Hypoxia suppresses cylindromatosis (CYLD) expression to promote inflammation in glioblastoma: possible link to acquired resistance to anti-VEGF therapy

Oncotarget. 2014 Aug 15;5(15):6353-64. doi: 10.18632/oncotarget.2216.

Abstract

Cylindromatosis (CYLD) is a tumor suppressor that regulates signaling pathways by acting as a deubiquitinating enzyme. CYLDdown-regulation occurred in several malignancies, with tumor-promoting effects. Although we found loss of CYLD expression in hypoxic regions of human glioblastoma multiforme (GBM), the most aggressive brain tumor, biological roles of CYLD in GBM remain unknown. This study aimed to determine the biological significance of CYLD down-regulation to GBM progression and therapy. CYLD mRNA transcription was dramatically down-regulated in hypoxic GBM cells, consistent with our clinical observations of human GBM tissues. Hypoxia enhanced both basal and tumor necrosis factor-α-induced expression of various proinflammatory cytokines, whereas CYLD overexpression strongly counteracted these responses. In addition, chronic anti-angiogenic therapy with bevacizumab, an anti-vascular endothelial growth factor (VEGF) antibody, with enhanced hypoxia produced responses similar to these CYLD-regulated proinflammatory responses in a xenograft mouse model. Histologically, CYLD clearly prevented massive immune cell infiltration surrounding necrotic regions, and pseudopalisades appeared in bevacizumab-treated control tumors. Furthermore, CYLD overexpression, which had no impact on survival by itself, significantly improved the prosurvival effect of bevacizumab. These data suggest that CYLD down-regulation is crucial for hypoxia-mediated inflammation in GBM, which may affect the long-term efficacy of anti-VEGF therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiogenesis Inhibitors / pharmacology*
  • Animals
  • Bevacizumab / pharmacology*
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / metabolism*
  • Cell Hypoxia / physiology*
  • Deubiquitinating Enzyme CYLD
  • Down-Regulation
  • Drug Resistance, Neoplasm
  • Glioblastoma / drug therapy
  • Glioblastoma / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, SCID
  • Signal Transduction
  • Tumor Suppressor Proteins / biosynthesis*
  • Tumor Suppressor Proteins / metabolism*
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors*
  • Vascular Endothelial Growth Factor A / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Angiogenesis Inhibitors
  • Tumor Suppressor Proteins
  • Vascular Endothelial Growth Factor A
  • Bevacizumab
  • CYLD protein, human
  • Deubiquitinating Enzyme CYLD