Signaling Pathways Relevant to Nerve Growth Factor-induced Upregulation of Transient Receptor Potential M8 Expression

Neuroscience. 2017 Dec 26:367:178-188. doi: 10.1016/j.neuroscience.2017.10.037. Epub 2017 Nov 7.

Abstract

Transient receptor potential melastatin 8 (TRPM8) is a nonselective cation channel that primarily detects the innocuous cold. In pathological conditions, TRPM8 plays a role in the development of cold hyperalgesia/allodynia. Nerve growth factor (NGF) is an important mediator involved in various pain disorders. In the present study, the NGF-TrkA pathway increased TRPM8 expression by stabilizing TRPM8 mRNA through the actions of phosphatidylinositol 3-kinase and p38 MAP kinase. Moreover, c-Jun N-terminal kinase and Src tyrosine kinase were identified as a positive and negative regulator of TRPM8 expression, respectively, via post-transcriptional mechanisms independent of mRNA stabilization. PTEN activity was found to increase protein TRPM8 expression. Calcium imaging confirmed that NGF induced TRPM8 functional upregulation. Time-lapse fluorescence microscopic analysis and a cell fractionation assay revealed that NGF promoted the trafficking of TRPM8 to the plasma membrane. In the presence of NGF, lysosome-associated membrane protein-2 (LAMP-2) was localized to TRPM8-positive dot-like and linear structures, the latter of which were observed in the periphery of the cytoplasm. It was inferred that LAMP-2 was involved in the vesicular transport of TRPM8. Pharmacological blockade of the proteasome with MG132 led to a further increase in NGF-induced TRPM8 expression, indicating that the proteasome system played a pivotal role in the degradation of TRPM8. Our findings provide novel insight into the signaling pathways involved in NGF-mediated TRPM8 upregulation and its reversion to the normal state.

Keywords: inflammatory pain; nerve growth factor (NGF); neuropathic pain; proteasome; receptor trafficking; transient receptor potential M8 (TRPM8).

MeSH terms

  • Analysis of Variance
  • Animals
  • Calcium / metabolism
  • Enzyme Inhibitors / pharmacology
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Nerve Growth Factor / pharmacology*
  • PC12 Cells
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Rats
  • Signal Transduction / drug effects*
  • Signal Transduction / genetics
  • TRPM Cation Channels / genetics
  • TRPM Cation Channels / metabolism*
  • Time Factors
  • Transfection
  • Up-Regulation / drug effects*

Substances

  • Enzyme Inhibitors
  • RNA, Messenger
  • RNA, Small Interfering
  • TRPM Cation Channels
  • TRPM5 protein, rat
  • Green Fluorescent Proteins
  • Nerve Growth Factor
  • Calcium