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. 1971 Sep;8(3):318–329. doi: 10.1128/jvi.8.3.318-329.1971

Ultrastructural Study of Long-Term Measles Infection in Cultures of Hamster Dorsal-Root Ganglion

Cedric S Raine 1,2, Lawrence A Feldman 1,2, Rachel D Sheppard 1,2, Murray B Bornstein 1,2
PMCID: PMC356245  PMID: 4107542

Abstract

The morphogenesis of the Edmonston strain of measles is described in cultures of hamster dorsal-root ganglion maintained for as long as 63 days postinoculation. The patterns observed confirmed those previously reported in both neural and non-neural tissue. However, in the present tissue, the development of viral material could be followed chronologically within different cell types such as neurons and Schwann cells. Active replication was visualized up to 63 days postinoculation. The appearance of cytoplasmic nucleocapsid preceded that of intranuclear nucleocapsid, the latter occurring after 14 days. These intranuclear inclusions were formed after the transformation of the nucleoli into bizarre pleomorphic bodies which eventually segregated into clumps of nucleocapsid. These intranuclear inclusions mimic those seen in subacute sclerosing panencephalitis, now known to be etiologically related to a measles-like virus.

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Selected References

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  1. ADAMS J. M., IMAGAWA D. T. Measles antibodies in multiple sclerosis. Proc Soc Exp Biol Med. 1962 Dec;111:562–566. doi: 10.3181/00379727-111-27855. [DOI] [PubMed] [Google Scholar]
  2. ALMEIDA J. D., HOWATSON A. F. A negative staining method for cell-associated virus. J Cell Biol. 1963 Mar;16:616–620. doi: 10.1083/jcb.16.3.616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anisimová E., Mares I., Kyncl F. Electron microscopic study of tissue culture cells infected with measles virus. Acta Virol. 1968 Jul;12(4):289–295. [PubMed] [Google Scholar]
  4. BORNSTEIN M. B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab Invest. 1958 Mar-Apr;7(2):134–137. [PubMed] [Google Scholar]
  5. Baringer J. R., Griffith J. F. Experimental measles virus encephalitis. A light, phase, fluorescence, and electron microscopic study. Lab Invest. 1970 Sep;23(3):335–346. [PubMed] [Google Scholar]
  6. Bunge M. B., Bunge R. P., Peterson E. R., Murray M. R. A light and electron microscope study of long-term organized cultures of rat dorsal root ganglia. J Cell Biol. 1967 Feb;32(2):439–466. doi: 10.1083/jcb.32.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Byington D. P., Castro A. E., Burnstein T. Adaptation to hamsters of neurotropic measles virus from subacute sclerosing panencephalitis. Nature. 1970 Feb 7;225(5232):554–555. doi: 10.1038/225554b0. [DOI] [PubMed] [Google Scholar]
  8. Chen T. T., Watanabe I., Zeman W., Mealey J., Jr Subacute sclerosing panencephalitis: propagation of measles virus from brain biopsy in tissue culture. Science. 1969 Mar 14;163(3872):1193–1194. doi: 10.1126/science.163.3872.1193. [DOI] [PubMed] [Google Scholar]
  9. Connolly J. H., Allen I. V., Hurwitz L. J., Millar J. H. Measles-virus antibody and antigen in subacute sclerosing panencephalitis. Lancet. 1967 Mar 11;1(7489):542–544. doi: 10.1016/s0140-6736(67)92117-4. [DOI] [PubMed] [Google Scholar]
  10. Feldman L. A., Sheppard R. D., Bornstein M. B. Herpes simplex virus-host cell relationships in organized cultures of mammalian nerve tissues. J Virol. 1968 Jun;2(6):621–628. doi: 10.1128/jvi.2.6.621-628.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Herndon R. M., Rubinstein L. J. Light and electron microscopy observations on the development of viral particles in the inclusions of Dawson's encephalitis (subacute sclerosing panencephalitis). Neurology. 1968 Jan;18(1 Pt 2):8–20. doi: 10.1212/wnl.18.1_part_2.008. [DOI] [PubMed] [Google Scholar]
  12. Horta-Barbosa L., Fuccillo D. A., Sever J. L., Zeman W. Subacute sclerosing panencephalitis: isolation of measles virus from a brain biopsy. Nature. 1969 Mar 8;221(5184):974–974. doi: 10.1038/221974a0. [DOI] [PubMed] [Google Scholar]
  13. KALLMAN F., ADAMS J. M., WILLIAMS R. C., IMAGAWA D. T. Fine structure of cellular inclusions in measles virus infections. J Biophys Biochem Cytol. 1959 Dec;6:379–382. doi: 10.1083/jcb.6.3.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Katz M., Oyanagi S., Koprowski H. Subacute sclerosing panencephalitis: structures resembling myxovirus nucleocapsids in cells cultured from brain. Nature. 1969 May 31;222(5196):888–890. doi: 10.1038/222888a0. [DOI] [PubMed] [Google Scholar]
  15. Kolár O., Zeman W. Immunoelectrophoretic changes of serum IgG during subacute inflammatory and demyelinating diseases of the central nervous system. Z Immunitatsforsch Allerg Klin Immunol. 1967 Dec;134(3):267–275. [PubMed] [Google Scholar]
  16. MANNWEILER K. ULTRASTRUCTURAL EXAMINATIONS OF TISSUE CULTURES AFTER INFECTION WITH MEASLES VIRUS. Arch Gesamte Virusforsch. 1965;16:89–96. doi: 10.1007/BF01253796. [DOI] [PubMed] [Google Scholar]
  17. Nakai M., Imagawa D. T. Electron microscopy of measles virus replication. J Virol. 1969 Feb;3(2):187–197. doi: 10.1128/jvi.3.2.187-197.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Oyanagi S., ter Meulen V., Katz M., Koprowski H. Comparison of subacute sclerosing panencephalitis and measles viruses: an electron microscope study. J Virol. 1971 Jan;7(1):176–187. doi: 10.1128/jvi.7.1.176-187.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Oyanagi S., ter Meulen V., Müller D., Katz M., Koprowski H. Electron microscopic observations in subacute sclerosing panencephalitis brain cell cultures: their correlation with cytochemical and immunocytological findings. J Virol. 1970 Sep;6(3):370–379. doi: 10.1128/jvi.6.3.370-379.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Payne F. E., Baublis J. V., Itabashi H. H. Isolation of measles virus from cell cultures of brain from a patient with subacute sclerosing panencephalitis. N Engl J Med. 1969 Sep 11;281(11):585–589. doi: 10.1056/NEJM196909112811103. [DOI] [PubMed] [Google Scholar]
  21. Périer O., Vanderhaeghen J. J., Pelc S. Subacute sclerosing leuco-encephalitis. Electron microscopic finding in two cases with inclusion bodies. Acta Neuropathol. 1967 Jul 5;8(4):362–380. doi: 10.1007/BF00696673. [DOI] [PubMed] [Google Scholar]
  22. RAPP F. PLAQUE DIFFERENTIATION AND REPLICATION OF VIRULENT AND ATTENUATED STRAINS OF MEASLES VIRUS. J Bacteriol. 1964 Nov;88:1448–1458. doi: 10.1128/jb.88.5.1448-1458.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Raine C. S., Feldman L. A., Sheppard R. D., Bornstein M. B. Ultrastructure of measles virus in cultures of hamster cerebellum. J Virol. 1969 Aug;4(2):169–181. doi: 10.1128/jvi.4.2.169-181.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tellez-Negal I., Harter D. H. Subacute sclerosing leukoencephalitis: ultrastructure of intranuclear and intracytoplasmic inclusions. Science. 1966 Nov 18;154(3751):899–901. doi: 10.1126/science.154.3751.899. [DOI] [PubMed] [Google Scholar]
  25. WATERSON A. P. MEASLES VIRUS. Arch Gesamte Virusforsch. 1965;16:57–80. doi: 10.1007/BF01253793. [DOI] [PubMed] [Google Scholar]
  26. Wear D. J., Rabin E. R., Richardson L. S., Rapp F. Virus replication and ultrastructural changes after induction of encephalitis in mice by measles virus. Exp Mol Pathol. 1968 Dec;9(3):405–417. doi: 10.1016/0014-4800(68)90029-4. [DOI] [PubMed] [Google Scholar]
  27. Zu Rhein G. M., Chou S. M. Subacute sclerosing panencephalitis. Ultrastructural study of a brain biopsy. Neurology. 1968 Jan;18(1 Pt 2):146–160. doi: 10.1212/wnl.18.1_part_2.146. [DOI] [PubMed] [Google Scholar]
  28. ter Meulen V., Müller D., Katz M., Käckell M. Y., Joppich G. Immunohistological, microscical and neurochemical studies on encephalitides. IV. Subacute sclerosing (progressive) panencephalitis. Histochemical and immunohistological findings in tissue cultures derived from SSPE brain biopsies. Acta Neuropathol. 1970;15(1):1–10. doi: 10.1007/BF00690684. [DOI] [PubMed] [Google Scholar]

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