1887

Abstract

In order to determine the influence of poliovirus receptor (PVR) expression on poliovirus cell tropism and neuropathogenesis, two transgenic (tg) mouse models were produced in which PVR was expressed under the transcriptional control of the human PVR gene promoter (hg–PVR mice) and the CAG promoter (CAG–PVR mice). Then the pathogenicity of poliovirus after intracerebral inoculation of the type 1 Mahoney strain was compared. These showed completely different clinical and pathological changes. In the former, the expression of PVR in neurons in the central nervous system (CNS) confered susceptibility to poliovirus, and a paralytic disease that resembled the human poliomyelitis occurred. In the latter, PVR expression was detected in glial and ependymal cells in addition to the neurons. Paralysis of the limbs and death were rarely observed and mice survived without showing substantial clinical abnormality. Histopathological examination revealed that glial and ependymal cells also became susceptible to poliovirus infection. Poliovirus antigens were mainly detected in ependymal and glial cells and hippocampal neurons near the lateral ventricles in the brain, but were not frequently detected in neurons in the brainstem unlike in the hg–PVR mice. The levels of viral antigens and virus recovered from the CNS of CAG–PVR mice began to decrease as early as 2 days after inoculation, which suggested induction of a fast immune response. These results suggest that the neuropathogenicity of poliovirus changes markedly depending on the specific expression of the PVR molecule in the CNS.

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2002-05-01
2024-12-06
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References

  1. Aoki J., Koike S., Ise I., Sato-Yoshida Y., Nomoto A. 1994; Amino acid residues on human poliovirus receptor involved in interaction with poliovirus. Journal of Biological Chemistry 269:8431–8438
    [Google Scholar]
  2. Bergelson J. M., Cunningham J. A., Droguet G., Kurt-Jones E. A., Krithivas A., Hong J. S., Horwitz M. S., Crowell R. L., Finberg R. W. 1997; Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320–1323
    [Google Scholar]
  3. Bergelson J. M., Krithivas A., Celi L., Droguett G., Horwitz M. S., Wickham T., Crowell R. L., Finberg R. W. 1998; The murine CAR homolog is a receptor for coxsackie B viruses and adenoviruses. Journal of Virology 72:415–419
    [Google Scholar]
  4. Bodian D. 1955; Emerging concept of poliomyelitis infection. Science 12:105–108
    [Google Scholar]
  5. Chomczynski P., Sacchi N. 1987; Single-step method of RNA isolation by acid guanidium thiocyanate–phenol–chloroform extraction. Analytical Biochemistry 162:156–159
    [Google Scholar]
  6. Fleming J. O., Trousdale M. D., El-Zaatari F. A. K., Stohlman S. A., Weiner L. P. 1986; Pathogenicity of antigenic variants of murine coronavirus JHM selected with monoclonal antibodies. Journal of Virology 58:869–875
    [Google Scholar]
  7. Holland J. J. 1961; Receptor affinities as major determinants of enterovirus tissue tropisms in humans. Virology 15:312–326
    [Google Scholar]
  8. Holland J. J., McLaren J. C., Syverton J. T. 1959; The mammalian cell virus relationship. IV. Infection of naturally insusceptible cells with enterovirus ribonucleic acid. Journal of Experimental Medicine 110:65–80
    [Google Scholar]
  9. Horie H., Koike S., Kurata T., Sato-Yoshida Y., Ise I., Ota Y., Abe S., Hioki K., Kato H., Taya C., Nomura T., Hashizume S., Yonekwa H., Nomoto A. 1994; Transgenic mice carrying the human poliovirus receptor: new animal models for study of poliovirus neurovirulence. Journal of Virology 68:681–688
    [Google Scholar]
  10. Horwitz M. S., Evans C. F., Killer F. G., Oldstone M. B. A. 1999; Detailed in vivo analysis of interferon-γ induced major histocompatibility complex expression in the central nervous system: astrocytes fail to express major histocompatibility complex class I and II molecules. Laboratory Investigation 79:235–242
    [Google Scholar]
  11. Johansson C. B., Momma S. D., Clarke L., Risling M., Lendahl U., Frisen J. 1999; Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25–34
    [Google Scholar]
  12. Johnson R. T. 1998; Meningitis, encephalitis and poliomyelitis. In Viral Infections of the Nervous System , 2nd edn. pp 87–100 Philadelphia: Lippincott–Raven;
    [Google Scholar]
  13. Johnson R. T., Johnson K. P., Edmonds C. J. 1967; Virus-induced hydrocephalus: development of aqueductal stenosis in hamsters after mumps infection. Science 157:1066–1067
    [Google Scholar]
  14. Joli E., Mucke L., Oldstone M. B. A. 1991; Viral persistence in neurons explained by lack of major histocompatibility class I expression. Science 253:1283–1285
    [Google Scholar]
  15. Koike S., Horie H., Ise I., Okitsu A., Yoshida M., Iizuka N., Takeuchi K., Takegami T., Nomoto A. 1990; The poliovirus receptor protein is produced both as membrane-bound and secreted forms. EMBO Journal 9:3217–3224
    [Google Scholar]
  16. Koike S., Taya C., Kurata T., Abe S., Ise I., Yonekawa H., Nomoto A. 1991; Transgenic mice susceptible to poliovirus. Proceedings of the National Academy of Sciences, USA 88:951–955
    [Google Scholar]
  17. Koike S., Ise I., Sato Y., Yonekawa H., Gotoh O., Nomoto A. 1992; A second gene for the African green monkey poliovirus receptor that has no putative N -glycosylation site in the functional N-terminal immunoglobulin-like domain. Journal of Virology 66:7059–7066
    [Google Scholar]
  18. Koike S., Taya C., Aoki J., Matsuda Y., Ise I., Takeda H., Matsuzaki T., Amanuma H., Yonekawa H., Nomoto A. 1994; Characterization of three different transgenic mouse lines that carry human poliovirus receptor gene – influence of the transgene expression on pathogenesis. Archives of Virology 139:351–363
    [Google Scholar]
  19. Kunin C. M., Jordan W. S. 1961; In vitro adsorption of poliovirus by noncultured tissues. Effect of species, age and malignancy. American Journal of Hygiene 73:245–257
    [Google Scholar]
  20. Melnick J. L. 1996; Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Fields Virology pp 655–712 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  21. Mendelsohn C. L., Wimmer E., Racaniello V. R. 1989; Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56:855–865
    [Google Scholar]
  22. Niwa H., Yamamura K., Miyazaki J. 1991; Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193–200
    [Google Scholar]
  23. Nomoto A., Koike S., Aoki J. 1994; Tissue tropism and species specificity of poliovirus infection. Trends in Microbiology 2:47–51
    [Google Scholar]
  24. Price R. A., Garcia J. H., Rightsel W. A. 1970; Choriomeningitis and myocarditis in an adolescent with isolation of coxsackie B-5 virus. American Journal of Clinical Pathology 53:825–831
    [Google Scholar]
  25. Ren R., Racaniello V. R. 1992; Human poliovirus receptor gene expression and poliovirus tissue tropism in transgenic mice. Journal of Virology 66:296–304
    [Google Scholar]
  26. Ren R. B., Costantini F., Gorgacz E. J., Lee J. J., Racaniello V. R. 1990; Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell 63:353–362
    [Google Scholar]
  27. Rueckert R. R. 1996; Picornaviridae: the viruses and their replication. In Fields Virology pp 609–654 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  28. Sabin A. 1956; Pathogenesis of poliomyelitis. Reappraisal in the light of new data. Science 123:1151–1157
    [Google Scholar]
  29. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Shiroki K., Ishi T., Aoki T., Kobashi M., Ohka S., Nomoto A. 1995; A new cis-acting element for RNA replication within the 5’ noncoding region of poliovirus type 1 RNA. Journal of Virology 69:6825–6832
    [Google Scholar]
  31. Tomko R. P., Xu R., Philipson L. 1997; HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proceedings of the National Academy of Sciences, USA 94:3352–3356
    [Google Scholar]
  32. Wolinsky J. S. 1996; Mumps virus. In Fields Virology pp 1243–1265 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  33. World Health Organization 1997; Manual for the Virological Investigation of Polio . pp 44–51 Edited by the Expanded Programme on Immunization Geneva: World Health Organization;
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