1887

Abstract

SUMMARY

We have previously described the capacity of neurites extending from cultured rat sensory dorsal root ganglia (DRG) neurons to transport rabies virus through axoplasm in the retrograde direction. Here we report the infection of cultured neurons derived from the DRG and the subsequent anterograde transport of rabies virus from the infected cell somas through the extending neurites to its release into the culture supernatant. Viral transport was monitored by titration of the virus yield in the external compartment. Both early and late transport mechanisms of rabies virions were identified. The first one occurred a few hours post-infection and was undetectable 6 h later, before the initiation of viral replication. The velocity of this first wave of infective virions was in the range of 100 to 400 mm/day. The early viral transport was probably the result of a direct translocation of infective virions from the somatic site of entry to the neuritic extensions and subsequent release into the culture medium without replication in the cellular perikaryon. The second virus transport peak was detected 48 h post-infection. In this case, the virions detected in the neuritic compartment were presumably the progeny of the inoculated virus which had replicated in the perikaryon before the viral transport occurs. Using a four-compartment culture device we were able to demonstrate, simultaneously, retrograde and anterograde transport of the virus. The presence of antirabies serum in contact with the exposed neurites did not inhibit either the retrograde or the anterograde transport mechanisms. The viral release from the neuritic extensions after the fast anterograde transport was evaluated to be in the range of 150 to 300 infectious virions per bundle of neurites per day.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-70-8-2075
1989-08-01
2021-11-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/70/8/JV0700082075.html?itemId=/content/journal/jgv/10.1099/0022-1317-70-8-2075&mimeType=html&fmt=ahah

References

  1. Aquino D. A., Bisby M. A., Ledeen W. W. 1987; Bidirectional transport of gangliosides, glycoproteins and neutral glycosphingolipids in the sensory neurons of rat sciatic nerve. Neuroscience 20:1023–1029
    [Google Scholar]
  2. Atanasiu P., Gamet A., Tsiang H. 1974a; Nouveau vaccin antirabique humain de culture cellulaire primaire. Annales de microbiologie 12SB419–432
    [Google Scholar]
  3. Atanasiu P., Perrin P., Favre S., Chevallier G., Tsiang H. 1974b; Immunofluoresence and immunoperoxidase in the diagnosis of rabies. In Viral Immunodiagnostics 9141–155 Kurstak E., Morisset R. New York & London: Academic Press;
    [Google Scholar]
  4. Baer G. M. 1975; Pathogenesis to the central nervous system. In The Natural History of Rabies181–198 Baer G. M. New York & London: Academic Press;
    [Google Scholar]
  5. Baer G. M., Shantaveerappa T. R., Bourne G. H. 1965; Studies on the pathogenesis of fixed rabies virus in rats. Bulletin of the World Health Organization 33:783–794
    [Google Scholar]
  6. Bak I. J., Markham C. H., Cook M. L., Stevens J. 1977; Intraaxonal transport of herpes simplex virus in the rat central nervous system. Brain Research 136:415–429
    [Google Scholar]
  7. Biilenga G., Heaney T. 1978; Post-exposure local treatment of mice infected with rabies with two axonal flow inhibitors, colchicine and vinblastine. Journal of General Virology 39:381–385
    [Google Scholar]
  8. Campenot R. B. 1977; Local control of neurite development by nerve growth factor. Proceedings of the National Academy of SciencesU.S.A 74:4516–4518
    [Google Scholar]
  9. Carbone K. M., Duchala C. S., Griffin I. W., Kincaid A. L., Narayan O. 1987; Pathogenesis of Borna disease in rats: evidence that intra-axonal spread is the major route for virus dissemination and the determinant for disease incubation. Journal of Virology 61:3431–3440
    [Google Scholar]
  10. Ceccaldi P. E., Gillet J. P., Lycke E., Tsiang H. 1988; Colchicine-mediated inhibition of viral transport in cultured neurons and in the brain. In Structure and Function of the Cytoskeleton: Biological and Physiological Aspects 171387–392 Rousset B. A. F. London: John Libbey;
    [Google Scholar]
  11. Ceccaldi P. E., Gillet J. P., Tsiang H. 1989; Inhibition of rabies virus transport in the central nervous system. Journal of Neuropathology and Experimental Neurology in press
    [Google Scholar]
  12. Clark H. F. 1978; Rabies virus increase in virulence when propagated in neuroblastoma cells. Science 199:1072–1075
    [Google Scholar]
  13. Conti C, Hauttecoeur B, Morelec M. J., Bizzini B., Orsi N., Tsiang H. 1988; Inhibition of rabies virus infection by a soluble membrane fraction from the central nervous system. Archives of Virology 98:73–86
    [Google Scholar]
  14. Couraud J. Y., Digiamberardino L. 1980; Axonal transport of the molecular forms of acetylcholinesterase in chick sciatic nerve. Journal of Neurochemistry 35:1053–1066
    [Google Scholar]
  15. Dal canto M. C, Barbano R. L., Iubelt B. 1986; Ultrastructural immunochemical localization of poliovirus during virulent infection of mice. Journal of Neuropathology and Experimental Neurology 45:613–618
    [Google Scholar]
  16. Dean D. J., Evans W. M., Mccre R. C. . 1963; Pathogenesis of rabies. Bulletin of the World Health Organization 29:803–811
    [Google Scholar]
  17. Dietzschold B., Wiktor T. J., Troianowski J. Q., Macfarlan R. I., Wunner W. H., Torres-Anjel M. J., Koprowski H. 1985; Differences in cell-to-cell spread of pathogenic and apathogenic rabies virus in vivo and in vitro. Journal of Virology 56:12–18
    [Google Scholar]
  18. Gilbert S. P., Allen R. D., Svoboda R. D. 1985; Translocation of vesicles from squid axoplasm on flagellar microtubules. Nature, London 315:245–248
    [Google Scholar]
  19. Gillet J. P., Derer P., Tsiang H. 1986; Axonal transport of rabies virus in the central nervous system of the rat. Journal of Neuropathology and Experimental Neurology 45:619–634
    [Google Scholar]
  20. Honda Y., Kawai A., Matsumoto S. 1984; Comparative studies of rabies and Sindbis virus replication in human neuroblastoma (SYM-I) cells that can produce interferon. Journal of General Virology 65:1645–1653
    [Google Scholar]
  21. Iwasaki Y., Clark H. F. 1975; Cell to cell transmission of virus in the central nervous system. II. Experimental rabies in mouse. Laboratory Investigation 33:391–399
    [Google Scholar]
  22. Iwasaki Y., Clark H. F. 1977; Rabies virus infection in mouse neuroblastoma cells. Laboratory Investigation 36:578–584
    [Google Scholar]
  23. Iwasaki Y., Liu D. S., Yamamoto T., Konno H. 1985; On the replication and spread of rabies virus in the human central nervous system. Journal of Neuropathology and Experimental Neurology 44:185–195
    [Google Scholar]
  24. Johnson R. T. 1965; Experimental rabies. Studies of vulnerability and pathogenesis using fluorescent antibody staining. Journal of Neuropathology and Experimental Neurology 24:662–675
    [Google Scholar]
  25. Kaluza G., Lell G., Reinacher M., Stitz L., Willems W. R. 1987; Neurogenic spread of Semliki Forest virus in mice. Archives of Virology 93:97–110
    [Google Scholar]
  26. Kimberlin R. H., Walker C. A. 1986; Pathogenesis of scrapie (strain 263K) in hamsters infected intracerebrally, intraperitoneally or intraocularly. Journal of General Virology 67:255–263
    [Google Scholar]
  27. Klein R. J., Destefano E. 1983; Dissemination of herpes simplex in ganglia after footpad inoculation in neurectomized and non-neurectomized mice. Archives of Virology 77:231–238
    [Google Scholar]
  28. Kristensson K., Lycke E., Sjöstrand I. 1971; Spread of herpes simplex virus in peripheral nerves. Acta neuropathologica 17:44–53
    [Google Scholar]
  29. Kristensson K., Lycke E., Röyttä M., Svennerholm B., Vahlne A. 1986; Neuritic transport of herpes simplex virus in rat sensory neurons in vitro. Effects of substances interacting with microtubular function and axonal flow [nocodazole, taxol and erythro-9-3-(2-hydroxynonyl)adenine]. Journal of General Virology 67:2023–2028
    [Google Scholar]
  30. Kucera P., Dolivo M., Coulon P., Flamand A. 1985; Pathway of the early progression of virulent and avirulent rabies strains from the eye to the brain. Journal of Virology 55:158–162
    [Google Scholar]
  31. Lodmell D. L., Ewalt L. C. 1987; Immune sera and antiglycoprotein monoclonal antibodies inhibit in vitro cell-to-cell spread of pathogenic rabies viruses. Journal of Virology 61:3314–3318
    [Google Scholar]
  32. Lorenz T., Willard M. 1978; Subcellular fractionation of intra-axonally transported polypeptides in the rabbit visual system. Proceedings of the National Academy of SciencesU.S.A 75:505–509
    [Google Scholar]
  33. Lubinska L., Niemierko B. 1971; Velocity and intensity of bidirectional migration of acetylcholinesterase in transected nerves. Brain Research 27:329–342
    [Google Scholar]
  34. Lycke E., Tsiang H. 1987; Rabies virus infection of cultured rat sensory neurons. Journal of Virology 61:2733–2741
    [Google Scholar]
  35. Lycke E., Kristensson K., Svennerholm B., Vahlne A., Ziegler R. 1984; Uptake and transport of herpes simplex virus in neurites of rat dorsal root ganglia cells in culture. Journal of General Virology 65:55–64
    [Google Scholar]
  36. Matsumoto S. 1975; Electron microscopy of central nervous system. In The Natural History of Rabies217–235 Baer G. M. New York & London: Academic Press;
    [Google Scholar]
  37. Murphy F. A. 1977; Rabies pathogenesis. Brief review. Archives of Virology 54:279–297
    [Google Scholar]
  38. Ochs S. 1972; Fast transport of material in mammalian nerve fibers. Science 176:252–260
    [Google Scholar]
  39. Roux E. 1888; Sur la presence du virus rabique dans les nerfs. Annales de I’Institut Pasteur 2:18–27
    [Google Scholar]
  40. Schwab M. 1977; Ultrastructural localization of a nerve growth factor horseradish peroxidase (NGF-HRP)coupling product after retrograde axonal transport in adrenergic neurons. Brain Research 130:190–196
    [Google Scholar]
  41. Smith A. L., Tignor G. H., Mifune K., Motohashi T. 1977; Isolation and assay of rabies serogroup viruses in CER cells. Intervirology 8:92–99
    [Google Scholar]
  42. Stockel K., Schwab M., Thoenbn H. 1975; Comparison between the retrograde axonal transport of nerve growth factor and tetanus toxin in motor, sensory and adrenergic neurons. Brain Research 99:1–16
    [Google Scholar]
  43. Sung J. H., Hayano M., Mastri A. R., Okagaki T. 1976; A case of human rabies and ultrastructure of the Negri body. Journal of Neuropathology and Experimental Neurology 35:541–559
    [Google Scholar]
  44. Superti F., Derer M., Tsiang H. 1984; Mechanism of rabies virus entry into CER cells. Journal of General Virology 65:781–789
    [Google Scholar]
  45. Superti F., Hauttecoeur B., Morelec M. J., Goldoni P., Bizzini B., Tsiang H. 1986; Involvement of gangliosides in rabies virus infection. Journal of General Virology 67:47–56
    [Google Scholar]
  46. Tsiang H. 1979; Evidence for an intraaxonal transport of fixed and street rabies virus. Journal of Neuropathology and Experimental Neurology 38:286–296
    [Google Scholar]
  47. Tsiang H. 1988; Interactions of rabies virus and host cells. In Rabies67–100 Campbell J. B., Charlton K. M. Boston: Kluwer Academic Publishers;
    [Google Scholar]
  48. Tsiang H., Superti F. 1984; Ammonium chloride and chloroquine inhibit rabies virus infection in neuroblastoma cell. Archives of Virology 81:377–382
    [Google Scholar]
  49. Tsiang H., Derer M., Taxi J. 1983a; An in vivo and in vitro study of rabies virus infection of the rat superior cervical ganglia. Archives of Virology 76:231–243
    [Google Scholar]
  50. Tsiang H., Koulakoff A., Bizzini B., Berwald-netter Y. 1983b; Neurotropism of rabies virus. An in vitro study. Journal of Neuropathology and Experimental Neurology 42:439–452
    [Google Scholar]
  51. Tsiang H., Delaporte S., Ambroise D. J., Derer M., Koenig I. 1986; Infection of cultured rat myotubes and neurons from the spinal cord by rabies virus. Journal of Neuropathology and Experimental Neurology 45:28–42
    [Google Scholar]
  52. Tsukita S., Ishikawa H. 1980; The movement of membranous organelles in axons. Journal of Cell Biology 84:513–530
    [Google Scholar]
  53. Tyler K. L., Mcpee D. A., Fields B. N. 1987; Distinct pathways of viral spread in the host determined by reovirus S1 gene segment. Science 233:770–774
    [Google Scholar]
  54. Tytell M., Black M. M., Garner J. A., Lasek R. J. 1981; Axonal transport: each major component reflects the movement of distinct macromolecular complexes. Science 214:179–181
    [Google Scholar]
  55. Wisniewski H., Shelanski M. L., Terry R. D. 1968; Effects of mitotic spindle inhibitors on microtubules and neurofilaments in anterior horn cells. Journal of Cell Biology 38:224–229
    [Google Scholar]
  56. Ziegler R. J., Herman R. E. 1980; Peripheral infection in culture of rat sensory neurons by herpes simplexvirus. Infection and Immunity 28:620–623
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-70-8-2075
Loading
/content/journal/jgv/10.1099/0022-1317-70-8-2075
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error