1887

Abstract

Antibodies to CD9, a member of the tetraspan transmembrane-protein family, selectively inhibit (CDV)-induced cell–cell fusion. Neither CDV-induced virus–cell fusion nor cell–cell fusion induced by the closely related morbillivirus (MV) is affected by anti-CD9 antibodies. As CDV does not bind CD9, an unknown, indirect mechanism is responsible for the observed inhibition of cell–cell fusion. It was investigated whether this effect was restricted to only one viral glycoprotein, either the haemagglutinin (H) or the fusion (F) protein, which form a fusion complex on the surface of virions and infected cells, or whether it is dependent on both in transient co-transfection assays. The susceptibility to CD9 antibodies segregates with the H protein of CDV. By exchanging portions of the H proteins of CDV and MV, it was determined that the complete extracellular domain, including the predicted stem structure (stem 1, barrel strand 1 and stem 2) and globular head domain, of the CDV-H protein mediates the effect. This suggests that interaction of the CDV-H protein with an unknown cellular receptor(s) is regulated by CD9, rather than F protein-mediated membrane fusion.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81629-0
2006-06-01
2020-01-27
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/6/1635.html?itemId=/content/journal/jgv/10.1099/vir.0.81629-0&mimeType=html&fmt=ahah

References

  1. Appel, M. J. G. & Gillespie, J. H. ( 1972; ). Canine distemper virus. Virol Monogr 11, 1–96.
    [Google Scholar]
  2. Cathomen, T., Naim, H. Y. & Cattaneo, R. ( 1998a; ). Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 72, 1224–1234.
    [Google Scholar]
  3. Cathomen, T., Mrkic, B., Spehner, D., Drillien, R., Naef, R., Pavlovic, J., Aguzzi, A., Billeter, M. A. & Cattaneo, R. ( 1998b; ). A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J 17, 3899–3908.[CrossRef]
    [Google Scholar]
  4. de Parseval, A., Lerner, D. L., Borrow, P., Willett, B. J. & Elder, J. H. ( 1997; ). Blocking of feline immunodeficiency virus infection by a monoclonal antibody to CD9 is via inhibition of virus release rather than interference with receptor binding. J Virol 71, 5742–5749.
    [Google Scholar]
  5. Hemler, M. E. ( 2003; ). Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 19, 397–422.[CrossRef]
    [Google Scholar]
  6. Hu, A., Cattaneo, R., Schwartz, S. & Norrby, E. ( 1994; ). Role of N-linked oligosaccharide chains in the processing and antigenicity of measles virus haemagglutinin protein. J Gen Virol 75, 1043–1052.[CrossRef]
    [Google Scholar]
  7. Imai, T., Fukudome, K., Takagi, S., Nagira, M., Furuse, M., Fukuhara, N., Nishimura, M., Himuma, Y. & Yoshie, O. ( 1992; ). C33 antigen recognized by monoclonal antibodies inhibitory to human T cell leukemia virus type 1-induced syncytium formation is a member of a new family of transmembrane proteins including CD9, CD37, CD53, and CD63. J Immunol 149, 2879–2886.
    [Google Scholar]
  8. Iwatsuki, K., Tokiyoshi, S., Hirayama, N., Nakamura, K., Ohashi, K., Wakasa, C., Mikami, T. & Kai, C. ( 2000; ). Antigenic differences in the H proteins of canine distemper viruses. Vet Microbiol 71, 281–286.[CrossRef]
    [Google Scholar]
  9. Kaji, K., Oda, S., Shikano, T., Ohnuki, T., Uematsu, Y., Sakagami, J., Tada, N., Miyazaki, S. & Kudo, A. ( 2000; ). The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 24, 279–282.[CrossRef]
    [Google Scholar]
  10. Langedijk, J. P. M., Daus, F. J. & van Oirschot, J. T. ( 1997; ). Sequence and structure alignment of Paramyxoviridae attachment proteins and discovery of enzymatic activity for a morbillivirus hemagglutinin. J Virol 71, 6155–6167.
    [Google Scholar]
  11. Le Naour, F., Rubinstein, E., Jasmin, C., Prenant, M. & Boucheix, C. ( 2000; ). Severely reduced female fertility in CD9-deficient mice. Science 287, 319–321.[CrossRef]
    [Google Scholar]
  12. Liebert, U. G., Flanagan, S. G., Löffler, S., Baczko, K., ter Meulen, V. & Rima, B. K. ( 1994; ). Antigenic determinants of measles virus hemagglutinin associated with neurovirulence. J Virol 68, 1486–1493.
    [Google Scholar]
  13. Löffler, S., Lottspeich, F., Lanza, F., Azorsa, D. O., ter Meulen, V. & Schneider-Schaulies, J. ( 1997; ). CD9, a tetraspan transmembrane protein, renders cells susceptible to canine distemper virus. J Virol 71, 42–49.
    [Google Scholar]
  14. Massé, N., Ainouze, M., Néel, B., Wild, T. F., Buckland, R. & Langedijk, J. P. M. ( 2004; ). Measles virus (MV) hemagglutinin: evidence that attachment sites for MV receptors SLAM and CD46 overlap on the globular head. J Virol 78, 9051–9063.[CrossRef]
    [Google Scholar]
  15. McQuaid, S. & Cosby, S. L. ( 2002; ). An immunohistochemical study of the distribution of the measles virus receptors, CD46 and SLAM, in normal human tissues and subacute sclerosing panencephalitis. Lab Invest 82, 403–409.[CrossRef]
    [Google Scholar]
  16. Miyado, K., Yamada, G., Yamada, S. & 9 other authors ( 2000; ). Requirement of CD9 on the egg plasma membrane for fertilization. Science 287, 321–324.[CrossRef]
    [Google Scholar]
  17. Moeller, K., Duffy, I., Duprex, P. & 7 other authors ( 2001; ). Recombinant measles viruses expressing altered hemagglutinin (H) genes: functional separation of mutations determining H antibody escape from neurovirulence. J Virol 75, 7612–7620.[CrossRef]
    [Google Scholar]
  18. Moll, M., Klenk, H.-D., Herrler, G. & Maisner, A. ( 2001; ). A single amino acid change in the cytoplasmic domains of measles virus glycoproteins H and F alters targeting, endocytosis, and cell fusion in polarized Madin-Darby canine kidney cells. J Biol Chem 276, 17887–17894.[CrossRef]
    [Google Scholar]
  19. Plemper, R. K., Hammond, A. L. & Cattaneo, R. ( 2000; ). Characterization of a region of the measles virus hemagglutinin sufficient for its dimerization. J Virol 74, 6485–6493.[CrossRef]
    [Google Scholar]
  20. Schmid, E., Zurbriggen, A., Gassen, U., Rima, B., ter Meulen, V. & Schneider-Schaulies, J. ( 2000; ). Antibodies to CD9, a tetraspan transmembrane protein, inhibit canine distemper virus-induced cell-cell fusion but not virus-cell fusion. J Virol 74, 7554–7561.[CrossRef]
    [Google Scholar]
  21. Schneider-Schaulies, J., Schnorr, J.-J., Brinckmann, U., Dunster, L. M., Baczko, K., Liebert, U. G., Schneider-Schaulies, S. & ter Meulen, V. ( 1995; ). Receptor usage and differential downregulation of CD46 by measles virus wild-type and vaccine strains. Proc Natl Acad Sci U S A 92, 3943–3947.[CrossRef]
    [Google Scholar]
  22. Seki, F., Ono, N., Yamaguchi, R. & Yanagi, Y. ( 2003; ). Efficient isolation of wild strains of canine distemper virus in Vero cells expressing canine SLAM (CD150) and their adaptibility to marmoset B95a cells. J Virol 77, 9943–9950.[CrossRef]
    [Google Scholar]
  23. Summers, B. A. & Appel, M. J. G. ( 1994; ). Aspects of canine distemper virus and measles virus encephalomyelitis. Neuropathol Appl Neurobiol 20, 525–534.[CrossRef]
    [Google Scholar]
  24. Tachibana, I. & Hemler, M. E. ( 1999; ). Role of transmembrane 4 superfamily (TM4SF) proteins CD9 and CD81 in muscle cell fusion and myotube maintenance. J Cell Biol 146, 893–904.[CrossRef]
    [Google Scholar]
  25. Tanio, Y., Yamazaki, H., Kunisada, T., Miyake, K. & Hayashi, S.-I. ( 1999; ). CD9 molecule expressed on stromal cells is involved in osteoclastogenesis. Exp Hematol 27, 853–859.[CrossRef]
    [Google Scholar]
  26. Tatsuo, H. & Yanagi, Y. ( 2002; ). The morbillivirus receptor SLAM (CD150). Microbiol Immunol 46, 135–142.[CrossRef]
    [Google Scholar]
  27. Tatsuo, H., Ono, N. & Yanagi, Y. ( 2001; ). Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J Virol 75, 5842–5850.[CrossRef]
    [Google Scholar]
  28. Vandevelde, M. & Zurbriggen, A. ( 1995; ). The neurobiology of canine distemper virus infection. Vet Microbiol 44, 271–280.[CrossRef]
    [Google Scholar]
  29. von Messling, V., Zimmer, G., Herrler, G., Haas, L. & Cattaneo, R. ( 2001; ). The hemagglutinin of canine distemper virus determines tropism and cytopathogenicity. J Virol 75, 6418–6427.[CrossRef]
    [Google Scholar]
  30. von Messling, V., Springfeld, C., Devaux, P. & Cattaneo, R. ( 2003; ). A ferret model of canine distemper virus virulence and immunosuppression. J Virol 77, 12579–12591.[CrossRef]
    [Google Scholar]
  31. von Messling, V., Milosevic, D. & Cattaneo, R. ( 2004; ). Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc Natl Acad Sci U S A 101, 14216–14221.[CrossRef]
    [Google Scholar]
  32. Wild, T. F., Malvoisin, E. & Buckland, R. ( 1991; ). Measles virus: both the haemagglutinin and fusion glycoproteins are required for fusion. J Gen Virol 72, 439–442.[CrossRef]
    [Google Scholar]
  33. Willett, B. J., Hosie, M. J., Jarrett, O. & Neil, J. C. ( 1994; ). Identification of a putative cellular receptor for feline immunodeficiency virus as the feline homologue of CD9. Immunology 81, 228–233.
    [Google Scholar]
  34. Willett, B., Hosie, M., Shaw, A. & Neil, J. ( 1997; ). Inhibition of feline immunodeficiency virus infection by CD9 antibody operates after virus entry and is independent of virus tropism. J Gen Virol 78, 611–618.
    [Google Scholar]
  35. Zurbriggen, A., Graber, H. U., Wagner, A. & Vandevelde, M. ( 1995; ). Canine distemper virus persistence in the nervous system is associated with noncytolytic selective virus spread. J Virol 69, 1678–1686.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81629-0
Loading
/content/journal/jgv/10.1099/vir.0.81629-0
Loading

Data & Media loading...

Most cited articles

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