Mucosal adjuvanticity and mucosal booster effect of colibactin-depleted probiotic Escherichia coli membrane vesicles

Hum Vaccin Immunother. 2024 Dec 31;20(1):2337987. doi: 10.1080/21645515.2024.2337987. Epub 2024 Apr 24.

Abstract

There is a growing interest in development of novel vaccines against respiratory tract infections, due to COVID-19 pandemic. Here, we examined mucosal adjuvanticity and the mucosal booster effect of membrane vesicles (MVs) of a novel probiotic E. coli derivative lacking both flagella and potentially carcinogenic colibactin (ΔflhDΔclbP). ΔflhDΔclbP-derived MVs showed rather strong mucosal adjuvanticity as compared to those of a single flagellar mutant strain (ΔflhD-MVs). In addition, glycoengineered ΔflhDΔclbP-MVs displaying serotype-14 pneumococcal capsular polysaccharide (CPS14+MVs) were well-characterized based on biological and physicochemical parameters. Subcutaneous (SC) and intranasal (IN) booster effects of CPS14+MVs on systemic and mucosal immunity were evaluated in mice that have already been subcutaneously prime-immunized with the same MVs. With a two-dose regimen, an IN boost (SC-IN) elicited stronger IgA responses than homologous prime-boost immunization (SC-SC). With a three-dose regimen, serum IgG levels were comparable among all tested regimens. Homologous immunization (SC-SC-SC) elicited the highest IgM responses among all regimens tested, whereas SC-SC-SC failed to elicit IgA responses in blood and saliva. Furthermore, serum IgA and salivary SIgA levels were increased with an increased number of IN doses administrated. Notably, SC-IN-IN induced not only robust IgG response, but also the highest IgA response in both serum and saliva among the groups. The present findings suggest the potential of a heterologous three-dose administration for building both systemic and mucosal immunity, e.g. an SC-IN-IN vaccine regimen could be beneficial. Another important observation was abundant packaging of colibactin in MVs, suggesting increased applicability of ΔflhDΔclbP-MVs in the context of vaccine safety.

Keywords: Administration route; Streptococcus pneumoniae; capsular polysaccharide; heterologous prime-boost immunization; immunogenicity; membrane vesicles; mucosal adjuvanticity; probiotic Escherichia coli; respiratory tract infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic* / administration & dosage
  • Administration, Intranasal
  • Animals
  • COVID-19 Vaccines / administration & dosage
  • COVID-19 Vaccines / immunology
  • Escherichia coli* / immunology
  • Female
  • Immunity, Mucosal*
  • Immunization, Secondary* / methods
  • Immunoglobulin A
  • Immunoglobulin G / blood
  • Immunoglobulin M
  • Mice
  • Mice, Inbred BALB C*
  • Peptides / immunology
  • Polyketides*
  • Probiotics* / administration & dosage

Substances

  • colibactin
  • Adjuvants, Immunologic
  • Polyketides
  • Immunoglobulin A
  • Peptides
  • Immunoglobulin G
  • Immunoglobulin M
  • COVID-19 Vaccines

Grants and funding

This work was supported by grants from KAKENHI of the Japan Society for the Promotion of Science (JSPS) [nos. 19K22644, 20K09943, 21KK0164, and 21K18284] and Ministry of Education, Culture, Sports, Science and Technology (MEXT) [no. 20H03861].