Endogenous TRPV1 stimulation leads to the activation of the inositol phospholipid pathway necessary for sustained Ca2+ oscillations

Biochim Biophys Acta. 2016 Dec;1863(12):2905-2915. doi: 10.1016/j.bbamcr.2016.09.013. Epub 2016 Sep 20.

Abstract

Sensory neuron subpopulations as well as breast and prostate cancer cells express functional transient receptor potential vanilloid type 1 (TRPV1) ion channels; however little is known how TRPV1 activation leads to biological responses. Agonist-induced activation of TRPV1 resulted in specific spatiotemporal patterns of cytoplasmic Ca2+ signals in breast and prostate cancer-derived cells. Capsaicin (CAPS; 50μM) evoked intracellular Ca2+ oscillations and/or intercellular Ca2+ waves in all cell lines. As evidenced in prostate cancer Du 145 cells, oscillations were largely dependent on the expression of functional TRPV1 channels in the plasma membrane, phospholipase C activation and on the presence of extracellular Ca2+ ions. Concomitant oscillations of the mitochondrial matrix Ca2+ concentration resulted in mitochondria energization evidenced by increased ATP production. CAPS-induced Ca2+ oscillations also occurred in a subset of sensory neurons, yet already at lower CAPS concentrations (1μM). Stimulation of ectopically expressed TRPV1 channels in CAPS-insensitive NIH-3T3 cells didn't provoke CAPS-triggered Ca2+ oscillations; rather it resulted in low-magnitude, long-lasting elevations of the cytosolic Ca2+ concentration. This indicates that sole TRPV1 activation is not sufficient to generate Ca2+ oscillations. Instead the initial TRPV1-mediated signal leads to the activation of the inositol phospholipid pathway. This in turn suffices to generate a biologically relevant frequency-modulated Ca2+ signal.

Keywords: Ca(2+) oscillations; TRPV1; inositol trisphosphate; phospholipase C.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Calcium / metabolism*
  • Calcium Signaling
  • Capsaicin / analogs & derivatives
  • Capsaicin / pharmacology
  • Cell Line, Tumor
  • Diterpenes / pharmacology
  • Gene Expression
  • HEK293 Cells
  • Humans
  • Inositol 1,4,5-Trisphosphate / metabolism*
  • Mice
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • NIH 3T3 Cells
  • Primary Cell Culture
  • Sensory Receptor Cells / cytology
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / metabolism*
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism*
  • Trigeminal Ganglion / cytology
  • Trigeminal Ganglion / drug effects
  • Trigeminal Ganglion / metabolism*
  • Type C Phospholipases / genetics
  • Type C Phospholipases / metabolism*

Substances

  • Diterpenes
  • TRPV Cation Channels
  • TRPV1 protein, human
  • Inositol 1,4,5-Trisphosphate
  • Adenosine Triphosphate
  • resiniferatoxin
  • Type C Phospholipases
  • capsazepine
  • Capsaicin
  • Calcium