1887

Abstract

Using synthetic peptides we have shown that positively charged sequences present at the C terminus of the L1 protein and the N and C termini of the L2 protein of human papillomavirus type 16 (HPV-16) bind to both DNA and heparan sulfate receptors. Moreover, these short amino acid sequences are sufficient to mediate gene transfer in COS-7 cells. The L1 proteins of other HPVs were shown to contain one or two DNA- and heparin-binding sequences that have the capacity to transfer genes. These DNA-binding sequences also recognized the enhancing packaging sequence of bovine papillomavirus type 1. The results suggest that the L2 protein could participate in DNA packaging during maturation of virions.

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2003-01-01
2019-10-22
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References

  1. Baker, T. S., Newcomb, W. W., Olson, N. H., Cowsert, L. M., Olson, C. & Brown, J. C. ( 1991; ). Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophys J 60, 1445–1456.[CrossRef]
    [Google Scholar]
  2. Bousarghin, L., Touzé, A., Combita, A.-l., El Mehdaoui, S., Sizaret, P.-Y., Bravo, M. M. & Coursaget, P. ( 2002; ). Detection of neutralizing antibodies against human papillomaviruses (HPV) by inhibition of gene transfer mediated by HPV pseudovirions. J Clin Microbiol 40, 926–932.[CrossRef]
    [Google Scholar]
  3. Chen, X. S., Garcea, R. L., Goldberg, I., Casini, G. & Harrison, S. C. ( 2000; ). Structure of the small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol Cell 5, 557–567.[CrossRef]
    [Google Scholar]
  4. Combita, A. L., Touzé, A., Bousarghin, L., Sizaret, P.-Y., Munoz, N. & Coursaget, P. ( 2001; ). Gene transfer using human papillomavirus pseudovirions varies according to virus genotype and requires cell surface heparan sulfate. FEMS Microbiol Lett 204, 183–188.[CrossRef]
    [Google Scholar]
  5. El Mehdaoui, S., Touzé, A., Laurent, S., Sizaret, P. Y., Rasschaert, D. & Coursaget, P. ( 2000; ). Gene transfer using recombinant rabbit hemorrhagic disease virus capsids with genetically modified DNA encapsidation capacity by addition of packaging sequences from L1 or L2 protein of human papillomavirus type 16. J Virol 74, 10332–10340.[CrossRef]
    [Google Scholar]
  6. Evander, M., Frazer, I. H., Payne, E., Qi, Y. M., Hengst, K. & McMillan, N. A. ( 1997; ). Identification of the α6 integrin as a candidate receptor for papillomaviruses. J Virol 71, 2449–2456.
    [Google Scholar]
  7. Giroglou, T., Florin, L., Schafer, F., Streeck, R. E. & Sapp, M. ( 2001; ). Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75, 1565–1570.[CrossRef]
    [Google Scholar]
  8. Joyce, J. G., Tung, J. S., Przysieck, C. T., Cook, J. C., Lehman, E. D., Sands, J. A., Jansen, K. U. & Keller, P. M. ( 1999; ). The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J Biol Chem 274, 5810–5822.[CrossRef]
    [Google Scholar]
  9. Kawana, K., Yoshikawa, H., Taketani, Y., Yoshiike, K. & Kanda, T. ( 1998; ). In vitro construction of pseudovirions of human papillomavirus type 16: incorporation of plasmid DNA into reassembled L1/L2 capsids. J Virol 72, 10298–10300.
    [Google Scholar]
  10. Kichler, A., Pages, J. C. & Leborgne, C. & 7 other authors ( 2000; ). Efficient DNA transfection mediated by the C-terminal domain of human immunodeficiency virus type 1 viral protein R. J Virol 74, 5424–5431.[CrossRef]
    [Google Scholar]
  11. Kirnbauer, R., Taub, J., Greenstone, H., Roden, R., Durst, M., Gissmann, L., Lowy, D. R. & Schiller, J. T. ( 1993; ). Efficient self-assembly of human papillomavirus type 16 L1 and L1–L2 into virus-like particles. J Virol 67, 6929–6936.
    [Google Scholar]
  12. Li, M., Cripe, T. P., Estes, P. A., Lyon, M. K., Rose, R. C. & Garcea, R. L. ( 1997; ). Expression of the human papillomavirus type 11 L1 capsid protein in Escherichia coli: characterization of protein domains involved in DNA binding and capsid assembly. J Virol 71, 2988–2995.
    [Google Scholar]
  13. Liu, W. J., Gissmann, L., Sun, X. Y., Kanjanahaluethai, A., Muller, M., Doorbar, J. & Zhou, J. ( 1997; ). Sequence close to the N-terminus of L2 protein is displayed on the surface of bovine papillomavirus type 1 virions. Virology 227, 474–483.[CrossRef]
    [Google Scholar]
  14. McMillan, N. A., Payne, E., Frazer, I. H. & Evander, M. ( 1999; ). Expression of alpha 6 integrin confers papillomavirus binding upon receptor-negative B-cell. Virology 261, 271–274.[CrossRef]
    [Google Scholar]
  15. Mislick, K. A. & Baldeschweiler, J. D. ( 1996; ). Evidence for the role of proteoglycans in cation-mediated gene transfer. Proc Natl Acad Sci US A 93, 12349–12354.[CrossRef]
    [Google Scholar]
  16. Mounkes, L. C., Zhong, W., Cipres-Palacin, G., Heath, T. D. & Debs, R. B. ( 1999; ). Proteoglycans mediate cationic liposome–DNA complexes-based gene delivery in vitro and in vivo. J Biol Chem 273, 26164–26170.
    [Google Scholar]
  17. Müller, M., Gissmann, L., Cristiano, R. J., Sun, X. Y., Frazer, I. H., Jenson, A. B., Alonso, A., Zentgraf, H. & Zhou, J. ( 1995; ). Papillomavirus binding and uptake by cells from different tissues and species. J Virol 69, 948–954.
    [Google Scholar]
  18. Roden, R. B., Greenstone, H. L., Kirnbauer, R., Booy, F. P., Jessie, J., Lowy, D. & Schiller, J. T. ( 1996; ). In vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype. J Virol 70, 5875–5883.
    [Google Scholar]
  19. Roden, R. B. S., Day, P. M., Bronzo, B. K., Yutzy, W. H., IV Yang, Y., Lowy, D. R. & Schiller, J. T. ( 2001; ). Positively charged termini of the L2 minor capsid protein are necessary for papillomavirus infection. J Virol 75, 10493–10497.[CrossRef]
    [Google Scholar]
  20. Rossi, J. L., Gissmann, L., Jansen, K. & Müller, M. ( 2000; ). Assembly of human papillomavirus type 16 in Saccharomyces cerevisiae. Hum Gene Ther 20, 1165–1176.
    [Google Scholar]
  21. Schäfer, F., Florin, L. & Sapp, M. ( 2002; ). DNA binding of L1 is required for human papillomavirus morphogenesis in vivo. Virology 295, 172–181.[CrossRef]
    [Google Scholar]
  22. Schiller, J. T. & Roden, R. B. S. ( 1995; ). Papillomavirus-like particles. Papillomavirus Rep 6, 121–128.
    [Google Scholar]
  23. Stauffer, Y., Raj, K., Masternak, K. & Beard, P. ( 1998; ). Infectious human papillomavirus type 18 pseudovirions. J Mol Biol 283, 529–536.[CrossRef]
    [Google Scholar]
  24. Sun, X. Y., Frazer, I. H., Müller, M., Gissmann, L. & Zhou, J. ( 1995; ). Sequences required for the nuclear targeting and accumulation of human papillomavirus type 6B L2 protein. Virology 213, 321–327.[CrossRef]
    [Google Scholar]
  25. Touzé, A. & Coursaget, P. ( 1998; ). In vitro gene transfer using human papillomavirus-like particles. Nucleic Acids Res 26, 1317–1323.[CrossRef]
    [Google Scholar]
  26. Touzé, A., Mahé, D., El Mehdaoui, S., Combita, A. L., Bousarghin, L. & Coursaget, P. ( 2000; ). The 9 C-terminal amino acids of the major capsid protein of the human papillomavirus type 16 are essential for DNA binding and gene transfer capacity. FEMS Microbiol Lett 189, 121–127.[CrossRef]
    [Google Scholar]
  27. Touzé, A., Bousarghin, L., Ster, C., Combita, A.-L., Roingeard, P. & Coursaget, P. ( 2001; ). Gene transfer using human polyomavirus BK virus-like particles expressed in insect cells. J Gen Virol 82, 3005–3009.
    [Google Scholar]
  28. Unckell, F., Streeck, R. E. & Sapp, M. ( 1997; ). Generation of pseudovirions of human papillomavirus type 33. J Virol 71, 2934–2939.
    [Google Scholar]
  29. Zhao, K. N., Frazer, I. H., Jun Liu, W., Williams, M. & Zhou, J. ( 1999; ). Nucleotides 1506–1625 of bovine papillomavirus type 1 genome can enhance DNA packaging by L1/L2 capsids. Virology 259, 211–218.[CrossRef]
    [Google Scholar]
  30. Zhou, J., Doorbar, J., Sun, X. Y., Crawford, L. V., McLean, C. S. & Frazer, I. H. ( 1991; ). Identification of the nuclear localization signal of human papillomavirus type 16 L1 protein. Virology 185, 625–632.[CrossRef]
    [Google Scholar]
  31. Zhou, J., Sun, X. Y., Louis, K. & Frazer, I. H. ( 1994; ). Interaction of human papillomavirus (HPV) type 16 capsid proteins with HPV DNA requires an intact L2 N-terminal sequence. J Virol 68, 619–625.
    [Google Scholar]
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