Mucosally delivered Salmonella typhi expressing the Yersinia pestis F1 antigen elicits mucosal and systemic immunity early in life and primes the neonatal immune system for a vigorous anamnestic response to parenteral F1 boost

J Immunol. 2009 Jan 15;182(2):1211-22. doi: 10.4049/jimmunol.182.2.1211.

Abstract

Neonates respond poorly to conventional vaccines. This has been attributed, in part, to the immaturity of neonatal dendritic cells that lack full capacity for Ag presentation and T cell stimulation. We engineered an attenuated Salmonella Typhi strain to express and export the F1 Ag of Y. pestis (S. Typhi(F1)) and investigated its immunogenicity early in life using a heterologous prime-boost regimen. Newborn mice primed intranasally with a single dose of S. Typhi(F1) elicited mucosal Ab- and IFN-gamma-secreting cells 1 wk after immunization. They also developed a potent and fast anamnestic response to a subsequent parenteral boost with F1-alum, which surpassed those of mice primed and boosted with S. Typhi(F1) or F1-alum. Neonatal priming with S. Typhi(F1), as opposed to priming with F1-alum, resulted in a more balanced IgG2a/IgG1 profile, enhanced avidity maturation and stimulation of B memory cells, and strong Th1-type cell-mediated immunity. S. Typhi(F1) enhanced the activation and maturation of neonatal CD11c+ dendritic cells, shown by increased expression of CD80, CD86, CD40, and MHC-II cell surface markers and production of proinflammatory cytokines IL-12, TNF-alpha, IL-6, and MCP-1. S. Typhi(F1)-stimulated neonatal DC had improved capacity for Ag presentation and T cell stimulation in vitro and induced F1-specific CD4+ and CD8+ T cell responses when adoptively transferred to newborn mice. Mucosal immunization with S. Typhi expressing a foreign Ag effectively primes the neonatal immune system for potent, fast, and broader responses to a parenteral Ag boost. Such a strategy can prevent infectious diseases, including those considered biowarfare threats, early in life.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Administration, Intranasal
  • Animals
  • Animals, Newborn / immunology*
  • Antibodies, Bacterial / metabolism
  • Antibody Affinity / genetics
  • Antigens, Bacterial / administration & dosage
  • Antigens, Bacterial / genetics*
  • Antigens, Bacterial / immunology
  • Bacterial Capsules / biosynthesis
  • Bacterial Capsules / genetics
  • Bacterial Proteins / administration & dosage
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / immunology
  • Crosses, Genetic
  • Genetic Vectors / administration & dosage
  • Genetic Vectors / immunology
  • Immunity, Active / genetics
  • Immunity, Mucosal / genetics
  • Immunization, Secondary*
  • Immunologic Memory* / genetics
  • Mice
  • Mice, Inbred BALB C
  • Nasal Mucosa / immunology*
  • Nasal Mucosa / microbiology
  • Salmonella Vaccines / administration & dosage
  • Salmonella Vaccines / genetics
  • Salmonella Vaccines / immunology*
  • Salmonella typhi / genetics
  • Salmonella typhi / immunology*
  • Vaccines, Attenuated / administration & dosage
  • Vaccines, Attenuated / genetics
  • Vaccines, Attenuated / immunology
  • Vaccines, Synthetic / administration & dosage
  • Vaccines, Synthetic / genetics
  • Vaccines, Synthetic / immunology

Substances

  • Antibodies, Bacterial
  • Antigens, Bacterial
  • Bacterial Proteins
  • Salmonella Vaccines
  • Vaccines, Attenuated
  • Vaccines, Synthetic
  • caf1 protein, Yersinia pestis