FOXF2 deficiency permits basal-like breast cancer cells to form lymphangiogenic mimicry by enhancing the response of VEGF-C/VEGFR3 signaling pathway

Cancer Lett. 2018 Apr 28:420:116-126. doi: 10.1016/j.canlet.2018.01.069. Epub 2018 Jan 31.

Abstract

Lymphatic metastasis is the main route of breast cancer metastasis. It is known that lymphangiogenesis facilitates lymphatic metastasis through vascular endothelial growth factor-C (VEGF-C)/VEGF receptor 3 (VEGFR3) pathway-linked interactions between the tumor and its microenvironment. Here, we report a novel mechanism of lymphatic metastasis by which aggressive basal-like breast cancer (BLBC) cells form lymphatic vessel-like structures that are identified by the positive expression of lymphatic endothelial cell markers lymphatic vessel endothelial hyaluronan receptor 1 (LYVE-1), podoplanin, and VEGFR3, and termed as lymphangiogenic mimicry (LM), for the first time. Our clinical evidence and experimental data in vivo and in vitro revealed that forkhead box F2 (FOXF2) deficiency promotes the lymphatic metastasis of BLBC by conferring a lymphangiogenic mimetic feature upon cancer cells through directly activating VEGFR3 transcription. The fact that FOXF2 controls the activation of the VEGF-C/VEGFR3 signaling pathway in BLBC cells provides potential molecular diagnostic and therapeutic strategies for lymphatic metastasis in BLBC patients.

Keywords: Basal-like breast cancer; FOXF2; Lymphangiogenic mimicry; Lymphatic metastasis; VEGFR3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology*
  • Cell Line, Tumor
  • Forkhead Transcription Factors / deficiency*
  • Humans
  • Lymphatic Metastasis / genetics
  • Lymphatic Metastasis / pathology*
  • MCF-7 Cells
  • Membrane Glycoproteins / metabolism
  • Mice
  • Neoplasm Staging
  • Neoplasm Transplantation
  • Neoplasms, Basal Cell / genetics
  • Neoplasms, Basal Cell / metabolism
  • Neoplasms, Basal Cell / pathology*
  • Signal Transduction*
  • Tumor Microenvironment
  • Vascular Endothelial Growth Factor C / genetics
  • Vascular Endothelial Growth Factor C / metabolism
  • Vascular Endothelial Growth Factor Receptor-3 / genetics
  • Vascular Endothelial Growth Factor Receptor-3 / metabolism
  • Vesicular Transport Proteins / metabolism

Substances

  • FOXF2 protein, human
  • Forkhead Transcription Factors
  • LYVE1 protein, human
  • Membrane Glycoproteins
  • PDPN protein, human
  • VEGFC protein, human
  • Vascular Endothelial Growth Factor C
  • Vesicular Transport Proteins
  • FLT4 protein, human
  • Vascular Endothelial Growth Factor Receptor-3