ER Stress Sensor XBP1 Controls Anti-tumor Immunity by Disrupting Dendritic Cell Homeostasis

Cell. 2015 Jun 18;161(7):1527-38. doi: 10.1016/j.cell.2015.05.025. Epub 2015 Jun 11.

Abstract

Dendritic cells (DCs) are required to initiate and sustain T cell-dependent anti-cancer immunity. However, tumors often evade immune control by crippling normal DC function. The endoplasmic reticulum (ER) stress response factor XBP1 promotes intrinsic tumor growth directly, but whether it also regulates the host anti-tumor immune response is not known. Here we show that constitutive activation of XBP1 in tumor-associated DCs (tDCs) drives ovarian cancer (OvCa) progression by blunting anti-tumor immunity. XBP1 activation, fueled by lipid peroxidation byproducts, induced a triglyceride biosynthetic program in tDCs leading to abnormal lipid accumulation and subsequent inhibition of tDC capacity to support anti-tumor T cells. Accordingly, DC-specific XBP1 deletion or selective nanoparticle-mediated XBP1 silencing in tDCs restored their immunostimulatory activity in situ and extended survival by evoking protective type 1 anti-tumor responses. Targeting the ER stress response should concomitantly inhibit tumor growth and enhance anti-cancer immunity, thus offering a unique approach to cancer immunotherapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • DNA-Binding Proteins / metabolism*
  • Dendritic Cells / pathology*
  • Endoplasmic Reticulum Stress*
  • Female
  • Humans
  • Lipid Peroxidation
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Ovarian Neoplasms / immunology*
  • Ovarian Neoplasms / pathology*
  • Regulatory Factor X Transcription Factors
  • T-Lymphocytes / immunology
  • Transcription Factors / metabolism*
  • X-Box Binding Protein 1

Substances

  • DNA-Binding Proteins
  • Regulatory Factor X Transcription Factors
  • Transcription Factors
  • X-Box Binding Protein 1
  • XBP1 protein, human
  • Xbp1 protein, mouse

Associated data

  • GEO/GSE68472