Macrophage-Derived IL1β and TNFα Regulate Arginine Metabolism in Neuroblastoma

Cancer Res. 2019 Feb 1;79(3):611-624. doi: 10.1158/0008-5472.CAN-18-2139. Epub 2018 Dec 13.

Abstract

Neuroblastoma is the most common childhood solid tumor, yet the prognosis for high-risk disease remains poor. We demonstrate here that arginase 2 (ARG2) drives neuroblastoma cell proliferation via regulation of arginine metabolism. Targeting arginine metabolism, either by blocking cationic amino acid transporter 1 (CAT-1)-dependent arginine uptake in vitro or therapeutic depletion of arginine by pegylated recombinant arginase BCT-100, significantly delayed tumor development and prolonged murine survival. Tumor cells polarized infiltrating monocytes to an M1-macrophage phenotype, which released IL1β and TNFα in a RAC-alpha serine/threonine-protein kinase (AKT)-dependent manner. IL1β and TNFα established a feedback loop to upregulate ARG2 expression via p38 and extracellular regulated kinases 1/2 (ERK1/2) signaling in neuroblastoma and neural crest-derived cells. Proteomic analysis revealed that enrichment of IL1β and TNFα in stage IV human tumor microenvironments was associated with a worse prognosis. These data thus describe an immune-metabolic regulatory loop between tumor cells and infiltrating myeloid cells regulating ARG2, which can be clinically exploited. SIGNIFICANCE: These findings illustrate that cross-talk between myeloid cells and tumor cells creates a metabolic regulatory loop that promotes neuroblastoma progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / metabolism
  • Arginine / metabolism*
  • Cell Line, Tumor
  • Humans
  • Interleukin-1beta / immunology
  • Interleukin-1beta / metabolism*
  • MAP Kinase Signaling System
  • Macrophages / immunology
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Mice
  • Mice, Transgenic
  • Myeloid Cells / immunology
  • Myeloid Cells / metabolism
  • Myeloid Cells / pathology
  • Neuroblastoma / immunology
  • Neuroblastoma / metabolism*
  • Neuroblastoma / pathology
  • Sarcoma, Ewing / immunology
  • Sarcoma, Ewing / metabolism
  • Sarcoma, Ewing / pathology
  • Tumor Microenvironment
  • Tumor Necrosis Factor-alpha / immunology
  • Tumor Necrosis Factor-alpha / metabolism*

Substances

  • Interleukin-1beta
  • TNF protein, human
  • Tumor Necrosis Factor-alpha
  • Arginine
  • ARG2 protein, human
  • Arginase