Summary
Equine herpesviruses 1 and 4 (EHV-1 and EHV-4) cause equine respiratory disease worldwide. However, only EHV-1 is a cause of abortion and neurological disease, despite the two viruses having all 76 genes in common. In addition EHV-1 has a broader host range in cell culture than EHV-4, as exemplified by the rabbit kidney (RK) cell line that is permissive for EHV-1, but not for EHV-4. Here we describe that when EHV-4 produced in equine cells was inoculated onto RK cells expressing glycoprotein D of EHV-1 (RKgD1), infection developed as clusters of rounded cells, and this infectivity could be passaged in RKgD1 cells. The progeny virus could also infect single RK cells, consistent with EHV-4 acquiring EHV1 gD from the complementing cell line. No such infection was observed for EHV-4 in RK cells expressing EHV-1 glycoprotein C. The results are consistent with gD homologues being major determinants of host cell tropism and raise the possibility that gD may be a factor in the differential pathogenicity of EHV-1 and EHV-4.
Similar content being viewed by others
References
GP Allen JH Kydd JD Slater KC Smith (1999) Advances in understanding of the pathogenesis, epidemiology and immunological control of equine herpesvirus abortion U Wernery JF Wade JA Mumford O-R Kaaden (Eds) Equine infectious diseases VIII R & W Publications Newmarket 129–146
AR Awan YC Chong HJ Field (1990) ArticleTitleThe pathogenesis of equine herpesvirus type 1 in the mouse: a new model for studying host responses to the infection J Gen Virol 71 1131–1140 Occurrence Handle2161048
M Azmi HJ Field (1993) ArticleTitleInteractions between equine herpesvirus type 1 and equine herpesvirus type 4: T cell responses in a murine infection model J Gen Virol 74 2339–2345 Occurrence Handle8245851
A Carfi SH Willis JC Whitbeck C Krummenacher GH Cohen RJ Eisenberg DC Wiley (2001) ArticleTitleHerpes simplex virus glycoprotein D bound to the human receptor HveA Mol Cell 8 169–179 Occurrence Handle11511370 Occurrence Handle10.1016/S1097-2765(01)00298-2 Occurrence Handle1:CAS:528:DC%2BD3MXls1Wmsr4%3D
F Cocchi D Fusco L Menotti T Gianni RJ Eisenberg GH Cohen G Campadelli-Fiume (2004) ArticleTitleThe soluble ectodomain of herpes simplex virus gD contains a membrane-proximal pro-fusion domain and suffices to mediate virus entry Proc Nat Acad Sci USA 101 7445–7450 Occurrence Handle15123804 Occurrence Handle10.1073/pnas.0401883101 Occurrence Handle1:CAS:528:DC%2BD2cXksFaktrw%3D
SA Connolly DJ Landsburg A Carfi DC Wiley GH Cohen RJ Eisenberg (2003) ArticleTitleStructure-based mutagenesis of herpes simplex virus glycoprotein D defines three critical regions at the gD-HveA/HVEM binding interface J Virol 77 8127–8140 Occurrence Handle12829851 Occurrence Handle10.1128/JVI.77.14.8127-8140.2003 Occurrence Handle1:CAS:528:DC%2BD3sXlt1Kku7w%3D
SA Connolly DJ Landsburg A Carfi JC Whitbeck Y Zuo DC Wiley GH Cohen RJ Eisenberg (2005) ArticleTitlePotential nectin-1 binding site on herpes simplex virus glycoprotein D J Virol 79 1282–1295 Occurrence Handle15613355 Occurrence Handle10.1128/JVI.79.2.1282-1295.2005 Occurrence Handle1:CAS:528:DC%2BD2MXlt12lsg%3D%3D
BS Crabb MJ Studdert (1995) ArticleTitleEquine herpesviruses 4 (equine rhinopneumonitis virus) and 1 (equine abortion virus) Adv Virus Res 45 153–190 Occurrence Handle7793324 Occurrence Handle1:STN:280:DyaK2MzhtlKiuw%3D%3D
H Csellner C Walker JE Wellington LE McLure DN Love JM Whalley (2000) ArticleTitleEHV-1 glycoprotein D (EHV-1 gD) is required for virus entry and cell-cell fusion, and an EHV-1 gD deletion mutant induces a protective immune response in mice Arch Virol 145 2371–2385 Occurrence Handle11205124 Occurrence Handle10.1007/s007050070027 Occurrence Handle1:CAS:528:DC%2BD3MXhtFChurw%3D
AA Cullinane J Neilan L Wilson AJ Davison G Allen (1993) ArticleTitleThe DNA sequence of the equine herpesvirus-4 gene encoding glycoprotein gp17/18, the homologue of herpes simplex virus glycoprotein gD J Gen Virol 74 1959–1964 Occurrence Handle8397286 Occurrence Handle1:CAS:528:DyaK3sXms1ertb4%3D Occurrence Handle10.1099/0022-1317-74-9-1959
CC Flowers DJ Ocallaghan (1992) ArticleTitleEquine herpesvirus-1 glycoprotein-D – mapping of the transcript and a neutralization epitope J Virol 66 6451–6460 Occurrence Handle1383565 Occurrence Handle1:CAS:528:DyaK3sXhslehtQ%3D%3D
AR Frampton WF Goins JB Cohen J von Einem N Osterrieder DJ O’Callaghan JC Glorioso (2005) ArticleTitleEquine herpesvirus 1 utilizes a novel herpesvirus entry receptor J Virol 79 3169–3173 Occurrence Handle15709036 Occurrence Handle10.1128/JVI.79.5.3169-3173.2005 Occurrence Handle1:CAS:528:DC%2BD2MXitlejsL8%3D
J Gilkerson LR Jorm DN Love GL Lawrence JM Whalley (1994) ArticleTitleEpidemiologic investigation of equid herpesvirus 4 (EHV 4) excretion assessed by nasal swabs taken from thoroughbred foals Vet Microbiol 39 275–283 Occurrence Handle8042275 Occurrence Handle10.1016/0378-1135(94)90164-3 Occurrence Handle1:STN:280:DyaK2czhslakug%3D%3D
JH Kydd KC Smith GJ Livesay JA Mumford (1994) ArticleTitleDistribution of equid herpesvirus-1 (EHV1) in respiratory tract associated lymphoid tissue: implications for cellular immunity Equine Vet J 26 470–473 Occurrence Handle7889921 Occurrence Handle1:STN:280:DyaK2M7ps1Ogtg%3D%3D Occurrence Handle10.1111/j.2042-3306.1994.tb04052.x
RSB Milne AV Nicola JC Whitbeck RJ Eisenberg GH Cohen (2005) ArticleTitleGlycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1 J Virol 79 6655–6663 Occurrence Handle15890903 Occurrence Handle10.1128/JVI.79.11.6655-6663.2005 Occurrence Handle1:CAS:528:DC%2BD2MXksFKhur4%3D
AV Nicola AM McEvoy SE Straus (2003) ArticleTitleRoles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese Hamster Ovary cells J Virol 77 5324–5332 Occurrence Handle12692234 Occurrence Handle10.1128/JVI.77.9.5324-5332.2003 Occurrence Handle1:CAS:528:DC%2BD3sXjtFyku7s%3D
N Osterrieder (1999) ArticleTitleConstruction and characterization of an equine herpesvirus 1 glycoprotein C negative mutant Virus Res 59 165–177 Occurrence Handle10082388 Occurrence Handle10.1016/S0168-1702(98)00134-8 Occurrence Handle1:CAS:528:DyaK1MXnvVWjsg%3D%3D
JR Patel J Heldens (2005) ArticleTitleEquine herpesviruses 1 (EHV-1) and 4 (EHV-4) – epidemiology, disease and immunoprophylaxis: A brief review Vet J 170 14–23 Occurrence Handle15993786 Occurrence Handle10.1016/j.tvjl.2004.04.018 Occurrence Handle1:CAS:528:DC%2BD2MXlsl2rsbo%3D
M Sabine GR Robertson JM Whalley (1981) ArticleTitleDifferentiation of sub-types of equine herpesvirus 1 by restriction endonuclease analysis Aust Vet J 57 148–149 Occurrence Handle6266385 Occurrence Handle1:STN:280:DyaL3M3lsFGqtg%3D%3D
PG Spear (2004) ArticleTitleHerpes simplex virus: receptors and ligands for cell entry Cellular Microbiol 6 401–410 Occurrence Handle10.1111/j.1462-5822.2004.00389.x Occurrence Handle1:CAS:528:DC%2BD2cXjtlOltL8%3D
MJ Studdert MH Blackney (1979) ArticleTitleEquine herpesviruses: on the differentiation of respiratory from foetal strains of type 1 Aust Vet J 55 488–492 Occurrence Handle231960 Occurrence Handle1:STN:280:DyaL3c7ltlWjuw%3D%3D
EAR Telford MS Watson J Perry AA Cullinane AJ Davison (1998) ArticleTitleThe DNA sequence of equine herpesvirus-4 J Gen Virol 79 1197–1203 Occurrence Handle9603335 Occurrence Handle1:CAS:528:DyaK1cXivFOltbo%3D
JE Wellington AA Gooley DN Love JM Whalley (1996) ArticleTitleN-terminal sequence analysis of equine herpesvirus 1 glycoproteins D and B and evidence for internal cleavage of the gene 71 product J Gen Virol 77 75–82 Occurrence Handle8558130 Occurrence Handle1:CAS:528:DyaK28Xjtl2htA%3D%3D
JE Wellington GL Lawrence DN Love JM Whalley (1996) ArticleTitleExpression and characterization of equine herpesvirus 1 glycoprotein D in mammalian cell lines Arch Virol 141 1785–1793 Occurrence Handle8893800 Occurrence Handle10.1007/BF01718301 Occurrence Handle1:CAS:528:DyaK28XmvVChurc%3D
JE Wellington DN Love JM Whalley (1996) ArticleTitleEvidence for involvement of equine herpesvirus 1 glycoprotein B in cell-cell fusion Arch Virol 141 167–175 Occurrence Handle8629945 Occurrence Handle10.1007/BF01718598 Occurrence Handle1:CAS:528:DyaK28XhtlKqu7g%3D
M Whalley G Robertson C Bell D Love M Elphinstone L Wiley D Craven (1991) ArticleTitleIdentification and comparative sequence analysis of a gene in equine herpesvirus-1 with homology to the herpes simplex virus glycoprotein-D Gene Virus Genes 5 313–325 Occurrence Handle1665613 Occurrence Handle10.1007/BF00271530 Occurrence Handle1:CAS:528:DyaK3sXktVehtbY%3D
M Yoon PG Spear (2004) ArticleTitleRandom mutagenesis of the gene encoding a viral ligand for multiple cell entry receptors to obtain viral mutants altered for receptor usage Proc Natl Acad Sci USA 101 17252–17257 Occurrence Handle15557552 Occurrence Handle10.1073/pnas.0407892101 Occurrence Handle1:CAS:528:DC%2BD2cXhtFansr7P
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Whalley, J., Ruitenberg, K., Sullivan, K. et al. Host cell tropism of equine herpesviruses: glycoprotein D of EHV-1 enables EHV-4 to infect a non-permissive cell line. Arch Virol 152, 717–725 (2007). https://doi.org/10.1007/s00705-006-0885-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-006-0885-x