Resolving the assembly state of herpes simplex virus during axon transport by live-cell imaging

Journal of Virology

Volumn 84, Issue 24, 2010, Pages 13019-13030

  Antinone, Sarah E ^a   Zaichick, Sofia V ^a   Smith, Gregory A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; FLUORESCENCE MICROSCOPY; HERPES SIMPLEX VIRUS 1; MOLECULAR IMAGING; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; RAT; SECRETORY PATHWAY; SENSORY NERVE CELL; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS PARTICLE; VIRUS STRAIN;

ANIMALS; AXONAL TRANSPORT; AXONS; BLOTTING, WESTERN; CAPSID; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHICK EMBRYO; FLUORESCENT ANTIBODY TECHNIQUE; HERPES SIMPLEX; MICROSCOPY, ELECTRON; NEURONS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIMPLEXVIRUS; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRION; VIRUS REPLICATION;

HUMAN HERPESVIRUS 1; MIRIDAE; SIMPLEXVIRUS;

EID: 78649434392     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01296-10     Document Type: Article

References (71)

1. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image processing with ImageJ. Biophotonics Int. 11:36-42.
2. Ahmari, S. E., J. Buchanan, and S. J. Smith. 2000. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat. Neurosci. 3:445-451.
3. Ali, M. A., M. Butcher, and H. P. Ghosh. 1987. Expression and nuclear envelope localization of biologically active fusion glycoprotein gB of herpes simplex virus in mammalian cells using cloned DNA. Proc. Natl. Acad. Sci. U. S. A. 84:5675-5679.
4. Antinone, S. E., and G. A. Smith. 2010. Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J. Virol. 84:1504-1512.
5. Antinone, S. E., and G. A. Smith. 2006. Two modes of herpesvirus trafficking in neurons: membrane acquisition directs motion. J. Virol. 80:11235-11240.
6. Cai, W. H., 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.
7. Campbell, R. E., O. Tour, A. E. Palmer, P. A. Steinbach, G. S. Baird, D. A. Zacharias, and R. Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. U. S. A. 99:7877-7882.
8. 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.
9. 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.
10. 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.
11. Coller, K. E., J. I. Lee, A. Ueda, and G. A. Smith. 2007. The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J. Virol. 81:11790-11797.
12. Coller, K. E., and G. A. Smith. 2008. Two viral kinases are required for sustained long distance axon transport of a neuroinvasive herpesvirus. Traffic 9:1458-1470.
13. 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.
14. Curanovic, D., and L. W. Enquist. 2009. Directional transneuronal spread of α-herpesvirus infection. Future Virol. 4:591-603.
15. 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.
16. 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.
17. Dohner, K., A. Wolfstein, U. Prank, C. Echeverri, D. Dujardin, R. Vallee, and B. Sodeik. 2002. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13:2795-2809.
18. El Meskini, R., L. Jin, R. Marx, A. Bruzzaniti, J. Lee, R. Emeson, and R. Mains. 2001. A signal sequence is sufficient for green fluorescent protein to be routed to regulated secretory granules. Endocrinology 142:864-873. (Pubitemid 32222437)
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. Farnsworth, A., T. W. Wisner, M. Webb, R. Roller, G. Cohen, R. Eisenberg, and D. C. Johnson. 2007. Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane. Proc. Natl. Acad. Sci. U. S. A. 104:10187-10192.
21. 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.
22. Field, H. J., and T. J. Hill. 1974. The pathogenesis of pseudorabies in mice following peripheral inoculation. J. Gen. Virol. 23:145-157.
23. Fuller, A. O., R. E. Santos, and P. G. Spear. 1989. Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration. J. Virol. 63:3435-3443.
24. Fuller, A. O., and P. G. Spear. 1987. Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proc. Natl. Acad. Sci. U. S. A. 84:5454-5458.
25. Granzow, H., B. G. Klupp, and T. C. Mettenleiter. 2005. Entry of pseudorabies virus: an immunogold-labeling study. J. Virol. 79:3200-3205.
26. Hill, T. J., H. J. Field, and A. P. Roome. 1972. Intra-axonal location of herpes simplex virus particles. J. Gen. Virol. 15:233-235.
27. 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.
28. Kato, A., J. Arii, I. Shiratori, H. Akashi, H. Arase, and Y. Kawaguchi. 2009. Herpes simplex virus 1 protein kinase Us3 phosphorylates viral envelope glycoprotein B and regulates its expression on the cell surface. J. Virol. 83:250-261.
29. Klupp, B. G., W. Fuchs, H. Granzow, R. Nixdorf, and T. C. Mettenleiter. 2002. Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J. Virol. 76:3065-3071.
30. Knapp, A. C., and L. W. Enquist. 1997. Pseudorabies virus recombinants expressing functional virulence determinants gE and gI from bovine herpesvirus 1.1. J. Virol. 71:2731-2739.
31. Kristensson, K., B. Ghetti, and H. M. Wisniewski. 1974. Study on the propagation of herpes simplex virus (type 2) into the brain after intraocular injection. Brain Res. 69:189-201.
32. 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.
33. LaVail, J. H., K. S. Topp, P. A. Giblin, and J. A. Garner. 1997. Factors that contribute to the transneuronal spread of herpes simplex virus. J. Neurosci. Res. 49:485-496.
34. Liu, W. W., J. Goodhouse, N. L. Jeon, and L. W. Enquist. 2008. A microfluidic chamber for analysis of neuron-to-cell spread and axonal transport of an alpha-herpesvirus. PLoS One 3:e2382.
35. 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. U. S. A. 102:5832-5837.
36. Lycke, E., B. Hamark, M. Johansson, A. Krotochwil, J. Lycke, and B. Svennerholm. 1988. Herpes simplex virus infection of the human sensory neuron. An electron microscopy study. Arch. Virol. 101:87-104.
37. 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.
38. 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.
39. Maresch, C., H. Granzow, A. Negatsch, B. G. Klupp, W. Fuchs, J. P. Teifke, and T. C. Mettenleiter. 2010. Ultrastructural analysis of virion formation and anterograde intraaxonal transport of the alphaherpesvirus pseudorabies virus in primary neurons. J. Virol. 84:5528-5539.
40. Maurer, U. E., B. Sodeik, and K. Grunewald. 2008. Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc. Natl. Acad. Sci. U. S. A. 105:10559-10564.
41. 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.
42. 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.
43. 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.
44. Morgan, C., H. M. Rose, and B. Mednis. 1968. Electron microscopy of herpes simplex virus. I. Entry. J. Virol. 2:507-516.
45. Nagel, C. H., K. Dohner, M. Fathollahy, T. Strive, E. M. Borst, M. Messerle, and B. Sodeik. 2008. Nuclear egress and envelopment of herpes simplex virus capsids analyzed with dual-color fluorescence HSV1(17+). J. Virol. 82:3109-3124.
46. Nakata, T., S. Terada, and N. Hirokawa. 1998. Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J. Cell Biol. 140:659-674. (Pubitemid 28134068)
47. Negatsch, A., H. Granzow, C. Maresch, B. G. Klupp, W. Fuchs, J. P. Teifke, and T. C. Mettenleiter. 2010. Ultrastructural analysis of virion formation and intraaxonal transport of herpes simplex virus type 1 in primary rat neurons. J. Virol. 84:13031-13035.
48. Nicola, A. V., J. Hou, E. O. Major, and S. E. Straus. 2005. Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J. Virol. 79:7609-7616.
49. Ohara, P. T., A. N. Tauscher, and J. H. LaVail. 2001. Two paths for dissemination of herpes simplex virus from infected trigeminal ganglion to the murine cornea. Brain Res. 899:260-263.
50. Pasdeloup, D., D. Blondel, A. L. Isidro, and F. J. Rixon. 2009. Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J. Virol. 83:6610-6623.
51. 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.
52. Potel, C., K. Kaelin, I. Gautier, P. Lebon, J. Coppey, and F. Rozenberg. 2002. Incorporation of green fluorescent protein into the essential envelope glycoprotein B of herpes simplex virus type 1. J. Virol. Methods 105:13-23.
53. Qi, Y., J. K. Wang, M. McMillian, and D. M. Chikaraishi. 1997. Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation. J. Neurosci. 17:1217-1225.
54. Raviprakash, K., L. Rasile, K. Ghosh, and H. P. Ghosh. 1990. Shortened cytoplasmic domain affects intracellular transport but not nuclear localization of a viral glycoprotein. J. Biol. Chem. 265:1777-1782.
55. 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.
56. 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.
57. Smith, G. A., and L. W. Enquist. 1999. Construction and transposon mutagenesis in Escherichia coli of a full-length infectious clone of pseudorabies virus, an alphaherpesvirus. J. Virol. 73:6405-6414.
58. 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. U. S. A. 98:3466-3470.
59. 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. U. S. A. 101:16034-16039.
60. Smith, J. D., and E. de Harven. 1974. Herpes simplex virus and human cytomegalovirus replication in WI-38 cells. II. An ultrastructural study of viral penetration. J. Virol. 14:945-956.
61. 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.
62. 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.
63. 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.
64. Sugimoto, K., M. Uema, H. Sagara, M. Tanaka, T. Sata, Y. Hashimoto, and Y. Kawaguchi. 2008. Simultaneous tracking of capsid, tegument, and envelope protein localization in living cells infected with triply fluorescent herpes simplex virus 1. J. Virol. 82:5198-5211. (Pubitemid 351705229)
65. Szilagyi, J. F., and C. Cunningham. 1991. Identification and characterization of a novel non-infectious herpes simplex virus-related particle. J. Gen. Virol. 72:661-668.
66. Tanaka, M., H. Kagawa, Y. Yamanashi, T. Sata, and Y. Kawaguchi. 2003. Construction of an excisable bacterial artificial chromosome containing a full-length infectious clone of herpes simplex virus type 1: viruses reconstituted from the clone exhibit wild-type properties in vitro and in vivo. J. Virol. 77:1382-1391. (Pubitemid 36055560)
67. Tischer, B. K., J. von Einem, B. Kaufer, and N. Osterrieder. 2006. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40:191-197.
68. Topp, K. S., L. B. Meade, and J. H. LaVail. 1994. Microtubule polarity in the peripheral processes of trigeminal ganglion cells: relevance for the retrograde transport of herpes simplex virus. J. Neurosci. 14:318-325.
69. Turner, A., B. Bruun, T. Minson, and H. Browne. 1998. Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. J. Virol. 72:873-875. (Pubitemid 28048916)
70. Vittone, V., E. Diefenbach, D. Triffett, M. W. Douglas, A. L. Cunningham, and R. J. Diefenbach. 2005. Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 79:9566-9571.
71. Wisner, T. W., and D. C. Johnson. 2004. Redistribution of cellular and herpes simplex virus proteins from the trans-Golgi network to cell junctions without enveloped capsids. J. Virol. 78:11519-11535.