Aerobic Glycolysis Controls Myeloid-Derived Suppressor Cells and Tumor Immunity via a Specific CEBPB Isoform in Triple-Negative Breast Cancer

Cell Metab. 2018 Jul 3;28(1):87-103.e6. doi: 10.1016/j.cmet.2018.04.022. Epub 2018 May 24.

Abstract

Myeloid-derived suppressor cells (MDSCs) inhibit anti-tumor immunity. Aerobic glycolysis is a hallmark of cancer. However, the link between MDSCs and glycolysis is unknown in patients with triple-negative breast cancer (TNBC). Here, we detect abundant glycolytic activities in human TNBC. In two TNBC mouse models, 4T1 and Py8119, glycolysis restriction inhibits tumor granulocyte colony-stimulating factor (G-CSF) and granulocyte macrophage colony-stimulating factor (GM-CSF) expression and reduces MDSCs. These are accompanied with enhanced T cell immunity, reduced tumor growth and metastasis, and prolonged mouse survival. Mechanistically, glycolysis restriction represses the expression of a specific CCAAT/enhancer-binding protein beta (CEBPB) isoform, liver-enriched activator protein (LAP), via the AMP-activated protein kinase (AMPK)-ULK1 and autophagy pathways, whereas LAP controls G-CSF and GM-CSF expression to support MDSC development. Glycolytic signatures that include lactate dehydrogenase A correlate with high MDSCs and low T cells, and are associated with poor human TNBC outcome. Collectively, tumor glycolysis orchestrates a molecular network of the AMPK-ULK1, autophagy, and CEBPB pathways to affect MDSCs and maintain tumor immunosuppression.

Keywords: CEBPB; G-CSF; GM-CSF; LDHA; autophagy; breast cancer; glycolysis; immunotherapy; myeloid-derived suppressor cell; tumor immunity.

MeSH terms

  • Animals
  • CCAAT-Enhancer-Binding Protein-beta / metabolism*
  • Cell Line, Tumor
  • Disease Models, Animal
  • Female
  • Glycolysis*
  • Granulocyte Colony-Stimulating Factor / metabolism*
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism*
  • Humans
  • Immune Tolerance*
  • Mice
  • Myeloid-Derived Suppressor Cells / immunology*
  • Triple Negative Breast Neoplasms / immunology*

Substances

  • CCAAT-Enhancer-Binding Protein-beta
  • CEBPB protein, human
  • Cebpb protein, mouse
  • Granulocyte Colony-Stimulating Factor
  • Granulocyte-Macrophage Colony-Stimulating Factor