Intercellular transmission of the unfolded protein response promotes survival and drug resistance in cancer cells

Sci Signal. 2017 Jun 6;10(482):eaah7177. doi: 10.1126/scisignal.aah7177.

Abstract

Increased protein translation in cells and various factors in the tumor microenvironment can induce endoplasmic reticulum (ER) stress, which initiates the unfolded protein response (UPR). We have previously reported that factors released from cancer cells mounting a UPR induce a de novo UPR in bone marrow-derived myeloid cells, macrophages, and dendritic cells that facilitates protumorigenic characteristics in culture and tumor growth in vivo. We investigated whether this intercellular signaling, which we have termed transmissible ER stress (TERS), also operates between cancer cells and what its functional consequences were within the tumor. We found that TERS signaling induced a UPR in recipient human prostate cancer cells that included the cell surface expression of the chaperone GRP78. TERS also activated Wnt signaling in recipient cancer cells and enhanced resistance to nutrient starvation and common chemotherapies such as the proteasome inhibitor bortezomib and the microtubule inhibitor paclitaxel. TERS-induced activation of Wnt signaling required the UPR kinase and endonuclease IRE1. However, TERS-induced enhancement of cell survival was predominantly mediated by the UPR kinase PERK and a reduction in the abundance of the transcription factor ATF4, which prevented the activation of the transcription factor CHOP and, consequently, the induction of apoptosis. When implanted in mice, TERS-primed cancer cells gave rise to faster growing tumors than did vehicle-primed cancer cells. Collectively, our data demonstrate that TERS is a mechanism of intercellular communication through which tumor cells can adapt to stressful environments.

MeSH terms

  • Activating Transcription Factor 4 / genetics
  • Activating Transcription Factor 4 / metabolism
  • Animals
  • Antineoplastic Agents / pharmacology
  • Bortezomib / pharmacology*
  • Cell Survival / drug effects*
  • Drug Resistance*
  • Endoplasmic Reticulum Chaperone BiP
  • Endoplasmic Reticulum Stress / drug effects*
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Paclitaxel / pharmacology*
  • Prostatic Neoplasms / drug therapy
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology*
  • Transcription Factor CHOP / genetics
  • Transcription Factor CHOP / metabolism
  • Tubulin Modulators / pharmacology
  • Tumor Cells, Cultured
  • Unfolded Protein Response / drug effects*
  • Wnt Proteins / genetics
  • Wnt Proteins / metabolism
  • eIF-2 Kinase / genetics
  • eIF-2 Kinase / metabolism

Substances

  • Antineoplastic Agents
  • Endoplasmic Reticulum Chaperone BiP
  • HSPA5 protein, human
  • Heat-Shock Proteins
  • Hspa5 protein, mouse
  • Tubulin Modulators
  • Wnt Proteins
  • Activating Transcription Factor 4
  • Transcription Factor CHOP
  • Bortezomib
  • PERK kinase
  • eIF-2 Kinase
  • Paclitaxel