1887

Abstract

Several host proteins have been shown to play key roles in the life-cycle of vesicular stomatitis virus (VSV). We have identified an additional host protein, cyclophilin A (CypA), a chaperone protein possessing peptidyl prolyl-isomerase activity, as one of the cellular factors required for VSV replication. Inhibition of the enzymatic activity of cellular CypA by cyclosporin A (CsA) or SDZ-211-811 resulted in a drastic inhibition of gene expression by VSV New Jersey (VSV-NJ) serotype, while these drugs had a significantly reduced effect on the genome expression of VSV Indiana (VSV-IND) serotype. Overexpression of a catalytically inactive mutant of CypA resulted in the reduction of VSV-NJ replication, suggesting a requirement for functional CypA for VSV-NJ infection. It was also shown that CypA interacted with the nucleocapsid (N) protein of VSV-NJ and VSV-IND in infected cells and was incorporated into the released virions of both serotypes. VSV-NJ utilized CypA for post-entry intracellular primary transcription, since inhibition of CypA with CsA reduced primary transcription of VSV-NJ by 85–90 %, whereas reduction for VSV-IND was only 10 %. Thus, it seems that cellular CypA binds to the N protein of both serotypes of VSV. However, it performs an obligatory function on the N protein activity of VSV-NJ, while its requirement is significantly less critical for VSV-IND N protein function. The different requirements for CypA by two serologically different viruses belonging to the same family has highlighted the utilization of specific host factors during their evolutionary lineages.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.19074-0
2003-07-01
2019-11-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/7/vir841687.html?itemId=/content/journal/jgv/10.1099/vir.0.19074-0&mimeType=html&fmt=ahah

References

  1. Adam, S. A., Choi, Y. D. & Dreyfuss, G. ( 1986; ). Interaction of mRNA with proteins in vesicular stomatitis virus infected cells. J Virol 57, 614–622.
    [Google Scholar]
  2. Agresta, B. E. & Carter, C. ( 1997; ). Cyclophilin a induced alterations of human immunodeficiency virus type 1 CA protein in vitro. J Virol 71, 6921–6927.
    [Google Scholar]
  3. Alexanian, A. R. & Bamburg, J. R. ( 1999; ). Neuronal survival activity of s100ββ is enhanced by calcineurin inhibitors and requires activation of NF-κB. FASEB J 13, 1611–1620.
    [Google Scholar]
  4. Banerjee, A. K. ( 1987; ). Transcription and replication of rhabdoviruses. Microbiol Rev 51, 66–87.
    [Google Scholar]
  5. Banerjee, A. K., Rhodes, D. P. & Gill, D. S. ( 1984; ). Complete nucleotide sequence of the mRNA coding for the N protein of vesicular stomatitis virus (New Jersey serotype). Virology 137, 432–438.[CrossRef]
    [Google Scholar]
  6. Barik, S. & Banerjee, A. K. ( 1992; ). Phosphorylation by cellular casein kinase II is essential for transcriptional activity of vesicular stomatitis virus phosphoprotein P. Proc Natl Acad Sci U S A 89, 6570–6574.[CrossRef]
    [Google Scholar]
  7. Billich, A., Hammerschmid, F., Peichl, P., Wenger, R., Zenke, G., Quesniaux, V. & Rosenwirth, B. ( 1995; ). Mode of action of SDZ NIM 811, a nonimmunosuppressive cyclosporin A analog with activity against human immunodeficiency virus (HIV) type 1: interference with HIV protein–cyclophilin A interactions. J Virol 69, 2451–2461.
    [Google Scholar]
  8. Bilsel, P. A. & Nichol, S. T. ( 1990; ). Polymerase errors accumulating during natural evolution of the glycoprotein gene of vesicular stomatitis virus Indiana serotype isolates. J Virol 64, 4873–4883.
    [Google Scholar]
  9. Bose, S. & Banerjee, A. K. ( 2002; ). Role of heparan sulfate in human parainfluenza virus type 3 infection. Virology 298, 73–83.[CrossRef]
    [Google Scholar]
  10. Bose, S., Malur, A. & Banerjee, A. K. ( 2001; ). Polarity of human parainfluenza virus type 3 infection in polarized human lung epithelial A549 cells: role of microfilament and microtubule. J Virol 75, 1984–1989.[CrossRef]
    [Google Scholar]
  11. Braaten, D. & Luban, J. ( 2001; ). Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. EMBO J 20, 1300–1309.[CrossRef]
    [Google Scholar]
  12. Braaten, D., Franke, E. K. & Luban, J. ( 1996a; ). Cyclophilin is required for an early step in the life cycle of human immunodeficiency virus type 1 before the initiation of reverse transcription. J Virol 70, 3551–3560.
    [Google Scholar]
  13. Braaten, D., Franke, E. K. & Luban, J. ( 1996b; ). Cyclophilin A is required for the replication of group M human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency virus SIVCPZGAB but not group O HIV-1 or other primate immunodeficiency viruses. J Virol 70, 4220–4227.
    [Google Scholar]
  14. Chong, D. D. & Rose, J. K. ( 1993; ). Membrane association of functional vesicular stomatitis virus matrix protein in vivo. J Virol 67, 407–414.
    [Google Scholar]
  15. Choudhary, S., De, B. P. & Banerjee, A. K. ( 2000; ). Specific phosphorylated forms of glyceraldehyde 3-phosphate dehydrogenase associate with human parainfluenza virus type 3 and inhibit viral transcription in vitro. J Virol 74, 3634–3641.[CrossRef]
    [Google Scholar]
  16. Choudhary, S., Gao, J., Leaman, D. W. & De, B. P. ( 2001; ). Interferon action against human parainfluenza virus type 3: involvement of a novel antiviral pathway in the inhibition of transcription. J Virol 75, 4823–4831.[CrossRef]
    [Google Scholar]
  17. Colgan, J., Yuan, H. H., Franke, E. K. & Luban, J. ( 1996; ). Binding of the human immunodeficiency virus type 1 gag polyprotein to cyclophilin A is mediated by the central region of capsid and requires gag dimerization. J Virol 70, 4299–4310.
    [Google Scholar]
  18. Das, T., Gupta, A. K., Sims, P. W., Gelfand, C. A., Jentoft, J. E. & Banerjee, A. K. ( 1995; ). Role of cellular casein kinase II in the function of the phosphoprotein (P) subunit of RNA polymerase of vesicular stomatitis virus. J Biol Chem 270, 24100–24107.[CrossRef]
    [Google Scholar]
  19. Das, T., Mathur, M., Gupta, A. K., Janssen, G. M. & Banerjee, A. K. ( 1998; ). RNA polymerase of vesicular stomatitis virus specifically associates with translational elongation factor-1 αβγ for its activity. Proc Natl Acad Sci U S A 95, 1449–1454.[CrossRef]
    [Google Scholar]
  20. De, B. P., Thornton, G. B., Luk, D. & Banerjee, A. K. ( 1982; ). Purified matrix protein of vesicular stomatitis virus blocks viral transcription in vitro. Proc Natl Acad Sci U S A 79, 7137–7141.[CrossRef]
    [Google Scholar]
  21. De, B. P., Lesoon, A. & Banerjee, A. K. ( 1991; ). Human parainfluenza virus type 3 transcription in vitro: role of cellular actin in mRNA synthesis. J Virol 65, 3268–3275.
    [Google Scholar]
  22. De, B. P., Hoffman, M. A., Choudhary, S., Huntley, C. C. & Banerjee, A. K. ( 2000; ). Role of NH2 and COOH terminal domains of the P protein of human parainfluenza virus type 3 in transcription and replication. J Virol 74, 5886–5895.[CrossRef]
    [Google Scholar]
  23. Dietrich, L., Ehrlich, L. S., LaGrassa, T. J., Ebbets-Reed, D. & Carter, C. ( 2001; ). Structural consequences of cyclophilin A binding on maturational refolding in human immunodeficiency virus type 1 capsid protein. J Virol 75, 4721–4733.[CrossRef]
    [Google Scholar]
  24. Dorfman, T. & Gottlinger, H. G. ( 1996; ). Capsid p2 domain confers sensitivity to the cyclophilin binding drug SDZ NIM 811. J Virol 70, 5751–5757.
    [Google Scholar]
  25. Franke, E. K., Yuan, H. E. & Luban, J. ( 1994; ). Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372, 359–362.[CrossRef]
    [Google Scholar]
  26. Frazier, C. L. & Shope, R. E. ( 1979; ). In Rhabdoviruses, vol. 1, pp. 43–63. Edited by D. H. L. Bishop. Boca Raton: CRC Press.
  27. Garry, R. F., Ulug, E. T. & Bose, H. R. ( 1983; ). Induction of stress proteins in Sindbis virus and vesicular stomatitis virus infected cells. Virology 129, 319–332.[CrossRef]
    [Google Scholar]
  28. Gothel, S. F. & Marahiel, M. A. ( 1999; ). Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 55, 423–436.[CrossRef]
    [Google Scholar]
  29. Gupta, A. K. & Banerjee, A. K. ( 1997; ). Expression and purification of N–P complex from Escherichia coli: role in genome RNA transcription and replication in vitro. J Virol 71, 4264–4271.
    [Google Scholar]
  30. Gupta, A. K., Drazba, J. A. & Banerjee, A. K. ( 1998; ). Specific interaction of heterogenous nuclear ribonucleoprotein particle U with the leader RNA sequence of vesicular stomatitis virus. J Virol 72, 8532–8540.
    [Google Scholar]
  31. Gurer, C., Cimarelli, A. & Luban, J. ( 2002; ). Specific incorporation of heat shock protein 70 family members into primate lentiviral virions. J Virol 76, 4666–4670.[CrossRef]
    [Google Scholar]
  32. Hanson, R. P. ( 1952; ). The natural history of vesicular stomatitis virus. Bacteriol Rev 15, 179–204.
    [Google Scholar]
  33. Harty, R. N., Paragas, J., Sudol, M. & Palese, P. ( 1999; ). A proline-rich motif within the matrix protein of vesicular stomatitis virus and rabies virus interacts with WW domains of cellular proteins: implications for viral budding. J Virol 73, 2921–2929.
    [Google Scholar]
  34. Harty, R. N., Brown, M. E., McGettigan, J. P., Wang, G., Jayakar, H. R., Huibregtse, J. M., Whitt, M. A. & Schnell, M. J. ( 2001; ). Rhabdoviruses and the cellular ubiquitin–proteasome system: a budding interaction. J Virol 75, 10623–10629.[CrossRef]
    [Google Scholar]
  35. Heggeness, M. H., Scheid, A. & Choppin, P. W. ( 1980; ). Conformation of the helical nucleocapsids of paramyxoviruses and vesicular stomatitis virus: reversible coiling and uncoiling induced by changes in salt concentration. Proc Natl Acad Sci U S A 77, 2631–2635.[CrossRef]
    [Google Scholar]
  36. Helekar, S. A. & Patrick, J. ( 1997; ). Peptidyl-prolyl cis-trans isomerase activity of cyclophilin A in functional homo-oligomeric receptor expression. Proc Natl Acad Sci U S A 94, 5432–5437.[CrossRef]
    [Google Scholar]
  37. Hu, J., Toft, D. & Seeger, C. ( 1997; ). Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids. EMBO J 16, 59–68.[CrossRef]
    [Google Scholar]
  38. Hu, J., Toft, D., Anselmo, D. & Wang, X. ( 2002; ). In vitro reconstitution of functional hepadnavirus reverse transcriptase with cellular chaperone proteins. J Virol 76, 269–279.[CrossRef]
    [Google Scholar]
  39. Jakob, U. & Buchner, J. ( 1994; ). Assisting spontaneity: the role of Hsp 90 and small Hsps as molecular chaperones. Trends Biochem Sci 19, 205–211.[CrossRef]
    [Google Scholar]
  40. Kopecky, S. A., Willingham, M. C. & Lyles, D. S. ( 2001; ). Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J Virol 75, 12169–12181.[CrossRef]
    [Google Scholar]
  41. Lodish, H. F. & Kong, N. ( 1991; ). Cyclosporin A inhibits an initial step in folding of transferrin within the endoplasmic reticulum. J Biol Chem 266, 14835–14838.
    [Google Scholar]
  42. Luban, J., Bossolt, K. L., Franke, E. K., Kalpana, G. V. & Goff, S. P. ( 1993; ). Human immunodeficiency virus type 1 gag protein binds to cyclophilins A and B. Cell 73, 1067–1078.[CrossRef]
    [Google Scholar]
  43. Lyles, D. S., McKensie, M. & Parce, J. W. ( 1992; ). Subunit interactions of vesicular stomatitis virus envelope glycoprotein stabilized by binding to viral matrix protein. J Virol 66, 349–358.
    [Google Scholar]
  44. Manders, E. K., Tilles, J. H. & Huang, A. S. ( 1972; ). Interferon mediated inhibition of virion directed transcription. Virology 49, 573–581.[CrossRef]
    [Google Scholar]
  45. Moyer, S. A., Baker, S. C. & Lessard, J. L. ( 1986; ). Tubulin: a factor necessary for the synthesis of both Sendai virus and vesicular stomatitis virus RNAs. Proc Natl Acad Sci U S A 83, 5405–5409.[CrossRef]
    [Google Scholar]
  46. Nauwynck, H. J., Duan, X., Favoreel, H. W., VanOostveldt, P. & Pensaert, M. B. ( 1999; ). Entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages via receptor mediated endocytosis. J Gen Virol 80, 297–305.
    [Google Scholar]
  47. Ono, K., Dubois-Dalcq, M. E., Schubert, M. & Lazzarini, R. A. ( 1987; ). A mutated membrane protein of vesicular stomatitis virus has an abnormal distribution within the infected cell and causes defective budding. J Virol 61, 1332–1341.
    [Google Scholar]
  48. Peluso, R. W. & Moyer, S. A. ( 1983; ). Initiation and replication of vesicular stomatitis virus genome RNA in a cell free system. Proc Natl Acad Sci U S A 80, 3198–3202.[CrossRef]
    [Google Scholar]
  49. Rodriguez, L. L. & Nichol, S. T. ( 1999; ). Vesicular stomatitis viruses. In Encyclopedia of Virology, vol. 5, 2nd edn, pp. 1910–1919. Edited by A. Granoff & R. G. Webster. San Diego: Academic Press.
  50. Rose, J. K. & Whitt, M. A. ( 2001; ). Rhabdoviridae: the viruses and their replication. In Fields Virology, 4th edn, pp. 1221–1244. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  51. Sagara, J. & Kawai, A. ( 1992; ). Identification of heat shock protein 70 in the rabies virion. Virology 190, 845–848.[CrossRef]
    [Google Scholar]
  52. Sanchez, E. R. & Ning, Y. M. ( 1996; ). Immunophilins, heat shock proteins, and glucocorticoid receptor actions in vivo. Methods 9, 188–200.[CrossRef]
    [Google Scholar]
  53. Saphire, A. C. S., Bobardt, M. D. & Gallay, P. A. ( 1999; ). Host cyclophilin A mediates HIV-1 attachment to target cells via heparans. EMBO J 18, 6771–6785.[CrossRef]
    [Google Scholar]
  54. Schneuwly, S., Shortridge, R. D., Larrivee, D. C., Ono, T., Ozaki, M. & Pak, W. L. ( 1989; ). Drosophilia ninaA gene encodes an eye specific cyclophilin. Proc Natl Acad Sci U S A 86, 5390–5394.[CrossRef]
    [Google Scholar]
  55. Steinmann, B., Bruckner, P. & Superti-Furga, A. ( 1991; ). Cyclosporin A slows collagen triple helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cis-trans isomerase. J Biol Chem 266, 1299–1303.
    [Google Scholar]
  56. Streblow, D. N., Kitabwalla, M., Malkovsky, M. & Pauza, C. D. ( 1998; ). Cyclophilin A modulates processing of human immunodeficiency virus type 1 p55 gag: mechanism for antiviral effects of cyclosporin A. Virology 245, 197–202.[CrossRef]
    [Google Scholar]
  57. Taigen, T., DeWindt, L. J., Lim, H. W. & Molkentin, J. D. ( 2000; ). Targeted inhibition of calcineurin prevents agonist induced cardiomyocyte hypertrophy. Proc Natl Acad Sci U S A 97, 1196–1201.[CrossRef]
    [Google Scholar]
  58. Takahashi, N., Hayano, T. & Suzuki, M. ( 1989; ). Peptidyl-prolyl cis-trans isomerase is the cyclosporin A binding protein cyclophilin. Nature 337, 473–475.[CrossRef]
    [Google Scholar]
  59. Thali, M., Bukovsky, A., Kondo, E., Rosenwirth, B., Walsh, C. T., Sodroski, J. & Gottlinger, H. G. ( 1994; ). Functional association of cyclophilin A with HIV-1 virions. Nature 372, 363–365.[CrossRef]
    [Google Scholar]
  60. Uittenbogaard, A., Ying, Y. & Smart, E. J. ( 1998; ). Characterization of a cytosolic heat shock protein caveolin chaperone complex. Involvement in cholesterol trafficking. J Biol Chem 273, 6525–6532.[CrossRef]
    [Google Scholar]
  61. Zhou, A., Paranjape, M. J. M., Hassel, B. A., Nie, H., Shah, S., Galinski, B. & Silverman, R. H. ( 1998; ). Impact of Rnase L overexpression on viral and cellular growth and death. J Interferon Cytokine Res 18, 953–961.
    [Google Scholar]
  62. Zydowsky, L. D., Etzkorn, F. A., Chang, H. Y., Ferguson, S. B., Stolz, L. A., Ho, S. I. & Walsh, C. T. ( 1992; ). Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci 1, 1092–1099.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.19074-0
Loading
/content/journal/jgv/10.1099/vir.0.19074-0
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