Enhanced protective efficacy against Mycobacterium tuberculosis afforded by BCG prime-DNA boost regimen in an early challenge mouse model is associated with increased splenic interleukin-2-producing CD4 T-cell frequency post-vaccination

Immunology. 2014 Dec;143(4):661-9. doi: 10.1111/imm.12348.

Abstract

The development of improved vaccines and vaccination strategies against Mycobacterium tuberculosis has been hindered by a limited understanding of the immune correlates of anti-tuberculosis protective immunity. Simple measurement of interferon-γ frequency or production per se does not provide adequate prediction of immune protection. In this study, we examined the relationship between T-cell immune responses and protective efficacy conferred by the heterologous vaccination strategy, bacillus Calmette-Guérin (BCG) prime-Ag85A DNA boost (B/D), in an early challenge mouse model of pulmonary tuberculosis. The results demonstrated that mice vaccinated with the B/D regimen had a significantly reduced bacillary load compared with BCG-vaccinated mice, and the reduction in colony-forming units was associated with decreased pathology and lower levels of inflammatory cytokines in the infected lungs. Further analysis of immunogenicity showed that the superior protection afforded by the B/D regimen was associated with significantly increased frequency of splenic interleukin-2 (IL-2) -producing CD4 T cells and increased IL-2 production when measured as integrated mean fluorescence intensity post-vaccination as well. These data suggest that measurement of elevated frequency of IL-2-producing CD4 T cells or IL-2 production in the spleens of vaccinated mice can predict vaccine efficacy, at least in the B/D strategy, and add to the accumulating body of evidence suggesting that BCG prime-boost strategies may be a useful approach to the control of M. tuberculosis infection.

Keywords: DNA vaccine; Mycobacterium tuberculosis; interleukin-2; multifunctional T cell; prime-boost; protective immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • BCG Vaccine / immunology*
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • Cytokines / metabolism
  • Disease Models, Animal
  • Female
  • Immunization, Secondary
  • Inflammation Mediators / metabolism
  • Interleukin-2 / biosynthesis*
  • Lung / immunology
  • Lung / metabolism
  • Lung / microbiology
  • Lung / pathology
  • Lymphocyte Count
  • Mice
  • Mycobacterium tuberculosis / immunology*
  • Spleen / immunology*
  • Spleen / metabolism
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Tuberculosis / immunology*
  • Tuberculosis / metabolism*
  • Tuberculosis / prevention & control
  • Vaccination

Substances

  • BCG Vaccine
  • Cytokines
  • Inflammation Mediators
  • Interleukin-2