Regulation of the temperature-dependent activation of transient receptor potential vanilloid 1 (TRPV1) by phospholipids in planar lipid bilayers

J Biol Chem. 2015 Feb 20;290(8):4741-4747. doi: 10.1074/jbc.M114.611459. Epub 2015 Jan 5.

Abstract

TRPV1 (transient receptor potential vanilloid 1) proteins are heat-activated nonselective cation channels. TRPV1 channels are polymodal in their function and exhibit multifaceted regulation with various molecular compounds. In this regard, phosphoinositides, particularly phosphatidylinositol 4,5-bisphosphate and phosphatidylinositol 4-phosphate, are important channel regulators. However, their effects on TRPV1 channel activity have not been conclusively determined. To characterize temperature-induced activation of TRPV1 in the presence of different phospholipids, we purified the TRPV1 protein from HEK-293 cells and incorporated it into planar lipid bilayers. In the presence of 2.5 μm phosphatidylinositol 4,5-bisphosphate, TRPV1 channels demonstrated rapid activation at 33-39 °C and achieved full channel opening at 42 °C. At this temperature range, TRPV1 heat activation exhibited steep temperature dependence (temperature coefficient (Q10) of 18), and the channel openings were accompanied by large changes in entropy and enthalpy, suggesting a substantial conformation change. At a similar temperature range, another phosphoinositide, phosphatidylinositol 4-phosphate, also potentiated heat activation of TRPV1, but with much lower efficiency. Negatively charged phosphatidylglycerol could also induce heat activation of TRPV1 channels, although with a small-conductance state. Our data demonstrate that phospholipids, specifically phosphoinositides, are important regulators of TRPV1 and are required for heat-induced channel activity.

Keywords: Calcium Channel; Inositol Phospholipid; Ion Channel; Lipid Bilayer; Phosphoinositide; Thermodynamics; Transient Receptor Potential Channels (TRP Channels).

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • HEK293 Cells
  • Hot Temperature*
  • Humans
  • Ion Channel Gating*
  • Lipid Bilayers / chemistry*
  • Lipid Bilayers / metabolism
  • Phospholipids / chemistry*
  • Phospholipids / metabolism
  • TRPV Cation Channels / chemistry*
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism

Substances

  • Lipid Bilayers
  • Phospholipids
  • TRPV Cation Channels
  • TRPV1 protein, human