HIF-1α induces VE-cadherin expression and modulates vasculogenic mimicry in esophageal carcinoma cells

World J Gastroenterol. 2014 Dec 21;20(47):17894-904. doi: 10.3748/wjg.v20.i47.17894.

Abstract

Aim: To investigate whether hypoxia inducible factor (HIF)-1α modulates vasculogenic mimicry (VM) by upregulating VE-cadherin expression in esophageal squamous cell carcinoma (ESCC).

Methods: Esophageal squamous cancer cell lines Eca109 and TE13 were transfected with plasmids harboring small interfering RNAs targeting HIF-1α or VE-cadherin. The proliferation and invasion of esophageal carcinoma cells were detected by MTT and Transwell migration assays. The formation of tubular networks of cells was analyzed by 3D culture in vitro. BALB/c nude mice were used to observe xenograft tumor formation. The relationship between the expression of HIF-1α and VE-cadherin, ephrinA2 (EphA2) and laminin5γ2 (LN5γ2) was measured by Western blot and real-time polymerase chain reaction.

Results: Knockdown of HIF-1α inhibited cell proliferation (32.3% ± 6.1% for Eca109 cells and 38.6% ± 6.8% for TE13 cells, P < 0.05). Both Eca109 and TE13 cells formed typical tubular networks. The number of tubular networks markedly decreased when HIF-1α or VE-cadherin was knocked down. Expression of VE-cadherin, EphA2 and LN5γ2 was dramatically inhibited, but the expression of matrix metalloproteinase 2 had no obvious change in HIF-1α-silenced cells. Knockdown of VE-cadherin significantly decreased expression of both EphA2 and LN5γ2 (P < 0.05), while HIF-1α expression was unchanged. The time for xenograft tumor formation was 6 ± 1.2 d for Eca109 cells and Eca109 cells transfected with HIF-1α Neo control short hairpin RNA (shRNA) vector, and 8.4 ± 2.1 d for Eca109 cells transfected with an shRNA against HIF-1α. Knockdown of HIF-1α inhibited vasculogenic mimicry (VM) and tumorigenicity in vivo.

Conclusion: HIF-1α may modulate VM in ESCC by regulating VE-cadherin expression, which affects VM formation through EphA2 and LN5γ2.

Keywords: Esophageal squamous cell carcinoma; Hypoxia-inducible factor-1α; RNA interference; VE-cadherin; Vasculogenic mimicry.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism*
  • Apoptosis
  • Cadherins / genetics
  • Cadherins / metabolism*
  • Carcinoma, Squamous Cell / blood supply*
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism*
  • Carcinoma, Squamous Cell / pathology
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Esophageal Neoplasms / blood supply*
  • Esophageal Neoplasms / genetics
  • Esophageal Neoplasms / metabolism*
  • Esophageal Neoplasms / pathology
  • Esophageal Squamous Cell Carcinoma
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Laminin / genetics
  • Laminin / metabolism
  • Mice, Inbred BALB C
  • Mice, Nude
  • Molecular Mimicry*
  • Neoplasm Invasiveness
  • Neovascularization, Pathologic*
  • RNA Interference
  • Receptor, EphA2 / genetics
  • Receptor, EphA2 / metabolism
  • Signal Transduction
  • Time Factors
  • Transfection
  • Tumor Burden

Substances

  • Antigens, CD
  • Cadherins
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • LAMC2 protein, human
  • Laminin
  • cadherin 5
  • Receptor, EphA2