Myc Cooperates with Ras by Programming Inflammation and Immune Suppression

Cell. 2017 Nov 30;171(6):1301-1315.e14. doi: 10.1016/j.cell.2017.11.013.

Abstract

The two oncogenes KRas and Myc cooperate to drive tumorigenesis, but the mechanism underlying this remains unclear. In a mouse lung model of KRasG12D-driven adenomas, we find that co-activation of Myc drives the immediate transition to highly proliferative and invasive adenocarcinomas marked by highly inflammatory, angiogenic, and immune-suppressed stroma. We identify epithelial-derived signaling molecules CCL9 and IL-23 as the principal instructing signals for stromal reprogramming. CCL9 mediates recruitment of macrophages, angiogenesis, and PD-L1-dependent expulsion of T and B cells. IL-23 orchestrates exclusion of adaptive T and B cells and innate immune NK cells. Co-blockade of both CCL9 and IL-23 abrogates Myc-induced tumor progression. Subsequent deactivation of Myc in established adenocarcinomas triggers immediate reversal of all stromal changes and tumor regression, which are independent of CD4+CD8+ T cells but substantially dependent on returning NK cells. We show that Myc extensively programs an immune suppressive stroma that is obligatory for tumor progression.

Keywords: CCL9; IL-23; Myc; NK cells; Ras; immune suppression; inflammation; lung cancer; oncogene cooperation; tumor microenvironment.

MeSH terms

  • Adenocarcinoma / immunology*
  • Adenocarcinoma / metabolism
  • Adenocarcinoma / pathology
  • Adenoma / genetics
  • Adenoma / immunology*
  • Adenoma / pathology
  • Animals
  • Carcinogenesis
  • Chemokines, CC / immunology
  • Disease Models, Animal
  • Female
  • Inflammation / immunology
  • Inflammation / metabolism
  • Interleukin-23 / immunology
  • Lung Neoplasms / genetics*
  • Lung Neoplasms / immunology*
  • Lung Neoplasms / pathology
  • Macrophage Inflammatory Proteins / immunology
  • Macrophages / immunology
  • Male
  • Mice
  • Proto-Oncogene Proteins c-myc / metabolism*
  • Proto-Oncogene Proteins p21(ras) / metabolism*
  • Tumor Microenvironment

Substances

  • Ccl9 protein, mouse
  • Chemokines, CC
  • Interleukin-23
  • Macrophage Inflammatory Proteins
  • Myc protein, mouse
  • Proto-Oncogene Proteins c-myc
  • Hras protein, mouse
  • Proto-Oncogene Proteins p21(ras)