Advertisement
No access
Research Articles

Mapping the Antigenic and Genetic Evolution of Influenza Virus

Science
16 Jul 2004
Vol 305, Issue 5682
pp. 371-376

Abstract

The antigenic evolution of influenza A (H3N2) virus was quantified and visualized from its introduction into humans in 1968 to 2003. Although there was remarkable correspondence between antigenic and genetic evolution, significant differences were observed: Antigenic evolution was more punctuated than genetic evolution, and genetic change sometimes had a disproportionately large antigenic effect. The method readily allows monitoring of antigenic differences among vaccine and circulating strains and thus estimation of the effects of vaccination. Further, this approach offers a route to predicting the relative success of emerging strains, which could be achieved by quantifying the combined effects of population level immune escape and viral fitness on strain evolution.

Get full access to this article

View all available purchase options and get full access to this article.

Supplementary Material

File (papv2.pdf)
File (papv3.pdf)
File (smith.som.rev.pdf)

References and Notes

1
G. K. Hirst, J. Exp. Med.78, 407 (1943).
2
D. D. Richman, T. Wrin, S. J. Little, C. J. Petropoulos, Proc. Natl. Acad. Sci. U.S.A.100, 4144 (2003).
3
D. H. O'Connor et al., Nature Med.8, 493 (2002).
4
A. Lapedes, R. Farber, J. Theor. Biol.212, 57 (2001).
5
K. Stohr, Lancet Infect. Dis.2, 517 (2002).
6
A. W. Hampson, in Influenza, C. W. Potter, Ed. (Elsevier, London, 2002), pp. 49–85.
7
J. E. Salk, P. C. Suriano, Am. J. Public Health39, 345 (1949).
8
E. D. Kilbourne et al., Proc. Natl. Acad. Sci. U.S.A.99, 10748 (2002).
9
Materials and methods are available as supporting material on Science Online. For software, see www.antigenic-cartography.org.
10
R. M. Bush, W. M. Fitch, C. A. Bender, N. J. Cox, Mol. Biol. Evol.16, 1457 (1999).
11
R. M. Bush, C. A. Bender, K. Subbarao, N. J. Cox, W. M. Fitch, Science286, 1921 (1999).
12
J. B. Plotkin, J. Dushoff, S. A. Levin, Proc. Natl. Acad. Sci. U.S.A.99, 6263 (2002).
13
N. M. Ferguson, A. P. Galvani, R. M. Bush, Nature422, 428 (2003).
14
P. H. A. Sneath, R. R. Sokal, Numerical Taxonomy (Freeman, San Francisco, 1973).
15
T. F. Weijers et al., J. Virol. Methods10, 241 (1985).
16
D. J. Alexander et al., Avian Pathol.26, 399 (1997).
17
P. A. Underwood, J. Gen. Virol.62 (Pt. 1), 153 (1982).
18
A. Dekker, G. Wensvoort, C. Terpstra, Vet. Microbiol.47, 317 (1995).
19
J. M. Daly et al., J. Gen. Virol.77 (Pt. 4), 661 (1996).
20
A. S. Perelson, G. F. Oster, J. Theor. Biol.81, 645 (1979).
21
L. Edelstein, R. Rosen, J. Theor. Biol.73, 181 (1978).
22
D. J. Smith, S. Forrest, A. S. Perelson, in Artificial Immune Systems and Their Applications, D. Dasgupta, Ed. (Springer Verlag, Berlin, 1998), pp. 105–114.
23
D. J. Smith, S. Forrest, D. H. Ackley, A. S. Perelson, Proc. Natl. Acad. Sci. U.S.A.96, 14001 (1999).
24
J. Kruskal, Psychometrika29, 115 (1964).
25
R. Shepherd, Hum. Factors5, 33 (1963).
26
Newly sequenced HA1 domain accession numbers: AY660991-AY661211. Previously published HA1 domain accession numbers are in the supporting material.
27
C. A. Macken, H. Lu, J. Goodman, L. Boykin, in Options for the Control of Influenza IV, A. D. M. E. Osterhaus, N. Cox, A. W. Hampson, Eds. (Elsevier Science B.V., Amsterdam, 2001), pp. 103–106.
28
D. C. Wiley, I. A. Wilson, J. J. Skehel, Nature289, 373 (1981).
29
I. A. Wilson, J. J. Skehel, D. C. Wiley, Nature289, 366 (1981).
30
G. W. Both, M. J. Sleigh, N. J. Cox, A. P. Kendal, J. Virol.48, 52 (1983).
31
A. J. Hay, V. Gregory, A. R. Douglas, Y. P. Lin, Philos. Trans. R. Soc. London B. Biol. Sci.356, 1861 (2001).
32
Single-letter abbreviations for the amino acid residues are as follows: I, Ile; K, Lys; N, Asn; and S, Ser.
33
J. R. Gog, B. T. Grenfell, Proc. Natl. Acad. Sci. U.S.A.99, 17209 (2002).
34
J. R. Gog, G. F. Rimmelzwaan, A. D. Osterhaus, B. T. Grenfell, Proc. Natl. Acad. Sci. U.S.A.100, 11143 (2003).
35
B. T. Grenfell et al., Science303, 327 (2004).
36
D. A. Lennette, in Diagnostic Procedures for Viral, Ricketssial and Chlamydial Infections, E. H. Lennette, D. A. Lennette, E. T. Lennette, Eds. (American Public Health Association, Washington, DC, 1995).
37
B. Korber et al., Science288, 1789 (2000).
38
We thank R. van Beek, W. Beyer, T. Bhattacharya, R. Bush, N. Cox, B. Grenfell, J. Gog, H. Gutowitz, A. Hay, R. Hightower, T. Jones, A. Tang, the contributors to the WHO global influenza surveillance network, and the maintainers of the Influenza Sequence Database (www.flu.lanl.gov). We acknowledge the support of the Santa Fe Institute and the Dutch National Institute of Public Health and the Environment (RIVM). D.J.S. was supported by European Union grant QLRT-2001-01034. A.S.L. was supported by the U.S. Department of Energy, contract W-7405-ENG-36, under the Laboratory-Directed Research and Development program. R.A.M.F. is a fellow of the Royal Dutch Academy of Arts and Sciences.

(0)eLetters

eLetters is a forum for ongoing peer review. eLetters are not edited, proofread, or indexed, but they are screened. eLetters should provide substantive and scholarly commentary on the article. Embedded figures cannot be submitted, and we discourage the use of figures within eLetters in general. If a figure is essential, please include a link to the figure within the text of the eLetter. Please read our Terms of Service before submitting an eLetter.

Log In to Submit a Response

No eLetters have been published for this article yet.

Information & Authors

Information

Published In

Science
Volume 305 | Issue 5682
16 July 2004

Article versions

You are viewing the most recent version of this article.

Submission history

Received: 26 February 2004
Accepted: 11 June 2004
Published in print: 16 July 2004

Permissions

Request permissions for this article.

Notes

Supporting Online Material
www.sciencemag.org/cgi/content/full/1097211/DC1
Materials and Methods
Figs. S1 to S3
Table S1
References and Notes

Authors

Affiliations

Derek J. Smith,* [email protected]
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.
National Influenza Center and Department of Virology, Erasmus Medical Center, Dr. Molewaterplein 50, 3015GE Rotterdam, Netherlands.
Alan S. Lapedes*
Theoretical Division, T-13, MS B213, Los Alamos National Laboratory, Los Alamos, NM 87545, USA.
Jan C. de Jong
National Influenza Center and Department of Virology, Erasmus Medical Center, Dr. Molewaterplein 50, 3015GE Rotterdam, Netherlands.
Theo M. Bestebroer
National Influenza Center and Department of Virology, Erasmus Medical Center, Dr. Molewaterplein 50, 3015GE Rotterdam, Netherlands.
Guus F. Rimmelzwaan
National Influenza Center and Department of Virology, Erasmus Medical Center, Dr. Molewaterplein 50, 3015GE Rotterdam, Netherlands.
Albert D. M. E. Osterhaus
National Influenza Center and Department of Virology, Erasmus Medical Center, Dr. Molewaterplein 50, 3015GE Rotterdam, Netherlands.
Ron A. M. Fouchier*
National Influenza Center and Department of Virology, Erasmus Medical Center, Dr. Molewaterplein 50, 3015GE Rotterdam, Netherlands.

Notes

To whom correspondence should be addressed. E-mail: [email protected]

Metrics & Citations

Metrics

Article Usage

Altmetrics

Citations

Cite as

Export citation

Select the format you want to export the citation of this publication.

Cited by

  1. Comparative analysis of SARS-CoV-2 neutralization titers reveals consistency between human and animal model serum and across assays, Science Translational Medicine, 16, 747, (2024)./doi/10.1126/scitranslmed.adl1722
    Abstract
  2. Antigenic distance between primary and secondary dengue infections correlates with disease risk, Science Translational Medicine, 16, 744, (2024)./doi/10.1126/scitranslmed.adk3259
    Abstract
  3. Hierarchical sequence-affinity landscapes shape the evolution of breadth in an anti-influenza receptor binding site antibody, eLife, 12, (2023).https://doi.org/10.7554/eLife.83628
    Crossref
  4. Characterization of Influenza A(H1N1)pdm09 Viruses Isolated in the 2018–2019 and 2019–2020 Influenza Seasons in Japan, Viruses, 15, 2, (535), (2023).https://doi.org/10.3390/v15020535
    Crossref
  5. Mapping the Antibody Repertoires in Ferrets with Repeated Influenza A/H3 Infections: Is Original Antigenic Sin Really “Sinful”?, Viruses, 15, 2, (374), (2023).https://doi.org/10.3390/v15020374
    Crossref
  6. Electrostatic Surface Potential as a Key Parameter in Virus Transmission and Evolution: How to Manage Future Virus Pandemics in the Post-COVID-19 Era, Viruses, 15, 2, (284), (2023).https://doi.org/10.3390/v15020284
    Crossref
  7. First Impressions Matter: Immune Imprinting and Antibody Cross-Reactivity in Influenza and SARS-CoV-2, Pathogens, 12, 2, (169), (2023).https://doi.org/10.3390/pathogens12020169
    Crossref
  8. Genetic, Antigenic, and Pathobiological Characterization of H9 and H6 Low Pathogenicity Avian Influenza Viruses Isolated in Vietnam from 2014 to 2018, Microorganisms, 11, 2, (244), (2023).https://doi.org/10.3390/microorganisms11020244
    Crossref
  9. Convergent Evolution in SARS-CoV-2 Spike Creates a Variant Soup from Which New COVID-19 Waves Emerge, International Journal of Molecular Sciences, 24, 3, (2264), (2023).https://doi.org/10.3390/ijms24032264
    Crossref
  10. Rise of the BQ.1.1.37 SARS-CoV-2 Sublineage, Italy, Diagnostics, 13, 5, (1000), (2023).https://doi.org/10.3390/diagnostics13051000
    Crossref
  11. See more
Loading...

View Options

Check Access

Log in to view the full text

AAAS ID LOGIN

AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.

Log in via OpenAthens.
Log in via Shibboleth.

More options

Purchase digital access to this article

Download and print this article for your personal scholarly, research, and educational use.

Purchase this issue in print

Buy a single issue of Science for just $15 USD.

View options

PDF format

Download this article as a PDF file

Download PDF

Full Text

FULL TEXT

Media

Figures

Multimedia

Tables

Share

Share

Share article link

Share on social media