IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis

J Immunol. 2000 Jun 15;164(12):6406-16. doi: 10.4049/jimmunol.164.12.6406.

Abstract

To dissect the controversial roles of type 1 and type 2 cytokines to the pathogenesis of schistosomiasis, we generated IL-10/IL-4- and IL-10/IL-12-deficient mice that develop highly polarized type 1 and type 2 cytokine responses, respectively. Interestingly, the Th1-polarized IL-10/IL-4-deficient mice rapidly lost weight at the onset of egg-laying and displayed 100% mortality by wk 9 postinfection. This acute mortality was linked to overexpression of the proinflammatory mediators IFN-gamma, TNF-alpha, and inducible NO and the formation of nonfibrotic granulomas. Elevated serum aspartate transaminase levels confirmed that mortality was in part attributable to acute hepatotoxicity. In contrast, the Th2-polarized IL-10/IL-12-deficient mice developed a progressive wasting disease that correlated with increased hepatic fibrosis, formation of large eosinophil-rich granulomas, a 10-fold increase in IL-4 and IL-13, and significant mortality during the chronic stages of infection. Surprisingly, IL-10-deficient mice displayed pathological features that were characteristic of both extremes, while wild-type mice developed relatively successful long term chronic infections. These data demonstrate that IL-10 significantly suppresses type 1 and type 2 cytokine development in IL-4- and IL-12-deficient mice, respectively, thereby impeding the development of severe egg-induced pathology in the single cytokine-deficient animals. Together, these findings reveal the central regulatory role of IL-10 in the pathogenesis of schistosomiasis and illustrate that excessive type 1 and type 2 cytokine responses trigger distinct, but equally detrimental, forms of pathology following infection.

MeSH terms

  • Animals
  • Chronic Disease
  • Eosinophilia / immunology
  • Eosinophilia / pathology
  • Fibroblasts / immunology
  • Fibroblasts / pathology
  • Interferon-gamma / blood
  • Interleukin-10 / deficiency
  • Interleukin-10 / genetics
  • Interleukin-10 / physiology*
  • Interleukin-12 / physiology
  • Interleukin-4 / deficiency
  • Interleukin-4 / genetics
  • Interleukin-4 / physiology
  • Liver Cirrhosis, Experimental / immunology
  • Liver Cirrhosis, Experimental / pathology
  • Liver Diseases, Parasitic / immunology
  • Liver Diseases, Parasitic / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nitric Oxide / biosynthesis
  • Ovum / immunology
  • Schistosomiasis mansoni / immunology*
  • Schistosomiasis mansoni / metabolism
  • Schistosomiasis mansoni / mortality
  • Schistosomiasis mansoni / pathology*
  • Th1 Cells / immunology*
  • Th1 Cells / metabolism*
  • Th1 Cells / pathology
  • Th2 Cells / immunology*
  • Th2 Cells / metabolism*
  • Th2 Cells / pathology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Interleukin-12
  • Interleukin-4
  • Nitric Oxide
  • Interferon-gamma