Glycoproteins E and I facilitate neuron-to-neuron spread of herpes simplex virus

Journal of Virology

Volumn 69, Issue 11, 1995, Pages 7087-7098

  Dingwell, Kevin S ^a   Doering, Laurie C ^a   Johnson, David C ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; GLYCOPROTEIN;

ARTICLE; CELL CULTURE; CELL SPREADING; GENE EXPRESSION; HERPES SIMPLEX VIRUS; PRIORITY JOURNAL; TRIGEMINUS GANGLION; VIRUS CELL INTERACTION; VIRUS REPLICATION;

EID: 0028849767     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.69.11.7087-7098.1995     Document Type: Article

References (62)

1. Adler, R., J. C. Glorioso, J. Cossman, and M. Levine. 1978. Possible role of Fc receptors on cells infected and transformed by herpes virus: escape from immune cytolysis. Infect. Immun. 21:442-447.
2. 1a. Babic, N., T. C. Mettenleiter, A. Flamand, and G. Ugolini. 1993. Role of essential glycoproteins gII and gp50 in transneuronal transfer of pseudorabies virus from the hypoglossal nerves of mice. J. Virol. 67:4421-4426.
3. L16 are dispensable for the replication of herpes simplex virus 1 in cell culture. J. Virol. 65:938-944.
4. L10 gene of herpes simplex virus 1 encodes a novel viral glycoprotein, gM, which is present in the virion and in the plasma membrane of infected cells. J. Virol. 67:1441-1452.
5. Balan, P., N. Davis-Poynter, S. Bell, H. Atkinson, H. Browne, and T. Minson. 1994. An 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.
6. Bell, S., M. Cranage, L. Borysiewicz, and T. Minson. 1990. Induction of immunoglobulin G by Fc receptors by recombinant vaccinia viruses expressing glycoproteins E and I of herpes simplex virus type 1. J. Virol. 64:2181-2186.
7. Brunetti, C. R., R. L. Burke, B. Hoflack, T. Ludwig, K. S. Dingwell, and D. C. Johnson. 1995. Role of mannose-6-phosphate receptors in herpes simplex virus entry into cells and cell-to-cell transmission. J. Virol. 69:3517-3528.
8. Cai, W., B. Gu, and S. Person. 1988. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J. Virol. 62:2596-2604.
9. Card, J. P., L. Rinaman, R. B. Lynn, B.-H. Lee, R. P. Meade, R. R. Miselis, and L. W. Enquist. 1993. Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis. J. Neurorosci. 13:2515-2539.
10. Card, J. P., M. E. Whealy, A. K. Robbins, and L. W. Enquist. 1992. Pseudorabies virus envelope glycoprotein gI influences both neurotropism and virulence during infection of the rat visual system. J. Virol. 66:3032-3041.
11. Card, J. P., M. E. Whealy, A. K. Robbins, R. Y. Moore, and L. W. Enquist. 1991. Two α-herpesvirus strains are transported differentially in the rodent visual system. Neuron 6:957-969.
12. Cook, M. L., and J. G. Stevens. 1973. Pathogenesis of herpetic neuritis and ganglionitis in mice: evidence for intra-axonal transport of infection. Infect. Immun. 7:272-288.
13. DeVries, S. H., and D. A. Baylor. 1993. Synaptic circuitry of the retina and olfactory bulb. Cell, 72/Neuron, 10(Suppl.): 139-149.
14. Dingwell, K. S., C. R. Brunetti, R. L. Hendricks, Q. Tang, M. Tang, A. J. Rainbow, and D. C. Johnson. 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.
15. Dingwell, K. S., and D. C. Johnson. Unpublished data.
16. Dotti, C. G., and K. Simons. 1990. Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell 62:63-72.
17. Dowler, K. W., and R. W. Veltri. 1984. In vitro neutralization of HSV-2: inhibition by binding of normal IgG and purified Fc to virion Fc receptor (FcR). J. Med. Virol. 13:251-259.
18. Ejercito, P. M., E. D. Kieff, and B. Roizman. 1968. Characterization of herpes simplex virus strains differing in their effect on social behaviour of infected cells. J. Gen. Virol. 2:357-364.
19. Enquist, L. W., J. Dubin, M. E. Whealy, and J. P. Card. 1994. Complementation analysis of pseudorabies virus gE and gI mutants in retinal ganglion cell neurotropism. J. Virol. 68:5275-5279.
20. Forrester, A., H. Farrell, G. Wilkinson, J. Kaye, N. Davis-Poynter, and T. Minson. 1992. Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted. J. Virol. 66:341-348.
21. Frank, I., and H. M. Friedman. 1989. A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J. Virol. 63:4479-4488.
22. Hanke, T., F. L. Graham, V. Lulitanond, and D. C. Johnson. 1990. Herpes simplex virus IgG receptors induced using recombinant adenovirus vectors expressing glycoproteins E and I. Virology 177:437-444.
23. Higgins, D., P. J. Lein, D. J. Osterhout, and M. I. Johnson. 1991. Tissue culture of mammalian autonomic neurons, p. 177-205. In G. Banker and K. Goslin (ed.), Culturing nerve cells. MIT Press, Cambridge, Mass.
24. Hill, T. J., H. J. Field, and A. P. C. Roome. 1972. Intra-axonal location of herpes simplex virus particles. J. Gen. Virol. 15:253-255.
25. Hutchinson, L., and D. C. Johnson. 1995. Herpes simplex virus glycoprotein K promotes egress of virus particles. J. Virol. 69:5401-5413.
26. Jacobs, L., W. A. M. Mulder, J. T. Van Oirschot, A. L. J. Gielkens, and T. G. Kimman. 1993. Deleting two amino acids in glycoprotein gI of pseudorabies virus decreases virulence and neurotropism for pigs, but does not affect immunogenicity. J. Gen. Virol. 74:2201-2206.
27. Johnson, D. C., M. C. Frame, M. V. Ligas, A. M. Cross, and N. D. Stow. 1988. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J. Virol. 62:1347-1354.
28. Johnson, D. C., and M. W. Ligas. 1988. Herpes simplex viruses lacking glycoprotein D are unable to inhibit virus penetration: quantitative evidence for virus-specific cell surface receptors. J. Virol. 62:4605-4612.
29. Kaneko, A. 1979. Physiology of the retina. Annu. Rev. Neurosci. 2:169-191.
30. Kimman, T. G., N. de Wind, N. Oei-Lie, J. M. A. Pol, A. J. M. Berns, and A. L. J. Geilkens. 1992. Contribution of single genes within the unique short region of Aujeszky's disease virus (suid herpesvirus type 1) to virulence, pathogenesis and immunogenicity. J. Gen. Virol. 73:243-251.
31. Kristensson, K., E. Lycke, M. Roytta, B. Svennerholm, and A. Vahlne. 1986. Neuritic transport of herpes simplex virus in rat sensory neurons in vitro. Effects of substances interacting with microtubular function and axonal flow [nocodazole, taxol and erythro-9-3-(2-hydroxynonyl)adenine]. J. Gen. Virol. 67:2023-2028.
32. Kristensson, K., E. Lycke, and J. Sjostrand. 1971. Spread of herpes simplex virus in peripheral nerves. Acta Neuropathol. 17:44-53.
33. Kristensson, K., I. Nennesmo, L. Persson, and E. Lycke. 1982. Neuron to neuron transmission of herpes simplex virus. J. Neurol. Sci. 54:149-156.
34. Kritas, S. K., M. B. Pensaert, and T. C. Mettenleiter. 1994. Role of envelope glycoproteins gI, gp63, and gIII in the invasion and spread of Aujeszky's disease virus in the olfactory nervous pathway of the pig. J. Gen. Virol. 75:2319-2327.
35. Ligas, M. W., and D. C. Johnson. 1988. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by β-galactosidase sequences binds to but is unable to penetrate into cells. J. Virol. 62:1486-1494.
36. Linden, R., and V. H. Perry. 1983. Massive retinotectal projection in rats. Brain Res. 272:145-149.
37. Longnecker, R., S. Chatterjee, R. J. Whitley, and B. Roizman. 1987. Identification of a herpes simplex virus 1 glycoprotein gene within a gene cluster dispensable for growth in cell culture. Proc. Natl. Acad. Sci. USA 84:4303-4307.
38. Longnecker, R., and B. Roizman. 1986. Generation of an inverting herpes simplex virus 1 mutant lacking the L-S junction a sequences, an origin of DNA synthesis, and several genes including those specifying glycoprotein E and the α47 gene. J. Virol. 58:583-591.
39. Longnecker, R., and B. Roizman. 1987. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome. Science 236: 573-576.
40. McGeoch, D. J. 1990. Evolutionary relationships of virion glycoprotein genes in the S regions of alphaherpesvirus genomes. J. Gen. Virol. 71:2361-2367.
41. McLean, J. H., M. T. Shipley, and D. I. Bernstein. 1989. Golgi-like transneuronal retrograde labelling with CNS injections of herpes simplex virus type 1. Brain. Res. Bull. 22:867-881.
42. Neidhardt, H., C. H. Schroder, and H. C. Kaerner. 1987. Herpes simplex virus type 1 glycoprotein E is not indispensable for viral infection. J. Virol. 61:600-603.
43. Norgren, R. B., and M. N. Lehman. 1989. Retrograde transneuronal transport of herpes simplex virus in the retina after injection in the superior colliculus, hypothalamus and optic chiasm. Brain Res. 479:374-378.
44. Norgren, R. B., J. H. McLean, H. C. Bubel, A. Wander, D. I. Bernstein, and M. N. Lehman. 1992. Anterograde transport of HSV-1 and HSV-2 in the visual system. Brain. Res. Bull. 28:393-399.
45. Parnavelas, J. G., A. Dinopoulos, and S. W. Davies. 1989. The central visual pathways, p. 1-164. In A. Bjorklund, T. Hokfelt, and L. W. Swanson (ed.), Handbook of chemical neuroanatomy, vol. 7. Integrated systems of the CNS, part III. Elsevier Science Publishers, New York.
46. Peeters, B., N. de Wind, M. Hooisma, F. Wagenaar, A. Gielkens, and R. Moormann. 1992. Pseudorabies virus envelope glycoproteins gp50 and gII are essential for virus penetration, but only gII is involved in membrane fusion. J. Virol. 66:894-905.
47. Peeters, B., J. Pol, A. Gielkens, and R. Moormann. 1993. Envelope glycoprotein gp50 of pseudorabies virus is essential for virus entry but is not required for viral spread in mice. J. Virol. 67:170-177.
48. Penfold, M. E. E., P. Armati, and A. L. Cunningham. 1994. Axonal transport of herpes simplex virions to epidermal cells: evidence for a specialized mode of virus transport and assembly. Proc. Natl. Acad. Sci. USA 91:6529-6533.
49. Rajcani, J., U. Herget, and H. C. Kaerner. 1990. Spread of herpes simplex virus (HSV) strains SC16, ANG, ANGpath and its glyC minus and glyE minus mutants in DBA-2 mice. Acta Virol. 34:305-320.
50. Rodieck, R. W. 1979. Visual pathways. Annu. Rev. Neurosci. 2:193-225
51. Roop, C., L. Hutchinson, and D. C. Johnson. 1993. A mutant herpes simplex virus type 1 unable to express glycoprotein L cannot enter cells, and its particles lack glycoprotein H. J. Virol. 67:2285-2297.
52. Ruyechan, W. T., L. S. Morse, D. M. Knipe, and B. Roizman. 1979. Molecular genetics of herpes simplex virus. II. Mapping of the major viral glycoproteins and of the genetic loci specifying the social behavior of infected cells. J. Virol. 29:677-697.
53. Simmons, A., D. Tscharke, and P. Speck. 1992. The role of immune mechanisms in control of herpes simplex virus infection of the peripheral nervous system. Curr. Top. Microbiol. Immunol. 179:31-56.
54. Smiley, J. R., D. C. Johnson, L. I. Pizer, and R. D. Everett. 1992. The ICP4 binding sites in the herpes simplex virus type 1 glycoprotein D (gD) promoter are not essential for efficient gD transcription during virus infection J. Virol. 66:623-631.
55. Ugolini, G., H. G. J. M. Kuypers, and A. Simmons. 1987. Retrograde transneuronal transfer of herpes simplex virus type 1 (HSV 1) from motoneurones. Brain Res. 422:242-256.
56. Ugolini, G., H. G. J. M. Kuypers, and P. L. Strick. 1989. Transneuronal transfer of herpes virus from peripheral nerves to cortex and brainstem. Science 243:89-91.
57. Vahlne, A., B. Nystrom, M. Sandberg, A. Hamberger, and E. Lycke. 1987 Attachment of herpes simplex virus to neurons and glial cells. J. Gen. Virol. 40:359-371.
58. Weber, P. C., M. Levine, and J. C. Glorioso. 1987. Rapid identification of nonessential genes of herpes simplex virus type 1 by Tn5 mutagenesis. Science 236:576-579.
59. Whealy, M. E., J. P. Card, A. K. Robbins, J. R. Dubin, H.-J. Rziha, and L. W. Enquist. 1993. Specific pseudorabies virus infection of the rat visual system requires both gI and gp63 glycoproteins. J. Virol. 67:3786-3797.
60. York, I. A., and D. C. Johnson. 1995. Inhibition of humoral and cellular immune recognition by herpes simplex viruses, p. 89-110. In G. McFadden (ed.), Viroceptors, virokines and related immune modulators encoded by DNA viruses. R. G. Landes Company, Austin, Tex.
61. York, I. A., C. Roop, D. W. Andrews, S. R. Riddell, F. L. Graham, and D. C. Johnson. 1994. A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell 77:525-535.
62. Zsak, L., F. Zuckermann, N. Sugg, and T. Ben-Porat. 1992. Glycoprotein gI of pseudorabies virus promotes cell fusion and virus spread via direct cell-to-cell transmission. J. Virol. 66:2316-2325.