Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2009 Jun;83(12):6115-24.
doi: 10.1128/JVI.00128-09. Epub 2009 Apr 8.

The herpes simplex virus type 1 glycoprotein D (gD) cytoplasmic terminus and full-length gE are not essential and do not function in a redundant manner for cytoplasmic virion envelopment and egress

Affiliations

The herpes simplex virus type 1 glycoprotein D (gD) cytoplasmic terminus and full-length gE are not essential and do not function in a redundant manner for cytoplasmic virion envelopment and egress

Hyun Cheol Lee et al. J Virol. 2009 Jun.

Abstract

Herpes simplex virus type 1 (HSV-1) acquires its final envelope by budding into cytoplasmic vesicles thought to be derived from trans-Golgi network membranes. This process is facilitated by interactions among the carboxyl termini of viral glycoproteins and tegument proteins. To directly investigate the relative importance of the carboxyl terminus of glycoprotein D (gD) in the presence or absence of gE, a recombinant virus (gDDeltact) was constructed to specify a truncated gD lacking the carboxy-terminal 29 amino acids. Furthermore, two additional recombinant viruses were constructed by mutating from ATG to CTG the initiation codons of gE (gEctg) or both gE and gM (gEctg+gMctg), causing lack of expression of gE or both gE and gM, respectively. A fourth mutant virus was constructed to specify the gEctg+gDDeltact mutations. The replication properties of these viruses were compared to those of a newly constructed recombinant virus unable to express UL20 due to alteration of the two initiation codons of UL20 (UL20ctgctg). All recombinant viruses were constructed by using the double-Red, site-directed mutagenesis system implemented on the HSV-1(F) genome cloned into a bacterial artificial chromosome. The gEctg, gEctg+gMctg, gDDeltact, and gEctg+gDDeltact viruses produced viral plaques on African monkey kidney cells (Vero), as well as other cells, that were on average approximately 30 to 50% smaller than those produced by the wild-type virus HSV-1(F). In contrast, the UL20ctgctg virus produced very small plaques containing three to five cells, as reported previously for the DeltaUL20 virus lacking the entire UL20 gene. Viral replication kinetics of intracellular and extracellular viruses revealed that all recombinant viruses produced viral titers similar to those produced by the wild-type HSV-1(F) virus intracellularly and extracellularly at late times postinfection, with the exception of the UL20ctgctg and DeltaUL20 viruses, which replicated more than two-and-a-half logs less efficiently than HSV-1(F). Electron microscopy confirmed that all viruses, regardless of their different gene mutations, efficiently produced enveloped virions within infected cells, with the exception of the UL20ctgctg and DeltaUL20 viruses, which accumulated high levels of unenveloped virions in the cytoplasm. These results show that the carboxyl terminus of gD and the full-length gE, either alone or in a redundant manner, are not essential in cytoplasmic virion envelopment and egress from infected cells. Similarly, gM and gE do not function alone or in a redundant manner in cytoplasmic envelopment and virion egress, confirming previous findings.

PubMed Disclaimer

Figures

FIG. 1.
FIG. 1.
Genomic map of mutated genes. (a) Represents the prototypic arrangement of the HSV-1 genome with the unique long (UL) and unique short (US) regions flanked by the terminal repeat (TR) and internal repeat (IR) regions. (b) Shows expanded genomic regions of the UL10, UL20, US6, and US8 open reading frames. (c) Shows the effect of ATG mutagenesis on gM, gE, and UL20 gene expression (cross-hatched regions), as well truncation of gD after gDΔct mutagenesis (cross-hatched gD region).
FIG. 2.
FIG. 2.
Plaque phenotypes of wild-type, gEctg, gDΔct, gEctg+gMctg, gEctg+gDΔct, and ΔUL20 viruses. (A) Confluent Vero cell monolayers were infected with each virus at an MOI of 0.001, and viral plaques were visualized at 48 hpi by immunohistochemistry as described in Materials and Methods. (B) Fifty different viral plaques were randomly selected, imaged, measured, and statistically analyzed as described in Materials and Methods. Natural log-transformed data for each mutant and the wild-type virus are depicted as bar graphs with standard errors. Similar results were obtained when 50 viral plaques were measured at 24 hpi (not shown).
FIG. 3.
FIG. 3.
Viral replication kinetics. Comparison of virus replication characteristics of wild-type (WT) and mutant viruses. Viral titers at different times after infection of Vero cells at an MOI of 2 were determined for intracellular virus (A) or extracellular virus (B). The experiment was performed a second time, the titers obtained averaged, and the standard deviation calculated for each time point.
FIG. 4.
FIG. 4.
Western immunoblot analysis of glycoproteins specified by mutant viruses. (A) anti-gB monoclonal antibody (MAb) was used to detect gB. (B) gC detection using anti-gC MAb. (C) gD detection using anti-gD MAb. For all panels, lane 1 is wild-type virus cellular extracts; lane 2 is gDΔct; lane 3 is gEctg+gDΔct; lane 4 is gEctg-rescued virus; lane 5 is gEctg; lane 6 is gEctg+gMctg; and lane 7 is mock-infected Vero cell extracts.
FIG. 5.
FIG. 5.
Immunofluorescence detection of gE expression. Vero cells were infected at an MOI of 1, and gE expression was detected by indirect immunofluorescence at 36 hpi. The panels in the left column are phase-contrast micrographs of infected cells. The panels in the center column are fluorescent micrographs of mutant viruses lacking gE with anti-gE monoclonal antibody. The panels in the right column are fluorescent micrographs of mutant and wild-type viruses that express gE. All mutant viruses containing the ATG-to-CTG mutations in gE (gEctg) failed to react with anti-gE antibody (panels B, E, and H), while viruses expressing the wild-type gE reacted with the anti-gE antibody (panels C, F, and I).
FIG. 6.
FIG. 6.
Ultrastructural morphologies of mutant viruses. Electron micrographs of Vero cells infected at an MOI of 5 with different viruses and processed for electron microscopy at 16 hpi are shown. Enlarged sections of each micrograph are included as insets in each panel. ΔUL20 (constructed previously) is the mutant virus that has the entire UL20 gene deleted (25). UL20ctgctg is the mutant virus containing two ATG-to-CTG codon initiation mutations six bases apart. Nucleus (n), cytoplasm (c), and extracellular space (e) are marked.

Similar articles

Cited by

References

    1. Ace, C. I., T. A. McKee, J. M. Ryan, J. M. Cameron, and C. M. Preston. 1989. Construction and characterization of a herpes simplex virus type 1 mutant unable to transinduce immediate-early gene expression. J. Virol. 632260-2269. - PMC - PubMed
    1. Atanasiu, D., J. C. Whitbeck, T. M. Cairns, B. Reilly, G. H. Cohen, and R. J. Eisenberg. 2007. Bimolecular complementation reveals that glycoproteins gB and gH/gL of herpes simplex virus interact with each other during cell fusion. Proc. Natl. Acad. Sci. USA 10418718-18723. - PMC - PubMed
    1. Avitabile, E., C. Forghieri, and G. Campadelli-Fiume. 2007. Complexes between herpes simplex virus glycoproteins gD, gB, and gH detected in cells by complementation of split enhanced green fluorescent protein. J. Virol. 8111532-11537. - PMC - PubMed
    1. Bowzard, J. B., R. J. Visalli, C. B. Wilson, J. S. Loomis, E. M. Callahan, R. J. Courtney, and J. W. Wills. 2000. Membrane targeting properties of a herpesvirus tegument protein-retrovirus Gag chimera. J. Virol. 748692-8699. - PMC - PubMed
    1. Brack, A. R., J. M. Dijkstra, H. Granzow, B. G. Klupp, and T. C. Mettenleiter. 1999. Inhibition of virion maturation by simultaneous deletion of glycoproteins E, I, and M of pseudorabies virus. J. Virol. 735364-5372. - PMC - PubMed

Publication types

Substances

LinkOut - more resources