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Journal of Virology, September 2000, p. 8502-8512, Vol. 74, No. 18
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Early Alterations of the Receptor-Binding Properties of H1, H2, and H3 Avian Influenza Virus Hemagglutinins after Their Introduction into Mammals

Mikhail Matrosovich,1,2,* Alexander Tuzikov,3 Nikolai Bovin,3 Alexandra Gambaryan,2 Alexander Klimov,4 Maria R. Castrucci,5 Isabella Donatelli,5 and Yoshihiro Kawaoka1,6,7

Department of Virology and Molecular Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 381051; M. P. Chumakov Institute of Poliomyelitis and Viral Encephalitides, 142 782 Moscow,2 and Shemyakin Institute of Bioorganic Chemistry, 117871 Moscow,3 Russia; Influenza Branch, Centers for Disease Control and Prevention, Atlanta, Georgia 303334; Department of Virology and WHO National Influenza Centre, Instituto Superiore di Sanita, Rome 00161, Italy5; Department of Pathology, University of Tennessee at Memphis, Memphis, Tennessee 381636; and Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, Wisconsin 537067

Received 24 February 2000/Accepted 20 June 2000

Interspecies transmission of influenza A viruses circulating in wild aquatic birds occasionally results in influenza outbreaks in mammals, including humans. To identify early changes in the receptor binding properties of the avian virus hemagglutinin (HA) after interspecies transmission and to determine the amino acid substitutions responsible for these alterations, we studied the HAs of the initial isolates from the human pandemics of 1957 (H2N2) and 1968 (H3N2), the European swine epizootic of 1979 (H1N1), and the seal epizootic of 1992 (H3N3), all of which were caused by the introduction of avian virus HAs into these species. The viruses were assayed for their ability to bind the synthetic sialylglycopolymers 3'SL-PAA and 6'SLN-PAA, which contained, respectively, 3'-sialyllactose (the receptor determinant preferentially recognized by avian influenza viruses) and 6'-sialyl(N-acetyllactosamine) (the receptor determinant for human viruses). Avian and seal viruses bound 6'SLN-PAA very weakly, whereas the earliest available human and swine epidemic viruses bound this polymer with a higher affinity. For the H2 and H3 strains, a single mutation, 226Qright-arrowL, increased binding to 6'SLN-PAA, while among H1 swine viruses, the 190Eright-arrowD and 225Gright-arrowE mutations in the HA appeared important for the increased affinity of the viruses for 6'SLN-PAA. Amino acid substitutions at positions 190 and 225 with respect to the avian virus consensus sequence are also present in H1 human viruses, including those that circulated in 1918, suggesting that substitutions at these positions are important for the generation of H1 human pandemic strains. These results show that the receptor-binding specificity of the HA is altered early after the transmission of an avian virus to humans and pigs and, therefore, may be a prerequisite for the highly effective replication and spread which characterize epidemic strains.

* Corresponding author. Mailing address: Department of Virology and Molecular Biology, St. Jude Children's Research Hospital, 332 North Lauderdale, Memphis, TN 38105-2794. Phone: (901) 495-3412. Fax: (901) 523-2622. E-mail: Mikhail.Matrosovich{at}stjude.org.

Journal of Virology, September 2000, p. 8502-8512, Vol. 74, No. 18
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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