In vitro analysis of transneuronal spread of an alphaherpesvirus infection in peripheral nervous system neurons

Journal of Virology

Volumn 81, Issue 13, 2007, Pages 6846-6857

  Feierbach, B ^a   Bisher, M ^a   Goodhouse, J ^a   Enquist, L W ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS PROTEIN; VIRUS PROTEIN GB; VIRUS PROTEIN GD; VIRUS PROTEIN GE; VIRUS PROTEIN GI; VIRUS PROTEIN US9;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FLUORESCENCE; HERPES; HERPES VIRUS; IN VITRO STUDY; MEMBRANE FUSION; NERVE CELL; NERVE FIBER; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS; RAT; SYNAPSE; ULTRASTRUCTURE; VIRION; VIRUS CELL INTERACTION; VIRUS INFECTIVITY;

ANIMALS; AXONS; BIOLOGICAL TRANSPORT; CATTLE; CELL LINE; HERPESVIRUS 1, SUID; PERIPHERAL NERVES; SWINE; SYNAPSES; VIRAL ENVELOPE PROTEINS;

ANIMALIA; SUID HERPESVIRUS 1;

EID: 34250840529     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00069-07     Document Type: Article

References (33)

1. Antinone, S. E., and G. A. Smith. 2006. Two modes of herpesvirus trafficking in neurons: membrane acquisition directs motion. J. Virol. 80:11235-11240.
2. 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. Banker, G., and K. Goslin. 1991. Culturing nerve cells. MIT Press, Cambridge, MA.
4. Campenot, R. B. 1982. Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor. Dev. Biol. 93:13-21.
5. Ch'ng, T.-H., E. A. Flood, and L. W. Enquist. 2004. Culturing primary and transformed neuronal cells for studying pseudorabies virus infection. Humana Press, Totowa, NJ.
6. Ch'ng, T. H., and L. W. Enquist. 2006. An in vitro system to study transneuronal spread of pseudorabies virus infection. Vet. Microbiol. 113:193-197.
7. Demmin, G. L., A. C. Clase, J. A. Randall, L. W. Enquist, and B. W. Banfield. 2001. Insertions in the gG gene of pseudorabies virus reduce expression of the upstream Us3 protein and inhibit cell-to-cell spread of virus infection. J. Virol. 75:10856-10869.
8. De Regge, N., H. W. Favoreel, K. Geenen, and H. J. Nauwynck. 2006. A homologous in vitro model to study interactions between alphaherpesviruses and trigeminal ganglion neurons. Vet. Microbiol. 113:251-255.
9. De Regge, N., H. J. Nauwynck, K. Geenen, C. Krummenacher, G. H. Cohen, R. J. Eisenberg, T. C. Mettenleiter, and H. W. Favoreel. 2006. Alpha-herpesvirus glycoprotein D interaction with sensory neurons triggers formation of varicosities that serve as virus exit sites. J. Cell Biol. 174:267-275.
10. Enquist, L. W. 2002. Exploiting circuit-specific spread of pseudorabies virus in the central nervous system: insights to pathogenesis and circuit tracers. J. Infect. Dis. 186(Suppl. 2):S209-S214.
11. Enquist, L. W., and J. P. Card. 2003. Recent advances in the use of neurotropic viruses for circuit analysis. Curr. Opin. Neurobiol. 13:603-606.
12. Enquist, L. W., P. J. Husak, B. W. Banfield, and G. A. Smith. 1998. Infection and spread of alphaherpesviruses in the nervous system. Adv. Virus Res. 51:237-347.
13. Holland, D. J., M. Miranda-Saksena, R. A. Boadle, P. Armati, and A. L. Cunningham. 1999. Anterograde transport of herpes simplex virus proteins in axons of peripheral human fetal neurons: an immunoelectron microscopy study. J. Virol. 73:8503-8511.
14. Jons, A., and T. C. Mettenleiter. 1997. Green fluorescent protein expressed by recombinant pseudorabies virus as an in vivo marker for viral replication. J. Virol. Methods 66:283-292.
15. Lomniczi, B., M. L. Blankenship, and T. Ben-Porat. 1984. Deletions in the genomes of pseudorabies virus vaccine strains and existence of four isomers of the genomes. J. Virol. 49:970-979.
16. Lomniczi, B., S. Watanabe, T. Ben-Porat, and A. S. Kaplan. 1984. Genetic basis of the neurovirulence of pseudorabies virus. J. Virol. 52:198-205.
17. Lycke, E., K. Kristensson, B. Svennerholm, A. Vahlne, and R. Ziegler. 1984. Uptake and transport of herpes simplex virus in neurites of rat dorsal root ganglia cells in culture. J. Gen. Virol. 65:55-64.
18. Mettenleiter, T. C., N. Lukacs, and H.-J. Rziha. 1985. Pseudorabies virus avirulent strains fail to express a major glycoprotein. J. Virol. 56:307-311.
19. Mikloska, Z., and A. L. Cunningham. 2001. Alpha and gamma interferons inhibit herpes simplex virus type 1 infection and spread in epidermal cells after axonal transmission. J. Virol. 75:11821-11826.
20. Mikloska, Z., P. P. Sanna, and A. L. Cunningham. 1999. Neutralizing antibodies inhibit axonal spread of herpes simplex virus type 1 to epidermal cells in vitro. J. Virol. 73:5934-5944.
21. Mulder, W., J. Pol, T. Kimman, G. Kok, J. Priem, and B. Peeters. 1996. Glycoprotein D-negative pseudorabies virus can spread transneuronally via direct neuron-to-neuron transmission in its natural host, the pig, but not after additional inactivation of gE or gI. J. Virol. 70:2191-2200.
22. Peeters, B., N. de Wind, R. Broer, A. Gielkens, and R. Moormann. 1992. Glycoprotein H of pseudorabies virus is essential for entry and cell-to-cell spread of the virus. J. Virol. 66:3888-3892.
23. 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.
24. 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.
25. Penfold, M. 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.
26. Petrovskis, E. A., J. G. Timmins, T. M. Gierman, and L. E. Post. 1986. Deletions in vaccine strains of pseudorabies virus and their effect on synthesis of glycoprotein gp63. J. Virol. 60:1166-1169.
27. Pickard, G. E., C. A. Smeraski, C. C. Tomlinson, B. W. Banfield, J. Kaufman, C. L. Wilcox, L. W. Enquist, and P. J. Sollars. 2002. Intravitreal injection of the attenuated pseudorabies virus PRV Bartha results in infection of the hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits. J. Neurosci. 22:2701-2710.
28. Rauh, I., and T. C. Mettenleiter. 1991. Pseudorabies virus glycoproteins gII and gp50 are essential for virus penetration. J. Virol. 65:5348-5356.
29. Saksena, M. M., H. Wakisaka, B. Tijono, R. A. Boadle, F. Rixon, H. Takahashi, and A. L. Cunningham. 2006. Herpes simplex virus type 1 accumulation, envelopment, and exit in growth cones and varicosities in mid-distal regions of axons. J. Virol. 80:3592-3606.
30. Smith, G. A., S. P. Gross, and L. W. Enquist. 2001. Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc. Natl. Acad. Sci. USA 98:3466-3470.
31. Spear, P. G. 2004. Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol. 6:401-410.
32. Watson, D. H., W. C. Russell, and P. Wildy. 1963. Electron microscopic particle counts on herpes virus using the phosphotungstate negative staining technique. Virology 19:250-260.
33. 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.