HIF-2α promotes the formation of vasculogenic mimicry in pancreatic cancer by regulating the binding of Twist1 to the VE-cadherin promoter

Oncotarget. 2017 Jul 18;8(29):47801-47815. doi: 10.18632/oncotarget.17999.

Abstract

Vasculogenic mimicry (VM) is a blood supply modality that occurs independently of endothelial cell angiogenesis. Hypoxia and the epithelial-mesenchymal transition (EMT) induce VM formation by remodeling the extracellular matrix. Our previous study demonstrated that hypoxia-inducible factor-2 alpha (HIF-2α) promotes the progress of EMT in pancreatic cancer; however, whether HIF-2α promotes VM formation in pancreatic cancer remains unknown. In this study, we investigated HIF-2α expression and VM by immunohistochemistry in 70 pancreatic cancer patients as well as the role of Twist1and Twist2 in HIF-2α-induced VM in vitro and in vivo. We found that the overexpression of HIF-2α and VM were correlated with poor tumor differentiation, late clinical stage and lymph node metastasis, and a poor prognosis in pancreatic cancer. Moreover, the upregulation of HIF-2α in SW1990 cells induced VM formation, whereas the opposite results were found after silencing HIF-2α in AsPC-1 cells. A mechanistic study indicated that HIF-2α might regulate the binding of twist1 to vascular endothelial cadherin (VE-cadherin) to promote VM formation in pancreatic cancer cells, and that the P1 (-421bp) and P4 (-2110bp) regions of the Twist1 binding sequences are positive regulatory elements for VE-cadherin. In addition, we confirmed that the overexpression of HIF-2α increased Twist1 expression and promoted tumor growth and VM formation in pancreatic cancer xenografts in nude mice. These findings indicated that HIF-2α might play a critical role in VM and that HIF-2α and the pathway of HIF-2α inducing VM formation are potential therapeutic targets for pancreatic cancer.

Keywords: HIF-2α; Twist; VE-cadherin; pancreatic cancer; vasculogenic mimicry (VM).

MeSH terms

  • Aged
  • Aged, 80 and over
  • Animals
  • Antigens, CD / genetics*
  • Antigens, CD34 / metabolism
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Cadherins / genetics*
  • Cell Line, Tumor
  • Cell Movement / genetics
  • Disease Models, Animal
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Heterografts
  • Humans
  • Male
  • Mice
  • Middle Aged
  • Neoplasm Grading
  • Neoplasm Metastasis
  • Neovascularization, Pathologic / metabolism*
  • Nuclear Proteins / metabolism*
  • Pancreatic Neoplasms / etiology*
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology
  • Promoter Regions, Genetic*
  • Protein Binding
  • Twist-Related Protein 1 / metabolism*

Substances

  • Antigens, CD
  • Antigens, CD34
  • Basic Helix-Loop-Helix Transcription Factors
  • Cadherins
  • Nuclear Proteins
  • TWIST1 protein, human
  • Twist-Related Protein 1
  • cadherin 5
  • endothelial PAS domain-containing protein 1