Cutting edge: Hypoxia-induced Nanog favors the intratumoral infiltration of regulatory T cells and macrophages via direct regulation of TGF-β1

J Immunol. 2013 Dec 15;191(12):5802-6. doi: 10.4049/jimmunol.1302140. Epub 2013 Nov 13.

Abstract

Emerging evidence suggests a link between tumor hypoxia and immune suppression. In this study, we investigated the role of hypoxia-induced Nanog, a stemness-associated transcription factor, in immune suppression. We observed that hypoxia-induced Nanog correlated with the acquisition of stem cell-like properties in B16-F10 cells. We further show that Nanog was selectively induced in hypoxic areas of B16-F10 tumors. Stable short hairpin RNA-mediated depletion of Nanog, combined with melanocyte differentiation Ag tyrosinase-related protein-2 peptide-based vaccination, resulted in complete inhibition of B16-F10 tumor growth. Nanog targeting significantly reduced immunosuppressive cells (regulatory T cells and macrophages) and increased CD8(+) T effector cells in tumor bed in part by modulating TGF-β1 production. Additionally, Nanog regulated TGF-β1 under hypoxia by directly binding the TGF-β1 proximal promoter. Collectively, our data establish a novel functional link between hypoxia-induced Nanog and TGF-β1 regulation and point to a major role of Nanog in hypoxia-driven immunosuppression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Hypoxia / genetics*
  • Cell Line, Tumor
  • Gene Expression Regulation, Neoplastic*
  • Genetic Therapy
  • Homeodomain Proteins / antagonists & inhibitors
  • Homeodomain Proteins / biosynthesis
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / physiology*
  • Immunotherapy
  • Intramolecular Oxidoreductases / immunology
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Lymphopoiesis
  • Macrophages / immunology*
  • Melanoma, Experimental / genetics
  • Melanoma, Experimental / immunology*
  • Melanoma, Experimental / metabolism
  • Melanoma, Experimental / therapy
  • Mice, Inbred C57BL
  • Nanog Homeobox Protein
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology*
  • Neoplastic Stem Cells / cytology*
  • Neoplastic Stem Cells / enzymology
  • Neoplastic Stem Cells / immunology
  • Peptide Fragments / immunology
  • Promoter Regions, Genetic
  • RNA Interference
  • RNA, Small Interfering
  • Spheroids, Cellular
  • T-Lymphocytes, Regulatory / immunology*
  • Transforming Growth Factor beta1 / biosynthesis
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta1 / metabolism
  • Transforming Growth Factor beta1 / physiology*
  • Tumor Escape / genetics
  • Tumor Escape / immunology*
  • Tumor Microenvironment
  • Up-Regulation
  • Vaccination

Substances

  • Homeodomain Proteins
  • Nanog Homeobox Protein
  • Nanog protein, mouse
  • Neoplasm Proteins
  • Peptide Fragments
  • RNA, Small Interfering
  • Transforming Growth Factor beta1
  • Intramolecular Oxidoreductases
  • dopachrome isomerase