1887

Abstract

Neural involvement following infections of influenza viruses can be serious. The neural transport of influenza viruses from the periphery to the central nervous system has been indicated by using mouse models. However, no direct evidence for neuronal infection has been obtained and the mechanisms of neural transmission of influenza viruses have not been reported. In this study, the transneural transmission of a neurotropic influenza A virus was examined using compartmentalized cultures of neurons from mouse dorsal root ganglia, and the results were compared with those obtained using the pseudorabies virus, a virus with well-established neurotransmission. Both viruses reached the cell bodies of the neurons via the axons. This is the first report on axonal transport of influenza A virus . In addition, the role of the cytoskeleton (microtubules, microfilaments and intermediate filaments) in the neural transmission of influenza virus was investigated by conducting cytoskeletal perturbation experiments. The results indicated that the transport of avian influenza A virus in the neurons was independent of microtubule integrity but was dependent on the integrity of intermediate filaments, whereas pseudorabies virus needed both for neural spread.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80704-0
2005-04-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/4/vir861131.html?itemId=/content/journal/jgv/10.1099/vir.0.80704-0&mimeType=html&fmt=ahah

References

  1. Arcangeletti C., Olink-Coux M., Minisini R., Huesca M., Chezzi C., Scherrer K. 1992; Patterns of cytodistribution of prosomal antigens on the vimentin and cytokeratin networks of monkey kidney cells. Eur J Cell Biol 59:464–476
    [Google Scholar]
  2. Arcangeletti M. C., Pinardi F., Missorini S., De Conto F., Conti G., Portincasa P., Scherrer K., Chezzi C. 1997; Modification of cytoskeleton and prosome networks in relation to protein synthesis in influenza A virus-infected LLC-MK2 cells. Virus Res 51:19–34 [CrossRef]
    [Google Scholar]
  3. Ashok A., Atwood W. J. 2003; Contrasting roles of endosomal pH and the cytoskeleton in infection of human glial cells by JC virus and simian virus 40. J Virol 77:1347–1356 [CrossRef]
    [Google Scholar]
  4. Brask J., Owe-Larsson B., Hill R. H., Kristensson K. 2001; Changes in calcium currents and GABAergic spontaneous activity in cultured rat hippocampal neurons after a neurotropic influenza A virus infection. Brain Res Bull 55:421–429 [CrossRef]
    [Google Scholar]
  5. Campenot R. B. 1977; Local control of neurite development by nerve growth factor. Proc Natl Acad Sci U S A 74:4516–4519 [CrossRef]
    [Google Scholar]
  6. Campenot R. B., Martin G. 2001; Construction and use of compartmented cultures for studies of cell biology of neurons. In Protocols for Neural Cell Culture , 3rd edn. pp  49–57 Edited by Fedoroff S., Richardson A. Totowa, NJ: Humana;
    [Google Scholar]
  7. Card J. P., Rinaman L., Schwaber J. S., Miselis R. R., Whealy M. E., Robbins A. K., Enquist L. W. 1990; Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J Neurosci 10:1974–1994
    [Google Scholar]
  8. Centers for Disease Control & Prevention; 2004; Cases of influenza A (H5N1)-Thailand, 2004. Morb Mortal Wkly Rep 53:100–103
    [Google Scholar]
  9. Cheung H. T., Terry D. S. 1980; Effects of nocodazole, a new synthetic microtubule inhibitor, on movement and spreading of mouse peritoneal macrophages. Cell Biol Int Rep 4:1125–1129 [CrossRef]
    [Google Scholar]
  10. Claas E. C. J., Osterhaus A. D. M. E., van Beek R., De Jong J. C., Rimmelzwaan G. F., Senne D. A., Krauss S., Shortridge K. F., Webster R. G. 1998; Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351:472–477 [CrossRef]
    [Google Scholar]
  11. Cooper J. A. 1987; Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473–1478 [CrossRef]
    [Google Scholar]
  12. Cordo S. M., Candurra N. A. 2003; Intermediate filament integrity is required for Junin virus replication. Virus Res 97:47–55 [CrossRef]
    [Google Scholar]
  13. Coulombe P. A., Wong P. 2004; Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat Cell Biol 6:699–706 [CrossRef]
    [Google Scholar]
  14. Cudmore S., Cossart P., Griffiths G., Way M. 1995; Actin-based motility of vaccinia virus. Nature 378:636–638 [CrossRef]
    [Google Scholar]
  15. Cudmore S., Rechmann I., Way M. 1997; Viral manipulations of the actin cytoskeleton. Trends Microbiol 5:142–148 [CrossRef]
    [Google Scholar]
  16. Dotti C. G., Simons K. 1990; Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell 62:63–72 [CrossRef]
    [Google Scholar]
  17. Dotti C. G., Kartenbeck J., Simons K. 1993; Polarized distribution of the viral glycoproteins of vesicular stomatitis, fowl plague and Semliki Forest viruses in hippocampal neurons in culture: a light and electron microscopy study. Brain Res 610:141–147 [CrossRef]
    [Google Scholar]
  18. Eckert B. S. 1985; Alteration of intermediate filament distribution in PtK1 cells by acrylamide. Eur J Cell Biol 37:169–174
    [Google Scholar]
  19. Enquist L. W., Tomishima M. J., Gross S., Smith G. A. 2002; Directional spread of an α -herpesvirus in the nervous system. Vet Microbiol 86:5–16 [CrossRef]
    [Google Scholar]
  20. Field H. J., Hill T. J. 1974; The pathogenesis of pseudorabies in mice following peripheral inoculation. J Gen Virol 23:145–157 [CrossRef]
    [Google Scholar]
  21. Frankova V., Jirasek A., Tumova B. 1977; Type A influenza: postmortem virus isolations from different organs in human lethal cases. Arch Virol 53:265–268 [CrossRef]
    [Google Scholar]
  22. Hakoda S., Nakatani T. 2000; A pregnant woman with influenza A encephalopathy in whom influenza A/Hong Kong virus (H3) was isolated from cerebrospinal fluid. Arch Intern Med 160:1041–1045 [CrossRef]
    [Google Scholar]
  23. Hayashi H., Campenot R. B., Vance D. E., Vance J. E. 2004; Glial lipoproteins stimulate axon growth of central nervous system neurons in compartmented cultures. J Biol Chem 279:14009–14015 [CrossRef]
    [Google Scholar]
  24. Itakura C., Nakatsuka J., Goto M. 1981; An incidence of pseudorabies (Aujeszky's disease) in piglets in Japan. Nippon Juigaku Zasshi 43:923–927 [CrossRef]
    [Google Scholar]
  25. Ito T., Goto H., Yamamoto E., Tanaka H., Takeuchi M., Kuwayama M., Kawaoka Y., Otsuki K. 2001; Generation of a highly pathogenic avian influenza A virus from an avirulent field isolate by passaging in chickens. J Virol 75:4439–4443 [CrossRef]
    [Google Scholar]
  26. Kaelin K., Dezélée S., Masse M. J., Bras F., Flamand A. 2000; The UL25 protein of pseudorabies virus associates with capsids and localizes to the nucleus and to microtubules. J Virol 74:474–482 [CrossRef]
    [Google Scholar]
  27. Kida H., Yanagawa R., Matsuoka Y. 1980; Duck influenza lacking evidence of disease signs and immune response. Infect Immun 30:547–553
    [Google Scholar]
  28. Kida H., Kawaoka Y., Naeve C. W., Webster R. G. 1987; Antigenetic and genetic conservation of H3 influenza virus in wild ducks. Virology 159:109–119 [CrossRef]
    [Google Scholar]
  29. Kimpinski K., Jelinski S., Mearow K. 1999; The anti-p75 antibody, MC192, and brain-derived neurotrophic factor inhibit nerve growth factor-dependent neurite growth from adult sensory neurons. Neuroscience 93:253–263 [CrossRef]
    [Google Scholar]
  30. Lakadamyali M., Rust M. J., Babcock H. P., Zhuang X. 2003; Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 100:9280–9285 [CrossRef]
    [Google Scholar]
  31. Lee J. C., Field D. J., Lee L. L. 1980; Effects of nocodazole on structures of calf brain tubulin. Biochemistry 19:6209–6215 [CrossRef]
    [Google Scholar]
  32. Levine J., Buchman C. A., Fregien N. 2003; Influenza A virus infection of human Schwann cells in vitro. Acta Otolaryngol 123:41–45
    [Google Scholar]
  33. LoPachin R. M. 2004; The changing view of acrylamide neurotoxicity. Neurotoxicology 25:617–630 [CrossRef]
    [Google Scholar]
  34. LoPachin R. M., Ross J. F., Lehning E. J. 2002; Nerve terminals as the primary site of acrylamide action: a hypothesis. Neurotoxicology 23:43–59 [CrossRef]
    [Google Scholar]
  35. Lycke E., Tsiang H. 1987; Rabies virus infection of cultured rat sensory neurons. J Virol 61:2733–2741
    [Google Scholar]
  36. Matsuda K., Park C. H., Sunden Y., Kimura T., Ochiai K., Kida H., Umemura T. 2004; The vagus nerve is one route of transneural invasion for intranasally inoculated influenza A virus in mice. Vet Pathol 41:101–107 [CrossRef]
    [Google Scholar]
  37. Mounts A. W., Kwong H., Izurieta H. S. 10 other authors 1999; Case-control study of risk factors for avian influenza A (H5N1) disease. Hong Kong 1997 J Infect Dis 180:505–508 [CrossRef]
    [Google Scholar]
  38. Olink-Coux M., Huesca M., Scherrer K. 1992; Specific types of prosomes are associated to subnetworks of the intermediate filaments in PtK1 cells. Eur J Cell Biol 59:148–159
    [Google Scholar]
  39. Park C. H., Ishinaka M., Takada A., Kida H., Kimura T., Ochiai K., Umemura T. 2002; The invasion routes of neurovirulent A/Hong Kong/483/97 (H5N1) influenza virus into the central nervous system after respiratory infection in mice. Arch Virol 147:1425–1436 [CrossRef]
    [Google Scholar]
  40. Ploubidou A., Way M. 2001; Viral transport and the cytoskeleton. Curr Opin Cell Biol 13:97–105 [CrossRef]
    [Google Scholar]
  41. Price R. W., Rubenstein R., Khan A. 1982; Herpes simplex virus infection of isolated autonomic neurons in culture: viral replication and spread in a neuronal network. Arch Virol 71:127–140 [CrossRef]
    [Google Scholar]
  42. Scherrer K., Bey F. 1994; The prosomes (multicatalytic proteinases; proteasomes) and their relationship to the untranslated messenger ribonucleoproteins, the cytoskeleton, and cell differentiation. Prog Nucleic Acid Res Mol Biol 49:1–64
    [Google Scholar]
  43. Shinya K., Silvano F. D., Morita T., Shimada A., Nakajima M., Ito T., Otsuki K., Umemura T. 1998; Encephalitis in mice inoculated intranasally with an influenza virus strain originated from a water bird. J Vet Med Sci 60:627–629 [CrossRef]
    [Google Scholar]
  44. Shinya K., Shimada A., Ito T., Otsuki K., Morita T., Tanaka H., Takada A., Kida H., Umemura T. 2000; Avian influenza virus intranasally inoculated infects the central nervous system of mice through the general visceral afferent nerve. Arch Virol 145:187–195 [CrossRef]
    [Google Scholar]
  45. Silvano F. D., Yoshikawa M., Shimada A., Otsuki K., Umemura T. 1997; Enhanced neuropathogenicity of avian influenza A virus by passages through air sac and brain of chicks. J Vet Med Sci 59:143–148 [CrossRef]
    [Google Scholar]
  46. Sodeik B. 2000; Mechanisms of viral transport in the cytoplasm. Trends Microbiol 8:465–472 [CrossRef]
    [Google Scholar]
  47. Takahashi M., Yamada T., Nakanishi K., Fujita K., Nakajima K., Nobusawa E., Yamamoto T., Kato T., Okada H. 1997; Influenza A virus infection of primary cultured cells from rat fetal brain. Parkinsonism Relat Disord 3:97–102 [CrossRef]
    [Google Scholar]
  48. Tanaka H., Park C. H., Ninomiya A., Ozaki H., Takada A., Umemura T., Kida H. 2003; Neurotropism of the 1997 Hong Kong H5N1 influenza virus in mice. Vet Microbiol 95:1–13 [CrossRef]
    [Google Scholar]
  49. Tennyson V. M., Gershon M. D. 1975; Light and electron microscopy of dorsal root, sympathetic, and enteric ganglia. In Peripheral Neuropathy , 2nd edn. vol 1121–155 Edited by Dyck P. J., Thomas P. K., Griffin J. W., Low P. A., Poduslo J. F. London: Saunders;
    [Google Scholar]
  50. Thomas P. K., Berthold C. H., Ochoa J. L. 1993; Microscopic anatomy of the peripheral nervous system. In Peripheral Neuropathy , 3rd edn. vol 1 pp  28–91 Edited by Dyck P. J., Thomas P. K., Griffin J. W., Low P. A., Poduslo J. F. London: Saunders;
    [Google Scholar]
  51. Togashi T., Matsuzono Y., Anakura M., Nerome K. 1997; Acute encephalitis and encephalopathy at the height of influenza in childhood. Nippon Rinsho 55:2699–2705
    [Google Scholar]
  52. Tomishima M. J., Smith G. A., Enquist L. W. 2001; Sorting and transport of alpha herpesviruses in axons. Traffic 2:429–436 [CrossRef]
    [Google Scholar]
  53. Tran T. H., Nguyen T. L., Nguyen T. D. 27 other authors 2004; Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med 350:1179–1188 [CrossRef]
    [Google Scholar]
  54. Turner D., Wailoo A., Nicholson K., Cooper N., Sutton A., Abrams K. 2003; Systematic review and economic decision modelling for the prevention and treatment of influenza A and B. Health Technol Assess 7:1–182
    [Google Scholar]
  55. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y. 1992; Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179
    [Google Scholar]
  56. Yamada K. M., Spooner B. S., Wessells N. K. 1971; Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol 49:614–635 [CrossRef]
    [Google Scholar]
  57. Yuen K. Y., Chan P. K. S., Peiris M. 8 other authors 1998; Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351:467–471 [CrossRef]
    [Google Scholar]
  58. Ziegler R. J., Herman R. E. 1980; Peripheral infection in culture of rat sensory neurons by herpes simplex virus. Infect Immun 28:620–623
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80704-0
Loading
/content/journal/jgv/10.1099/vir.0.80704-0
Loading

Data & Media loading...

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