Ultrastructural analysis of virion formation and anterograde intraaxonal transport of the alphaherpesvirus pseudorabies virus in primary neurons

Journal of Virology

Volumn 84, Issue 11, 2010, Pages 5528-5539

  Maresch, Christina ^a   Granzow, Harald ^a   Negatsch, Alexandra ^a   Klupp, Barbara G ^a   Fuchs, Walter ^a   Teifke, Jens P ^a   Mettenleiter, Thomas C ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GLYCOPROTEIN GB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS MEMBRANE; CELL POLARITY; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; EXOCYTOSIS; GROWTH CONE; MICROTUBULE; NERVE CELL; NERVE CELL CULTURE; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS; SUPERIOR CERVICAL GANGLION; TRANSMISSION ELECTRON MICROSCOPY; VIRION; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; WILD TYPE;

ALPHAHERPESVIRINAE; AXONS; BIOLOGICAL TRANSPORT; CYTOPLASMIC VESICLES; HERPESVIRUS 1, SUID; NEURONS; NUCLEOCAPSID; VIRION; VIRUS REPLICATION;

HERPESVIRIDAE; MIRIDAE; RATTUS; SUID HERPESVIRUS 1;

EID: 77951982824     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00067-10     Document Type: Article

References (44)

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. (Pubitemid 23180775)
3. Ch'ng, T. H., and L. W. Enquist. 2005. Efficient axonal localization of alphaherpesvirus structural proteins in cultured sympathetic neurons requires viral glycoprotein E. J. Virol. 79:8835-8846.
4. Ch'ng, T. H., E. A. Flood, and L. W. Enquist. 2005. Culturing primary and transformed neuronal cells for studying pseudorabies virus infection. Methods Mol. Biol. 292:299-316.
5. Ch'ng, T. H., and L. W. Enquist. 2005. Neuron-to-cell spread of pseudorabies virus in a compartmented neuronal culture system. J. Virol. 79:10875-10889.
6. Curanovic, D., and L. W. Enquist. 2009. Virion-incorporated glycoprotein B mediates transneuronal spread of pseudorabies virus. J. Virol. 83:7796-7804.
7. Curanovic, D., and L. W. Enquist. 2009. Directional transneuronal spread of α-herpesvirus infection. Fut. Virol. 4:591-603.
8. Davison, A. J., R. Eberle, B. Ehlers, G. S. Hayward, D. J. McGeoch, A. C. Minson, P. E. Pellett, B. Roizman, M. J. Studdert, and E. Thiry. 2009. The order Herpesvirales. Arch. Virol. 154:171-177.
9. del Rio, T., T. H. Ch'ng, E. A. Flood, S. P. Gross, and L. W. Enquist. 2005. Heterogeneity of a fluorescent tegument component in single pseudorabies virus virions and enveloped axonal assemblies. J. Virol. 79:3903-3919.
10. De Regge, N., H. J. Nauwynck, K. Geenen, C. Krummenacher, G. H. Cohen, R. J. Eisenberg, T. C. Mettenleiter, and H. W. Favoreel. 2006. Alphaherpesvirus glycoprotein D interaction with sensory neurons triggers formation of varicosities that serve as virus exit sites. J. Cell Biol. 174:267-275. (Pubitemid 44079861)
11. Diefenbach, R. J., M. Miranda-Saksena, M. W. Douglas, and A. L. Cunningham. 2008. Transport and egress of herpes simplex virus in neurons. Rev. Med. Virol. 18:35-51.
12. Döhner, K., K. Radtke, S. Schmidt, and B. Sodeik. 2006. Eclipse phase of herpes simplex virus type 1 infection: efficient dynein-mediated capsid transport without the small capsid protein VP26. J. Virol. 80:8211-8224. (Pubitemid 44182321)
13. 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.
14. Feierbach, B., M. Bisher, J. Goodhouse, and L. W. Enquist. 2007. In vitro analysis of transneuronal spread of an alphaherpesvirus infection in peripheral nervous system neurons. J. Virol. 81:6846-6857.
15. Granzow, H., B. G. Klupp, W. Fuchs, J. Veits, N. Osterrieder, and T. C. Mettenleiter. 2001. Egress of alphaherpesviruses: comparative ultrastructural study. J. Virol. 75:3675-3684. (Pubitemid 32246377)
16. Granzow, H., F. Weiland, A. Jons, B. G. Klupp, A. Karger, and T. C. Mettenleiter. 1997. Ultrastructural analysis of the replication cycle of pseudorabies virus in cell culture: a reassessment. J. Virol. 71:2072-2082. (Pubitemid 27078585)
17. 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.
18. Kaplan, A. S., and A. E. Vatter. 1959. A comparison of herpes simplex and pseudorabies viruses. Virology 7:394-407.
19. Klupp, B. G., H. Granzow, and T. C. Mettenleiter. 2000. Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J. Virol. 74:10063-10073.
20. LaVail, J. H., A. N. Tauscher, A. Sucher, O. Harrabi, and R. Brandimarti. 2007. Viral regulation of the long distance axonal transport of herpes simplex virus nucleocapsid. Neuroscience 146:974-985.
21. LaVail, J. H., A. N. Tauscher, J. W. Hicks, O. Harrabi, G. T. Melroe, and D. M. Knipe. 2005. Genetic and molecular in vivo analysis of herpes simplex virus assembly in murine visual system neurons. J. Virol. 79:11142-11150.
22. Leestma, J. E., M. B. Bornstein, R. D. Sheppard, and L. A. Feldman. 1969. Ultrastructural aspects of herpes simplex virus infection in organized cultures of mammalian nervous tissue. Lab. Invest. 20:70-78.
23. Lyman, M. G., B. Feierbach, D. Curanovic, M. Bisher, and L. W. Enquist. 2007. Pseudorabies virus Us9 directs axonal sorting of viral capsids. J. Virol. 81:11363-11371.
24. Lyman, M. G., C. D. Kemp, M. P. Taylor, and L. W. Enquist. 2009. Comparison of the pseudorabies virus Us9 protein with homologs from other veterinary and human alphaherpesviruses. J. Virol. 83:6978-6986.
25. Lyman, M. G., D. Curanovic, and L. W. Enquist. 2008. Targeting of pseudorabies virus structural proteins to axons requires association of the viral Us9 protein with lipid rafts. PLoS Pathog. 4:e1000065. doi:10.1371/journal.ppat.1000065.
26. Mettenleiter, T. C. 2008. Pseudorabies virus, p. 341-351. In B. W. J. Mahy and M. Van Regenmortel (ed.), Encyclopedia of virology, 3rd ed., vol. 5. Elsevier, Oxford, United Kingdom.
27. Mettenleiter, T. C. 2003. Pathogenesis of neurotropic herpesviruses: role of viral glycoproteins in neuroinvasion and transneuronal spread. Virus Res. 92:197-206.
28. Mettenleiter, T. C., B. G. Klupp, and H. Granzow. 2009. Herpesvirus assembly: an update. Virus Res. 143:222-234.
29. Miranda-Saksena, M., P. Armati, R. A. Boadle, D. J. Holland, and A. L. Cunningham. 2000. Anterograde transport of herpes simplex virus type 1 in cultured, dissociated human and rat dorsal root ganglion neurons. J. Virol. 74:1827-1839. (Pubitemid 30434042)
30. Miranda-Saksena, M., R. A. Boadle, A. Aggarwal, B. Tijono, F. J. Rixon, R. J. Diefenbach, and A. L. Cunningham. 2009. Herpes simplex virus utilizes the large secretory vesicle pathway for anterograde transport of tegument and envelope proteins and for viral exocytosis from growth cones of human fetal axons. J. Virol. 83:3187-3199.
31. Miranda-Saksena, M., R. A. Boadle, P. Armati, and A. L. Cunningham. 2002. In rat dorsal root ganglion neurons, herpes simplex virus type 1 tegument forms in the cytoplasm of the cell body. J. Virol. 76:9934-9951.
32. Nixdorf, R., B. G. Klupp, A. Karger, and T. C. Mettenleiter. 2000. Effects of truncation of the carboxy terminus of pseudorabies virus glycoprotein B on infectivity. J. Virol. 74:7137-7145. (Pubitemid 30470698)
33. Peeters, B., W. N. de, 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.
34. 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. U. S. A. 91:6529-6533.
35. Radtke, K., K. Döhner, and B. Sodeik. 2006. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol. 8:387-400. (Pubitemid 43356030)
36. Rauh, I., and T. C. Mettenleiter. 1991. Pseudorabies virus glycoproteins gII and gp50 are essential for virus penetration. J. Virol. 65:5348-5356.
37. 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.
38. Snyder, A., B. Bruun, H. M. Browne, and D. C. Johnson. 2007. A herpes simplex virus gD-YFP fusion glycoprotein is transported separately from viral capsids in neuronal axons. J. Virol. 81:8337-8340. (Pubitemid 47101518)
39. Snyder, A., K. Polcicova, and D. C. Johnson. 2008. Herpes simplex virus gE/gI and US9 proteins promote transport of both capsids and virion glycoproteins in neuronal axons. J. Virol. 82:10613-10624. (Pubitemid 352691178)
40. Snyder, A., T. W. Wisner, and D. C. Johnson. 2006. Herpes simplex virus capsids are transported in neuronal axons without an envelope containing the viral glycoproteins. J. Virol. 80:11165-11177. (Pubitemid 44706556)
41. Sodeik, B. 2000. Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8:465-472.
42. Tomishima, M. J., and L. W. Enquist. 2001. A conserved alphaherpesvirus protein necessary for axonal localization of viral membrane proteins. J. Cell Biol. 154:741-752.
43. Tomishima, M. J., G. A. Smith, and L. W. Enquist. 2001. Sorting and transport of alpha herpesviruses in axons. Traffic 2:429-436.
44. Yamada, K. M., B. S. Spooner, and N. K. Wessells. 1971. Ultrastructure and function of growth cones and axons of cultured nerve cells. J. Cell Biol. 49:614-635.