Piezo1-Pannexin1 complex couples force detection to ATP secretion in cholangiocytes

J Gen Physiol. 2021 Dec 6;153(12):e202112871. doi: 10.1085/jgp.202112871. Epub 2021 Oct 25.

Abstract

Cholangiocytes actively contribute to the final composition of secreted bile. These cells are exposed to abnormal mechanical stimuli during obstructive cholestasis, which has a deep impact on their function. However, the effects of mechanical insults on cholangiocyte function are not understood. Combining gene silencing and pharmacological assays with live calcium imaging, we probed molecular candidates essential for coupling mechanical force to ATP secretion in mouse cholangiocytes. We show that Piezo1 and Pannexin1 are necessary for eliciting the downstream effects of mechanical stress. By mediating a rise in intracellular Ca2+, Piezo1 acts as a mechanosensor responsible for translating cell swelling into activation of Panx1, which triggers ATP release and subsequent signal amplification through P2X4R. Co-immunoprecipitation and pull-down assays indicated physical interaction between Piezo1 and Panx1, which leads to stable plasma membrane complexes. Piezo1-Panx1-P2X4R ATP release pathway could be reconstituted in HEK Piezo1 KO cells. Thus, our data suggest that Piezo1 and Panx1 can form a functional signaling complex that controls force-induced ATP secretion in cholangiocytes. These findings may foster the development of novel therapeutic strategies for biliary diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate*
  • Animals
  • Calcium / metabolism
  • Cell Membrane / metabolism
  • Connexins* / genetics
  • Epithelial Cells* / metabolism
  • Ion Channels* / genetics
  • Ion Channels* / metabolism
  • Mice
  • Nerve Tissue Proteins* / genetics
  • Signal Transduction

Substances

  • Connexins
  • Ion Channels
  • Nerve Tissue Proteins
  • Panx1 protein, mouse
  • Piezo1 protein, mouse
  • Adenosine Triphosphate
  • Calcium