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See detailA herpesvirus alters the behavior of its host to enhance its replication
Ronsmans, Maygane ULg

Conference (2015, December 18)

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See detailFrom mucosal resistance of larvae to behavioral fever of fingerlings: a journey in the innate immune defenses of common carp against cyprinid herpesvirus 3
Ronsmans, Maygane ULg

Doctoral thesis (2015)

Cyprinid herpesvirus 3 (CyHV-3) is a highly pathogenic virus responsible for a lethal disease in both common and koi carp (Cyprinus carpio). The common carp is one of the most important freshwater species ... [more ▼]

Cyprinid herpesvirus 3 (CyHV-3) is a highly pathogenic virus responsible for a lethal disease in both common and koi carp (Cyprinus carpio). The common carp is one of the most important freshwater species cultivated for human consumption. Its colourful subspecies koi is grown for personal pleasure and exhibitions. Both common and koi carp are economically important and since its description in the late 1990s, the CyHV-3 has caused severe financial losses in these two carp industries worldwide. Because of its economic importance and its numerous original biological properties, CyHV 3 became rapidly an attractive subject for both applied and fundamental research. The objectives of this thesis were to investigate the role of two unrelated innate immune mechanisms of carp in anti-CyHV-3 immunity. The first objective was to determine the role of epidermal mucus as an innate immune barrier against CyHV-3 entry during the early developmental stages of carp. To test this hypothesis, we investigated the sensitivity and the permissivity of carp to CyHV-3 during the early stages of its development. This hypothesis was tested using a recombinant CyHV-3 strain expressing luciferase as a constitutive reporter gene and in vivo bioluminescence imaging system. We demonstrated that carp are sensitive and permissive to CyHV 3 infection since hatching, but that their sensitivity remains relatively low in the two early developmental stages. Similarly to adults, we confirmed that the skin is the main portal of entry for the virus at early stages, and our results stress out the role of epidermal mucus as an innate immune defense of carp against pathogens even and especially at the early stages of development. The results of this study have been published in Veterinary research. The second objective of this thesis consisted to investigate whether carp express behavioral fever when infected by CyHV-3; and if so, what could be the effect of this innate immune reaction on the development of CyHV 3 disease. When infected by pathogens, both endotherms and ectotherms can express a salutary reaction by increasing their body temperature. While in endotherms this reaction is called fever and depends on intrinsic thermogenesis, ectotherms like teleosts can only upregulate their body temperature by moving to warmer places, hence the term behavioral fever. When studying the pathogenesis of CyHV-3, we observed that carp infected at 24°C (the thermal preference of healthy carp) tended to concentrate around the tank heater when it was running. This observation led us to postulate that infected subjects could express behavioral fever in natural environments where temperature gradients exist. Using multi-chamber tanks encompassing a gradient from 24°C to 32°C, we observed that carp infected by CyHV-3 express a salutary behavioral fever that completely suppresses virus induced mortalities. The relatively late onset of behavioral fever with respect to clinical signs, viral replication and cytokine upregulation led us to postulate that this phenomenon could be delayed by the virus to retain its host at a permissive temperature thereby favoring its replication and spreading. As some herpesviruses have been shown to express soluble decoy cytokine receptors, we hypothesized that CyHV-3 could express such receptor(s) able to neutralize putative pyrogenic cytokines produced by the fish. We found that CyHV-3 ORF12 encodes a soluble decoy receptor for carp Tnfα and that this viral protein makes the virus capable of delaying the migration of infected fish to warmer environments. Remarkably, the study of the molecular mechanism through which the virus alters its host’s behavior led to the discovery of the first pyrogenic cytokine in ectotherms (Tnfα). This study is the first to report the ability of a vertebrate virus to alter the behavior of its host through the expression of a single gene. This second study was submitted for publication when this thesis was printed. In conclusion, we investigated two innate immune mechanisms expressed by carp against CyHV 3 infection. The results generated in this thesis bring findings related to several scientific fields such as virology, immunology, animal behavior, evolution, ecology and even animal welfare. [less ▲]

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See detailRational Development of an Attenuated Recombinant Cyprinid Herpesvirus 3 Vaccine Using Prokaryotic Mutagenesis and In Vivo Bioluminescent Imaging
Boutier, Maxime ULg; Ronsmans, Maygane ULg; Ouyang, Ping et al

in PLoS Pathogens (2015), 11(2), 1004690

Cyprinid herpesvirus 3 (CyHV 3) is causing severe economic losses worldwide in common and koi carp industries, and a safe and efficacious attenuated vaccine compatible with mass vaccination is needed. We ... [more ▼]

Cyprinid herpesvirus 3 (CyHV 3) is causing severe economic losses worldwide in common and koi carp industries, and a safe and efficacious attenuated vaccine compatible with mass vaccination is needed. We produced single deleted recombinants using prokaryotic mutagenesis. When producing a recombinant lacking open reading frame 134 (ORF134), we unexpectedly obtained a clone with additional deletion of ORF56 and ORF57. This triple deleted recombinant replicated efficiently in vitro and expressed an in vivo safety/efficacy profile compatible with use as an attenuated vaccine. To determine the role of the double ORF56-57 deletion in the phenotype and to improve further the quality of the vaccine candidate, a series of deleted recombinants was produced and tested in vivo. These experiments led to the selection of a double deleted recombinant lacking ORF56 and ORF57 as a vaccine candidate. The safety and efficacy of this strain were studied using an in vivo bioluminescent imaging system (IVIS), qPCR, and histopathological examination, which demonstrated that it enters fish via skin infection similar to the wild type strain. However, compared to the parental wild type strain, the vaccine candidate replicated at lower levels and spread less efficiently to secondary sites of infection. Transmission experiments allowing water contamination with or without additional physical contact between fish demonstrated that the vaccine candidate has a reduced ability to spread from vaccinated fish to naïve sentinel cohabitants. Finally, IVIS analyses demonstrated that the vaccine candidate induces a protective mucosal immune response at the portal of entry. Thus, the present study is the first to report the rational development of a recombinant attenuated vaccine against CyHV 3 for mass vaccination of carp. We also demonstrated the relevance of the CyHV 3 carp model for studying alloherpesvirus transmission and mucosal immunity in teleost skin. [less ▲]

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See detailCyprinid herpesvirus 3 : an archetype of fish alloherpesviruses
Boutier, Maxime ULg; Ronsmans, Maygane ULg; Rakus, Krzysztof ULg et al

in Advances in Virus Research (2015), 93

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See detailThe IL-10 homologue encoded by cyprinid herpesvirus 3 is essential neither for viral replication in vitro nor for virulence in vivo
Ouyang, Ping ULg; Rakus, Krzysztof ULg; Boutier, Maxime ULg et al

in Veterinary Research (2013)

Cyprinid herpesvirus 3 (CyHV-3), a member of the family Alloherpesviridae, is the causative agent of a lethal disease in common and koi carp. CyHV-3 ORF134 encodes an interleukin-10 (IL-10) homologue. The ... [more ▼]

Cyprinid herpesvirus 3 (CyHV-3), a member of the family Alloherpesviridae, is the causative agent of a lethal disease in common and koi carp. CyHV-3 ORF134 encodes an interleukin-10 (IL-10) homologue. The present study was devoted to this ORF. Transcriptomic analyses revealed that ORF134 is expressed as a spliced gene belonging to the early-late class. Proteomic analyses of CyHV-3 infected cell supernatant demonstrated that the ORF134 expression product is one of the most abundant proteins of the CyHV-3 secretome. To investigate the role of ORF134 in viral replication in vitro and in virulence in vivo, a deleted strain and a derived revertant strain were produced using BAC cloning technologies. The recombinant ORF134 deleted strain replicated in vitro comparably to the parental and the revertant strains. Infection of fish by immersion in water containing the virus induced comparable CyHV-3 disease for the three virus genotypes tested (wild type, deleted and revertant). Quantification of viral DNA by real time TaqMan PCR (in the gills and the kidney) and analysis of carp cytokine expression (in the spleen) by RT-qPCR at different times post-infection did not revealed any significant difference between the groups of fish infected with the three virus genotypes. Similarly, histological examination of the gills and the kidney of infected fish revealed no significant differences between fish infected with ORF134 deleted virus versus fish infected with the control parental or revertant strains. All together, the results of the present study demonstrate that the IL-10 homologue encoded by CyHV-3 is essential neither for viral replication in vitro nor for virulence in common carp. [less ▲]

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See detailCyprinid herpesvirus 3 : an intersting virus for applied and fundamental research
Rakus; Ouyang, Ping; Boutier, Maxime ULg et al

in Veterinary Research (2013), 44

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See detailLaboratory validation of a lateral flow device for the detection of CyHV-3 antigens in gill swabs
Vrancken, Robert; Boutier, Maxime ULg; Ronsmans, Maygane ULg et al

in Journal of Virological Methods (2013), 193

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See detailSkin mucus of Cyprinus carpio inhibits cyprinid herpesvirus 3 binding to epidermal cells
RAJ, Victor; Fournier, Guillaume ULg; Rakus, Krzysztof ULg et al

in Veterinary Research (2011), 42(92),

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