Repair of the UL21 locus in pseudorabies virus Bartha enhances the kinetics of retrograde, transneuronal infection in vitro and in vivo

Journal of Virology

Volumn 83, Issue 3, 2009, Pages 1173-1183

  Curanovic D ^a   Lyman, M G ^a   Bou Abboud, C ^b   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

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA REPAIR; GENE AMPLIFICATION; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS; RAT; VIRUS GENE; VIRUS INFECTION; VIRUS MUTATION; VIRUS STRAIN; ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; MALE; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VIROLOGY;

SUID HERPESVIRUS 1;

CAPSID PROTEIN; UL21 PROTEIN, PSEUDORABIES VIRUS;

ANIMALS; CAPSID PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HERPESVIRUS 1, SUID; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 59749106353     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02102-08     Document Type: Article

References (42)

1. Bartha, A. 1961. Experimental reduction of virulence of Aujeszky's disease virus. Magy. Allatorv. Lapja 16:42-45.
2. 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.
3. Card, J. P., J. R. Dubin, M. E. Whealy, and L. W. Enquist. 1995. Influence of infectious dose upon productive replication and transynaptic passage of pseudorabies virus in rat central nervous system. J. Neurovirol. 1:349-358.
4. Card, J. P., and L. W. Enquist. 1999. Transneuronal circuit analysis with pseudorabies viruses, vol. 1. John Wiley & Sons, San Diego, CA.
5. Card, J. P., L. W. Enquist, and R. Y. Moore. 1999. Neuroinvasiveness of pseudorabies virus injected intracerebrally is dependent on viral concentration and terminal field density. J. Comp. Neurol. 407:438-452.
6. Card, J. P., L. Rinaman, J. S. Schwaber, R. R. Miselis, M. E. Whealy, A. K. Robbins, and L. W. Enquist. 1990. Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J. Neurosci. 10:1974-1994.
7. Card, J. P., P. Levitt, M. Y. Gluhovsky, and L. Rinaman. 2005. Early experience modifies the postnatal assembly of autonomic emotional motor circuits in rats. J. Neurosci. 25:9102-9111.
8. Card, J. P., M. E. Whealy, A. K. Robbins, R. Y. Moore, and L. W. Enquist. 1991. Two alphaherpesvirus strains are transported differentially in the rodent visual system. Neuron 6:957-969.
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. Neurosci. 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. 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. 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.
13. de Wind, N., F. Wagenaar, J. Pol, T. Kimman, and A. Berns. 1992. The pseudorabies virus homology of the herpes simplex virus UL21 gene product is a capsid protein which is involved in capsid maturation. J. Virol. 66:7096-7103.
14. Dijkstra, C. D., E. A. Dopp, P. Joling, and G. Kraal. 1985. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54:589-599.
15. Dijkstra, J. M., T. C. Mettenleiter, and B. G. Klupp. 1997. Intracellular processing of pseudorabies virus glycoprotein M (gM): gM of strain Bartha lacks N-glycosylation. Virology 237:113-122.
16. Ekstrand, M. I., L. W. Enquist, and L. E. Pomeranz. 2008. The alpha-herpesviruses: molecular pathfinders in nervous system circuits. Trends Mol. Med. 14:134-140.
17. 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.
18. Goodpasture, E. W., and O. Teague. 1923. Transmission of the virus of herpes fibrils along nerves in experimentally infected rabbits. J. Med. Res. 44:139-184.
19. Hill, T. J., and H. J. Field. 1973. The interaction of herpes simplex virus with cultures of peripheral nervous tissue: an electron microscopic study. J. Gen. Virol. 21:123-133.
20. Klupp, B. G., H. Kern, and T. C. Mettenleiter. 1992. The virulence-determining genomic BamHI fragment 4 of pseudorabies virus contains genes corresponding to the UL15 (partial), UL18, UL19, UL20, and UL21 genes of herpes simplex virus and a putative origin of replication. Virology 191: 900-908.
21. Klupp, B. G., B. Lomniczi, N. Visser, W. Fuchs, and T. C. Mettenleiter. 1995. Mutations affecting the UL21 gene contribute to avirulence of pseudorabies virus vaccine strain Bartha. Virology 212:466-473.
22. 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.
23. 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.
24. 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.
25. McFerran, J. B., and C. Dow. 1975. Studies on immunisation of pigs with the Bartha strain of Aujeszky's disease virus. Res. Vet. Sci. 19:17-22.
26. McLean, I. W., and P. K. Nakane. 1974. Periodate-lysine- paraformaldehyde fixative. A new fixative for immunoelectron microscopy. J. Histochem. Cytochem. 22:1077-1083.
27. Mettenleiter, T. C., L. Zsak, A. S. Kaplan, T. Ben-Porat, and B. Lomniczi. 1987. Role of a structural glycoprotein of pseudorabies in virus virulence. J. Virol. 61:4030-4032.
28. Michael, K., B. G. Klupp, A. Karger, and T. C. Mettenleiter. 2007. Efficient incorporation of tegument proteins pUL46, pUL49, and pUS3 into pseudorabies virus particles depends on the presence of pUL21. J. Virol. 81:1048-1051.
29. National Resource Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
30. O'Donnell, P., A. Lavin, L. W. Enquist, A. A. Grace, and J. P. Card. 1997. Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. J. Neurosci. 17:2143-2167.
31. 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.
32. 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.
33. Potter, D. D., S. C. Landis, S. G. Matsumoto, and E. J. Furshpan. 1986. Synaptic functions in rat sympathetic neurons in microcultures. II. Adrenergic/ cholinergic dual status and plasticity. J. Neurosci. 6:1080-1098.
34. Rinaman, L., J. P. Card, and L. W. Enquist. 1993. Spatiotemporal responses of astrocytes, ramified microglia, and brain macrophages to central neuronal infection with pseudorabies virus. J. Neurosci. 13:685-702.
35. Rinaman, L., P. Levitt, and J. P. Card. 2000. Progressive postnatal assembly of limbic-autonomic circuits revealed by central transneuronal transport of pseudorabies virus. J. Neurosci. 20:2731-2741.
36. Rinaman, L., M. R. Roesch, and J. P. Card. 1999. Retrograde transynaptic pseudorabies virus infection of central autonomic circuits in neonatal rats. Dev. Brain Res. 114:207-216.
37. Robbins, A. K., J. P. Ryan, M. E. Whealy, and L. W. Enquist. 1989. The gene encoding the gIII envelope protein of pseudorabies virus vaccine strain Bartha contains a mutation affecting protein localization. J. Virol. 63:250-258.
38. 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 13:3466-3470.
39. U.S. Department of Health and Human Services. 1999. Biosafety in microbiological and biomedical laboratories. U.S. Department of Health and Human Services publication no. (CDC) 88-8395. U.S. Department of Health and Human Services, Washington, DC.
40. Wagenaar, F., J. M. Pol, N. de Wind, and T. G. Kimman. 2001. Deletion of the UL21 gene in pseudorabies virus results in the formation of DNA-deprived capsids: an electron microscopy study. Vet. Res. 32:47-54.
41. Watson, R. E., S. T. Wiegand, R. W. Clough, and G. E. Hoffman. 1986. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155-159.
42. 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.