Inhibition of Tunneling Nanotubes between Cancer Cell and the Endothelium Alters the Metastatic Phenotype

Int J Mol Sci. 2021 Jun 7;22(11):6161. doi: 10.3390/ijms22116161.

Abstract

The interaction of tumor cells with blood vessels is one of the key steps during cancer metastasis. Metastatic cancer cells exhibit phenotypic state changes during this interaction: (1) they form tunneling nanotubes (TNTs) with endothelial cells, which act as a conduit for intercellular communication; and (2) metastatic cancer cells change in order to acquire an elongated phenotype, instead of the classical cellular aggregates or mammosphere-like structures, which it forms in three-dimensional cultures. Here, we demonstrate mechanistically that a siRNA-based knockdown of the exocyst complex protein Sec3 inhibits TNT formation. Furthermore, a set of pharmacological inhibitors for Rho GTPase-exocyst complex-mediated cytoskeletal remodeling is introduced, which inhibits TNT formation, and induces the reversal of the more invasive phenotype of cancer cell (spindle-like) into a less invasive phenotype (cellular aggregates or mammosphere). Our results offer mechanistic insights into this nanoscale communication and shift of phenotypic state during cancer-endothelial interactions.

Keywords: 3D culture; RhoGTPase inhibitor; actin remodeling; cellular aggregates; exocyst complex; mammosphere; metastasis; phenotypic plasticity; tunneling nanotube (TNT).

MeSH terms

  • Breast Neoplasms / pathology*
  • Cell Communication*
  • Cell Culture Techniques
  • Cytoplasm / metabolism
  • Cytoskeleton / metabolism
  • Endothelium, Vascular / pathology*
  • Female
  • Humans
  • Nanotubes / chemistry*
  • Neoplasm Metastasis
  • Phenotype
  • Tumor Cells, Cultured
  • Vesicular Transport Proteins / genetics
  • Vesicular Transport Proteins / metabolism*
  • rho GTP-Binding Proteins / genetics
  • rho GTP-Binding Proteins / metabolism*

Substances

  • Vesicular Transport Proteins
  • rho GTP-Binding Proteins