Mechanosensitive pannexin-1 channels mediate microvascular metastatic cell survival

Nat Cell Biol. 2015 Jul;17(7):943-52. doi: 10.1038/ncb3194. Epub 2015 Jun 22.

Abstract

During metastatic progression, circulating cancer cells become lodged within the microvasculature of end organs, where most die from mechanical deformation. Although this phenomenon was first described over a half-century ago, the mechanisms enabling certain cells to survive this metastasis-suppressive barrier remain unknown. By applying whole-transcriptome RNA-sequencing technology to isogenic cancer cells of differing metastatic capacities, we identified a mutation encoding a truncated form of the pannexin-1 (PANX1) channel, PANX1(1-89), as recurrently enriched in highly metastatic breast cancer cells. PANX1(1-89) functions to permit metastatic cell survival during traumatic deformation in the microvasculature by augmenting ATP release from mechanosensitive PANX1 channels activated by membrane stretch. PANX1-mediated ATP release acts as an autocrine suppressor of deformation-induced apoptosis through P2Y-purinergic receptors. Finally, small-molecule therapeutic inhibition of PANX1 channels is found to reduce the efficiency of breast cancer metastasis. These data suggest a molecular basis for metastatic cell survival on microvasculature-induced biomechanical trauma.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Breast Neoplasms / blood supply
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / metabolism
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Cells, Cultured
  • Connexins / antagonists & inhibitors
  • Connexins / genetics*
  • Connexins / metabolism
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Humans
  • Immunoblotting
  • Interleukin Receptor Common gamma Subunit / genetics
  • Interleukin Receptor Common gamma Subunit / metabolism
  • Mice, Inbred NOD
  • Mice, Knockout
  • Mice, SCID
  • Microscopy, Confocal
  • Mutation
  • Neoplasm Metastasis
  • Neovascularization, Pathologic / genetics*
  • Neovascularization, Pathologic / metabolism
  • Neovascularization, Pathologic / prevention & control
  • Nerve Tissue Proteins / antagonists & inhibitors
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Oligonucleotide Array Sequence Analysis
  • RNA Interference
  • Small Molecule Libraries / pharmacology
  • Stress, Mechanical
  • Transcriptome
  • Transplantation, Heterologous

Substances

  • Connexins
  • Il2rg protein, mouse
  • Interleukin Receptor Common gamma Subunit
  • Nerve Tissue Proteins
  • PANX1 protein, human
  • Small Molecule Libraries
  • Adenosine Triphosphate

Associated data

  • GEO/GSE45162