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[Preprint]. 2024 May 19:2024.05.18.594815. [Version 1] doi: 10.1101/2024.05.18.594815

Clade-defining mutations in human H1N1 hemagglutinin protein from 2021-2023 have opposing effects on in vitro fitness and antigenic drift

Nicholas J Swanson, Jyothsna Girish, Madeline Yunker, Hisuan Liu, Julie Norton, Christa Han, Heba Mostafa, Katherine Fenstermacher, Richard Eric Rothman, Andrew Pekosz
PMCID: PMC11118561  PMID: 38798637

Abstract

Seasonal influenza viruses frequently acquire mutations that have the potential to alter both virus replication and antigenic profile. Recent seasonal H1N1 viruses have acquired mutations to their hemagglutinin (HA) protein receptor binding site (RBS) and antigenic sites, and have branched into the clades 5a.2a and 5a.2a.1. Both clades demonstrated improved in vitro fitness compared with the parental 5a.2 clade as measured through plaque formation, infectious virus production in human nasal epithelial cells, and receptor binding diversity. Both clades also showed reduced neutralization by serum from healthcare workers vaccinated in the 2022-23 Northern Hemisphere influenza season compared to the vaccine strain. To investigate the phenotypic impact of individual clade-defining mutations, recombinant viruses containing single HA mutations were generated on a 5a.2 genetic background. The 5a.2a mutation Q189E improved plaque formation and virus replication, but was more efficiently neutralized by serum from individuals vaccinated in 2022-23. In contrast, the 5a.2a mutation E224A and both 5a.2a.1 mutations P137S and K142R impaired aspects of in vitro fitness but contributed significantly to antigenic drift. Surprisingly, the E224A mutation and not Q189E caused broader receptor binding diversity seen in clinical isolates of 5a.2a and 5a.2a.1, suggesting that receptor binding diversity alone may not be responsible for the phenotypic effects of the Q189E mutation. These data document an evolutionary trade-off between mutations that improve viral fitness and those that allow for the evasion of existing host immunity.

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