Autocrine production of IL-11 mediates tumorigenicity in hypoxic cancer cells

J Clin Invest. 2013 Apr;123(4):1615-29. doi: 10.1172/JCI59623. Epub 2013 Mar 15.

Abstract

IL-11 and its receptor, IL-11Ra, are expressed in human cancers; however, the functional role of IL-11 in tumor progression is not known. We found that IL11 is a hypoxia-inducible, VHL-regulated gene in human cancer cells and that expression of IL11 mRNA was dependent, at least in part, on HIF-1. A cooperative interaction between HIF-1 and AP-1 mediated transcriptional activation of the IL11 promoter. Additionally, we found that human cancer cells expressed a functional IL-11Ra subunit, which triggered signal transduction either by exogenous recombinant human IL-11 or by autocrine production of IL-11 in cells cultured under hypoxic conditions. Silencing of IL11 dramatically abrogated the ability of hypoxia to increase anchorage-independent growth and significantly reduced tumor growth in xenograft models. Notably, these results were phenocopied by partial knockdown of STAT1 in a human prostate cancer cell line (PC3), suggesting that this pathway may play an important role in mediating the effects of IL-11 under hypoxic conditions. In conclusion, these results identify IL11 as an oxygen- and VHL-regulated gene and provide evidence of a pathway "hijacked" by hypoxic cancer cells that may contribute to tumor progression.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigens, Neoplasm / genetics
  • Antigens, Neoplasm / metabolism
  • Autocrine Communication
  • Basic Helix-Loop-Helix Transcription Factors / physiology
  • Binding Sites
  • Carbonic Anhydrase IX
  • Carbonic Anhydrases / genetics
  • Carbonic Anhydrases / metabolism
  • Cell Hypoxia
  • Cell Proliferation
  • Cell Transformation, Neoplastic / metabolism*
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Gene Knockdown Techniques
  • HCT116 Cells
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology
  • Interleukin-11 / genetics
  • Interleukin-11 / metabolism*
  • Interleukin-11 / physiology
  • Interleukin-11 Receptor alpha Subunit / genetics
  • Interleukin-11 Receptor alpha Subunit / metabolism*
  • Interleukin-11 Receptor alpha Subunit / physiology
  • MAP Kinase Signaling System
  • Mice
  • Mice, Nude
  • Neoplasm Transplantation
  • Phosphorylation
  • Protein Processing, Post-Translational
  • RNA Interference
  • Response Elements
  • STAT1 Transcription Factor / metabolism
  • Transcription Factor AP-1 / physiology
  • Transcriptional Activation
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism
  • Von Hippel-Lindau Tumor Suppressor Protein / physiology

Substances

  • Antigens, Neoplasm
  • Basic Helix-Loop-Helix Transcription Factors
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • IL11 protein, human
  • IL11RA protein, human
  • Interleukin-11
  • Interleukin-11 Receptor alpha Subunit
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Transcription Factor AP-1
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • endothelial PAS domain-containing protein 1
  • Von Hippel-Lindau Tumor Suppressor Protein
  • CA9 protein, human
  • Carbonic Anhydrase IX
  • Carbonic Anhydrases
  • VHL protein, human

Associated data

  • GEO/GSE43608