Role of pseudorabies virus Us3 protein kinase during neuronal infection

Journal of Virology

Volumn 80, Issue 13, 2006, Pages 6387-6398

  Olsen, L M ^a   Ch'ng, T H ^a   Card, J P ^b   Enquist, L W ^a  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE US3; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFECTION; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME ACTIVITY; HERPES VIRUS; NERVE FIBER; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS; RAT; SENSORY NERVE; VIRAL EYE INFECTION; VIRUS MUTANT; VIRUS REPLICATION; VIRUS VIRULENCE;

ANIMALS; AXONS; COCULTURE TECHNIQUES; EYE; EYE INFECTIONS, VIRAL; HERPESVIRUS 1, SUID; MUTATION; PC12 CELLS; PROTEIN-SERINE-THREONINE KINASES; PSEUDORABIES; RATS; VIRUS REPLICATION;

RODENTIA; SUID HERPESVIRUS 1;

EID: 33745284607     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00352-06     Document Type: Article

References (53)

1. Asano, S., T. Honda, F. Goshima, Y. Nishiyama, and Y. Sigiura. 2000. Us3 protein kinase of herpes simplex virus protects primary afferent neurons from virus-induced apoptosis in ICR mice. Neurosci. Lett. 294:105-108.
2. Banfield, B. W., J. D. Kaufman, J. A. Randall, and G. E. Pickard. 2003. Development of pseudorabies virus strains expressing red fluorescent proteins: new tools for multisynaptic labeling applications. J. Virol. 77:10106-10112.
3. Banfield, B. W., G. S. Yap, A. C. Knapp, and L. W. Enquist. 1998. A chicken embryo eye model for the analysis of alphaherpesvirus neuronal spread and virulence. J. Virol. 72:4580-4588.
4. Bartha, A. 1961. Experimental reduction of virulence of Aujeszky's disease virus. Magy. Allat. Lapja 16:42-45.
5. Brittle, E. E., A. E. Reynolds, and L. W. Enquist. 2004. Two modes of pseudorabies virus neuroinvasion and lethality in mice. J. Virol. 78:12951-12963.
6. Calton, C. M., J. A. Randall, M. W. Adkins, and B. W. Banfield. 2004. The pseudorabies virus serine/threonine kinase Us3 contains mitochondrial, nuclear and membrane localization signals. Virus Genes 29:131-145.
7. Card, J. P., M. E. Whealy, A. K. Robbins, and L. W. Enquist. 1992. Pseudorabies virus envelope glycoprotein gl influences both neurotropism and virulence during infection of the rat visual system. J. Virol. 66:3032-3041.
8. Card, J. P., M. E. Whealy, A. K. Robbins, R. Y. Moore, and L. W. Enquist. 1991. Two alpha herpesvirus strains are transported differentially in the rodent visual system. Neuron 6:957-969.
9. 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, N.J.
10. 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.
11. 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.
12. del Rio, T., T. H. Ch'ng, E. A. Flood, S. P. Gross, and L. W. Enquisi. 2005. Heterogeneity of a fluorescent tegument component in single pseudorabies virus virions and enveloped axonal assemblies. J. Virol. 79:3903-3919.
13. 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.
14. de Wind, N., A. Zijderveld, K. Glazenburg, A. Gielkens, and A. Berns. 1990. Linker insertion mutagenesis of herpesviruses: inactivation of single genes within the Us region of pseudorabies virus. J. Virol. 64:4691-4696.
15. Dohner, K., A. Wolfstein, U. Prank, C. Echeverri, D. Dujardin, R. Vallee, and B. Sodiek. 2002. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13:2795-2809.
16. Dohner, K., C.-H. Nagel, and B. Sodiek. 2005. Viral stop-and-go along microtubules: taking a ride with dynein and kinesins. Trends Microbiol. 13:320-327.
17. 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.
18. Enquist, L. W., P. J. Husak, B. W. Banfield, and G. A. Smith. 1998. Infection and spread of alpha herpesviruses in the nervous system. Adv. Virus Res. 58:237-347.
19. Enquist, L. W., M. J. Tomishima, S. Gross, and G. A. Smith. 2002. Directional spread of an alpha herpesvirus in the nervous system. Vet. Microbiol. 86:5-16.
20. Geenen, K., H. W. Favoreel, and H. J. Nauwynck. 2005. Higher resistance of porcine trigeminal ganglion neurons towards pseudorabies virus-induced cell death compared with other porcine cell types in vitro. J. Gen. Virol. 86:1251-1260.
21. Geenen, K., H. W. Favoreel, L. Olsen, L. W. Enquist, and H. J. Nauwynck. 2004. The pseudorabies virus Us3 protein kinase possesses anti-apoptotic activity that protects cells from apoptosis during infection and after treatment with sorbitol or staurosporine. Virology 331:144-150.
22. Granzow, H., B. G. Klupp, and T. C. Mettenleiter. 2004. The pseudorabies virus Us3 protein is a component of primary and of mature virions. J. Virol. 78:1314-1323.
23. Granzow, H., B. G. Klupp, and T. C. Mettenleiter. 2005. Entry of pseudorabies virus: an immunogold-labeling study. J. Virol. 79:3200-3205.
24. Greene, L. A., S. E. Farinelli, M. E. Cunningham, and D. S. Park. 1998. Culture and experimental use of PC12 rat pheochromocytoma cell line, p. 161-187. In G. Banker and K. Goslin (ed.), Culturing nerve cells, 2nd ed. MIT Press, Cambridge, Mass.
25. Klopfleisch, R., J. P. Teifke, W. Fuchs, M. Kopp, B. G. Klupp, and T. C. Mettenleiter. 2004. Influence of tegument proteins of pseudorabies virus on neuroinvasion and transneuronal spread in the nervous system of adult mice after intranasal inoculation. J. Virol. 78:2956-2966.
26. Kurachi, R., T. Daikoku, T. Tsurumi, K. Maeno, Y. Nishiyama, and T. Kurata. 1993. The pathogenicity of a Us3 protein kinase-deficient mutant of herpes simplex virus type 2 in mice. Arch. Virol. 133:259-273.
27. Kuypers, H., and G. Ugolini. 1990. Viruses as transneuronal tracers. Trends Neurosci. 13:71-75.
28. LaVail, J. H., A. N. Tauscher, J. W. Hicks, O. Harrabi, G. T. Melrose, 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.
29. Lomniczi, B., S. Watanabe, T. Ben-Porat, and A. S. Kaplan. 1987. Genome location and identification of functions defective in the Bartha vaccine strain of pseudorabies virus. J. Virol. 61:796-801.
30. Luxton, G. W., S. Haverlock, K. E. Coller, S. E. Antinone, A. Pincetic, and G. A. Smith. 2005. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl. Acad. Sci. USA 102:5832-5837.
31. Luxton, G. W., J. I. Lee, S. Haverlock-Moyns, J. M. Schober, and G. A. Smith. 2006. The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J. Virol. 80:201-209.
32. Lyman, M. G., G. L. Demmin, and B. W. Banfield. 2003. The attenuated pseudorabies virus strain Bartha fails to package the tegument proteins Us3 and VP22. J. Virol. 77:1403-1414.
33. Meignier, B., R. Longnecker, P. Mavromara-Nazos, A. E. Sears, and B. Roizman. 1988. Virulence of and establishment of latency by genetically engineered deletion mutants of herpes simplex virus I. Virology 162:251-254.
34. Mettenleiter, T. C. 2000. Aujeszky's disease (pseudorabies) virus: the virus and molecular pathogenesis-state of the art, June 1999. Vet. Res. 31:99-115.
35. Mettenleiter, T. C. 1996. Immunobiology of pseudorabies (Aujeszky's disease). Vet. Immunol. Immunopathol. 54:221-229.
36. Morrison, E. E., Y.-F. Wang, and D. M. Meridith. 1998. Phosphorylation of structural components promotes dissociation of the herpes simplex virus type 1 tegument. J. Virol. 72:7108-7114.
37. Nishiyama, Y., Y. Yamada, R. Karachi, and T. Daikoku. 1992. Construction of a Us3 lacZ insertion mutant of herpes simplex virus type 2 and characterization of its phenotype in vitro and in vivo. Virology 190:256-268.
38. 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.
39. Pomeranz, L. E., A. E. Reynolds, and C. J. Hengartner. 2005. Molecular biology of pseudorabies virus: impact on neurovirology and veterinary medicine. Microbiol. Mol. Biol. Rev. 69:462-500.
40. Smeraski, C. A., P. J. Sollars, M. D. Ogilvie, L. W. Enquist, and G. E. Pickard. 2004. Suprachiasmatic nucleus input to autonomic circuits identified by retrograde transsynaptic transport of pseudorabies virus from the eye. J. Comp. Neurol. 471:298-313.
41. Smith, G. A., and L. W. Enquist. 2002. Break ins and break outs: viral interactions with the cytoskeleton of mammalian cells. Annu. Rev. Cell Dev. Biol. 18:135-161.
42. Smith, G. A., and L. W. Enquist. 2000. A self-recombining bacterial artificial chromosome and its application for analysis of herpesvirus pathogenesis. Proc. Natl. Acad. Sci. USA 97:4873-4878.
43. Smith, G. A., L. Pomeranz, S. P. Gross, and L. W. Enquist. 2004. Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc. Natl. Acad. Sci. USA 101:16034-16039.
44. Sodeik, B. 2000. Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8:465-472.
45. Sodeik, B., M. W. Ebersold, and A. Helenius. 1997. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136:1007-1021.
46. Strack, A. M., and A. D. Loewy. 1990. Pseudorabies virus: a highly specific transneuronal cell body marker in the sympathetic nervous system. J. Neurosci. 10:2139-2147.
47. Tirabassi, R. S., and L. W. Enquist. 2000. Role of the pseudorabies virus gI cytoplasmic domain in neuroinvasion, virulence, and posttranslational N-linked glycosylation. J. Virol. 74:3505-3516.
48. Tomishima, M. J., and L. W. Enquist. 2001. A conserved alpha-herpesvirus protein necessary for axonal localization of viral membrane proteins. J. Cell Biol. 154:741-752.
49. Wagenaar, F., J. M. A. Pol, B. Peters, A. L. J. Gielkens, N. deWind, and T. G. Kimman. 1995. The Us3-encoded protein kinase from pseudorabies virus affects egress of virions from the nucleus. J. Gen. Virol. 76:1851-1859.
50. 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.
51. Willmann, G., and H. J. Rziha. 1989. Aujeszky's disease (pseudorabies) in pigs, p. 230-333. In G. Wittmann (ed.), Herpesvirus diseases of cattle, horse and pigs. Kluwer Academic, Boston, Mass.
52. Wolfstein, A., C.-H. Nagel, K. Radtke, K. Dohner, V. J. Allan, and B. Sodeik. 2006. The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7:227-237.
53. Yang, M., J. P. Card, R. S. Tirabassi, R. R. Miselis, and L. W. Enquist. 1999. Retrograde, transneuronal spread of pseudorabies virus in defined neuronal circuitry of the rat brain is facilitated by gE mutations that reduce virulence. J. Virol. 73:4350-4359.