miR-142-3p prevents macrophage differentiation during cancer-induced myelopoiesis

Immunity. 2013 Jun 27;38(6):1236-49. doi: 10.1016/j.immuni.2013.06.004.

Abstract

Tumor progression is accompanied by an altered myelopoiesis causing the accumulation of immunosuppressive cells. Here, we showed that miR-142-3p downregulation promoted macrophage differentiation and determined the acquisition of their immunosuppressive function in tumor. Tumor-released cytokines signaling through gp130, the common subunit of the interleukin-6 cytokine receptor family, induced the LAP∗ isoform of C/EBPβ transcription factor, promoting macrophage generation. miR-142-3p downregulated gp130 by canonical binding to its messenger RNA (mRNA) 3' UTR and repressed C/EBPβ LAP∗ by noncanonical binding to its 5' mRNA coding sequence. Enforced miR expression impaired macrophage differentiation both in vitro and in vivo. Mice constitutively expressing miR-142-3p in the bone marrow showed a marked increase in survival following immunotherapy with tumor-specific T lymphocytes. By modulating a specific miR in bone marrow precursors, we thus demonstrated the feasibility of altering tumor-induced macrophage differentiation as a potent tool to improve the efficacy of cancer immunotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Neoplasm / immunology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Differentiation / genetics
  • Cell Line, Tumor
  • Cytokine Receptor gp130 / metabolism
  • Immunotherapy / methods*
  • Immunotherapy / trends
  • Macrophages / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Myelopoiesis / genetics
  • Neoplasms, Experimental / genetics*
  • Neoplasms, Experimental / immunology*
  • Neoplasms, Experimental / therapy
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • Signal Transduction
  • Steroid Isomerases / genetics
  • Steroid Isomerases / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / transplantation
  • Transgenes / genetics
  • Tumor Escape

Substances

  • Antigens, Neoplasm
  • Carrier Proteins
  • MicroRNAs
  • Mirn142 microRNA, mouse
  • RNA, Messenger
  • Cytokine Receptor gp130
  • Ebp protein, mouse
  • Steroid Isomerases