Immune response in diseased and healthy common carp exposed to carp edema virus.
cell‐mediated cytotoxicity
complement cascade
mass spectrometry
qRT‐PCR
type I interferon pathway
Journal
Journal of fish diseases
ISSN: 1365-2761
Titre abrégé: J Fish Dis
Pays: England
ID NLM: 9881188
Informations de publication
Date de publication:
06 Sep 2024
06 Sep 2024
Historique:
revised:
15
08
2024
received:
13
02
2024
accepted:
19
08
2024
medline:
6
9
2024
pubmed:
6
9
2024
entrez:
6
9
2024
Statut:
aheadofprint
Résumé
The common carp is one of the most economically valuable freshwater fish worldwide and its aquaculture can be severely affected by the koi sleepy disease (KSD)/carp edema virus disease (CEVD). This study explores a natural outbreak of CEVD in a pond containing both clinically healthy and diseased fish of various origins exposed to the virus. We investigated mRNA expression of genes associated with known antiviral immune mechanisms, such as type I interferon signalling and cell-mediated cytotoxicity, and performed a comprehensive protein expression analysis to highlight differences between the two groups in various organs. Significant differences in expression profiles of common carp with and without clinical signs were found to be strongly dependent on the organ from which the sample originated. Components of the complement cascade, including various C3 proteins, exhibited upregulation only in less affected organs, specifically the head kidney and spleen. Other complement proteins such as B/C2 and C9 showed upregulation in the kidney, spleen, and gills but not in the skin. Conversely, lysozymes C and G, were observed to be upregulated in the most affected organs of the skin and gills. This study submits the first description of the immune system related proteome using a mass spectrometry on the samples isolated from fish infected with CEV. It also offers a unique comparison of immune reaction of CEV infected and healthy fish under an infectious pressure.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e14012Subventions
Organisme : European Regional Development Fund
Organisme : Ministerstvo Zemědělství
Informations de copyright
© 2024 The Author(s). Journal of Fish Diseases published by John Wiley & Sons Ltd.
Références
Abdel Rahman, A. N., Van Doan, H., Elsheshtawy, H. M., Dawood, A., Salem, S. M. R., Sheraiba, N. I., Masoud, S. R., Abdelnaeim, N. S., Khamis, T., Alkafafy, M., & Mahboub, H. H. (2022). Dietary Salvia officinalis leaves enhances antioxidant‐immune‐capacity, resistance to Aeromonas sobria challenge, and growth of Cyprinus carpio. Fish & Shellfish Immunology, 127, 340–348. https://doi.org/10.1016/j.fsi.2022.06.030
Adamek, M., El‐Rahman, S. A., Felten, M., Teitge, F., Jung‐Schroers, V., Paley, R., & Steinhagen, D. (2019). Abandon all hope? Is in vitro culturing of carp edema virus a lost cause? Presented at the 19th international conference on diseases of fish and shellfish, 19th international conference on diseases of fish and shellfish. Porto, Portugal.
Adamek, M., Hazerli, D., Matras, M., Teitge, F., Reichert, M., & Steinhagen, D. (2017). Viral infections in common carp lead to a disturbance of mucin expression in mucosal tissues. Fish & Shellfish Immunology, 71, 353–358. https://doi.org/10.1016/j.fsi.2017.10.029
Adamek, M., Jung‐Schroers, V., Hellmann, J., Teitge, F., Bergmann, S., Runge, M., Kleingeld, D., Way, K., Stone, D., & Steinhagen, D. (2016). Concentration of carp edema virus (CEV) DNA in koi tissues affected by koi sleepy disease (KSD). Diseases of Aquatic Organisms, 119, 245–251. https://doi.org/10.3354/dao02994
Adamek, M., Matras, M., Dawson, A., Piackova, V., Gela, D., Kocour, M., Adamek, J., Kaminski, R., Rakus, K., Bergmann, S. M., Stachnik, M., Reichert, M., & Steinhagen, D. (2019). Type I interferon responses of common carp strains with different levels of resistance to koi herpesvirus disease during infection with CyHV‐3 or SVCV. Fish & Shellfish Immunology, 87, 809–819. https://doi.org/10.1016/j.fsi.2019.02.022
Adamek, M., Oschilewski, A., Wohlsein, P., Jung‐Schroers, V., Teitge, F., Dawson, A., Gela, D., Piackova, V., Kocour, M., Adamek, J., Bergmann, S. M., & Steinhagen, D. (2017). Experimental infections of different carp strains with the carp edema virus (CEV) give insights into the infection biology of the virus and indicate possible solutions to problems caused by koi sleepy disease (KSD) in carp aquaculture. Veterinary Research, 48, 12. https://doi.org/10.1186/s13567‐017‐0416‐7
Adamek, M., Rakus, K., Brogden, G., Matras, M., Chyb, J., Hirono, I., Kondo, H., Aoki, T., Irnazarow, I., & Steinhagen, D. (2014). Interaction between type I interferon and cyprinid herpesvirus 3 in two genetic lines of common carp Cyprinus carpio. Diseases of Aquatic Organisms, 111, 107–118. https://doi.org/10.3354/dao02773
Adamek, M., Syakuri, H., Harris, S., Rakus, K. Ł., Brogden, G., Matras, M., Irnazarow, I., & Steinhagen, D. (2013). Cyprinid herpesvirus 3 infection disrupts the skin barrier of common carp (Cyprinus carpio L.). Veterinary Microbiology, 162, 456–470. https://doi.org/10.1016/j.vetmic.2012.10.033
Adamek, M., Teitge, F., Baumann, I., Jung‐Schroers, V., El Rahman, S. A., Paley, R., Piackova, V., Gela, D., Kocour, M., Rakers, S., Bergmann, S. M., Ganter, M., & Steinhagen, D. (2021). Koi sleepy disease as a pathophysiological and immunological consequence of a branchial infection of common carp with carp edema virus. Virulence, 12, 1855–1883. https://doi.org/10.1080/21505594.2021.1948286
Andersen, C. L., Jensen, J. L., & Ørntoft, T. F. (2004). Normalization of real‐time quantitative reverse transcription‐PCR data: A model‐based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research, 64, 5245–5250. https://doi.org/10.1158/0008‐5472.CAN‐04‐0496
Baloch, A. A., Steinhagen, D., Gela, D., Kocour, M., Piačková, V., & Adamek, M. (2023). Immune responses in carp strains with different susceptibility to carp edema virus disease. PeerJ, 11, e15614. https://doi.org/10.7717/peerj.15614
Beaz Hidalgo, R., Agüeria, D. A., Latif Eugenín, F., Yeannes, M. I., & Figueras, M. J. (2015). Molecular characterization of Shewanella and Aeromonas isolates associated with spoilage of common carp (Cyprinus carpio). FEMS Microbiology Letters, 362, 1–8. https://doi.org/10.1093/femsle/fnu029
Boudinot, P., Bird, S., Du Pasquier, L., & Collet, B. (2021). The repertoire of vertebrate STAT transcription factors: Origin and variations in fish. Developmental & Comparative Immunology, 116, 103929. https://doi.org/10.1016/j.dci.2020.103929
Boudinot, P., Langevin, C., Secombes, C., & Levraud, J.‐P. (2016). The peculiar characteristics of fish type I interferons. Viruses, 8, 298. https://doi.org/10.3390/v8110298
Buller, R. M., & Palumbo, G. J. (1991). Poxvirus pathogenesis. Microbiological Reviews, 55, 80–122. https://doi.org/10.1128/mr.55.1.80‐122.1991
Cano, I., Mulhearn, B., Akter, S., & Paley, R. (2020). Seroconversion and skin mucosal parameters during koi herpesvirus shedding in common carp, Cyprinus carpio. International Journal of Molecular Sciences, 21, 8482. https://doi.org/10.3390/ijms21228482
Chico, V., Salvador‐Mira, M. E., Nombela, I., Puente‐Marin, S., Perez, L., Mercado, L., & Ortega‐Villaizan, M. D. M. (2021). Antiviral function of NKEF against VHSV in rainbow trout. Biology (Basel), 10, 1045. https://doi.org/10.3390/biology10101045
Evans, D. L., Leary, J. H., & Jaso‐Friedmann, L. (2001). Nonspecific cytotoxic cells and innate immunity: Regulation by programmed cell death. Developmental & Comparative Immunology, 25, 791–805. https://doi.org/10.1016/S0145‐305X(01)00036‐2
FAOSTAT. (2023). Aquaculture Feed and Fertilizer Resources Information System. Retrieved April 2, 2022, from https://www.fao.org/faostat/en/#home
Fonnesbech Vogel, B., Venkateswaran, K., Satomi, M., & Gram, L. (2005). Identification of Shewanella baltica as the most important H2S‐producing species during iced storage of Danish marine fish. Applied and Environmental Microbiology, 71(11), 6689–6697. https://doi.org/10.1128/AEM.71.11.6689‐6697.2005
Fujiki, K., Shin, D. H., Nakao, M., & Yano, T. (2000). Molecular cloning of carp (Cyprinus carpio) leucocyte cell‐derived chemotaxin 2, glia maturation factor beta, CD45 and lysozyme C by use of suppression subtractive hybridisation. Fish & Shellfish Immunology, 10, 643–650. https://doi.org/10.1006/fsim.2000.0294
Gilad, O., Yun, S., Zagmutt‐Vergara, F. J., Leutenegger, C. M., Bercovier, H., & Hedrick, R. P. (2004). Concentrations of a koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real‐time TaqMan PCR. Diseases of Aquatic Organisms, 60(3), 179–187. https://doi.org/10.3354/dao060179
Gilliet, M., Cao, W., & Liu, Y.‐J. (2008). Plasmacytoid dendritic cells: Sensing nucleic acids in viral infection and autoimmune diseases. Nature Reviews Immunology, 8, 594–606. https://doi.org/10.1038/nri2358
Gjessing, M. C., Krasnov, A., Timmerhaus, G., Brun, S., Afanasyev, S., Dale, O. B., & Dahle, M. K. (2020). The Atlantic Salmon gill transcriptome response in a natural outbreak of Salmon gill pox virus infection reveals new biomarkers of gill pathology and suppression of mucosal defense. Frontiers in Immunology, 11, 2154. https://doi.org/10.3389/fimmu.2020.02154
Hoole, D., Bucke, D., Burgess, P., & Wellby, I. (2001). Diseases of carp and other cyprinid fishes. Oxford, UK: Fishing News Books, https://doi.org/10.1002/9780470999752
Janda, J. M., & Abbott, S. L. (2010). The genus Aeromonas: Taxonomy, pathogenicity, and infection. Clinical Microbiology Reviews, 23(1), 35–73. https://doi.org/10.1128/CMR.00039‐09
Koutná, M., Veselý, T., Psikal, I., & Hůlová, J. (2003). Identification of spring viraemia of carp virus (SVCV) by combined RT‐PCR and nested PCR. Diseases of Aquatic Organisms, 55(3), 229–235. https://doi.org/10.3354/dao055229
Kozińska, A., Figueras, M. J., Chacon, M. R., & Soler, L. (2002). Phenotypic characteristics and pathogenicity of Aeromonas genomospecies isolated from common carp (Cyprinus carpio L.). Journal of Applied Microbiology, 93(6), 1034–1041. https://doi.org/10.1046/j.1365‐2672.2002.01784.x
Langevin, C., Aleksejeva, E., Passoni, G., Palha, N., Levraud, J.‐P., & Boudinot, P. (2013). The antiviral innate immune response in fish: Evolution and conservation of the IFN system. Journal of Molecular Biology, 425, 4904–4920. https://doi.org/10.1016/j.jmb.2013.09.033
Lewisch, E., Gorgoglione, B., Way, K., & El‐Matbouli, M. (2015). Carp edema virus/koi sleepy disease: An emerging disease in central‐East Europe. Transboundary and Emerging Diseases, 62(1), 6–12. https://doi.org/10.1111/tbed.12293
Ma, Y. J., & Garred, P. (2018). Pentraxins in complement activation and regulation. Frontiers in Immunology, 9, 3046. https://doi.org/10.3389/fimmu.2018.03046
Magnadottir, B. (2010). Immunological control of fish diseases. Marine Biotechnology, 12, 361–379. https://doi.org/10.1007/s10126‐010‐9279‐x
Matějíčková, K., Pojezdal, Ľ., Pokorová, D., Reschová, S., Piačková, V., Palíková, M., Veselý, T., & Papežíková, I. (2020). Carp oedema virus disease outbreaks in Czech and Slovak aquaculture. Journal of Fish Diseases, 43, 971–978. https://doi.org/10.1111/jfd.13179
Matras, M., Stachnik, M., Borzym, E., Maj‐Paluch, J., & Reichert, M. (2019). Potential vector species of carp edema virus (CEV). Journal of Fish Diseases, 42, 959–964. https://doi.org/10.1111/jfd.13000
Mekata, T., Kawato, Y., & Ito, T. (2021). Complete genome sequence of carp edema virus isolated from koi carp. Microbiology Resource Announcements, 10, e00239–21. https://doi.org/10.1128/MRA.00239‐21
Nakanishi, T., Toda, H., Shibasaki, Y., & Somamoto, T. (2011). Cytotoxic T cells in teleost fish. Developmental & Comparative Immunology, Special Issue on Teleost Fish Immunology, 35, 1317–1323. https://doi.org/10.1016/j.dci.2011.03.033
Oros, M., Hanzelová, V., & Scholz, T. (2009). Tapeworm Khawia sinensis: Review of the introduction and subsequent decline of a pathogen of carp. Cyprinus Carpio. Veterinary Parasitology, 164(2–4), 217–222. https://doi.org/10.1016/j.vetpar.2009.05.010
Palíková, M., Pojezdal, Ľ., Dávidová‐Geržová, L., Nováková, V., Pikula, J., Papežíková, I., Minářová, H., Mikulíková, I., & Dyková, I. (2022). Carp edema virus infection associated gill pathobiome: A case report. Journal of Fish Diseases, 45(10), 1409–1417. https://doi.org/10.1111/jfd.13670
Pikula, J., Pojezdal, L., Papezikova, I., Minarova, H., Mikulikova, I., Bandouchova, H., Blahova, J., Bednarska, M., Mares, J., & Palikova, M. (2021). Carp edema virus infection is associated with severe metabolic disturbance in fish. Frontiers in Veterinary Science, 8, 679970. https://doi.org/10.3389/fvets.2021.679970
Poynter, S. J., & DeWitte‐Orr, S. J. (2016). Fish interferon‐stimulated genes: The antiviral effectors. Developmental & Comparative Immunology, 65, 218–225. https://doi.org/10.1016/j.dci.2016.07.011
Saurabh, S., & Sahoo, P. K. (2008). Lysozyme: An important defence molecule of fish innate immune system. Aquaculture Research, 39, 223–239. https://doi.org/10.1111/j.1365‐2109.2007.01883.x
Seet, B. T., Johnston, J. B., Brunetti, C. R., Barrett, J. W., Everett, H., Cameron, C., Sypula, J., Nazarian, S. H., Lucas, A., & McFadden, G. (2003). Poxviruses and Immune Evasion. Annual Review of Immunology, 21, 377–423. https://doi.org/10.1146/annurev.immunol.21.120601.141049
Shin, D., Fujiki, K., Nakao, M., & Yano, T. (2001). Organization of the NKEF gene and its expression in the common carp (Cyprinus carpio). Developmental & Comparative Immunology, 25, 597‐606. https://doi.org/10.1016/S0145‐305X(01)00021‐0
Sinha, A., Singh, A. K., Kadni, T. S., Mullick, J., & Sahu, A. (2021). Virus‐encoded complement regulators: Current status. Viruses, 13, 208. https://doi.org/10.3390/v13020208
Spiller, O. B., Blackbourn, D. J., Mark, L., Proctor, D. G., & Blom, A. M. (2003). Functional activity of the complement regulator encoded by Kaposi's sarcoma‐associated herpesvirus. Journal of Biological Chemistry, 278, 9283–9289. https://doi.org/10.1074/jbc.M211579200
Uribe, C., Folch, H., Enriquez, R., & Moran, G. (2011). Innate and adaptive immunity in teleost fish: A review. Veterinární Medicína, 56, 486–503. https://doi.org/10.17221/3294‐VETMED
Verrier, E. R., Langevin, C., Benmansour, A., & Boudinot, P. (2011). Early antiviral response and virus‐induced genes in fish. Developmental & Comparative Immunology, Special Issue on Teleost Fish Immunology, 35, 1204–1214. https://doi.org/10.1016/j.dci.2011.03.012
Yin, Z.‐X., He, J.‐G., Deng, W.‐X., & Chan, S.‐M. (2003). Molecular cloning, expression of orange‐spotted grouper goose‐type lysozyme cDNA, and lytic activity of its recombinant protein. Diseases of Aquatic Organisms, 55, 117–123. https://doi.org/10.3354/dao055117
Zelnickova, P., Matiasovic, J., Pavlova, B., Kudlackova, H., Kovaru, F., & Faldyna, M. (2008). Quantitative nitric oxide production by rat, bovine and porcine macrophages. Nitric Oxide, 19, 36–41. https://doi.org/10.1016/j.niox.2008.04.001
Zou, J., Tafalla, C., Truckle, J., & Secombes, C. J. (2007). Identification of a second Group of Type I IFNs in fish sheds light on IFN evolution in vertebrates. The Journal of Immunology, 179, 3859–3871. https://doi.org/10.4049/jimmunol.179.6.3859