Gallid alphaherpesvirus 1 (syn. infectious laryngotracheitis virus; ILTV) is the causative agent of infectious laryngotracheitis, a respiratory disease of chickens causing substantial economic losses in the poultry industry every year. Currently, the most efficient way to achieve protection against infection is immunization with live-attenuated vaccines. However, this vaccination strategy entails the risk of generating new pathogenic viruses resulting from spontaneous mutations or from recombination with field strains. This work presents a new approach based on virus-like particles (VLPs) displaying ILTV glycoproteins B (gB) or G (gG) on their surface. The main focus of this pilot study was to determine the tolerability of VLPs delivered in ovo and intramuscularly (i.m.) into chickens and to investigate the nature of the immune response elicited. The study revealed that the new vaccines were well tolerated in hybrid layer chicks independent of the administration method (in ovo or i.m.). Upon in ovo injection, vaccination with VLP-gG led to an antibody response, while a cellular immune response in VLP-gB-immunized chickens was hardly detectable. Since the administration of VLPs had no visible side effects in vivo and was shown to elicit an antibody-based immune response, we anticipate that VLPs will become a valuable platform for the development of new safe vaccines for poultry.
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PortzC, BeltrãoN, FurianTQ, JúniorAB, MacagnanM et al. Natural infection of turkeys by infectious laryngotracheitis virus. Vet Microbiol2008; 131:57–64 [View Article]
LeeS-W, MarkhamPF, CoppoMJC, LegioneAR, MarkhamJF et al. Attenuated vaccines can recombine to form virulent field viruses. Science2012; 337:188 [View Article]
BlackerHP, KirkpatrickNC, RubiteA, O'RourkeD, NoormohammadiAH. Epidemiology of recent outbreaks of infectious laryngotracheitis in poultry in Australia. Aust Vet J2011; 89:89–94 [View Article]
DavisonS, GingerichEN, CasavantS, EckroadeRJ. Evaluation of the efficacy of a live fowlpox-vectored infectious laryngotracheitis/avian encephalomyelitis vaccine against ILT viral challenge. Avian Dis2006; 50:50–54 [View Article]
TongGZ, ZhangSJ, WangL, QiuHJ, WangYF et al. Protection of chickens from infectious laryngotracheitis with a recombinant fowlpox virus expressing glycoprotein B of infectious laryngotracheitis virus. Avian Pathol2001; 30:143–148 [View Article]
GimenoIM, CortesAL, GuyJS, TurpinE, WilliamsC. Replication of recombinant herpesvirus of turkey expressing genes of infectious laryngotracheitis virus in specific pathogen free and broiler chickens following in ovo and subcutaneous vaccination. Avian Pathol2011; 40:395–403 [View Article]
EsakiM, NolandL, EddinsT, GodoyA, SaekiS et al. Safety and efficacy of a turkey herpesvirus vector laryngotracheitis vaccine for chickens. Avian Dis2013; 57:192–198 [View Article]
JohnsonDI, VagnozziA, DoreaF, RibletSM, MundtA et al. Protection against infectious laryngotracheitis by in ovo vaccination with commercially available viral vector recombinant vaccines. Avian Dis2010; 54:1251–1259 [View Article]
ChenH-Y, ZhaoL, WeiZ-Y, CuiB-A, WangZ-Y et al. Enhancement of the immunogenicity of an infectious laryngotracheitis virus DNA vaccine by a bicistronic plasmid encoding glycoprotein B and interleukin-18. Antiviral Res Elsevier B.V. 2010; 87:235–241 [View Article]
BachmannMF, RohrerUH, KündigTM, BürkiK, HengartnerH et al. The influence of antigen organization on B cell responsiveness. Science1993; 262:1448–1451 [View Article]
AhsanF, RivasIP, KhanMA, Torres SuárezAI. Targeting to macrophages: role of physicochemical properties of particulate carriers—liposomes and microspheres—on the phagocytosis by macrophages. J Control Release2002; 79:29–40 [View Article]
Kovacsovics-BankowskiM, ClarkK, BenacerrafB, RockKL. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci U S A1993; 90:4942–4946 [View Article]
ZarlingJM, MoranPA, BurkeRL, PachlC, BermanPW et al. Human cytotoxic T cell clones directed against herpes simplex virus-infected cells. IV. Recognition and activation by cloned glycoproteins gB and gD. J Immunol1986; 136:4669–4673
FaheyKJ, YorkJJ, BagustTJ. Laryngotracheitis herpesvirus infection in the chicken. II. the adoptive transfer of resistance with immune spleen cells. Avian Pathol1984; 13:265–275 [View Article]
FaheyKJ, BagustTJ, YorkJJ. Laryngotracheitis herpesvirus infection in the chicken: the role of humoral antibody in immunity to a graded challenge infection. Avian Pathol1983; 12:505–514 [View Article]
FaheyKJ, YorkJJ. The role of mucosal antibody in immunity to infectious laryngotracheitis virus in chickens. J Gen Virol1990; 71:2401–2405 [View Article]
HondaT, OkamuraH, TanenoA, YamadaS, TakahashiE. The role of cell-mediated immunity in chickens inoculated with the cell-associated vaccine of attenuated infectious laryngotracheitis virus. J Vet Med Sci1994; 56:1051–1055 [View Article]
AbrahamR, SinghN, MukhopadhyayA, BasuSK, BalV et al. Modulation of immunogenicity and antigenicity of proteins by maleylation to target scavenger receptors on macrophages. J Immunol1995; 154:1–8
HaberlandME, FogelmanAM. Scavenger receptor-mediated recognition of maleyl bovine plasma albumin and the demaleylated protein in human monocyte macrophages. Proc Natl Acad Sci U S A1985; 82:2693–2697 [View Article]
DevlinJM, LegioneAR, VazPK, LeeS-W, Gilkerson JRM et al. Infectious laryngotracheitis virus viral chemokine-binding protein glycoprotein G alters transcription of key inflammatory mediators in vitro and in vivo. J Virol2018; 92:1–17 [View Article]
DevlinJM, Viejo-BorbollaA, BrowningGF, NoormohammadiAH, GilkersonJR et al. Evaluation of immunological responses to a glycoprotein G deficient candidate vaccine strain of infectious laryngotracheitis virus. Vaccine2010; 28:1325–1332 [View Article]
FuchsW, MettenleiterTC. DNA sequence and transcriptional analysis of the UL1 to UL5 gene cluster of infectious laryngotracheitis virus. J Gen Virol1996; 77:2221–2229 [View Article]
SoneokaY, CannonPM, RamsdaleEE, GriffithsJC, RomanoG et al. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucl Acids Res1995; 23:628–633 [View Article]
KaiserP, RothwellL, GalyovEE, BarrowPA, BurnsideJ et al. Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. Microbiology2000; 146:3217–3226 [View Article]
KogutMH, RothwellL, KaiserP. Priming by recombinant chicken interleukin-2 induces selective expression of IL-8 and IL-18 mRNA in chicken heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella enterica serovar enteritidis. Mol Immunol2003; 40:603–610 [View Article]
BorrensM, GirodA, LelovasP, MorrisonF, TorresYS. The reporting of clinical signs in laboratory animals; 2015
KleinS, GrossmannR. Primary sex ratio in fertilized chicken eggs (Gallus Gallus domesticus) depends on reproductive age and selection. J Exp Zool A Ecol Genet Physiol2008; 309A:35–46 [View Article]
ParkJ-K, LeeD-H, YukS-S, Tseren-OchirE-O, KwonJ-H et al. Virus-like particle vaccine confers protection against a lethal Newcastle disease virus challenge in chickens and allows a strategy of differentiating infected from vaccinated animals. Clin Vaccine Immunol2014; 21:360–365 [View Article]
NohJ-Y, ParkJ-K, LeeD-H, YukS-S, KwonJ-H et al. Chimeric bivalent virus-like particle vaccine for H5N1 HpaI and nd confers protection against a lethal challenge in chickens and allows a strategy of differentiating infected from vaccinated animals (Diva). PLoS One2016; 11:e0162946–13 [View Article]
KapczynskiDR, TumpeyTM, HidajatR, ZsakA, ChrzastekK et al. Vaccination with virus-like particles containing H5 antigens from three H5N1 clades protects chickens from H5N1 and H5N8 influenza viruses. Vaccine2016; 34:1575–1581 [View Article]
WeissmannA, GottschalkJ, ReitemeierS, PreisingerR, EinspanierA. In ovo-gender identification in laying hen hybrids : Effects on hatching and production performance. Eur Poult Sci2014; 78:1–12
LowenthalJW, ConnickT, McWATERSPG, YorkJJ. Development of T cell immune responsiveness in the chicken. Immunol Cell Biol1994; 72:115–122 [View Article]
PetersMA, BrowningGF, WashingtonEA, CrabbBS, KaiserP. Embryonic age influences the capacity for cytokine induction in chicken thymocytes. Immunology2003; 110:358–367 [View Article]
AriaansMP, van de HaarPM, LowenthalJW, van EdenW, HensenEJ et al. ELISPOT and intracellular cytokine staining: novel assays for quantifying T cell responses in the chicken. Dev Comp Immunol2008; 32:1398–1404 [View Article]
BoydAC, Ruiz-HernandezR, PerovalMY, CarsonC, BalkissoonD et al. Towards a universal vaccine for avian influenza: protective efficacy of modified vaccinia virus Ankara and adenovirus vaccines expressing conserved influenza antigens in chickens challenged with low pathogenic avian influenza virus. Vaccine Elsevier Ltd 2013; 31:670–675 [View Article]
WuCC, ThiagarajanD, LinTL. Research notes: ELISPOT assay for detection of antibody secreting cells to infectious bursal disease virus in chickens. Poult Sci1998; 77:662–665 [View Article]
BeirãoBCB, FávaroC, NakaoLS, CaronLF, ZanataSM et al. Flow cytometric immune profiling of specific-pathogen-free chickens before and after infectious challenges. Vet Immunol Immunopathol2012; 145:32–41 [View Article]
BridleBW, JulianR, ShewenPE, VaillancourtJ-P, KaushikAK. T lymphocyte subpopulations diverge in commercially raised chickens. Can J Vet Res2006; 70:183–190
ChenH-Y, CuiP, CuiB-A, LiH-P, JiaoX-Q et al. Immune responses of chickens inoculated with a recombinant fowlpox vaccine coexpressing glycoprotein B of infectious laryngotracheitis virus and chicken IL-18. FEMS Immunol Med Microbiol2011; 63:289–295 [View Article]
GuptaA, AhmedKA, AyalewLE, PopowichS, KurukulasuriyaS et al. Immunogenicity and protective efficacy of virus-like particles and recombinant fiber proteins in broiler-breeder vaccination against fowl adenovirus (FAdV)-8b. Vaccine2017; 35:2716–2722 [View Article]
TaebipourMJ, DadrasH, NazifiS, AfsarM, Ansari-LariM. Evaluation of blood monocyte and lymphocyte population in broiler chicken after vaccination and experimental challenge with Newcastle disease virus. Vet Immunol Immunopathol2017; 190:31–38 [View Article]
KongsuwanK, JohnsonMA, PrideauxCT, SheppardM. Identification of an infectious laryngotracheitis virus gene encoding an immunogenic protein with a predicted M(r) of 32 kilodaltons. Virus Res1993; 29:125–140 [View Article]
GodlewskaR, KuczkowskiM, WyszyńskaA, KlimJ, DerlatkaK et al. Evaluation of a protective effect of in ovo delivered Campylobacter jejuni OMVs. Appl Microbiol Biotechnol2016; 100:8855–8864 [View Article]
KapczynskiDR, MartinA, HaddadEE, KingDJ. Protection from clinical disease against three highly virulent strains of Newcastle disease virus after in ovo application of an antibody-antigen complex vaccine in maternal antibody-positive chickens. Avian Dis2012; 56:555–560 [View Article]