Contact-dependent depletion of hydrogen peroxide by catalase is a novel mechanism of myeloid-derived suppressor cell induction operating in human hepatic stellate cells

J Immunol. 2015 Mar 15;194(6):2578-86. doi: 10.4049/jimmunol.1401046. Epub 2015 Feb 9.

Abstract

Myeloid-derived suppressor cells (MDSC) represent a unique cell population with distinct immunosuppressive properties that have been demonstrated to shape the outcome of malignant diseases. Recently, human hepatic stellate cells (HSC) have been reported to induce monocytic-MDSC from mature CD14(+) monocytes in a contact-dependent manner. We now report a novel and unexpected mechanism by which CD14(+)HLADR(low/-) suppressive cells are induced by catalase-mediated depletion of hydrogen peroxide (H2O2). Incubation of CD14(+) monocytes with catalase led to a significant induction of functional MDSC compared with media alone, and H2O2 levels inversely correlated with MDSC frequency (r = -0.6555, p < 0.05). Catalase was detected in primary HSC and a stromal cell line, and addition of the competitive catalase inhibitor hydroxylamine resulted in a dose-dependent impairment of MDSC induction and concomitant increase of H2O2 levels. The NADPH-oxidase subunit gp91 was significantly increased in catalase-induced MDSC as determined by quantitative PCR outlining the importance of oxidative burst for the induction of MDSC. These findings represent a so far unrecognized link between immunosuppression by MDSC and metabolism. Moreover, this mechanism potentially explains how stromal cells can induce a favorable immunological microenvironment in the context of tissue oxidative stress such as occurs during cancer therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blotting, Western
  • Catalase / antagonists & inhibitors
  • Catalase / immunology*
  • Catalase / metabolism
  • Cell Communication / immunology
  • Cell Line
  • Cell Line, Tumor
  • Cells, Cultured
  • Coculture Techniques
  • Dose-Response Relationship, Drug
  • Flow Cytometry
  • HLA-DR Antigens / genetics
  • HLA-DR Antigens / immunology
  • HLA-DR Antigens / metabolism
  • Hepatic Stellate Cells / drug effects
  • Hepatic Stellate Cells / immunology*
  • Hepatic Stellate Cells / metabolism
  • Humans
  • Hydrogen Peroxide / immunology*
  • Hydrogen Peroxide / metabolism
  • Hydroxylamine / pharmacology
  • Lipopolysaccharide Receptors / genetics
  • Lipopolysaccharide Receptors / immunology
  • Lipopolysaccharide Receptors / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology
  • Membrane Glycoproteins / metabolism
  • Monocytes / immunology
  • Monocytes / metabolism
  • Myeloid Cells / immunology*
  • Myeloid Cells / metabolism
  • NADPH Oxidase 2
  • NADPH Oxidases / genetics
  • NADPH Oxidases / immunology
  • NADPH Oxidases / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • HLA-DR Antigens
  • Lipopolysaccharide Receptors
  • Membrane Glycoproteins
  • Hydroxylamine
  • Hydrogen Peroxide
  • Catalase
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidases