Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses Free

Abstract

In order to determine how efficiently the polymerase proteins derived from human and avian influenza A viruses can interact with each other in the context of a mammalian cell, a genetic system that allows the reconstitution of active ribonucleoproteins was used. The ability to achieve replication of a viral-like reporter RNA in COS-1 cells was examined with heterospecific mixtures of the core proteins (PB1, PB2, PA and NP) from two strains of human viruses (A/Puerto Rico/8/34 and A/Victoria/3/75), two strains of avian viruses (A/Mallard/NY/6750/78 and A/FPV/-Rostock/34), and a strain of avian origin (A/Hong Kong/156/97) that was isolated from the first human case of H5N1 influenza in Hong Kong in 1997. In accordance with published observations on reassortant viruses, PB2 amino acid 627 was identified as a major determinant of the replication efficiency of heterospecific complexes in COS-1 cells. Moreover, the results showed that replication of the viral-like reporter RNA was more efficient when PB2 and NP were both derived from the same avian or human virus or when PB1 was derived from an avian virus, whatever the origin of the other proteins. Furthermore, the PB1 and PB2 proteins from the A/Hong- Kong/156/97 virus exhibited intermediate properties with respect to the corresponding proteins from avian or human influenza viruses, suggesting that some molecular characteristics of PB1 and PB2 proteins might at least partially account for the ability of the A/Hong Kong/156/97 virus to replicate in humans.

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2000-05-01
2024-03-28
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References

  1. Almond, J. W. (1977). A single gene determines the host range of influenza virus.Nature 270, 617-618.[CrossRef] [Google Scholar]
  2. Asano, Y. & Ishihama, A. (1997). Identification of two nucleotide-binding domains on the PB1 subunit of influenza virus RNA polymerase.Journal of Biochemistry 122, 627-634.[CrossRef] [Google Scholar]
  3. Beare, A. S. & Webster, R. G. (1991). Replication of avian influenza viruses in humans.Archives of Virology 119, 37-42.[CrossRef] [Google Scholar]
  4. Beaton, A. R. & Krug, R. M. (1986). Transcription antitermination during influenza viral template RNA synthesis requires the nucleocapsid protein and the absence of a 5′ capped end.Proceedings of the National Academy of Sciences, USA 83, 6282-6286.[CrossRef] [Google Scholar]
  5. Biswas, S. K. & Nayak, D. P. (1994). Mutational analysis of the conserved motifs of influenza A virus polymerase basic protein 1.Journal of Virology 68, 1819-1826. [Google Scholar]
  6. Biswas, S. K., Boutz, P. L. & Nayak, D. P. (1998). Influenza virus nucleoprotein interacts with influenza virus polymerase proteins.Journal of Virology 72, 5493-5501. [Google Scholar]
  7. Blaas, D., Patzelt, E. & Kuechler, E. (1982). Cap-recognizing protein of influenza virus.Virology 116, 339-348.[CrossRef] [Google Scholar]
  8. Blok, V., Cianci, C., Tibbles, K. W., Inglis, S. C., Krystal, M. & Digard, P. (1996). Inhibition of the influenza virus RNA-dependent RNA polymerase by antisera directed against the carboxy-terminal region of the PB2 subunit.Journal of General Virology 77, 1025-1033.[CrossRef] [Google Scholar]
  9. Braam, J., Ulmanen, I. & Krug, R. M. (1983). Molecular model of a eucaryotic transcription complex: functions and movements of influenza P proteins during capped RNA-primed transcription.Cell 34, 609-618. [Google Scholar]
  10. Buckler-White, A. J., Naeve, C. W. & Murphy, B. R. (1986). Characterization of a gene coding for M proteins which is involved in host range restriction of an avian influenza A virus in monkeys.Journal of Virology 57, 697-700. [Google Scholar]
  11. Centers for Disease Control & Prevention (1998). Update: isolation of avian influenza A (H5N1) viruses from humans – Hong Kong, 1997–1998. Morbidity & Mortality Weekly Report 46, 1245–1247. [Google Scholar]
  12. Claas, E. C., Osterhaus, A. D., van Beek, R., De Jong, J. C., Rimmelzwaan, G. F., Senne, D. A., Krauss, S., Shortridge, K. F. & Webster, R. G. (1998). Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus [published erratum appears in Lancet (1998) 351, 1292].Lancet 351, 472-477.[CrossRef] [Google Scholar]
  13. Clements, M. L., Snyder, M. H., Buckler-White, A. J., Tierney, E. L., London, W. T. & Murphy, B. R. (1986). Evaluation of avian–human reassortant influenza A/Washington/897/80×A/Pintail/119/79 virus in monkeys and adult volunteers.Journal of Clinical Microbiology 24, 47-51. [Google Scholar]
  14. Clements, M. L., Subbarao, E. K., Fries, L. F., Karron, R. A., London, W. T. & Murphy, B. R. (1992). Use of single-gene reassortant viruses to study the role of avian influenza A virus genes in attenuation of wild-type human influenza A virus for squirrel monkeys and adult human volunteers.Journal of Clinical Microbiology 30, 655-662. [Google Scholar]
  15. Desselberger, U., Racaniello, V. R., Zazra, J. J. & Palese, P. (1980). The 3′ and 5′-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity.Gene 8, 315-328.[CrossRef] [Google Scholar]
  16. Digard, P., Block, V. C. & Inglis, S. C. (1989). Complex formation between influenza virus polymerase proteins expressed in Xenopus oocytes.Virology 171, 162-169.[CrossRef] [Google Scholar]
  17. Gonzalez, S. & Ortin, J. (1999a). Distinct regions of influenza virus PB1 polymerase subunit recognize vRNA and cRNA templates.EMBO Journal 18, 3767-3775.[CrossRef] [Google Scholar]
  18. Gonzalez, S. & Ortin, J. (1999b). Characterization of influenza virus PB1 protein binding to viral RNA: two separate regions of the protein contribute to the interaction domain.Journal of Virology 73, 631-637. [Google Scholar]
  19. Gonzalez, S., Zurcher, T. & Ortin, J. (1996). Identification of two separate domains in the influenza virus PB1 protein involved in the interaction with the PB2 and PA subunits: a model for the viral RNA polymerase structure.Nucleic Acids Research 24, 4456-4463.[CrossRef] [Google Scholar]
  20. Guan, Y., Shortridge, K. F., Krauss, S. & Webster, R. G. (1999). Molecular characterization of H9N2 influenza viruses: were they the donors of the ‘internal’ genes of H5N1 viruses in Hong-Kong?Proceedings of the National Academy of Sciences, USA 96, 9363-9367.[CrossRef] [Google Scholar]
  21. Honda, A., Ueda, K., Nagata, K. & Ishihama, A. (1988). RNA polymerase of influenza virus: role of NP in RNA chain elongation.Journal of Biochemistry 104, 1021-1026. [Google Scholar]
  22. Kawaoka, Y., Krauss, S. & Webster, R. G. (1989). Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics.Journal of Virology 63, 4603-4608. [Google Scholar]
  23. Li, M. L., Ramirez, B. C. & Krug, R. M. (1998). RNA-dependent activation of primer RNA production by influenza virus polymerase: different regions of the same protein subunit constitute the two required RNA-binding sites.EMBO Journal 17, 5844-5852.[CrossRef] [Google Scholar]
  24. Lindstrom, S. E., Hiromoto, Y., Nerome, R., Omoe, K., Sugita, S., Yamasaki, Y., Takahashi, T. & Nerome, K. (1998). Phylogenetic analysis of the entire genome of influenza A (H3N2) viruses from Japan: evidence for genetic reassortment of the six internal genes.Journal of Virology 72, 8021-8031. [Google Scholar]
  25. Mandler, J., Muller, K. & Scholtissek, C. (1991). Mutants and revertants of an avian influenza A virus with temperature-sensitive defects in the nucleoprotein and PB2.Virology 181, 512-519.[CrossRef] [Google Scholar]
  26. Murphy, B. R., Hinshaw, V. S., Sly, D. L., London, W. T., Hosier, N. T., Wood, F. T., Webster, R. G. & Chanock, R. M. (1982). Virulence of avian influenza A viruses for squirrel monkeys.Infection and Immunity 37, 1119-1126. [Google Scholar]
  27. Pleschka, S., Jaskunas, R., Engelhardt, O. G., Zurcher, T., Palese, P. & Garcia-Sastre, A. (1996). A plasmid-based reverse genetics system for influenza A virus.Journal of Virology 70, 4188-4192. [Google Scholar]
  28. Poch, O., Sauvaget, I., Delarue, M. & Tordo, N. (1989). Identification of four conserved motifs among the RNA-dependent polymerase encoding elements.EMBO Journal 8, 3867-3874. [Google Scholar]
  29. Sanz-Ezquerro, J. J., de la Luna, S., Ortin, J. & Nieto, A. (1995). Individual expression of influenza virus PA protein induces degradation of coexpressed proteins.Journal of Virology 69, 2420-2426. [Google Scholar]
  30. Scholtissek, C., Rohde, W., von Hoyningen, V. & Rott, R. (1978). On the origin of the human influenza subtype H2N2 and H3N2.Virology 87, 13-20.[CrossRef] [Google Scholar]
  31. Scholtissek, C., Hinshaw, V. S. & Olsen, C. W. (1998). Influenza in pigs and their role as the intermediate host. In Textbook of Influenza, pp. 137-145. Edited by K. G. Nicholson, R. G. Webster & A. J. Hay. Oxford: Blackwell Science.
  32. Shi, L., Galarza, J. M. & Summers, D. F. (1996). Recombinant-baculovirus-expressed PB2 subunit of the influenza A virus RNA polymerase binds cap groups as an isolated subunit.Virus Research 42, 1-9.[CrossRef] [Google Scholar]
  33. Snyder, M. H., Buckler-White, A. J., London, W. T., Tierney, E. L. & Murphy, B. R. (1987). The avian influenza virus nucleoprotein gene and a specific constellation of avian and human virus polymerase genes each specify attenuation of avian–human influenza A/Pintail/79 reassortant viruses for monkeys.Journal of Virology 61, 2857-2863. [Google Scholar]
  34. Suarez, D. L., Perdue, M. L., Cox, N., Rowe, T., Bender, C., Huang, J. & Swayne, D. E. (1998). Comparisons of highly virulent H5N1 influenza A viruses isolated from humans and chickens from Hong Kong.Journal of Virology 72, 6678-6688. [Google Scholar]
  35. Subbarao, E. K., London, W. & Murphy, B. R. (1993). A single amino acid in the PB2 gene of influenza A virus is a determinant of host range.Journal of Virology 67, 1761-1764. [Google Scholar]
  36. Subbarao, K., Klimov, A., Katz, J., Regnery, H., Lim, W., Hall, H., Perdue, M., Swayne, D., Bender, C., Huang, J., Hemphill, M., Rowe, T., Shaw, M., Xu, X., Fukuda, K. & Cox, N. (1998). Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness [see comments].Science 279, 393-396.[CrossRef] [Google Scholar]
  37. Tian, S. F., Buckler-White, A. J., London, W. T., Reck, L. J., Chanock, R. M. & Murphy, B. R. (1985). Nucleoprotein and membrane protein genes are associated with restriction of replication of influenza A/Mallard/NY/78 virus and its reassortants in squirrel monkey respiratory tract.Journal of Virology 53, 771-775. [Google Scholar]
  38. Tomic, M., Sunjevaric, I., Savtchenko, E. S. & Blumenberg, M. (1990). A rapid and simple method for introducing specific mutations into any position of DNA leaving all other positions unaltered.Nucleic Acids Research 18, 1656.[CrossRef] [Google Scholar]
  39. Toyoda, T., Adyshev, D. M., Kobayashi, M., Iwata, A. & Ishihama, A. (1996). Molecular assembly of the influenza virus RNA polymerase: determination of the subunit–subunit contact sites.Journal of General Virology 77, 2149-2157.[CrossRef] [Google Scholar]
  40. Webster, R. G. & Bean, W. J.Jr (1998). Evolution and ecology of influenza viruses: interspecies transmission. In Textbook of Influenza, pp. 109-119. Edited by K. G. Nicholson, R. G. Webster & A. J. Hay. Oxford: Blackwell Science.
  41. Zürcher, T., de la Luna, S., Sanz-Ezquerro, J. J., Nieto, A. & Ortı́n, J. (1996). Mutational analysis of the influenza virus A/Victoria/3/75 PA protein: studies of interaction with PB1 protein and identification of a dominant negative mutant.Journal of General Virology 77, 1745-1749.[CrossRef] [Google Scholar]
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