G-CSF Promotes Neuroblastoma Tumorigenicity and Metastasis via STAT3-Dependent Cancer Stem Cell Activation

Cancer Res. 2015 Jun 15;75(12):2566-79. doi: 10.1158/0008-5472.CAN-14-2946. Epub 2015 Apr 23.

Abstract

Increasing evidence suggests that inflammatory cytokines play a critical role in tumor initiation and progression. A cancer stem cell (CSC)-like subpopulation in neuroblastoma is known to be marked by expression of the G-CSF receptor (G-CSFR). Here, we report on the mechanistic contributions of the G-CSFR in neuroblastoma CSCs. Specifically, we demonstrate that the receptor ligand G-CSF selectively activates STAT3 within neuroblastoma CSC subpopulations, promoting their expansion in vitro and in vivo. Exogenous G-CSF enhances tumor growth and metastasis in human xenograft and murine neuroblastoma tumor models. In response to G-CSF, STAT3 acts in a feed-forward loop to transcriptionally activate the G-CSFR and sustain neuroblastoma CSCs. Blockade of this G-CSF-STAT3 signaling loop with either anti-G-CSF antibody or STAT3 inhibitor depleted the CSC subpopulation within tumors, driving correlated tumor growth inhibition, decreased metastasis, and increased chemosensitivity. Taken together, our results define G-CSF as a CSC-activating factor in neuroblastoma, suggest a comprehensive reevaluation of the clinical use of G-CSF in these patients to support white blood cell counts, and suggest that direct targeting of the G-CSF-STAT3 signaling represents a novel therapeutic approach for neuroblastoma.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / physiology
  • Cell Differentiation / physiology
  • Cell Line, Tumor
  • Female
  • Granulocyte Colony-Stimulating Factor / metabolism*
  • Humans
  • Mice
  • Mice, Nude
  • Neoplasm Metastasis
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology*
  • Neuroblastoma / metabolism
  • Neuroblastoma / pathology*
  • Receptors, Granulocyte Colony-Stimulating Factor / metabolism
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction

Substances

  • Receptors, Granulocyte Colony-Stimulating Factor
  • STAT3 Transcription Factor
  • Granulocyte Colony-Stimulating Factor