Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1993 Jun;67(6):3375–3383. doi: 10.1128/jvi.67.6.3375-3383.1993

Spontaneous and differentiation-dependent regulation of measles virus gene expression in human glial cells.

S Schneider-Schaulies 1, J Schneider-Schaulies 1, M Bayer 1, S Löffler 1, V ter Meulen 1
PMCID: PMC237681  PMID: 8388504

Abstract

The expression of measles virus (MV) in six different permanent human glioma cell lines (D-54, U-251, U-138, U-105, U-373, and D-32) was analyzed. Although all cell lines were permissive for productive replication of all MV strains tested, U-251, D-54, and D-32 cells spontaneously revealed restrictions of MV transcription similar to those observed for primary rat astroglial cells and brain tissue. In vitro differentiation of D-54 and U-251 cells by substances affecting the intracellular cyclic AMP level caused a significant reduction of the expression of the viral proteins after 18, 72, and 144 h of infection. This pronounced restriction was not paralleled to a comparable level by an inhibition of the synthesis and biological activity in vitro of virus-specific mRNAs as shown by quantitative Northern (RNA) blot analyses and in vitro translation. The block in viral protein synthesis could not be attributed to the induction of type I interferon by any of the substances tested. Our findings indicate that down-regulation of MV gene expression in human brain cells can occur by a cell type-dependent regulation of the viral mRNA transcription and a differentiation-dependent regulation of translation, both of which may be crucial for the establishment of persistent MV infections in the central nervous system.

Full text

PDF
3375

Images in this article

3377Image
on p.3377
3379Image
on p.3379
3379Image
on p.3379
3380Image
on p.3380
3380Image
on p.3380
3380Image
on p.3380

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atwater J. A., Samuel C. E. Mechanism of interferon action: interferon inhibits the synthesis of viral proteins and induces protein P1 phosphorylation in both adenylate cyclase-deficient and cAMP-dependent protein kinase-deficient variants of mouse lymphoma cells. Virology. 1982 Nov;123(1):206–211. doi: 10.1016/0042-6822(82)90306-3. [DOI] [PubMed] [Google Scholar]
  2. Beushausen S., Narindrasorasak S., Sanwal B. D., Dales S. In vivo and in vitro models of demyelinating disease: activation of the adenylate cyclase system influences JHM virus expression in explanted rat oligodendrocytes. J Virol. 1987 Dec;61(12):3795–3803. doi: 10.1128/jvi.61.12.3795-3803.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bigner D. D., Bigner S. H., Pontén J., Westermark B., Mahaley M. S., Ruoslahti E., Herschman H., Eng L. F., Wikstrand C. J. Heterogeneity of Genotypic and phenotypic characteristics of fifteen permanent cell lines derived from human gliomas. J Neuropathol Exp Neurol. 1981 May;40(3):201–229. doi: 10.1097/00005072-198105000-00001. [DOI] [PubMed] [Google Scholar]
  4. Cattaneo R., Rebmann G., Baczko K., ter Meulen V., Billeter M. A. Altered ratios of measles virus transcripts in diseased human brains. Virology. 1987 Oct;160(2):523–526. doi: 10.1016/0042-6822(87)90031-6. [DOI] [PubMed] [Google Scholar]
  5. Cattaneo R., Rebmann G., Schmid A., Baczko K., ter Meulen V., Billeter M. A. Altered transcription of a defective measles virus genome derived from a diseased human brain. EMBO J. 1987 Mar;6(3):681–688. doi: 10.1002/j.1460-2075.1987.tb04808.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cervera M., Dreyfuss G., Penman S. Messenger RNA is translated when associated with the cytoskeletal framework in normal and VSV-infected HeLa cells. Cell. 1981 Jan;23(1):113–120. doi: 10.1016/0092-8674(81)90276-2. [DOI] [PubMed] [Google Scholar]
  7. Dildine S. L., Semler B. L. Conservation of RNA-protein interactions among picornaviruses. J Virol. 1992 Jul;66(7):4364–4376. doi: 10.1128/jvi.66.7.4364-4376.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dubois M. F., Galabru J., Lebon P., Safer B., Hovanessian A. G. Reduced activity of the interferon-induced double-stranded RNA-dependent protein kinase during a heat shock stress. J Biol Chem. 1989 Jul 25;264(21):12165–12171. [PubMed] [Google Scholar]
  9. Fort P., Marty L., Piechaczyk M., el Sabrouty S., Dani C., Jeanteur P., Blanchard J. M. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 1985 Mar 11;13(5):1431–1442. doi: 10.1093/nar/13.5.1431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Horikami S. M., Moyer S. A. Host range mutants of vesicular stomatitis virus defective in in vitro RNA methylation. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7694–7698. doi: 10.1073/pnas.79.24.7694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Horisberger M. A., Hochkeppel H. K. IFN-alpha induced human 78 kD protein: purification and homologies with the mouse Mx protein, production of monoclonal antibodies, and potentiation effect of IFN-gamma. J Interferon Res. 1987 Aug;7(4):331–343. doi: 10.1089/jir.1987.7.331. [DOI] [PubMed] [Google Scholar]
  12. Jacobs B. L., Miyamoto N. G., Samuel C. E. Mechanism of interferon action: studies on the activation of protein phosphorylation and the inhibition of translation in cell-free systems. J Interferon Res. 1988 Oct;8(5):617–631. doi: 10.1089/jir.1988.8.617. [DOI] [PubMed] [Google Scholar]
  13. Kobune K., Kobune F., Yamanouchi K., Nagashima K., Yoshikawa Y., Hayami M. Neurovirulence of rat brain-adapted measles virus. Jpn J Exp Med. 1983 Jun;53(3):177–180. [PubMed] [Google Scholar]
  14. Kraus E., Schneider-Schaulies S., Miyasaka M., Tamatani T., Sedgwick J. Augmentation of major histocompatibility complex class I and ICAM-1 expression on glial cells following measles virus infection: evidence for the role of type-1 interferon. Eur J Immunol. 1992 Jan;22(1):175–182. doi: 10.1002/eji.1830220126. [DOI] [PubMed] [Google Scholar]
  15. Meier E., Kunz G., Haller O., Arnheiter H. Activity of rat Mx proteins against a rhabdovirus. J Virol. 1990 Dec;64(12):6263–6269. doi: 10.1128/jvi.64.12.6263-6269.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Miller C. A., Carrigan D. R. Reversible repression and activation of measles virus infection in neural cells. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1629–1633. doi: 10.1073/pnas.79.5.1629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ogura H., Baczko K., Rima B. K., ter Meulen V. Selective inhibition of translation of the mRNA coding for measles virus membrane protein at elevated temperatures. J Virol. 1987 Feb;61(2):472–479. doi: 10.1128/jvi.61.2.472-479.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ogura H., Rima B. K., Tas P., Baczko K., ter Meulen V. Restricted synthesis of the fusion protein of measles virus at elevated temperatures. J Gen Virol. 1988 Apr;69(Pt 4):925–929. doi: 10.1099/0022-1317-69-4-925. [DOI] [PubMed] [Google Scholar]
  19. Pagliusi S., Antonicek H., Gloor S., Frank R., Moos M., Schachner M. Identification of a cDNA clone specific for the neural cell adhesion molecule AMOG. J Neurosci Res. 1989 Feb;22(2):113–119. doi: 10.1002/jnr.490220202. [DOI] [PubMed] [Google Scholar]
  20. Pavlovic J., Zürcher T., Haller O., Staeheli P. Resistance to influenza virus and vesicular stomatitis virus conferred by expression of human MxA protein. J Virol. 1990 Jul;64(7):3370–3375. doi: 10.1128/jvi.64.7.3370-3375.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Roach A., Boylan K., Horvath S., Prusiner S. B., Hood L. E. Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice. Cell. 1983 Oct;34(3):799–806. doi: 10.1016/0092-8674(83)90536-6. [DOI] [PubMed] [Google Scholar]
  22. Robbins S. J., Rapp F. Inhibition of measles virus replication by cyclic AMP. Virology. 1980 Oct 30;106(2):317–326. doi: 10.1016/0042-6822(80)90255-x. [DOI] [PubMed] [Google Scholar]
  23. Schneider-Schaulies S., Liebert U. G., Baczko K., Cattaneo R., Billeter M., ter Meulen V. Restriction of measles virus gene expression in acute and subacute encephalitis of Lewis rats. Virology. 1989 Aug;171(2):525–534. doi: 10.1016/0042-6822(89)90622-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schneider-Schaulies S., Liebert U. G., Baczko K., ter Meulen V. Restricted expression of measles virus in primary rat astroglial cells. Virology. 1990 Aug;177(2):802–806. doi: 10.1016/0042-6822(90)90553-4. [DOI] [PubMed] [Google Scholar]
  25. Staeheli P. Interferon-induced proteins and the antiviral state. Adv Virus Res. 1990;38:147–200. doi: 10.1016/s0065-3527(08)60862-3. [DOI] [PubMed] [Google Scholar]
  26. Staeheli P., Pavlovic J. Inhibition of vesicular stomatitis virus mRNA synthesis by human MxA protein. J Virol. 1991 Aug;65(8):4498–4501. doi: 10.1128/jvi.65.8.4498-4501.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Thomis D. C., Doohan J. P., Samuel C. E. Mechanism of interferon action: cDNA structure, expression, and regulation of the interferon-induced, RNA-dependent P1/eIF-2 alpha protein kinase from human cells. Virology. 1992 May;188(1):33–46. doi: 10.1016/0042-6822(92)90732-5. [DOI] [PubMed] [Google Scholar]
  28. Turano A., Scura G., Caruso A., Bonfanti C., Luzzati R., Bassetti D., Manca N. Inhibitory effect of papaverine on HIV replication in vitro. AIDS Res Hum Retroviruses. 1989 Apr;5(2):183–192. doi: 10.1089/aid.1989.5.183. [DOI] [PubMed] [Google Scholar]
  29. Wikstrand C. J., Grahmann F. C., McComb R. D., Bigner D. D. Antigenic heterogeneity of human anaplastic gliomas and glioma-derived cell lines defined by monoclonal antibodies. J Neuropathol Exp Neurol. 1985 May;44(3):229–241. doi: 10.1097/00005072-198505000-00002. [DOI] [PubMed] [Google Scholar]
  30. Yoshikawa Y., Yamanouchi K. Effect of papaverine treatment on replication of measles virus in human neural and nonneural cells. J Virol. 1984 May;50(2):489–496. doi: 10.1128/jvi.50.2.489-496.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES