Lack of endogenous IL-10 enhances production of proinflammatory cytokines and leads to Brucella abortus clearance in mice

PLoS One. 2013 Sep 17;8(9):e74729. doi: 10.1371/journal.pone.0074729. eCollection 2013.

Abstract

IL-10 is a cytokine that regulates the balance between pathogen clearance and immunopathology. Brucella abortus is an intracellular bacterium that causes chronic disease in humans and domestic animals. Here we evaluated the contribution of IL-10 in host immune response and pathology during B. abortus infection. To assess the role of IL-10 in vivo, IL-10 knockout (KO) or 129 Sv/Ev (wild-type) mice were infected with B. abortus and the number of viable bacteria from the spleen was determined at 1, 2, 3, 6 and 14-weeks postinfection. IL-10 KO mice showed reduced bacterial loads in the spleen when compared to wild-type mice during all time points studied. Additionally, at 14-weeks postinfection IL-10 KO mice had totally cleared the infection. This clearance was preceded by an enhanced IFN-γ, TNF-α and IL-17 responses in both the serum and the spleen of IL-10 KO mice. Additionally, dendritic cells from infected IL-10 KO mice produced elevated levels of IL-12 and TNF-α compared to wild-type animals. Histopathology analysis was performed and both KO and wild-type mice developed multifocal granulomas and necrosis in the liver. However, at six-weeks postinfection reduced numbers of granulomas was detected in IL-10 KO mice compared to wild-type animals. This reduced liver pathology at later stage of infection was accompanied by increased numbers of CD4+CD25+foxp3+ T cells and expression of TGF-β in IL-10 KO splenocytes. Taken together, our findings demonstrate that IL-10 modulates the proinflammatory immune response to B. abortus infection and the lack of IL-10 increases resistance to Brucella infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Load
  • Brucella abortus / immunology*
  • Brucellosis / genetics
  • Brucellosis / immunology*
  • Brucellosis / metabolism*
  • Brucellosis / microbiology
  • Cytokines / biosynthesis
  • Cytokines / metabolism*
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Dendritic Cells / microbiology
  • Gene Expression
  • Granuloma / genetics
  • Inflammation Mediators / metabolism*
  • Interleukin-10 / deficiency
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism*
  • Liver / metabolism
  • Liver / microbiology
  • Liver / pathology
  • Mice
  • Mice, Knockout
  • Spleen / cytology
  • Spleen / immunology
  • Spleen / metabolism
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Cytokines
  • Inflammation Mediators
  • Transforming Growth Factor beta1
  • Interleukin-10

Grants and funding

This work was supported by grants from CNPq, CNPq/CONICET, FAPEMIG, FAPEMIG/CNPq (PRONEX), CAPES/PNPD, CNPq/MAPA, CNPq/REPENSA and INCT-Vacinas. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.