CXCR4/YY1 inhibition impairs VEGF network and angiogenesis during malignancy

Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14484-9. doi: 10.1073/pnas.1008256107. Epub 2010 Jul 26.

Abstract

Tumor growth requires neoangiogenesis. VEGF is the most potent proangiogenic factor. Dysregulation of hypoxia-inducible factor (HIF) or cytokine stimuli such as those involving the chemokine receptor 4/stromal-derived cell factor 1 (CXCR4/SDF-1) axis are the major cause of ectopic overexpression of VEGF in tumors. Although the CXCR4/SDF-1 pathway is well characterized, the transcription factors executing the effector function of this signaling are poorly understood. The multifunctional Yin Yang 1 (YY1) protein is highly expressed in different types of cancers and may regulate some cancer-related genes. The network involving CXCR4/YY1 and neoangiogenesis could play a major role in cancer progression. In this study we have shown that YY1 forms an active complex with HIF-1alpha at VEGF gene promoters and increases VEGF transcription and expression observed by RT-PCR, ELISA, and Western blot using two different antibodies against VEGFB. Long-term treatment with T22 peptide (a CXCR4/SDF-1 inhibitor) and YY1 silencing can reduce in vivo systemic neoangiogenesis (P < 0.01 and P < 0.05 vs. control, respectively) during metastasis. Moreover, using an in vitro angiogenesis assay, we observed that YY1 silencing led to a 60% reduction in branches (P < 0.01) and tube length (P < 0.02) and a 75% reduction in tube area (P < 0.001) compared with control cells. A similar reduction was observed using T22 peptide. We demonstrated that T22 peptide determines YY1 cytoplasmic accumulation by reducing its phosphorylation via down-regulation of AKT, identifying a crosstalk mechanism involving CXCR4/YY1. Thus, YY1 may represent a crucial molecular target for antiangiogenic therapy during cancer progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Neoplasm Transplantation
  • Neoplasms / blood supply*
  • Neoplasms / metabolism
  • Neovascularization, Pathologic*
  • Peptides / pharmacology
  • Rats
  • Receptor Cross-Talk / physiology
  • Receptors, CXCR4 / antagonists & inhibitors*
  • Receptors, CXCR4 / metabolism
  • Transcription Factors
  • Transplantation, Heterologous
  • Vascular Endothelial Growth Factors / genetics*
  • YY1 Transcription Factor / metabolism*
  • YY1 Transcription Factor / physiology

Substances

  • Hif1a protein, rat
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Peptides
  • Receptors, CXCR4
  • T22 peptide
  • Transcription Factors
  • Vascular Endothelial Growth Factors
  • YY1 Transcription Factor
  • YY1 protein, human