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

. 2017 Feb 21 ; 48 (1) : 12. [epub] 20170221

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28222784
Odkazy

PubMed 28222784
PubMed Central PMC5320791
DOI 10.1186/s13567-017-0416-7
PII: 10.1186/s13567-017-0416-7
Knihovny.cz E-zdroje

Outbreaks of koi sleepy disease (KSD) caused by carp edema virus (CEV) may seriously affect populations of farmed common carp, one of the most important fish species for global food production. The present study shows further evidence for the involvement of CEV in outbreaks of KSD among carp and koi populations: in a series of infection experiments, CEV from two different genogroups could be transmitted to several strains of naïve common carp via cohabitation with fish infected with CEV. In recipient fish, clinical signs of KSD were induced. The virus load and viral gene expression results confirm gills as the target organ for CEV replication. Gill explants also allowed for a limited virus replication in vitro. The in vivo infection experiments revealed differences in the virulence of the two CEV genogroups which were associated with infections in koi or in common carp, with higher virulence towards the same fish variety as the donor fish. When the susceptibility of different carp strains to a CEV infection and the development of KSD were experimentally investigated, Amur wild carp showed to be relatively more resistant to the infection and did not develop clinical signs for KSD. However, the resistance could not be related to a higher magnitude of type I IFN responses of affected tissues. Despite not having a mechanistic explanation for the resistance of Amur wild carp to KSD, we recommend using this carp strain in breeding programs to limit potential losses caused by CEV in aquaculture.

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Food and Agriculture Organization of the United Nations yearbook. Fishery and Aquaculture Statistics 2012. http://www.fao.org/3/478cfa2b-90f0-4902-a836-94a5dddd6730/i3740t.pdf. Accessed 21 Jan 2017

Food and Agriculture Organization of the United Nations, Fisheries and Aquaculture Department http://www.fao.org/fishery/culturedspecies/Cyprinus_carpio/en. Accessed 21 Jan 2017

Bekefi E, Varadi L. Multifunctional pond fish farms in Hungary. Aquacult Int. 2007;15:227–233. doi: 10.1007/s10499-007-9090-5. DOI

Baruš V, Peňáz M, Kohlmann K. Cyprinus carpio (Linnaeus, 1758) In: Bănărescu P, Paepke HJ, editors. The Freshwater Fishes of Europe. Wiebelsheim: AULA-Verlag GmbH; 2002.

Sunarto A, Rukyani A, Itami T. Indonesian experience on the outbreak of koi herpesvirus in koi and carp (Cyprinus carpio) Bull Fish Res Agen Suppl. 2005;2:15–21.

Miyazaki T, Isshiki T, Katsuyuki H. Histopathological and electron microscopy studies on sleepy disease of koi Cyprinus carpio koi in Japan. Dis Aquat Organ. 2005;65:197–207. doi: 10.3354/dao065197. PubMed DOI

Oyamatsu T, Hata N, Yamada K, Sano T, Fukuda H. An etiological study on mass mortality of cultured colorcarp juveniles showing edema. Fish Pathol. 1997;32:81–88. doi: 10.3147/jsfp.32.81. DOI

Way K, Stone D. Emergence of Carp edema virus-like (CEV-like) disease in the UK. CEFAS Finfish News. 2013;15:32–34.

Bachmann J, Keilholz S. Frühjahrsverluste in der fränkischen Karpfenteichwirtschaft—Viraler Erreger als Ursache? Erstnachweise der KSD/CEV in Bayern. Fisch Teichwirt. 2016;03:91–92.

Hedrick RP, Antonio DB, Munn RJ. Poxvirus like agent associated with epizootic mortality in juvenile koi (Cyprinus carpio) FHS Newsletter. 1997;25:1–2.

Murakami Y, Shitanaka M, Toshida S, Matsuzato T (1976) Studies on mass mortality of juvenile carp: about mass mortality showing edema. Bull Hiroshima Fresh Water Fish Exp Stn 19–33 (in Japanese)

Haenen O, Way K, Stone D, Engelsma M. ‘Koi Sleepy Disease’ found for the first time in Koi Carps in the Netherlands. Tijdschr Diergeneeskd. 2014;4:26–29. PubMed

Lewisch E, Gorgoglione B, Way K, El-Matbouli M. Carp edema virus/Koi sleepy disease: an emerging disease in Central-East Europe. Transbound Emerg Dis. 2015;62:6–12. doi: 10.1111/tbed.12293. PubMed DOI

Jung-Schroers V, Adamek M, Teitge F, Hellmann J, Bergmann SM, Schutze H, Kleingeld DW, Way K, Stone D, Runge M, Keller B, Hesami S, Waltzek T, Steinhagen D. Another potential carp killer? Carp edema virus disease in Germany. BMC Vet Res. 2015;11:114. doi: 10.1186/s12917-015-0424-7. PubMed DOI PMC

Matras M, Borzym E, Stone D, Way K, Stachnik M, Maj-Paluch J, Palusińska M, Reichert M. Carp edema virus in Polish aquaculture—evidence of significant sequence divergence and a new lineage in common carp Cyprinus carpio (L.) J Fish Dis. 2017;40:319–325. doi: 10.1111/jfd.12518. PubMed DOI

Oyamatsu T (1996) Study on edema disease of carp. Ph.D. Thesis, Tokyo University of Fisheries, Tokyo. Dissertation No. 142

Haenen O, Way K, Gorgoglione B, Ito T, Paley R, Bigarre L, Waltzek T. Novel viral infections threatening Cyprinid fish. Bull Eur Assoc Fish Pathol. 2016;36:11–23.

Piačková V, Flajšhans M, Pokorová D, Reschová S, Gela D, Čížek A, Veselý T. Sensitivity of common carp, Cyprinus carpio L., strains and crossbreeds reared in the Czech Republic to infection by cyprinid herpesvirus 3 (CyHV-3; KHV) J Fish Dis. 2013;36:75–80. doi: 10.1111/jfd.12007. PubMed DOI

Rakus KL, Wiegertjes GF, Adamek M, Siwicki AK, Lepa A, Irnazarow I. Resistance of common carp (Cyprinus carpio L.) to Cyprinid herpesvirus-3 is influenced by major histocompatibility (MH) class II B gene polymorphism. Fish Shellfish Immunol. 2009;26:737–743. doi: 10.1016/j.fsi.2009.03.001. PubMed DOI

Shapira Y, Magen Y, Zak T, Koder M, Hulata G, Levavi-Sivan B. Differential resistance to koi herpes virus (KHV)/carp interstitial nephritis and gill necrosis virus (CNGV) among common carp (Cyprinus carpio L.) strains and crossbreds. Aquaculture. 2005;245:1–11. doi: 10.1016/j.aquaculture.2004.11.038. DOI

Fischer MA, Davies ML, Reider IE, Heipertz EL, Epler MR, Sei JJ, Ingersoll MA, Rooijen NV, Randolph GJ, Norbury CC. CD11b(+), Ly6G(+) cells produce type I interferon and exhibit tissue protective properties following peripheral virus infection. PLoS Pathog. 2011;7:e1002374. doi: 10.1371/journal.ppat.1002374. PubMed DOI PMC

Arndt WD, Cotsmire S, Trainor K, Harrington H, Hauns K, Kibler KV, Huynh TP, Jacobs BL. Evasion of the innate immune type I interferon system by monkeypox virus. J Virol. 2015;89:10489–10499. doi: 10.1128/JVI.00304-15. PubMed DOI PMC

Kocour M, Gela D, Rodina M, Linhart O. Testing of performance in common carp Cyprinus carpio L. under pond husbandry conditions I: top-crossing with Northern mirror carp. Aquac Res. 2005;36:1207–1215. doi: 10.1111/j.1365-2109.2005.01340.x. DOI

Gilad O, Yun S, Zagmutt-Vergara FJ, Leutenegger CM, Bercovier H, Hedrick RP. Concentrations of a Koi herpesvirus (KHV) in tissues of experimentally infected Cyprinus carpio koi as assessed by real-time TaqMan PCR. Dis Aquat Organ. 2004;60:179–187. doi: 10.3354/dao060179. PubMed DOI

García-Valtanen P, Martinez-Lopez A, Ortega-Villaizan M, Perez L, Coll JM, Estepa A. In addition to its antiviral and immunomodulatory properties, the zebrafish β-defensin 2 (zfBD2) is a potent viral DNA vaccine molecular adjuvant. Antiviral Res. 2014;101:136–147. doi: 10.1016/j.antiviral.2013.11.009. PubMed DOI

Adamek M, Jung-Schroers V, Hellmann J, Teitge F, Bergmann SM, Runge M, Kleingeld DW, Way K, Stone DM, Steinhagen D. Concentration of carp edema virus (CEV) DNA in koi tissues affected by koi sleepy disease (KSD) Dis Aquat Organ. 2016;119:245–251. doi: 10.3354/dao02994. PubMed DOI

Granzow H, Fichtner D, Schütze H, Lenk M, Dresenkamp B, Nieper H, Mettenleiter TC. Isolation and partial characterization of a novel virus from different carp species suffering gill necrosis—ultrastructure and morphogenesis. J Fish Dis. 2014;37:559–569. doi: 10.1111/jfd.12150. PubMed DOI

Ganzhorn J, LaPatra SE. General Procedures for Virology. In: Thoesen John C., editor. Suggested procedures for the detection and identification of certain finfish and shellfish pathogens. Bethesda: American Fisheries Society; 2014.

Adamek M, Syakuri H, Harris S, Rakus KŁ, Brogden G, Matras M, Irnazarow I, Steinhagen D. Cyprinid herpesvirus 3 infection disrupts the skin barrier of common carp (Cyprinus carpio L.) Vet Microbiol. 2013;162:456–470. doi: 10.1016/j.vetmic.2012.10.033. PubMed DOI

Neukirch M, Kunz U. Isolation and preliminary characterization of several viruses from koi (Cyprinus carpio) suffering gill necrosis and mortality. Bull Eur Assoc Fish Pathol. 2001;21:125–135.

Evans DH, Piermarini PM, Choe KP. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev. 2005;85:97–177. doi: 10.1152/physrev.00050.2003. PubMed DOI

Negenborn J, van der Marel MC, Ganter M, Steinhagen D. Cyprinid herpesvirus-3 (CyHV-3) disturbs osmotic balance in carp (Cyprinus carpio L.)—a potential cause of mortality. Vet Microbiol. 2015;177:280–288. doi: 10.1016/j.vetmic.2015.03.018. PubMed DOI

Miwa S, Kiryu I, Yuasa K, Ito T, Kaneko T. Pathogenesis of acute and chronic diseases caused by cyprinid herpesvirus-3. J Fish Dis. 2015;38:695–712. doi: 10.1111/jfd.12282. PubMed DOI

Leef MJ, Harris JO, Powell MD. Respiratory pathogenesis of amoebic gill disease (AGD) in experimentally infected Atlantic salmon Salmo salar. Dis Aquat Organ. 2005;66:205–213. doi: 10.3354/dao066205. PubMed DOI

Haller SL, Peng C, McFadden G, Rothenburg S. Poxviruses and the evolution of host range and virulence. Infect Genet Evol. 2014;21:15–40. doi: 10.1016/j.meegid.2013.10.014. PubMed DOI PMC

Brownstein DG, Bhatt PN, Gras L. Ectromelia virus replication in major target organs of innately resistant and susceptible mice after intravenous infection. Arch Virol. 1993;129:65–75. doi: 10.1007/BF01316885. PubMed DOI

Bidgood SR, Mercer J. Cloak and dagger: alternative immune evasion and modulation strategies of poxviruses. Viruses. 2015;7:4800–4825. doi: 10.3390/v7082844. PubMed DOI PMC

Mahalingam S, Foster PS, Lobigs M, Farber JM, Karupiah G. Interferon-inducible chemokines and immunity to poxvirus infections. Immunol Rev. 2000;177:127–133. doi: 10.1034/j.1600-065X.2000.17720.x. PubMed DOI

Verrier ER, Langevin C, Tohry C, Houel A, Ducrocq V, Benmansour A, Quillet E, Boudinot P. Genetic resistance to rhabdovirus infection in teleost fish is paralleled to the derived cell resistance status. PLoS One. 2012;7:e33935. doi: 10.1371/journal.pone.0033935. PubMed DOI PMC

Adamek M, Rakus KL, Brogden G, Matras M, Chyb J, Hirono I, Kondo H, Aoki T, Irnazarow I, Steinhagen D. Interaction between type I interferon and Cyprinid herpesvirus 3 in two genetic lines of common carp Cyprinus carpio. Dis Aquat Organ. 2014;111:107–118. doi: 10.3354/dao02773. PubMed DOI

Brownstein DG, Bhatt PN, Gras L, Jacoby RO. Chromosomal locations and gonadal dependence of genes that mediate resistance to ectromelia (mousepox) virus-induced mortality. J Virol. 1991;65:1946–1951. PubMed PMC

Brownstein DG, Gras L. Chromosome mapping of Rmp-4, a gonad-dependent gene encoding host resistance to mousepox. J Virol. 1995;69:6958–6964. PubMed PMC

Kocour M, Piackova V, Vesely T, Gela D, Pokorova D, Flajshans M (2012) Perspectives for utilization of Amur mirror carp strains in cross-breeding program of common carp, Cyprinus carpio L., in the Central Europe. In: Abstract Book of AQUA 2012 Conference, Global Aquaculture: securing our future, Prague, September 2012, World Aquaculture Society, p 356

Ono SI, Nagai A, Sugai N. A histopathological study on Juvenile Colorcarp, Cyprinus carpio showing edema. Fish Pathol. 1986;21:167–175. doi: 10.3147/jsfp.21.167. DOI

Wada S, Kurata O, Hatai K, Ishii H, Kasuya K, Watanabe Y. Proliferative branchitis associated with pathognomonic, atypical gill epithelial cells in cultured ayu Plecoglossus altivelis. Fish Pathol. 2008;43:89–91. doi: 10.3147/jsfp.43.89. DOI

Nylund A, Watanabe K, Nylund S, Karlsen M, Sæther PA, Arnesen CE, Karlsbakk E. Morphogenesis of salmonid gill poxvirus associated with proliferative gill disease in farmed Atlantic salmon (Salmo salar) in Norway. Arch Virol. 2008;153:1299–1309. doi: 10.1007/s00705-008-0117-7. PubMed DOI

McFadden G. Poxvirus tropism. Nat Rev Microbiol. 2005;3:201–213. doi: 10.1038/nrmicro1099. PubMed DOI PMC

Neukirch M, Böttcher R, Bunnajirakul S. Isolation of a virus from koi with altered gills. Bull Eur Assoc Fish Pathol. 1999;19:221–223.

Hedrick RP, Gilad O, Yun S, Spangenberg JV, Marty GD, Nordhausen RW, Kebus MJ, Bercovier H, Eldar A. A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. J Aquat Anim Health. 2000;12:44–57. doi: 10.1577/1548-8667(2000)012<0044:AHAWMM>2.0.CO;2. PubMed DOI

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