Some paramyxoviruses form long filamentous virus particles: however, the determinants of filament formation and the role of such particles in virus transmission and pathogenicity are not clearly defined. By using conventional immunofluorescence microscopy, we found that human parainfluenza virus type 2 (HPIV2) forms filamentous particles ranging from 5 to 15 μm in length in virus-infected, polarized epithelial cells. The formation of filamentous particles was found to be virus type-specific and was not observed when the same cell types were infected with parainfluenza virus type 3 or Sendai virus, suggesting that different paramyxovirus genera exhibit distinct morphological properties. HPIV2 filamentous particle formation was found to be inhibited by cytochalasin D (CD) or jasplakinolide treatment in a dose-dependent manner. In the presence of 4 μg/ml CD or 1 μM jasplakinolide, the formation of filamentous particles was completely abolished, although similar haemagglutination and p.f.u. titres of virus were found to be released into the culture medium at 24 h post-infection. These observations indicate that host cell components, including the actin microfilament network, are important determinants of the morphology of parainfluenza viruses. The predominance of filamentous particles in polarized epithelial cells may reflect specific pathogenic roles of these particles in infection of human epithelial tissues.


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  1. Ada, G. L., Perry, B. T. & Abbot, A. (1958). Biological and physical properties of the Ryan strain of filamentous influenza virus.Journal of General Microbiology 19, 23-39.[CrossRef] [Google Scholar]
  2. Armstrong, J. A., Pereira, H. G. & Valentine, R. C. (1962). Morphology and development of respiratory syncytial virus in cell cultures.Nature 196, 1179-1181.[CrossRef] [Google Scholar]
  3. Bächi, T. & Howe, C. (1973). Morphogenesis and ultrastructure of respiratory syncytial virus.Journal of Virology 12, 1173-1180. [Google Scholar]
  4. Bass, D. M., Baylor, M., Chen, C. & Upadhyayula, U. (1995). Dansylcadaverine and cytochalasin D enhance rotavirus infection of murine L cells.Virology 212, 429-437.[CrossRef] [Google Scholar]
  5. Bedows, E., Rao, K. M. K. & Welsh, M. J. (1983). Fate of microfilaments in Vero cells infected with measles virus and herpes simplex virus type 1.Molecular and Cellular Biology 3, 712-719. [Google Scholar]
  6. Berthiaume, L., Joncas, J. & Pavilanis, V. (1974). Comparative structure, morphogenesis and biological characteristics of the respiratory syncytial (RS) virus and the pneumonia virus of mice (PVM).Archiv für die gesamte Virusforschung 45, 39-51.[CrossRef] [Google Scholar]
  7. Bohn, W., Rutter, G., Hohenberg, H., Mannweiler, K. & Nobis, P. (1986). Involvement of actin filaments in budding of measles virus: studies on cytoskeletons of infected cells.Virology 149, 91-106.[CrossRef] [Google Scholar]
  8. Bubb, M. R., Senderowicz, A. M. J., Sausville, E. A., Duncan, K. L. K. & Korn, E. D. (1994). Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin.Journal of Biological Chemistry 269, 14869-14871. [Google Scholar]
  9. Choppin, P. W. (1963). Multiplication of two kinds of influenza A virus particles in monkey kidney cells.Virology 21, 242-252.[CrossRef] [Google Scholar]
  10. Choppin, P. W. & Compans, R. W. (1975). Reproduction of paramyxoviruses In Comprehensive Virology, pp. 95-178. Edited by H. Fraenkel-Conrat & R. R. Wagner. New York: Plenum Press.
  11. Compans, R. W., Holmes, K. V., Dales, S. & Choppin, P. W. (1966). An electron microscopic study of moderate and virulent virus–cell interactions of the parainfluenza virus SV5.Virology 30, 411-426.[CrossRef] [Google Scholar]
  12. Compans, R. W., Harter, D. H. & Choppin, P. W. (1967). Studies on pneumonia virus of mice (PVM) in cell culture. II. Structure and morphogenesis of the virus particle.Journal of Experimental Medicine 126, 267-276.[CrossRef] [Google Scholar]
  13. Cudmore, S., Cossart, P., Griffiths, G. & Way, M. (1995). Actin-based motility of vaccinia virus.Nature 378, 636-638.[CrossRef] [Google Scholar]
  14. Cudmore, S., Reckmann, I. & Way, M. (1997). Viral manipulations of the actin cytoskeleton.Trends in Microbiology 5, 142-148.[CrossRef] [Google Scholar]
  15. Damsky, C. H., Sheffield, J. B., Tuszynski, G. P. & Warren, L. (1977). Is there a role for actin in virus budding?Journal of Cell Biology 75, 593-605.[CrossRef] [Google Scholar]
  16. Enami, M. & Enami, K. (1996). Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein.Journal of Virology 70, 6653-6657. [Google Scholar]
  17. Genty, N. & Bussereau, F. (1980). Is cytoskeleton involved in vesicular stomatitis virus reproduction?Journal of Virology 34, 777-781. [Google Scholar]
  18. Giuffre, R. M., Tovell, D. R., Kay, C. M. & Tyrrell, D. L. S. (1982). Evidence for an interaction between the membrane protein of a paramyxovirus and actin.Journal of Virology 42, 963-968. [Google Scholar]
  19. Griffin, J. A. & Compans, R. W. (1979). Effect of cytochalasin B on the maturation of enveloped viruses.Journal of Experimental Medicine 150, 379-391.[CrossRef] [Google Scholar]
  20. Griffin, J. A., Basak, S. & Compans, R. W. (1983). Effects of hexose starvation and the role of sialic acid in influenza virus release.Virology 125, 324-334.[CrossRef] [Google Scholar]
  21. Howe, C., Morgan, C., Vaux St Cyr, C. de, Hsu, K. C. & Rose, H. M. (1967). Morphogenesis of type 2 parainfluenza virus examined by light and electron microscopy.Journal of Virology 1, 215-237. [Google Scholar]
  22. Hughey, P. G., Roberts, P. C., Holsinger, L. J., Zebedee, S. L., Lamb, R. A. & Compans, R. W. (1995). Effects of antibody to the influenza A virus M2 protein on M2 surface expression and virus assembly.Virology 212, 411-421.[CrossRef] [Google Scholar]
  23. Jin, H., Leser, G. P., Zhang, J. & Lamb, R. A. (1997). Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape.EMBO Journal 16, 1236-1247.[CrossRef] [Google Scholar]
  24. Kilbourne, E. D. (1963). Influenza virus genetics.Progress in Medical Virology 5, 79-126. [Google Scholar]
  25. Lamb, R. A. & Kolakofsky, D. (1996).Paramyxoviridae: the viruses and their replication. In Fields Virology, pp. 1177-1204. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott–Raven.
  26. Lee, E., Shelden, E. A. & Knecht, D. A. (1998). Formation of F-actin aggregates in cells treated with actin stabilizing drugs.Cell Motility and the Cytoskeleton 39, 122-133.[CrossRef] [Google Scholar]
  27. Mitnaul, L. J., Castrucci, M. R., Murti, K. G. & Kawaoka, Y. (1996). The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication.Journal of Virology 70, 873-879. [Google Scholar]
  28. Miyata, H., Kishikawa, M., Kondo, H., Kai, C., Watanabe, Y., Ohsawa, K. & Sato, H. (1995). New isolates of pneumonia virus of mice (PVM) from Japanese rat colonies and their characterization.Experimental Animals 44, 95-104.[CrossRef] [Google Scholar]
  29. Morrison, T. G. & McGinnes, L. J. (1985). Cytochalasin D accelerates the release of Newcastle disease virus from infected cells.Virus Research 4, 93-106.[CrossRef] [Google Scholar]
  30. Mousa, G. Y., Trevithick, J. R., Bechberger, J. & Blair, D. G. (1978). Cytochalasin D induces the capping of both leukaemia viral proteins and actin in infected cells.Nature 274, 808-809.[CrossRef] [Google Scholar]
  31. Naito, S. & Matsumoto, S. (1978). Identification of cellular actin within the rabies virus.Virology 91, 151-163.[CrossRef] [Google Scholar]
  32. Nishimura, H., Hara, M., Sugawara, K., Kitame, F., Takiguchi, K., Umetsu, Y., Tonosaki, A. & Nakamura, K. (1990). Characterization of the cord-like structures emerging from the surface of influenza C virus-infected cells.Virology 179, 179-188.[CrossRef] [Google Scholar]
  33. Örvell, C. (1978). Structural polypeptides of mumps virus.Journal of General Virology 41, 527-539.[CrossRef] [Google Scholar]
  34. Payne, L. G. & Kristensson, K. (1982). The effect of cytochalasin D and monensin on enveloped vaccinia virus release.Archives of Virology 74, 11-20.[CrossRef] [Google Scholar]
  35. Pearce-Pratt, R., Malamud, D. & Phillips, D. M. (1994). Role of the cytoskeleton in cell-to-cell transmission of human immunodeficiency virus.Journal of Virology 68, 2898-2905. [Google Scholar]
  36. Ravkov, E. V., Nichol, S. T., Peters, C. J. & Compans, R. W. (1998). Role of actin microfilaments in Black Creek Canal virus morphogenesis.Journal of Virology 72, 2865-2870. [Google Scholar]
  37. Roberts, P. C. & Compans, R. W. (1998). Host cell dependence of viral morphology.Proceedings of the National Academy of Sciences, USA 95, 5746-5751.[CrossRef] [Google Scholar]
  38. Roberts, S. R., Compans, R. W. & Wertz, G. W. (1995). Respiratory syncytial virus matures at the apical surfaces of polarized epithelial cells.Journal of Virology 69, 2667-2673. [Google Scholar]
  39. Roberts, P. C., Lamb, R. A. & Compans, R. W. (1998). The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation.Virology 240, 127-137.[CrossRef] [Google Scholar]
  40. Sawitzky, H., Liebe, S., Willingale-Theune, J. & Menzel, D. (1999). The anti-proliferative agent jasplakinolide rearranges the actin cytoskeleton of plant cells.European Journal of Cell Biology 78, 424-433.[CrossRef] [Google Scholar]
  41. Senderowicz, A. M., Kaur, G., Sainz, E., Laing, C., Inman, W. D., Rodriguez, J., Crews, P., Malspeis, L., Grever, M. R., Sausville, E. A. & Duncan, K. L. K. (1995). Jasplakinolide’s inhibition of the growth of prostate carcinoma cells in vitro with disruption of the actin cytoskeleton.Journal of the National Cancer Institute 87, 46-51.[CrossRef] [Google Scholar]
  42. Smirnov, Yu. A., Kuznetsova, M. A. & Kaverin, N. V. (1991). The genetic aspects of influenza virus filamentous particle formation.Archives of Virology 118, 279-284.[CrossRef] [Google Scholar]
  43. Stallcup, K. C., Raine, C. S. & Fields, B. N. (1983). Cytochalasin B inhibits the maturation of measles virus.Virology 124, 59-74.[CrossRef] [Google Scholar]
  44. Sundqvist, K.-G. & Ehrnst, A. (1976). Cytoskeletal control of surface membrane mobility.Nature 264, 226-231.[CrossRef] [Google Scholar]
  45. Tyrrell, D. L. & Ehrnst, A. (1979). Transmembrane communication in cells chronically infected with measles virus.Journal of Cell Biology 81, 396-402.[CrossRef] [Google Scholar]
  46. Tyrrell, D. L. J. & Norrby, E. (1978). Structural polypeptides of measles virus.Journal of General Virology 39, 219-229.[CrossRef] [Google Scholar]
  47. Vainionpaa, R. & Hyypia, T. (1994). Biology of parainfluenza viruses.Clinical Microbiology Reviews 7, 265-275. [Google Scholar]
  48. Wang, E., Wolf, B. A., Lamb, R. A., Choppin, P. W. & Goldberg, A. R. (1976). The presence of actin in enveloped viruses. In Cell Motility, pp. 589–599. Edited by R. Goldman, T. Pollard & F. Rosenbaum. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.

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