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A glycoprotein I- and glycoprotein E-deficient mutant of infectious laryngotracheitis virus exhibits impaired cell-to-cell spread in cultured cells

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Summary.

In alphaherpesviruses, glycoprotein I (gI) and glycoprotein E (gE) form a heterodimer that functions in cell-to-cell spread of the virus. Generally, alphaherpesvirus mutants that lack these glycoproteins are replication competent in cell culture but show a reduced capacity for cell-to-cell spread and hence smaller plaque sizes. Infectious laryngotracheitis virus (ILTV), or Gallid herpesvirus 1, is an alphaherpesvirus that causes respiratory disease in chickens. The roles of gI and gE in ILTV have not been investigated previously. In this study, a glycoprotein I and glycoprotein E deletion mutant of ILTV (gI/gE-ve ILTV) was generated by replacing the region of the ILTV genome coding for the adjacent gI and gE genes with the gene for enhanced green fluorescent protein (eGFP). This gI/E-ve ILTV was readily propagated in cell culture in the presence of wildtype ILTV (wt ILTV). However, in the absence of wt ILTV the propagation of gI/gE-ve ILTV was severely impaired. Infection of permissive cell cultures with gI/gE-ve ILTV failed to produce plaques but single infected cells could be identified by fluorescence microscopy. This suggests that gI/gE has a more significant role in the cell-to-cell spread of ILTV in vitro than in many other alphaherpesviruses.

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References

  • P Balan N Davis-Poynter S Bell H Atkinson H Browne T Minson (1994) ArticleTitleAn analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ J Gen Virol 75 1245–1258 Occurrence Handle8207391 Occurrence Handle1:CAS:528:DyaK2cXktlSlurY%3D

    PubMed  CAS  Google Scholar 

  • A Brack H Dijkstra H Granzow BG Klupp TC Mettenleiter (1999) ArticleTitleInhibition of virion maturation by simultaneous deletion of glycoproteins E, I and M of pseudorabies virus J Virol 73 5364–5372 Occurrence Handle10364283 Occurrence Handle1:CAS:528:DyaK1MXjvFylu7k%3D

    PubMed  CAS  Google Scholar 

  • BW Calnek HK Adldinger DE Kahn (1970) ArticleTitleFeather follicle epithelium: a source of enveloped and infectious cell-free herpesvirus from Marek’s disease Avian Dis 14 219–233 Occurrence Handle4316765 Occurrence Handle1:STN:280:CS%2BB3s%2FgsFA%3D Occurrence Handle10.2307/1588466

    Article  PubMed  CAS  Google Scholar 

  • JI Cohen H Nguyen (1997) ArticleTitleVaricella-zoster virus glycoprotein I is essential for growth of virus in Vero cells J Virol 71 6813–6920

    Google Scholar 

  • WJ Collins DC Johnson (2003) ArticleTitleHerpes simplex virus gE/I expressed in epithelial cells interferes with cell-to-cell spread J Virol 77 2686–3695 Occurrence Handle12552008 Occurrence Handle1:CAS:528:DC%2BD3sXpvVGlug%3D%3D Occurrence Handle10.1128/JVI.77.4.2686-2695.2003

    Article  PubMed  CAS  Google Scholar 

  • AJ Davison JE Scott (1986) ArticleTitleThe complete DNA sequence of varicella-zoster virus J Gen Virol 67 1759–1816 Occurrence Handle3018124 Occurrence Handle1:CAS:528:DyaL2sXhtlams7Y%3D Occurrence Handle10.1099/0022-1317-67-9-1759

    Article  PubMed  CAS  Google Scholar 

  • KS Dingwell CR Brunetti RL Hendricks Q Tang M Tang AJ Rainbow DC Johnson (1994) ArticleTitleHerpes simplex virus glycoproteins E and I faciliate cell-to-cell spread in vivo and across junctions in cultured cells J Virol 68 834–845 Occurrence Handle8289387 Occurrence Handle1:CAS:528:DyaK2cXhtVWrtLk%3D

    PubMed  CAS  Google Scholar 

  • KS Dingwell DC Johnson (1998) ArticleTitleThe herpes simplex virus gE-gI complex facilitates cell-to-cell spread and binds to components of cell junctions J Virol 7 8933–8942

    Google Scholar 

  • KJ Fahey TJ Bagust JJ York (1983) ArticleTitleLaryngotracheitis herpesvirus infection in the chicken: the role of humoral antibody in immunity to a graded challenge of infection Avian Pathol 12 505–514

    Google Scholar 

  • A Farnsworth K Goldsmith DC Johnson (2003) ArticleTitleHerpes simplex virus glycoproteins gD and gE/I serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm J Virol 77 8481–8494 Occurrence Handle12857917 Occurrence Handle1:CAS:528:DC%2BD3sXlslWru74%3D Occurrence Handle10.1128/JVI.77.15.8481-8494.2003

    Article  PubMed  CAS  Google Scholar 

  • W Fuchs TC Mettenleiter (1996) ArticleTitleDNA sequence and transcriptional analysis of the UL1 to UL5 gene cluster of infectious laryngotracheitis virus J Gen Virol 77 2221–2229 Occurrence Handle8811022 Occurrence Handle1:CAS:528:DyaK28XltlKksLo%3D

    PubMed  CAS  Google Scholar 

  • W Fuchs TC Mettenleiter (1999) ArticleTitleDNA sequence of the UL6 to UL20 genes of infectious laryngotracheitis virus and characterization of the UL10 gene product as a nonglycosylated and nonessential virion protein J Gen Virol 80 2173–2182 Occurrence Handle10466817 Occurrence Handle1:CAS:528:DyaK1MXlt1ejsr4%3D

    PubMed  CAS  Google Scholar 

  • W Fuchs K Ziemann JP Teifke O Werner TC Mettenleiter (2000) ArticleTitleThe non-essential UL50 gene of avian infectious laryngotracheitis virus encodes a functional dUTPase which is not a virulence factor J Gen Virol 81 627–638 Occurrence Handle10675400 Occurrence Handle1:CAS:528:DC%2BD3cXhs1Wqsbw%3D

    PubMed  CAS  Google Scholar 

  • W Fuchs D Wiesner J Veits JP Teifke TC Mettenleiter (2005) ArticleTitleIn vitro and in vivo relevance of infectious laryngotracheitis virus gJ proteins that are expressed from spliced and nonspliced mRNSs J Virol 79 705–716 Occurrence Handle15613298 Occurrence Handle1:CAS:528:DC%2BD2MXlt12jsQ%3D%3D Occurrence Handle10.1128/JVI.79.2.705-716.2005

    Article  PubMed  CAS  Google Scholar 

  • MD Gershon AA Gershon (1999) ArticleTitleRole of glycoproteins in varicella-zoster virus infection Contrib Microbiol 3 43–60 Occurrence Handle10599520 Occurrence Handle1:STN:280:DC%2BD3c%2FmslKhtQ%3D%3D

    PubMed  CAS  Google Scholar 

  • RM Horton HD Hunt SN Ho JK Pullen LR Pease (1989) ArticleTitleEngineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension Gene 77 61–68 Occurrence Handle2744488 Occurrence Handle1:CAS:528:DyaL1MXktVais7k%3D Occurrence Handle10.1016/0378-1119(89)90359-4

    Article  PubMed  CAS  Google Scholar 

  • DC Johnson M Webb TW Wisner C Brunetti (2001) ArticleTitleHerpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread J Virol 75 821–833 Occurrence Handle11134295 Occurrence Handle1:CAS:528:DC%2BD3MXhsFWqug%3D%3D Occurrence Handle10.1128/JVI.75.2.821-833.2001

    Article  PubMed  CAS  Google Scholar 

  • DC Johnson MT Huber (2002) ArticleTitleDirected egress of animal viruses promotes cell-to-cell spread J Virol 76 1–8 Occurrence Handle11739666 Occurrence Handle1:CAS:528:DC%2BD3MXptFCnurs%3D Occurrence Handle10.1128/JVI.76.1.1-8.2002

    Article  PubMed  CAS  Google Scholar 

  • TK Kawaguchi K Nomura Y Hirayama T Kitagawa (1987) ArticleTitleEstablishment and characterization of a chicken hepato-cellular carcinoma cell line, LMH Cancer Res 47 4460–4464 Occurrence Handle3607775 Occurrence Handle1:STN:280:BiiB2szisFU%3D

    PubMed  CAS  Google Scholar 

  • S Mallory M Sommer AM Arvin (1997) ArticleTitleMutational analysis of the role of glycoprotein I in varicella-zoster virus replication and its effects on glycoprotein E conformation and trafficking J Virol 71 8279–8288 Occurrence Handle9343180 Occurrence Handle1:CAS:528:DyaK2sXmvV2iu7k%3D

    PubMed  CAS  Google Scholar 

  • S Mallory M Sommer AM Arvin (1998) ArticleTitleAnalysis of the glycoproteins I and E of varicella-zoster virus (VZV) using deletional mutations of VZV cosmids J Infect Dis 178 S22–S26 Occurrence Handle9852968 Occurrence Handle1:CAS:528:DyaK1cXns1Wmurg%3D

    PubMed  CAS  Google Scholar 

  • TN McMillian DC Johnson (2001) ArticleTitleCytoplasmic domain of herpes simplex virus gE causes accumulation in the trans-Golgi network, a site of virus envelopment and sorting of virions to cell junctions J Virol 75 1928–1940 Occurrence Handle10.1128/JVI.75.4.1928-1940.2001

    Article  Google Scholar 

  • H Otsuka X Xuan (1996) ArticleTitleConstruction of bovine herpesvirus-1 (BHV-1) recombinants which express psuedorabies virus (PRV) glycoproteins gB, gC, gD, gE Arch Virol 70 57–71 Occurrence Handle10.1007/BF01718588

    Article  Google Scholar 

  • B Roizman DM Knipe (2001) Herpes simplex viruses and their replication DM Knipe PM Howley (Eds) Fields virology EditionNumber4 NumberInSeries2 Lippincott Williams and Wilkins Philadelphia 2399–2460

    Google Scholar 

  • D Schumacher BK Tischer SM Reddy N Osterrieder (2001) ArticleTitleGlycoproteins E and I of Marek’s disease virus serotype 1 are essential for virus growth in cultured cells J Virol 75 11307–11318 Occurrence Handle11689611 Occurrence Handle1:CAS:528:DC%2BD3MXotlartbk%3D Occurrence Handle10.1128/JVI.75.23.11307-11318.2001

    Article  PubMed  CAS  Google Scholar 

  • C Seyboldt H Granzow N Osterrieder (2000) ArticleTitleEquine herpesvirus 1 (EHV-1) glycoprotein M: effect of deletions of transmembrane domains Virology 278 477–489 Occurrence Handle11118370 Occurrence Handle1:CAS:528:DC%2BD3cXovVCmsL0%3D Occurrence Handle10.1006/viro.2000.0664

    Article  PubMed  CAS  Google Scholar 

  • X Tan P Brunovskis LF Velicer (2001) ArticleTitleTranscriptional analysis of Marek’s disease virus glycoprotein D, I, and E genes: gD expression is undetectable in cell culture J Virol 75 2067–2075 Occurrence Handle11160711 Occurrence Handle1:CAS:528:DC%2BD3MXhtlGgsL4%3D Occurrence Handle10.1128/JVI.75.5.2067-2075.2001

    Article  PubMed  CAS  Google Scholar 

  • MA Wild S Cook M Cochran (1996) ArticleTitleA genomic map of infectious laryngotracheitis virus and the sequence and organization of genes present in the unique short and flanking regions Virus Genes 12 107–116 Occurrence Handle8879127 Occurrence Handle1:CAS:528:DyaK28XltlKitrc%3D Occurrence Handle10.1007/BF00572949

    Article  PubMed  CAS  Google Scholar 

  • T Wisner C Brunetti K Dingwell DC Johnson (2000) ArticleTitleThe extracellular domain of herpes simplex virus gE is sufficient for accumulation at cell junctions but not cell-to-cell spread J Virol 74 2278–2287 Occurrence Handle10666258 Occurrence Handle1:CAS:528:DC%2BD3cXhtF2kt7Y%3D Occurrence Handle10.1128/JVI.74.5.2278-2287.2000

    Article  PubMed  CAS  Google Scholar 

  • K Ziemann TC Mettenleiter W Fuchs (1998) ArticleTitleGene arrangement within the unique long genome region of infectious laryngotracheitis virus is distinct from that of other alphaherpesviruses J Virol 72 847–852 Occurrence Handle9420298 Occurrence Handle1:CAS:528:DyaK1cXhvFCktA%3D%3D

    PubMed  CAS  Google Scholar 

  • Zuckermann FA, Mettenleiter TC, Schreurs NS, Ben-Porat T (1988) Complex between glycoproteins gI and gp63 of psuedorabies virus: its effect on virus replication. J Virol: 4622–4626

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Devlin, J., Browning, G. & Gilkerson, J. A glycoprotein I- and glycoprotein E-deficient mutant of infectious laryngotracheitis virus exhibits impaired cell-to-cell spread in cultured cells. Arch Virol 151, 1281–1289 (2006). https://doi.org/10.1007/s00705-005-0721-8

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