Dissecting immunological mechanisms underlying influenza viral nucleoprotein-induced mucosal immunity against diverse viral strains

Emerg Microbes Infect. 2024 Dec;13(1):2427792. doi: 10.1080/22221751.2024.2427792. Epub 2024 Nov 21.

Abstract

The nucleoprotein (NP) of type A influenza virus (IAV) is highly conserved across all virus strains, making it an attractive candidate antigen for universal vaccines. While various studies have explored NP-induced mucosal immunity, here we interrogated the mechanistic differences between intramuscular (IM) and intranasal (IN) delivery of a recombinant adenovirus carrying NP fused with a bifunctional CD40 ligand. Despite being less effective than IM delivery in inducing systemic cellular immune responses and antibody-dependent cellular cytotoxicity (ADCC), IN immunization elicited superior antigen-specific recall humoral and cellular response in the nasal associated lymphoid tissue (NALT) of the upper respiratory tract, the initial site of immune recognition and elimination of inhaled pathogens. IN vaccination also induced significantly stronger pulmonary T cell responses in the lower respiratory tract than IM vaccination, in particular the CD8 T cells. Moreover, blocking lymphocyte circulation abrogated IM but not IN immunization induced protection, illustrating the critical role of local memory immune response upon viral infection. Notably, the CD40-targeted nasal delivery not only improved the magnitude but also the breadth of protection, including against lethal challenge with a newly isolated highly pathogenic avian H5N1 strain. These findings are informative for the design of universal mucosal vaccines, where the predominant mode of protection is independent of neutralizing antibodies.

Keywords: H5N1; Influenza; intramuscular; intranasal; nucleoprotein; universal vaccine.

MeSH terms

  • Adenoviridae / genetics
  • Adenoviridae / immunology
  • Administration, Intranasal*
  • Animals
  • Antibodies, Viral / immunology
  • CD40 Ligand / genetics
  • CD40 Ligand / immunology
  • CD8-Positive T-Lymphocytes / immunology
  • Female
  • Humans
  • Immunity, Mucosal*
  • Influenza A Virus, H5N1 Subtype / genetics
  • Influenza A Virus, H5N1 Subtype / immunology
  • Influenza A virus / genetics
  • Influenza A virus / immunology
  • Influenza Vaccines* / administration & dosage
  • Influenza Vaccines* / immunology
  • Injections, Intramuscular
  • Mice
  • Mice, Inbred BALB C
  • Nucleocapsid Proteins* / genetics
  • Nucleocapsid Proteins* / immunology
  • Nucleoproteins / genetics
  • Nucleoproteins / immunology
  • Orthomyxoviridae Infections* / immunology
  • Orthomyxoviridae Infections* / prevention & control
  • Orthomyxoviridae Infections* / virology
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / immunology
  • Viral Core Proteins / genetics
  • Viral Core Proteins / immunology

Substances

  • Influenza Vaccines
  • Nucleocapsid Proteins
  • Antibodies, Viral
  • NP protein, Influenza A virus
  • Viral Core Proteins
  • RNA-Binding Proteins
  • CD40 Ligand
  • Nucleoproteins

Grants and funding

This work was supported by Government of Canada: [Grant Number ].