinhagen, Dieter & Jung‐Schroers, Verena
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Koi sleepy disease as a pathophysiological and immunological consequence of a branchial infection of common carp with carp edema virus. Virulence, 12(1), 1855–1883.
Adamek, Mikolaj; Teitge, Felix; Baumann, Ilka; Jung-Schroers, Verena; El Rahman, Sahar Abd; Paley, Richard; Piackova, Veronica; Gela, David; Kocour, Martin; Rakers, Sebastian; Bergmann, Sven M.; Ganter, Martin & Steinhagen, Dieter
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CEV- Infection Induced Cortisol Release and Immunosuppression are Associated with High Mortality of Susceptible Koi Carp. 9th International Symposium on Aquatic Animal Health (ISAAH 9th) “Enhancing aquatic animal health towards One Health” Centro de Extensión, Universidad Católica de Chile 5-8.09.2022
Zawisza M. Rebl A. Piackova V. Gela D. Kocour M. Chadzinska M. Rakus K. & Adamek M.
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Don’t Let It Get Under Your Skin! – Vaccination Protects the Skin Barrier of Common Carp From Disruption Caused by Cyprinid Herpesvirus 3. Frontiers in Immunology, 13.
Adamek, Mikolaj,Matras, Marek,Rebl, Alexander Stachnik, Magdalena, Falco, Alberto Bauer, Julia, Miebach, Anne-Carina,Teitge, Felix,Jung-Schroers, Verena ,Abdullah, Muhammad,Krebs, Torben,Schröder, Lars,Fuchs, Walter , Reichert, Michal & Steinhagen, Dieter
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Identification of the impact of carp edema virus (CEV) infection on T and B cell responses and vaccination success in common carp. Oral Abstracts - From the Fourth Congress of the International Society of Fish & Shellfish Immunology. Fish & Shellfish Immunology, 131, 1286-1311.
Zawisza M.; Chan J.T.H.; Mojzesz M.; Fuchs W.; Chadzinska M.; Korytar T.; Adamek M. & Rakus K.
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Immunological insights into the resistance of Nile tilapia strains to an infection with tilapia lake virus. Fish & Shellfish Immunology, 124, 118–133.
Adamek, Mikolaj; Rebl, Alexander; Matras, Marek; Lodder, Christian; Abd El Rahman, Sahar; Stachnik, Magdalena; Rakus, Krzysztof; Bauer, Julia; Falco, Alberto; Jung-Schroers, Verena; Piewbang, Chutchai; Techangamsuwan, Somporn; Surachetpong, Win; Reichert, Michal; Tetens, Jens & Steinhagen, Dieter
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Poster Abstracts. Protection of skin and gill functions is essential for the survival of fish from infections caused by epitheliotropic viruses. 4th Congress of the International Society of Fish & Shellfish Immunology, 131, 1312-1334.
Adamek, M., Rakus, K., Matras, M., Rebl, A., Zawisza, M., Stachnik, M., Abdullah, M., Krebs, T., Jung-Schroers, V., Schröder, L., Fuchs, W., Reichert, M. & Steinhagen, D.
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Proteomics and flow cytometry give new insight into immunosuppression observed during carp edema virus-induced gill disease. Oral Abstracts - From the Fourth Congress of the International Society of Fish & Shellfish Immunology. Fish & Shellfish Immunology, 131, 1286-1311.
Adamek M.; Chan J.T.H.; Dietrich M.; Zawisza M.; Teitge F.; Kodzik N.; Jung-Schroers V.; Chadzinska M.; Falco A.; Ciereszko A.; Rakus K.; Korytar T. & Steinhagen D.
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The influence of viral infection on cell line characteristics: Lessons learned from working with new cell lines from common carp. Journal of Fish Diseases, 45(11), 1767-1780.
Felten, Martin; Adamek, Mikolaj; Gebert, Marina; Rakers, Sebastian & Steinhagen, Dieter
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When sleep meets death - how gill disease can induce secondary pathology in the brain. 9th International Symposium on Aquatic Animal Health (ISAAH 9th) “Enhancing aquatic animal health towards One Health” Centro de Extensión, Universidad Católica de Chile 5-8.09.2022
Adamek M. Müller F.E. Orzechowska U. Zawisza M. Rakus K. Chadzińska M. Jung-Schroers V. Teitge F. Piackova V. Gela D. Kocour M. & Steinhagen D.
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BAD NEWS - GOOD NEWS SITUATION: SALT TREATMENT OF KOI SLEEPY DISEASE DE- LIVERS BOTH: LONG PERSISTENCE OF CARP EDEMA VIRUS AND SUCCESSFUL PROTEC- TION AGAINST CEV RE-INFECTION. Aquaculture Europe 2023, Vienna, Austria 18-21.09.2023
Adamek M. Teitge F. Zawisza M. Miebach A.C. Jung-Schroers V. Steinhagen D. Korytar T. & Rakus K.
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Carp edema virus in Ukraine – The evidence for the furthest east presence of CEV genogroup I in Europe. Aquaculture Reports, 29, 101500.
Rud, Yuriy; Zaloilo, Olga; Buchatsky, Leonid; Matras, Marek; Steinhagen, Dieter & Adamek, Mikolaj
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Carp edema virus infection induces cortisol release and leads to temperature-dependent immunosuppression. 21. EAFP Conference on Diseases of Fish and Shellfish, Aberdeen, UK 11-14.09.2023
Adamek M. Zawisza M. Rebl A. Piackova V. Gela D. Kocour M. Jung-Schroers V. Steinhagen D. Chadzinska M. & Rakus K.
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Gill disorders in fish: Lessons from poxvirus infections. Reviews in Aquaculture, 16(1), 234-253.
Zawisza, Maria; Chadzinska, Magdalena; Steinhagen, Dieter; Rakus, Krzysztof & Adamek, Mikołaj
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Immune responses in carp strains with different susceptibility to carp edema virus disease. PeerJ, 11, e15614.
Baloch, Ali Asghar; Steinhagen, Dieter; Gela, David; Kocour, Martin; Piačková, Veronika & Adamek, Mikolaj
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New insights into the immunosuppression observed during carp edema virus-induced gill disease provided by proteomics and flow cytometry. 21. EAFP Conference on Diseases of Fish and Shellfish, Aberdeen, UK 11-14.09.2023
Adamek M. Chan J.T.H. Dietrich M. Zawisza M. Teitge F. Kodzik N. Jung-Schroers V. Chadzinska M. Falco A. Ciereszko A. Rakus K. Korytar T. & Steinhagen D.
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Tilapia Lake Virus Vaccine Development: A Review on the Recent Advances. Vaccines, 11(2), 251.
Kembou-Ringert, Japhette E.; Steinhagen, Dieter; Readman, John; Daly, Janet M. & Adamek, Mikolaj
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UNRAVELING THE IM- PACT OF KOI HERPESVIRUS (KHV) AND CARP EDEMA VIRUS (CEV) INFECTIONS ON COM- MON CARP (CYPRINUS CARPIO) SEMINAL PLASMA PROTEOME. Aquaculture Europe 2023, Vienna, Austria 18-21.09.2023
Dietrich M. Adamek M. Malinowska A. Świderska B. Rebl A. & Ciereszko A.
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Habilitation: When Hypnos Meets Thanatos: Emergence, Diagnostics, Pathophysiological and Immunological Consequences of “Koi Sleepy Disease” Caused by Carp Edema Virus Infection of Common Carp in Europe, Hannover
Adamek, M.
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Knowns and unknowns of TiLV-associated neuronal disease. Virulence, 15(1).
Kembou-Ringert, Japhette E.; Hotio, Fortune N.; Steinhagen, Dieter; Thompson, Kim D.; Surachetpong, Win; Rakus, Krzysztof; Daly, Janet M.; Goonawardane, Niluka & Adamek, Mikolaj
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Secreted novel AID/APOBEC-like deaminase 1 (SNAD1) – a new important player in fish immunology. Frontiers in Immunology, 15.
Majewska, Anna M.; Dietrich, Mariola A.; Budzko, Lucyna; Adamek, Mikołaj; Figlerowicz, Marek & Ciereszko, Andrzej
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Stressing out—carp edema virus induces stress and modulates immune response in common carp. Frontiers in Immunology, 15.
Zawisza, Maria; Rebl, Alexander; Teitge, Felix; Krzystyniak, Barbara; Piackova, Veronika; Gela, David; Kocour, Martin; Chadzinska, Magdalena; Adamek, Mikolaj & Rakus, Krzysztof
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Modulation of Sodium and Ammonia Transporters in the Context of Viral Gill Diseases in Common Carp (Cyprinus carpio). Journal of Fish Diseases, 48(10).
Zawisza, Maria; Abdullah, Muhammad; Marcinkowska, Magdalena; Matras, Marek; Rakus, Krzysztof & Adamek, Mikolaj
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Poxvirus pathology and pathogenesis in agriculturally important species. Veterinary Pathology, 62(6), 849-866.
MacNeill, Amy L.; Micheloud, Juan Francisco; Parvin, Rokshana; Gjessing, Mona; Airas, Niina A.; Sant’Ana, Fabiano José Ferreira de & Adamek, Mikolaj
