Taxane chemotherapy induces stromal injury that leads to breast cancer dormancy escape

PLoS Biol. 2023 Sep 12;21(9):e3002275. doi: 10.1371/journal.pbio.3002275. eCollection 2023 Sep.

Abstract

A major cause of cancer recurrence following chemotherapy is cancer dormancy escape. Taxane-based chemotherapy is standard of care in breast cancer treatment aimed at killing proliferating cancer cells. Here, we demonstrate that docetaxel injures stromal cells, which release protumor cytokines, IL-6 and granulocyte colony stimulating factor (G-CSF), that in turn invoke dormant cancer outgrowth both in vitro and in vivo. Single-cell transcriptomics shows a reprogramming of awakened cancer cells including several survival cues such as stemness, chemoresistance in a tumor stromal organoid (TSO) model, as well as an altered tumor microenvironment (TME) with augmented protumor immune signaling in a syngeneic mouse breast cancer model. IL-6 plays a role in cancer cell proliferation, whereas G-CSF mediates tumor immunosuppression. Pathways and differential expression analyses confirmed MEK as the key regulatory molecule in cancer cell outgrowth and survival. Antibody targeting of protumor cytokines (IL-6, G-CSF) or inhibition of cytokine signaling via MEK/ERK pathway using selumetinib prior to docetaxel treatment prevented cancer dormancy outgrowth suggesting a novel therapeutic strategy to prevent cancer recurrence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cytokines
  • Docetaxel / pharmacology
  • Granulocyte Colony-Stimulating Factor
  • Interleukin-6*
  • Mice
  • Mitogen-Activated Protein Kinase Kinases
  • Neoplasms*
  • Taxoids / pharmacology
  • Taxoids / therapeutic use

Substances

  • Docetaxel
  • Interleukin-6
  • taxane
  • Taxoids
  • Cytokines
  • Granulocyte Colony-Stimulating Factor
  • Mitogen-Activated Protein Kinase Kinases

Grants and funding

This work was supported by startup funds provided to VPS, MKB and SSB by Emory University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.