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

doi:10.1128/JVI.74.18.8502-8512.2000

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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 outbreaksin mammals, including humans. To identify early changes in thereceptor binding properties of the avian virus hemagglutinin (HA)after interspecies transmission and to determine the amino acidsubstitutions responsible for these alterations, we studied theHAs 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 causedby the introduction of avian virus HAs into these species. Theviruses were assayed for their ability to bind the synthetic sialylglycopolymers3'SL-PAA and 6'SLN-PAA, which contained, respectively, 3'-sialyllactose(the receptor determinant preferentially recognized by avian influenzaviruses) and 6'-sialyl(N-acetyllactosamine) (the receptor determinantfor human viruses). Avian and seal viruses bound 6'SLN-PAA veryweakly, whereas the earliest available human and swine epidemicviruses bound this polymer with a higher affinity. For the H2and H3 strains, a single mutation, 226Q $right-arrow$ L, increased binding to6'SLN-PAA, while among H1 swine viruses, the 190E $right-arrow$ D and 225G $right-arrow$ Emutations in the HA appeared important for the increased affinityof the viruses for 6'SLN-PAA. Amino acid substitutions at positions190 and 225 with respect to the avian virus consensus sequenceare also present in H1 human viruses, including those that circulatedin 1918, suggesting that substitutions at these positions areimportant for the generation of H1 human pandemic strains. Theseresults show that the receptor-binding specificity of the HA isaltered early after the transmission of an avian virus to humansand pigs and, therefore, may be a prerequisite for the highlyeffective replication and spread which characterize epidemicstrains.

^* 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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