Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1994 Jun;68(6):3499–3504. doi: 10.1128/jvi.68.6.3499-3504.1994

Subtype cross-reactive, infection-enhancing antibody responses to influenza A viruses.

M Tamura 1, R G Webster 1, F A Ennis 1
PMCID: PMC236853  PMID: 8189489

Abstract

Antibody-dependent enhancement of the uptake of influenza A virus by Fc receptor-bearing cells was analyzed by using virus strains of the three human influenza A virus subtypes, A/PR/8/34 (H1N1), A/Japan/305/57 (H2N2), and A/Port Chalmers/1/73 (H3N2). Immune sera obtained from mice following primary infection with an H1N1, H2N2, or H3N2 subtype virus neutralized only virus of the same subtype; however, immune sera augmented the uptake of virus across subtypes. Immune sera from H1N1-infected mice augmented uptake of the homologous (H1N1) and H2N2 viruses. Antisera to the H2N2 virus augmented the uptake of virus of all subtypes (H1N1, H2N2, or H3N2). Antisera to the H3N2 virus augmented the uptake of the homologous (H3N2) and H2N2 viruses. These results show that subtype cross-reactive, nonneutralizing antibodies augment the uptake of influenza A virus strains of different subtypes. Antibodies to neuraminidase may contribute to the enhanced uptake of viruses of a different subtype, because N2-specific monoclonal antibodies augmented the uptake of both A/Japan/305/57 (H2N2) and A/Port Chalmers/1/73 (H3N2) viruses.

Full text

PDF
3499

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allan W. H., Madeley C. R., Kendal A. P. Studies with avian influenza A viruses: cross protection experiments in chickens. J Gen Virol. 1971 Aug;12(2):79–84. doi: 10.1099/0022-1317-12-2-79. [DOI] [PubMed] [Google Scholar]
  2. Antibody-dependent enhancement of HIV infection. Lancet. 1988 Jun 4;1(8597):1285–1286. [PubMed] [Google Scholar]
  3. Burstin S. J., Brandriss M. W., Schlesinger J. J. Infection of a macrophage-like cell line, P388D1 with reovirus; effects of immune ascitic fluids and monoclonal antibodies on neutralization and on enhancement of viral growth. J Immunol. 1983 Jun;130(6):2915–2919. [PubMed] [Google Scholar]
  4. Celis E., Chang T. W. Antibodies to hepatitis B surface antigen potentiate the response of human T lymphocyte clones to the same antigen. Science. 1984 Apr 20;224(4646):297–299. doi: 10.1126/science.6231724. [DOI] [PubMed] [Google Scholar]
  5. Colman P. M., Ward C. W. Structure and diversity of influenza virus neuraminidase. Curr Top Microbiol Immunol. 1985;114:177–255. doi: 10.1007/978-3-642-70227-3_5. [DOI] [PubMed] [Google Scholar]
  6. Gotoff R., Tamura M., Janus J., Thompson J., Wright P., Ennis F. A. Primary influenza A virus infection induces cross-reactive antibodies that enhance uptake of virus into Fc receptor-bearing cells. J Infect Dis. 1994 Jan;169(1):200–203. doi: 10.1093/infdis/169.1.200. [DOI] [PubMed] [Google Scholar]
  7. Halstead S. B., O'Rourke E. J. Antibody-enhanced dengue virus infection in primate leukocytes. Nature. 1977 Feb 24;265(5596):739–741. doi: 10.1038/265739a0. [DOI] [PubMed] [Google Scholar]
  8. Kilbourne E. D., Laver W. G., Schulman J. L., Webster R. G. Antiviral activity of antiserum specific for an influenza virus neuraminidase. J Virol. 1968 Apr;2(4):281–288. doi: 10.1128/jvi.2.4.281-288.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Koren H. S., Handwerger B. S., Wunderlich J. R. Identification of macrophage-like characteristics in a cultured murine tumor line. J Immunol. 1975 Feb;114(2 Pt 2):894–897. [PubMed] [Google Scholar]
  10. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  11. Manca F., Fenoglio D., Li Pira G., Kunkl A., Celada F. Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies. J Exp Med. 1991 Jan 1;173(1):37–48. doi: 10.1084/jem.173.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Monto A. S., Kendal A. P. Effect of neuraminidase antibody on Hong Kong influenza. Lancet. 1973 Mar 24;1(7804):623–625. doi: 10.1016/s0140-6736(73)92196-x. [DOI] [PubMed] [Google Scholar]
  13. Ochiai H., Kurokawa M., Hayashi K., Niwayama S. Antibody-mediated growth of influenza A NWS virus in macrophagelike cell line P388D1. J Virol. 1988 Jan;62(1):20–26. doi: 10.1128/jvi.62.1.20-26.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ochiai H., Kurokawa M., Kuroki Y., Niwayama S. Infection enhancement of influenza A H1 subtype viruses in macrophage-like P388D1 cells by cross-reactive antibodies. J Med Virol. 1990 Apr;30(4):258–265. doi: 10.1002/jmv.1890300406. [DOI] [PubMed] [Google Scholar]
  15. Okuno Y., Isegawa Y., Sasao F., Ueda S. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol. 1993 May;67(5):2552–2558. doi: 10.1128/jvi.67.5.2552-2558.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Palese P., Tobita K., Ueda M., Compans R. W. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology. 1974 Oct;61(2):397–410. doi: 10.1016/0042-6822(74)90276-1. [DOI] [PubMed] [Google Scholar]
  17. Peiris J. S., Porterfield J. S. Antibody-mediated enhancement of Flavivirus replication in macrophage-like cell lines. Nature. 1979 Nov 29;282(5738):509–511. doi: 10.1038/282509a0. [DOI] [PubMed] [Google Scholar]
  18. Rott R., Becht H., Orlich M. The significance of influenza virus neuraminidase in immunity. J Gen Virol. 1974 Jan;22(1):35–41. doi: 10.1099/0022-1317-22-1-35. [DOI] [PubMed] [Google Scholar]
  19. Schalke B. C., Klinkert W. E., Wekerle H., Dwyer D. S. Enhanced activation of a T cell line specific for acetylcholine receptor (AChR) by using anti-AChR monoclonal antibodies plus receptors. J Immunol. 1985 Jun;134(6):3643–3648. [PubMed] [Google Scholar]
  20. Schulman J. L., Khakpour M., Kilbourne E. D. Protective effects of specific immunity to viral neuraminidase on influenza virus infection of mice. J Virol. 1968 Aug;2(8):778–786. doi: 10.1128/jvi.2.8.778-786.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shulman M., Wilde C. D., Köhler G. A better cell line for making hybridomas secreting specific antibodies. Nature. 1978 Nov 16;276(5685):269–270. doi: 10.1038/276269a0. [DOI] [PubMed] [Google Scholar]
  22. Takeda A., Tuazon C. U., Ennis F. A. Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science. 1988 Oct 28;242(4878):580–583. doi: 10.1126/science.2972065. [DOI] [PubMed] [Google Scholar]
  23. Tamura M., Webster R. G., Ennis F. A. Antibodies to HA and NA augment uptake of influenza A viruses into cells via Fc receptor entry. Virology. 1991 May;182(1):211–219. doi: 10.1016/0042-6822(91)90664-w. [DOI] [PubMed] [Google Scholar]
  24. Tamura M., Webster R. G., Ennis F. A. Neutralization and infection-enhancement epitopes of influenza A virus hemagglutinin. J Immunol. 1993 Aug 1;151(3):1731–1738. [PubMed] [Google Scholar]
  25. Webster R. G., Brown L. E., Laver W. G. Antigenic and biological characterization of influenza virus neuraminidase (N2) with monoclonal antibodies. Virology. 1984 May;135(1):30–42. doi: 10.1016/0042-6822(84)90114-4. [DOI] [PubMed] [Google Scholar]
  26. Webster R. G., Hinshaw V. S., Laver W. G. Selection and analysis of antigenic variants of the neuraminidase of N2 influenza viruses with monoclonal antibodies. Virology. 1982 Feb;117(1):93–104. doi: 10.1016/0042-6822(82)90510-4. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES