Skip to main content

Advertisement

SpringerLink
Log in

A block in glycoprotein processing correlates with small plaque morphology and virion targetting to cell-cell junctions for an oral and an anal strain of herpes simplex virus type-1

  • Original Papers
  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary

The characteristics of two clinical isolates of HSV-1 obtained from an oral (424) and an anal (490) lesion were compared with the highly passaged KOS strain. In contrast to KOS, the clinical isolates produced small plaques, were more cell-associated and the predominant viral glycoprotein species for gC and gD in infected cell lysates was the precursor, high mannose glycoform. Total virus production in Vero cells was equivalent for the three virus strains in one-step growths. Pulse-chase studies of glycoprotein C processing showed a reduction in rate at 7.5h post infection and a significant block in processing at 10.5h post infection for 424 and 490 but not KOS. Similar results were obtained for gD. The significant reduction in glycoprotein processing for 424 and 490 suggests a block in transport of viral glycoproteins or virions to and through the Golgi apparatus. Extracellular virions and the cell surface, prior to cell lysis, contained the processed gC glycoform suggesting a competent cellular glycan processing system. Upon co-infection of 424 or 490 with KOS or a gC− KOS strain, gC was processed to levels equivalent to KOS indicating that 424 and 490 are not inhibitory but that an activity(s) encoded by KOS facilitates maturation of gC from 424 and 490. Unlike KOS infected Vero cells, virion-containing vacuoles were observed in the cytoplasm at 12h p.i. and extracellular virions were concentrated at cell-cell junctions of 424 or 490 infected cells but not in the perinuclear region. These results suggest that intracellular transport of viral glycoproteins and virions in 424 and 490 infected cells is different from KOS infected cells. The reduced level of viral glycoprotein maturation, virus release, cell surface presence and presence of virions at cell-cell junctions are consistent with small plaque production in tissue culture cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Baines JD, Roizman B (1992) The UL11 gene of HSV 1 encodes a function that facilitates nucleocapsid envelopment and egress from cells. J Virol 66: 5168–5174

    Google Scholar 

  2. Baines JD, Ward PL, Campadelli-Fiume G, Roizman B (1991) The UL 20 gene of HSV 1 encodes a function necessary for viral egress. J Virol 65: 6414–6424

    Google Scholar 

  3. Baines JD, Koyama AH, Huang T, Roizman B (1994) The UL 21 gene products of HSV 1 are dispensable for growth in cultured cells. J Virol 68: 2929–2936

    Google Scholar 

  4. Blackshear PJ (1984) Systems for polyacrylamide gel electrophoresis. Methods Enzymol 104: 237–255

    Google Scholar 

  5. Brown SM, MacLean AR, Aitken JD, Harland J (1994) ICP34.5 influences herpes simplex virus type 1 maturation and egress from infected cells in vitro. J Virol 75: 3679–3686

    Google Scholar 

  6. Campadelli G, Brandimarti R, Di Lazzaro C, Ward PL, Roizman B, Torrisi MR (1993) Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc Natl Acad Sci U.S.A. 90: 2798–2802

    Google Scholar 

  7. Campadelli-Fiume G, Lombardo MT, Foa-Tomasi L, Avitabile E, Serafina-Cessi F (1988) Individual HSV-1 glycoproteins display characteristic rates of maturation from precursor to mature form both in infected cells and in cells that constitutively express the glycoproteins. Virus Res 10: 29–40

    Google Scholar 

  8. Campadelli-Fiume G, Serafini-Cessi F (1985) Processing of oligosaccharide side chains of herpes simplex type 1. In: Roizman B (ed) The herpesviruses vol 3. Plenum Press, New York, pp 315–356

    Google Scholar 

  9. Constanzo F, Borgatti M, Bartoletti AM, Foa-Tomashi F, Cassai E, Mannini-Palenzona A (1986) Further characterization of virus obtained from herpes simplex virus type 1 recurrences and primary infections, influence of the temperature of incubation upon glycoprotein synthesis and virus release. Arch Virol 88: 293–299

    Google Scholar 

  10. Desai PM, Schaffer PA, Minson AC (1988) Excretion of noninfectious virus particles lacking glycoprotein H by a temperature-sensitive mutant of herpes simplex virus type 1: evidence that gH is essential for virion infectivity. J Gen Virol 69: 1147–1156

    Google Scholar 

  11. Dingwell KS, Brunetti C, Brunetti R, Hendricks R, Tang Q, Tang M, Rainbow A, Johnson DC (1994) Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. J Virol 68: 834–845

    Google Scholar 

  12. Dix, RD, McKendall RR, Baringer JR (1983) Comparative neurovirulence of herpes simplex virus type 1 strains after peripheral or intracerebral inoculation of Balb C mice. Infect Immun 40: 103–112

    Google Scholar 

  13. Ejercito PM, Kieff ED, Roizman B (1968) Characterization of HSV strains differing in their effects on social behavior of infected cells. J Gen Virol 2: 357–364

    Google Scholar 

  14. Epstein AL, Lyon M, Michal Y, Jacquemont B (1990) In vitro divergence of HSV-1 populations propagated in different cell lines. Arch Virol 111: 133–140

    Google Scholar 

  15. Fenwick ML (1984) The effects of herpesviruses on cellular macromolecular synthesis. In: Fraenkel-Conrat H, Wagner R (eds) Comprehensive virology, Vol 19. Plenum Press, New York, pp 359–390

    Google Scholar 

  16. Fitzgerald-Bocarsly P (1993) Human natural interferon-α producing cells. Pharmac Ther 60: 39–62

    Google Scholar 

  17. Homa FL, Otal TM, Glorioso JC, Levine M (1986) Transcriptional control signals of a HSV type 1 late (gamma2) gene lie within bases −34 to +124 relative to the 5′ terminus of the mRNA. Mol Cell Biol 6: 3652–3666

    Google Scholar 

  18. Izumi KM, Stevens JG (1990) Molecular and biological characterization of a HSV-1 neuroinvasion gene. J Exp Med 172: 487–496

    Google Scholar 

  19. Johnson DC, Spear PG (1982) Monensin inhibits the processing of HSV glycoproteins, their transport to the cell surface, and the egress of virions from infected cells. J Virol 43: 1102–1112

    Google Scholar 

  20. Katsumoto T, Hirano A, Kurimura T, Takagi A (1981) The electron microscopical observation of cells infected with herpes simplex virus. J Gen Virol 52: 267–278

    Google Scholar 

  21. Kuismanen E, Saraste J (1989) Low temperature induced transport blocks as tools to manipulate membrane traffic. Methods Cell Biol 32: 260–274

    Google Scholar 

  22. Lundstrom M, Jeansson S, Olofsson S (1987) Host cell induced differences in the O-glycosylation of herpes simplex virus gC-1. Virology 161: 395–402

    Google Scholar 

  23. Mannini-Palenzona A, Bartoletti AM, Foa-Tomasi L, Costanzo F, Bargatti M, Tognon M, Cassai E (1985) Study of herpes simplex virus type 1 populations obtained from recurrences and primary infections. J Med Virol 15: 17–28

    Google Scholar 

  24. Marsden H (1987) Herpes simplex virus glycoproteins and pathogenesis. In: Russell WC, Almond JW (eds) Molecular basis of virus disease: 40th Symposium for the Society for General Microbiology. Cambridge University Press, Cambridge, pp 259–288

    Google Scholar 

  25. McGeoch DJ, Dalrymple MA, Davison AJ, Dolan A, Frame MC, McNab D, Perry LJ, Scott JE, Taylor P (1988) The complete DNA sequence of the long unique region in the genome of HSV-1. J Gen Virol 69: 1531–1574

    Google Scholar 

  26. Pancake BA, Aschman DP, Schaffer PA (1983) Genetic and phenotypic analysis of herpes simplex virus type 1 mutants conditionally resistant to immune cytolysis. J Virol 47: 568–585

    Google Scholar 

  27. Pellett PE, Jenkins FJ, Ackermann M, Sarmiento M, Roizman B (1986) Transcription initiation sites and nucleotide sequence of a herpes simplex virus gene conserved in the Epstein-Barr virus genome and reported to affect the transport of viral glycoproteins. J Virol 60: 1134–1140

    Google Scholar 

  28. Rajcani J (1992) DNA regions and genes determining the virulence of herpes simplex virus. Acta Virol 36: 208–22

    Google Scholar 

  29. Robbins AK, Whealy ME, Enquist LW (1988) Centrifugation procedures for studying herpes viruses using the Sorvall RC-28 SUPRAspeed centrifuge. Biotechnol Update 3: 1–3

    Google Scholar 

  30. Roizman B, Sears AE (1990) Herpes viruses and their replication. In: Fields B, Knipe DM (eds) Virology. Raven Press, New York, pp 1795–1843

    Google Scholar 

  31. Rosenthal KS, Shuman H, Strominger JL (1981) Induction of several new antigens, including a T-cell associated antigen following conversion of the EBV-negative B cell line Ramos to EHRB-Ramos by Epstein-Barr virus. J Immunol 127: 746–754

    Google Scholar 

  32. Smiley ML, Friedman HM (1985) Binding of complement component C3b to glycoprotein C is modulated by sialic acid on herpes simplex virus type 1 infected cells. J Virol 55: 857–861

    Google Scholar 

  33. Smith KO (1964) Relationship between the envelope and the infectivity of herpes simplex virus. Proc Soc Exp Biol Med 115: 814–816

    Google Scholar 

  34. Sommer M, Courtney RJ (1991) Differential rates of processing and transport of herpes simplex virus type 1 glycoproteins gB and gC. J Virol 65: 520–525

    Google Scholar 

  35. Spear P (1985) Glycoproteins specified by HSV. In: Roizman B (ed) The herpes viruses. Plenum Press, New York, pp 315–356

    Google Scholar 

  36. Stevens JG (1993) HSV-1 neuroinvasiveness. Intervirology 35: 152–163

    Google Scholar 

  37. Tengelsen LA, Pederson NE, Shaver PR, Wathen MW, Homa FL (1993) Herpes simplex virus type 1 DNA cleavage and encapsidation require the product of the UL28 gene: isolation and characterization of two UL28 delation mutants. J Virol 67: 3470–3480

    Google Scholar 

  38. Thompson RL, Cook ML, Devi-Rap GB, Wagner EK, Stevens JG (1986) Functional and molecular analyses of the avirulent wile-type herpes simplex virus type 1 strain KOS. J Virol 58: 203–211

    Google Scholar 

  39. Van Genderen IL, Branimarti R, Torrisi MR, Campadelli G, van Meer G (1994) The phospholipid composition of extracellular herpes simplex virions differs from that of host cell nuclei. Virology 200: 831–836

    Google Scholar 

  40. Van Strijp JAG, Van Kessel KPM, Miltenburg LAM, Fluit AC, Verhoef J (1988) Attachment of human polymorphonuclear leukocytes to HSV infected fibroblasts mediated by antibody-independent complement activation. J Virol 62: 847–850

    Google Scholar 

  41. Wander AH, Centifanto YM, Kaufman HE (1980) Strain specificity of clinical isolates of HSV. Arch Opthamol 98: 1458–1461

    Google Scholar 

  42. Ward PL, Campadelli-Fiume G, Avitabile E, Roizman B (1994) Localization and putative function of the UL20 membrane protein in cells infected with herpes simplex virus 1. J Virol 68: 7406–7417

    Google Scholar 

  43. York IA, Johnson DC (1993) Direct contact with herpes simplex virus-infected cells results in inhibition of lymphokine-activated killer cells because of cell-to-cell spread of virus. J Infect Dis 168: 1127–1132

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Northeastern Ohio Universities College of Medicine, Rootstown, Ohio, USA

    J. W. Dick & K. S. Rosenthal

Authors
  1. J. W. Dick
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. S. Rosenthal
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Portions of this work were presented in the 17th International Herpesvirus Workshop, Pittsburgh, PA, 1993.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dick, J.W., Rosenthal, K.S. A block in glycoprotein processing correlates with small plaque morphology and virion targetting to cell-cell junctions for an oral and an anal strain of herpes simplex virus type-1. Archives of Virology 140, 2163–2181 (1995). https://doi.org/10.1007/BF01323238

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01323238

Keywords

Search

Navigation