CD4+ T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism

J Immunol. 2003 Feb 15;170(4):1958-63. doi: 10.4049/jimmunol.170.4.1958.

Abstract

Abscess formation associated with intra-abdominal sepsis causes severe morbidity and can be fatal. Previous studies have implicated T cells in the pathogenesis of abscess formation, and we have recently shown that CD4(+) T cells activated in vitro by zwitterionic capsular polysaccharides from abscess-inducing bacteria such as Staphylococcus aureus and Bacteroides fragilis initiate this host response when transferred to naive rats. In this study, we show that mice deficient in alphabetaTCR-bearing T cells or CD4(+) T cells fail to develop abscesses following challenge with B. fragilis or abscess-inducing zwitterionic polysaccharides, compared with CD8(-/-) or wild-type animals. Transfer of CD4(+) T cells from wild-type mice to alphabetaTCR(-/-) animals reconstituted this ability. The induction of abscesses required T cell costimulation via the CD28-B7 pathway, and T cell transfer experiments with STAT4(-/-) and STAT6(-/-) mice demonstrated that this host response is dependent on STAT4 signaling. Significantly higher levels of IL-17, a proinflammatory cytokine produced almost exclusively by activated CD4(+) T cells, were associated with abscess formation in Th2-impaired (STAT6(-/-)) mice, while STAT4(-/-) mice had significantly lower levels of this cytokine than control animals. The formation of abscesses was preceded by an increase in the number of activated CD4(+) T cells in the peritoneal cavity 24 h following bacterial challenge. Confocal laser-scanning microscopy analysis revealed that CD4(+) T cells comprise the abscess wall in these animals and produce IL-17 at this site. Administration of a neutralizing Ab specific for IL-17 prevented abscess formation following bacterial challenge in mice. These data delineate the specific T cell response necessary for the development of intra-abdominal abscesses and underscore the role of IL-17 in this disease process.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Abdominal Abscess / genetics
  • Abdominal Abscess / immunology*
  • Abdominal Abscess / pathology
  • Abdominal Abscess / prevention & control
  • Animals
  • Antigens, CD / physiology
  • B7-1 Antigen / physiology
  • B7-2 Antigen
  • Bacteroides Infections / genetics
  • Bacteroides Infections / immunology
  • Bacteroides Infections / pathology
  • Bacteroides Infections / prevention & control
  • Bacteroides fragilis / immunology
  • CD28 Antigens / genetics
  • CD28 Antigens / physiology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • Cell Movement / genetics
  • Cell Movement / immunology
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology
  • Immune Sera / administration & dosage
  • Immunity, Cellular / genetics
  • Immunophenotyping
  • Interleukin-17 / antagonists & inhibitors
  • Interleukin-17 / biosynthesis
  • Interleukin-17 / immunology
  • Interleukin-17 / physiology*
  • Kinetics
  • Membrane Glycoproteins / physiology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Peritoneal Cavity / microbiology
  • Peritoneal Cavity / pathology
  • STAT4 Transcription Factor
  • STAT6 Transcription Factor
  • Sepsis / genetics
  • Sepsis / immunology*
  • Sepsis / pathology
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Trans-Activators / deficiency
  • Trans-Activators / genetics
  • Trans-Activators / physiology

Substances

  • Antigens, CD
  • B7-1 Antigen
  • B7-2 Antigen
  • CD28 Antigens
  • Cd86 protein, mouse
  • DNA-Binding Proteins
  • Immune Sera
  • Interleukin-17
  • Membrane Glycoproteins
  • STAT4 Transcription Factor
  • STAT6 Transcription Factor
  • Stat4 protein, mouse
  • Stat6 protein, mouse
  • Trans-Activators