1887

Abstract

A recombinant measles virus (MV) expressing red fluorescent protein (MVDsRed1) was used to produce a persistently infected cell line (piNT2-MVDsRed1) from human neural precursor (NT2) cells. A similar cell line (piNT2-MVeGFP) was generated using a virus that expresses enhanced green fluorescent protein. Intracytoplasmic inclusions containing the viral nucleocapsid protein were evident in all cells and viral glycoproteins were present at the cell surface. Nevertheless, the cells did not release infectious virus nor did they fuse to generate syncytia. Uninfected NT2 cells express the MV receptor CD46 uniformly over their surface, whereas CD46 was present in cell surface aggregates in the piNT2 cells. There was no decrease in the overall amount of CD46 in piNT2 compared to NT2 cells. Cell-to-cell fusion was observed when piNT2 cells were overlaid onto confluent monolayers of MV receptor-positive cells, indicating that the viral glycoproteins were correctly folded and processed. Infectious virus was released from the underlying cells, indicating that persistence was not due to gross mutations in the virus genome. Persistently infected cells were superinfected with MV or canine distemper virus and cytopathic effects were not observed. However, mumps virus could readily infect the cells, indicating that superinfection immunity is not caused by general soluble antiviral factors. As MVeGFP and MVDsRed1 are antigenically indistinguishable but phenotypically distinct it was possible to use them to measure the degree of superinfection immunity in the absence of any cytopathic effect. Only small numbers of non-fusing green fluorescent piNT2-MVDsRed1 cells (1 : 300 000) were identified in which superinfecting MVeGFP entered, replicated and expressed its genes.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81052-0
2005-08-01
2019-11-12
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/8/vir862291.html?itemId=/content/journal/jgv/10.1099/vir.0.81052-0&mimeType=html&fmt=ahah

References

  1. Allen, I. V., McQuaid, S., McMahon, J., Kirk, J. & McConnell, R. ( 1996; ). The significance of measles virus antigen and genome distribution in the CNS in SSPE for mechanisms of viral spread and demyelination. J Neuropathol Exp Neurol 55, 471–480.[CrossRef]
    [Google Scholar]
  2. Altfeld, M., Allen, T. M., Yu, X. G. & 13 other authors ( 2002; ). HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature 420, 434–439.[CrossRef]
    [Google Scholar]
  3. Baczko, K., Lampe, J., Liebert, U. G. & 7 other authors ( 1993; ). Clonal expansion of hypermutated measles virus in a SSPE brain. Virology 197, 188–195.[CrossRef]
    [Google Scholar]
  4. Baird, G. S., Zacharias, D. A. & Tsien, R. Y. ( 2000; ). Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc Natl Acad Sci U S A 97, 11984–11989.[CrossRef]
    [Google Scholar]
  5. Basle, M. F., Fournier, J. G., Rozenblatt, S., Rebel, A. & Bouteille, M. ( 1986; ). Measles virus RNA detected in Paget's disease bone tissue by in situ hybridization. J Gen Virol 67, 907–913.[CrossRef]
    [Google Scholar]
  6. Bock, M., Heinkelein, M., Lindemann, D. & Rethwilm, A. ( 1998; ). Cells expressing the human foamy virus (HFV) accessory Bet protein are resistant to productive HFV superinfection. Virology 250, 194–204.[CrossRef]
    [Google Scholar]
  7. Bour, S., Boulerice, F. & Wainberg, M. A. ( 1991; ). Inhibition of gp160 and CD4 maturation in U937 cells after both defective and productive infections by human immunodeficiency virus type 1. J Virol 65, 6387–6396.
    [Google Scholar]
  8. Breiner, K. M., Urban, S., Glass, B. & Schaller, H. ( 2001; ). Envelope protein-mediated down-regulation of hepatitis B virus receptor in infected hepatocytes. J Virol 75, 143–150.[CrossRef]
    [Google Scholar]
  9. Burnstein, T., Jacobsen, L. B., Zeman, W. & Chen, T. T. ( 1974; ). Persistent infection of BSC-1 cells by defective measles virus derived from subacute sclerosing panencephalitis. Infect Immun 10, 1378–1382.
    [Google Scholar]
  10. Calain, P. & Roux, L. ( 1993; ). The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol 67, 4822–4830.
    [Google Scholar]
  11. Cathomen, T., Naim, H. Y. & Cattaneo, R. ( 1998; ). Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 72, 1224–1234.
    [Google Scholar]
  12. Cattaneo, R. & Billeter, M. A. ( 1992; ). Mutations and A/I hypermutations in measles virus persistent infections. Curr Top Microbiol Immunol 176, 63–74.
    [Google Scholar]
  13. Cattaneo, R., Rebmann, G., Baczko, K., ter Meulen, V. & Billeter, M. A. ( 1987; ). Altered ratios of measles virus transcripts in diseased human brains. Virology 160, 523–526.[CrossRef]
    [Google Scholar]
  14. Cattaneo, R., Schmid, A., Eschle, D., Baczko, K., ter Meulen, V. & Billeter, M. A. ( 1988; ). Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55, 255–265.[CrossRef]
    [Google Scholar]
  15. Collins, A. R. & Flanagan, T. D. ( 1977; ). Interferon production and response to exogenous interferon in two cell lines of mouse brain origin persistently infected with Sendai virus. Arch Virol 53, 313–321.[CrossRef]
    [Google Scholar]
  16. Cosby, S. L., Lyons, C., Fitzgerald, S. P., Martin, S. J., Pressdee, S. & Allen, I. V. ( 1981; ). The isolation of large and small plaque canine distemper viruses which differ in their neurovirulence for hamsters. J Gen Virol 52, 345–353.[CrossRef]
    [Google Scholar]
  17. Crimeen-Irwin, B., Ellis, S., Christiansen, D., Ludford-Menting, M. J., Milland, J., Lanteri, M., Loveland, B. E., Gerlier, D. & Russell, S. M. ( 2003; ). Ligand binding determines whether CD46 is internalized by clathrin-coated pits or macropinocytosis. J Biol Chem 278, 46927–46937.[CrossRef]
    [Google Scholar]
  18. de la Torre, J. C., Davila, M., Sobrino, F., Ortin, J. & Domingo, E. ( 1985; ). Establishment of cell lines persistently infected with foot-and-mouth disease virus. Virology 145, 24–35.[CrossRef]
    [Google Scholar]
  19. Duprex, W. P., Duffy, I., McQuaid, S., Hamill, L., Cosby, S. L., Billeter, M. A., Schneider-Schaulies, J., ter Meulen, V. & Rima, B. K. ( 1999a; ). The H gene of rodent brain-adapted measles virus confers neurovirulence to the Edmonston vaccine strain. J Virol 73, 6916–6922.
    [Google Scholar]
  20. Duprex, W. P., McQuaid, S., Hangartner, L., Billeter, M. A. & Rima, B. K. ( 1999b; ). Observation of measles virus cell-to-cell spread in astrocytoma cells by using a green fluorescent protein-expressing recombinant virus. J Virol 73, 9568–9575.
    [Google Scholar]
  21. Elliott, G. & O'Hare, P. ( 1999; ). Intercellular trafficking of VP22-GFP fusion proteins. Gene Ther 6, 149–151.[CrossRef]
    [Google Scholar]
  22. Esiri, M. M., Oppenheimer, D. R., Brownell, B. & Haire, M. ( 1982; ). Distribution of measles antigen and immunoglobulin-containing cells in the CNS in subacute sclerosing panencephalitis (SSPE) and atypical measles encephalitis. J Neurol Sci 53, 29–43.[CrossRef]
    [Google Scholar]
  23. Fernandez-Muñoz, R. & Celma, M. L. ( 1992; ). Measles virus from a long-term persistently infected human T lymphoblastoid cell line, in contrast to the cytocidal parental virus, establishes an immediate persistence in the original cell line. J Gen Virol 73, 2195–2202.[CrossRef]
    [Google Scholar]
  24. Firsching, R., Buchholz, C. J., Schneider, U., Cattaneo, R., ter Meulen, V. & Schneider-Schaulies, J. ( 1999; ). Measles virus spread by cell–cell contacts: uncoupling of contact-mediated receptor (CD46) downregulation from virus uptake. J Virol 73, 5265–5273.
    [Google Scholar]
  25. Furuta, T., Tomioka, R., Taki, K., Nakamura, K., Tamamaki, N. & Kaneko, T. ( 2001; ). In vivo transduction of central neurons using recombinant Sindbis virus: Golgi-like labeling of dendrites and axons with membrane-targeted fluorescent proteins. J Histochem Cytochem 49, 1497–1508.[CrossRef]
    [Google Scholar]
  26. Garcia, J. V. & Miller, A. D. ( 1991; ). Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 350, 508–511.[CrossRef]
    [Google Scholar]
  27. Hangartner, H. ( 1997; ). Development of Measles virus as a vector. MSc thesis, University of Zürich, Switzerland.
  28. Hirano, A., Yant, S., Iwata, K., Korte-Sarfaty, J., Seya, T., Nagasawa, S. & Wong, T. C. ( 1996; ). Human cell receptor CD46 is down regulated through recognition of a membrane-proximal region of the cytoplasmic domain in persistent measles virus infection. J Virol 70, 6929–6936.
    [Google Scholar]
  29. Ho, C. K. & Babiuk, L. A. ( 1979; ). Mechanisms of heterotypic immunity against canine distemper. Experientia 35, 1179–1180.[CrossRef]
    [Google Scholar]
  30. Horga, M. A., Gusella, G. L., Greengard, O., Poltoratskaia, N., Porotto, M. & Moscona, A. ( 2000; ). Mechanism of interference mediated by human parainfluenza virus type 3 infection. J Virol 74, 11792–11799.[CrossRef]
    [Google Scholar]
  31. Huang, W. Y., Aramburu, J., Douglas, P. S. & Izumo, S. ( 2000; ). Transgenic expression of green fluorescence protein can cause dilated cardiomyopathy. Nat Med 6, 482–483.[CrossRef]
    [Google Scholar]
  32. Husain, M. & Moss, B. ( 2001; ). Vaccinia virus F13L protein with a conserved phospholipase catalytic motif induces colocalization of the B5R envelope glycoprotein in post-Golgi vesicles. J Virol 75, 7528–7542.[CrossRef]
    [Google Scholar]
  33. Jakobs, S., Subramaniam, V., Schonle, A., Jovin, T. M. & Hell, S. W. ( 2000; ). EFGP and DsRed expressing cultures of Escherichia coli imaged by confocal, two-photon and fluorescence lifetime microscopy. FEBS Lett 479, 131–135.[CrossRef]
    [Google Scholar]
  34. Jobbagy, Z., Garfield, S., Baptiste, L., Eiden, M. V. & Anderson, W. B. ( 2000; ). Subcellular redistribution of Pit-2 P(i) transporter/amphotropic leukaemia virus (A-MuLV) receptor in A-MuLV-infected NIH 3T3 fibroblasts: involvement in superinfection interference. J Virol 74, 2847–2854.[CrossRef]
    [Google Scholar]
  35. Joseph, B. S., Lampert, P. W. & Oldstone, M. B. ( 1975; ). Replication and persistence of measles virus in defined subpopulations of human leukocytes. J Virol 16, 1638–1649.
    [Google Scholar]
  36. Levine, B. & Griffin, D. E. ( 1993; ). Molecular analysis of neurovirulent strains of Sindbis virus that evolve during persistent infection of SCID mice. J Virol 67, 6872–6875.
    [Google Scholar]
  37. Liu, H. S., Jan, M. S., Chou, C. K., Chen, P. H. & Ke, N. J. ( 1999; ). Is green fluorescent protein toxic to the living cells? Biochem Biophys Res Commun 260, 712–717.[CrossRef]
    [Google Scholar]
  38. Locher, C. P., Blackbourn, D. J., Barnett, S. W. & 8 other authors ( 1997; ). Superinfection with human immunodeficiency virus type 2 can reactivate virus production in baboons but is contained by a CD8 T cell antiviral response. J Infect Dis 176, 948–959.[CrossRef]
    [Google Scholar]
  39. Mahlknecht, U., Deng, C., Lu, M. C., Greenough, T. C., Sullivan, J. L., O'Brien, W. A. & Herbein, G. ( 2000; ). Resistance to apoptosis in HIV-infected CD4+ T lymphocytes is mediated by macrophages: role for Nef and immune activation in viral persistence. J Immunol 165, 6437–6446.[CrossRef]
    [Google Scholar]
  40. Maisner, A., Zimmer, G., Liszewski, M. K., Lublin, D. M., Atkinson, J. P. & Herrler, G. ( 1997; ). Membrane cofactor protein (CD46) is a basolateral protein that is not endocytosed. Importance of the tetrapeptide FTSL at the carboxyl terminus. J Biol Chem 272, 20793–20799.[CrossRef]
    [Google Scholar]
  41. Matz, M. V., Fradkov, A. F., Labas, Y. A., Savitsky, A. P., Zaraisky, A. G., Markelov, M. L. & Lukyanov, S. A. ( 1999; ). Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 17, 969–973.[CrossRef]
    [Google Scholar]
  42. McQuaid, S., Campbell, S., Wallace, I. J., Kirk, J. & Cosby, S. L. ( 1998; ). Measles virus infection and replication in undifferentiated and differentiated human neuronal cells in culture. J Virol 72, 5245–5250.
    [Google Scholar]
  43. Menna, J. H., Collins, A. R. & Flanagan, T. D. ( 1975; ). Characterization of an in vitro persistent-state measles virus infection: establishment and virological characterization of the BGM/MV cell line. Infect Immun 11, 152–158.
    [Google Scholar]
  44. Mills, B. G., Frausto, A., Singer, F. R., Ohsaki, Y., Demulder, A. & Roodman, G. D. ( 1994; ). Multinucleated cells formed in vitro from Paget's bone marrow express viral antigens. Bone 15, 443–448.[CrossRef]
    [Google Scholar]
  45. Mizuno, H., Sawano, A., Eli, P., Hama, H. & Miyawaki, A. ( 2001; ). Red fluorescent protein from Discosoma as a fusion tag and a partner for fluorescence resonance energy transfer. Biochemistry 40, 2502–2510.[CrossRef]
    [Google Scholar]
  46. Modlin, J. F., Jabbour, J. T., Witte, J. J. & Halsey, N. A. ( 1977; ). Epidemiologic studies of measles, measles vaccine, and subacute sclerosing panencephalitis. Pediatrics 59, 505–512.
    [Google Scholar]
  47. 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]
  48. Morrison, T. G. & McGinnes, L. W. ( 1989; ). Avian cells expressing the Newcastle disease virus hemagglutinin-neuraminidase protein are resistant to Newcastle disease virus infection. Virology 171, 10–17.[CrossRef]
    [Google Scholar]
  49. Moss, J. B., Price, A. L., Raz, E., Driever, W. & Rosenthal, N. ( 1996; ). Green fluorescent protein marks skeletal muscle in murine cell lines and zebrafish. Gene 173, 89–98.[CrossRef]
    [Google Scholar]
  50. Naniche, D., Varior-Krishnan, G., Cervoni, F., Wild, T. F., Rossi, B., Rabourdin-Combe, C. & Gerlier, D. ( 1993a; ). Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67, 6025–6032.
    [Google Scholar]
  51. Naniche, D., Wild, T. F., Rabourdin-Combe, C. & Gerlier, D. ( 1993b; ). Measles virus haemagglutinin induces down-regulation of gp57/67, a molecule involved in virus binding. J Gen Virol 74, 1073–1079.[CrossRef]
    [Google Scholar]
  52. Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M. & Kobayashi, H. ( 1999; ). Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. Plant J 18, 455–463.[CrossRef]
    [Google Scholar]
  53. Oomens, A. G. & Wertz, G. W. ( 2004; ). The baculovirus GP64 protein mediates highly stable infectivity of a human respiratory syncytial virus lacking its homologous transmembrane glycoproteins. J Virol 78, 124–135.[CrossRef]
    [Google Scholar]
  54. Pavio, N., Couderc, T., Girard, S., Sgro, J. Y., Blondel, B. & Colbere-Garapin, F. ( 2000; ). Expression of mutated poliovirus receptors in human neuroblastoma cells persistently infected with poliovirus. Virology 274, 331–342.[CrossRef]
    [Google Scholar]
  55. Pleasure, S. J. & Lee, V. M. ( 1993; ). NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J Neurosci Res 35, 585–602.[CrossRef]
    [Google Scholar]
  56. Radecke, F., Spielhofer, P., Schneider, H., Kaelin, K., Huber, M., Dotsch, C., Christiansen, G. & Billeter, M. A. ( 1995; ). Rescue of measles viruses from cloned DNA. EMBO J 14, 5773–5784.
    [Google Scholar]
  57. Rager-Zisman, B., Egan, J. E., Kress, Y. & Bloom, B. R. ( 1984; ). Isolation of cold-sensitive mutants of measles virus from persistently infected murine neuroblastoma cells. J Virol 51, 845–855.
    [Google Scholar]
  58. Reddy, S. V., Menaa, C., Singer, F. R., Cundy, T., Cornish, J., Whyte, M. P. & Roodman, G. D. ( 1999; ). Measles virus nucleocapsid transcript expression is not restricted to the osteoclast lineage in patients with Paget's disease of bone. Exp Hematol 27, 1528–1532.[CrossRef]
    [Google Scholar]
  59. Reed, L. & Muench, H. ( 1938; ). A simple method for estimating fifty percent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  60. Rima, B. K. ( 1999; ). Paramyxoviruses and chronic human diseases. Bone 5, S23–S26.
    [Google Scholar]
  61. Rima, B. K., Davidson, W. B. & Martin, S. J. ( 1977; ). The role of defective interfering particles in persistent infection of Vero cells by measles virus. J Gen Virol 35, 89–97.[CrossRef]
    [Google Scholar]
  62. Rima, B. K., Earle, J. A., Baczko, K. & 7 other authors ( 1997; ). Sequence divergence of measles virus haemagglutinin during natural evolution and adaptation to cell culture. J Gen Virol 78, 97–106.
    [Google Scholar]
  63. Rubin, H. ( 1960; ). A virus in chick embryos which induces resistance in vitro to infection with Rous sarcoma virus. Proc Natl Acad Sci U S A 46, 1105–1119.[CrossRef]
    [Google Scholar]
  64. Rustigan, R. ( 1966; ). Persistent infection of cells in culture by measles virus. II. Effect of measles antibody on persistently infected HeLa sublines and recovery of a HeLa clonal line persistently infected with incomplete virus. J Bacteriol 92, 1805–1811.
    [Google Scholar]
  65. Sacchetti, A., Subramaniam, V., Jovin, T. M. & Alberti, S. ( 2002; ). Oligomerization of DsRed is required for the generation of a functional red fluorescent chromophore. FEBS Lett 525, 13–19.[CrossRef]
    [Google Scholar]
  66. Schneider-Schaulies, S., Schneider-Schaulies, J., Bayer, M., Loffler, S. & ter Meulen, V. ( 1993; ). Spontaneous and differentiation-dependent regulation of measles virus gene expression in human glial cells. J Virol 67, 3375–3383.
    [Google Scholar]
  67. Schneider-Schaulies, J., ter Meulen, V. & Schneider-Schaulies, S. ( 2003; ). Measles infection of the central nervous system. J Neurovirol 9, 247–252.[CrossRef]
    [Google Scholar]
  68. Singh, I. R., Suomalainen, M., Varadarajan, S., Garoff, H. & Helenius, A. ( 1997; ). Multiple mechanisms for the inhibition of entry and uncoating of superinfecting Semliki Forest virus. Virology 231, 59–71.[CrossRef]
    [Google Scholar]
  69. Suarez-Quian, C. A., Goldstein, S. R., Pohida, T., Smith, P. D., Peterson, J. I., Wellner, E., Ghany, M. & Bonner, R. F. ( 1999; ). Laser capture microdissection of single cells from complex tissues. Biotechniques 26, 328–335.
    [Google Scholar]
  70. Tanaka, Y., Kameoka, M., Ota, K., Itaya, A., Ikuta, K. & Yoshihara, K. ( 1999; ). Establishment of persistent infection with HIV-1 abrogates the caspase-3-dependent apoptotic signaling pathway in U937 cells. Exp Cell Res 247, 514–524.[CrossRef]
    [Google Scholar]
  71. Terskikh, A. V., Fradkov, A. F., Zaraisky, A. G., Kajava, A. V. & Angres, B. ( 2002; ). Analysis of DsRed mutants. Space around the fluorophore accelerates fluorescence development. J Biol Chem 277, 7633–7636.[CrossRef]
    [Google Scholar]
  72. Teuchert, M., Maisner, A. & Herrler, G. ( 1999; ). Importance of the carboxyl-terminal FTSL motif of membrane cofactor protein for basolateral sorting and endocytosis. Positive and negative modulation by signals inside and outside the cytoplasmic tail. J Biol Chem 274, 19979–19984.[CrossRef]
    [Google Scholar]
  73. Villuendas, G., Gutierrez-Adan, A., Jimenez, A., Rojo, C., Roldan, E. R. & Pintado, B. ( 2001; ). CMV-driven expression of green fluorescent protein (GFP) in male germ cells of transgenic mice and its effect on fertility. Int J Androl 24, 300–305.[CrossRef]
    [Google Scholar]
  74. 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]
  75. Wall, M. A., Socolich, M. & Ranganathan, R. ( 2000; ). The structural basis for red fluorescence in the tetrameric GFP homolog DsRed. Nat Struct Biol 7, 1133–1138.[CrossRef]
    [Google Scholar]
  76. Walters, K. A., Joyce, M. A., Addison, W. R., Fischer, K. P. & Tyrrell, D. L. ( 2004; ). Superinfection exclusion in duck hepatitis B virus infection is mediated by the large surface antigen. J Virol 78, 7925–7937.[CrossRef]
    [Google Scholar]
  77. Williams, M. P., Brawner, T. A., Riggs, H. G., Jr & Roehrig, J. T. ( 1981; ). Characteristics of a persistent rubella infection in a human cell line. J Gen Virol 52, 321–328.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81052-0
Loading
/content/journal/jgv/10.1099/vir.0.81052-0
Loading

Data & Media loading...

Most Cited This Month

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