H5N1 influenza binding and cell entry via human class II MHC, and blocking by cross-reactive antibodies.

Taylor Pursell Artem Mikelov Oliver F Wirz Jordan T Ort Shuk Hang Li Reilly K Atkinson Jefferson J S Santos Jiabao Zhong Shilpa A Joshi Jumana Afaghani Xiaorui Han Emily Haraguchi Ramona A Hoh Ji-Yeun Lee Brandon Lam Alexander Stanford Andrew T DeLaitsch Jackson Schuetz Katharina Röltgen Donna Smith Brian Ha Sean Van Slyck Claus U Niemann Scott E Hensley Scott D Boyd

Abstract

Highly pathogenic avian influenza (HPAI) H5N1 clade 2.3.4.4b viruses are currently responsible for a multi-species outbreak affecting wild birds, poultry, numerous mammalian species, and humans. Influenza A viruses typically initiate infection through binding to sialic acid, although select bat and human influenza viruses can also exploit class II major histocompatibility complex (MHC-II) molecules for cell entry. Here we show that emerging H5N1 clade 2.3.4.4b viruses, but not historical H5 lineages, bind human MHC-II HLA-DR and mediate sialic acid-independent cell entry. Hemagglutinin binding to primary human immune cells varies with MHC-II expression and is further shaped by HLA-DR allelic variation, identifying host genetic determinants that may influence susceptibility to infection. Mammalian-adaptive substitutions within the hemagglutinin sialic acid receptor-binding domain reduce MHC-II binding, suggesting this interaction is remodeled during clade 2.3.4.4b H5 adaptation to a human host. Lastly, cross-reactive monoclonal antibodies isolated from clade 2.3.4.4b H5-naive humans can block the hemagglutinin-MHC-II interaction. These findings identify a previously unrecognized receptor pathway in contemporary H5N1 viruses and reveal that both human genetic variation and pre-existing humoral immunity can modulate this interaction, with implications for host range, cellular tropism, spillover risk, and therapeutic intervention.

Supporting text Virus Host Location

Evidence records

5 total
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE11941
Key finding

HPAI H5N1 clade 2.3.4.4b is reported as causing a multi-species outbreak affecting wild birds, poultry, multiple mammalian species, and humans.

Virus
Host
Natural host
Location
Not specified
Supporting text

Highly pathogenic avian influenza (HPAI) H5N1 clade 2.3.4.4b viruses are currently responsible for a multi-species outbreak affecting wild birds, poultry, numerous mammalian species, and humans.

Transmission direction
unknown
Outbreak time
currently
Outbreak scale
multi-species outbreak
Experimental Infection
1 records · 1 evidence types
Evidence type
1 records
OVE11939
Key finding

H5N1 clade 2.3.4.4b hemagglutinin binds human MHC-II (HLA-DR) and enables sialic acid–independent entry, with binding to primary human immune cells varying by MHC-II expression and HLA-DR allele.

Virus
Host
Experimental system Experimental system
Location
Not specified
Supporting text

Here we show that emerging H5N1 clade 2.3.4.4b viruses, but not historical H5 lineages, bind human MHC-II HLA-DR and mediate sialic acid-independent cell entry. Hemagglutinin binding to primary human immune cells varies with MHC-II expression and is further shaped by HLA-DR allelic variation.

Method
hemagglutinin binding assays | cell entry assays (sialic acid–independent entry) | receptor-binding studies to human MHC-II HLA-DR | allelic variation analysis of HLA-DR
Experimental system
cell-entry and binding assays using primary human immune cells and MHC-II (HLA-DR) receptor systems
Functional Mechanism
3 records · 2 evidence types
Evidence type
2 records
OVE11937
Key finding

Emerging H5N1 clade 2.3.4.4b binds human MHC-II HLA-DR and can mediate sialic acid–independent cell entry, unlike historical H5 lineages.

Virus
Host
Location
Not specified
Supporting text

Here we show that emerging H5N1 clade 2.3.4.4b viruses, but not historical H5 lineages, bind human MHC-II HLA-DR and mediate sialic acid-independent cell entry.

Method
receptor binding assay | cell entry assay demonstrating sialic acid-independent entry
Receptors
human MHC-II HLA-DR
OVE11938
Key finding

Cross-reactive monoclonal antibodies from H5-naive humans block the hemagglutinin–MHC-II interaction of clade 2.3.4.4b H5.

Virus
Host
Location
Not specified
Supporting text

Lastly, cross-reactive monoclonal antibodies isolated from clade 2.3.4.4b H5-naive humans can block the hemagglutinin-MHC-II interaction.

Method
antibody blocking assay of hemagglutinin–MHC-II interaction
Receptors
MHC-II
Host factors
cross-reactive monoclonal antibodies
Evidence type
1 records
OVE11940
Key finding

Mammalian-adaptive substitutions in the H5 hemagglutinin sialic acid receptor-binding domain reduce binding to human MHC-II, indicating remodeling of this interaction during adaptation to humans.

Virus
Host
Not specified
Location
Not specified
Supporting text

Mammalian-adaptive substitutions within the hemagglutinin sialic acid receptor-binding domain reduce MHC-II binding, suggesting this interaction is remodeled during clade 2.3.4.4b H5 adaptation to a human host.

Genes or proteins
hemagglutinin | MHC-II
Receptors
MHC-II
Mechanism types
receptor binding | host entry