A novel HIF-1α-integrin-linked kinase regulatory loop that facilitates hypoxia-induced HIF-1α expression and epithelial-mesenchymal transition in cancer cells

Oncotarget. 2015 Apr 10;6(10):8271-85. doi: 10.18632/oncotarget.3186.

Abstract

Here, we described a novel regulatory feedback loop in which hypoxia induces integrin-linked kinase (ILK) expression through a HIF-1α-dependent mechanism and ILK, in turn, stimulates HIF-1α expression through cell type- and cell context-dependent pathways. HIF-1α increased ILK via transcriptional activation. ILK increased HIF-1α levels by promoting mTOR-mediated translation in PC-3 and MCF-7 cells, and by blocking GSK3β-mediated degradation in LNCaP cells, consistent with the cell line-/cellular context-specific functions of ILK as a Ser473-Akt kinase. We show that ILK can account for the effects of hypoxia on Akt, mTOR, and GSK3β phosphorylation. Also, ILK can de-repress HIF-1α signaling through the YB-1-mediated inhibition of Foxo3a expression. In concert with HIF-1α, these downstream effectors promote epithelial-mesenchymal transition (EMT) through modulation of Snail and Zeb1. Thus, the ILK-HIF-1α regulatory loop could underlie the maintenance of high HIF-1α expression levels and the promotion of EMT under hypoxic conditions. Finally, we show that the small-molecule ILK inhibitor T315 can disrupt this regulatory loop in vivo and suppress xenograft tumor growth, thereby providing proof-of-concept that targeting ILK represents an effective strategy to block HIF-1α expression and aggressive phenotype in cancer cells.

Keywords: Foxo3a; YB-1; epithelial-mesenchymal transition; hypoxia-inducible factor-1α; integrin-linked kinase.

Publication types

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

MeSH terms

  • Animals
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Hypoxia / physiology
  • Cell Line, Tumor
  • Epithelial-Mesenchymal Transition / physiology*
  • Female
  • Heterografts
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • MCF-7 Cells
  • Male
  • Mice
  • Mice, Nude
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • Protein Serine-Threonine Kinases / metabolism*
  • Signal Transduction
  • Transfection

Substances

  • Hypoxia-Inducible Factor 1, alpha Subunit
  • integrin-linked kinase
  • Protein Serine-Threonine Kinases