Lipin-1-derived diacylglycerol activates intracellular TRPC3 which is critical for inflammatory signaling

Cell Mol Life Sci. 2021 Dec;78(24):8243-8260. doi: 10.1007/s00018-021-03999-0. Epub 2021 Nov 10.

Abstract

Exposure to Gram-negative bacterial LPS exacerbates host immune responses and may lead to sepsis, a life-threatening condition. Despite its high mortality and morbidity, no drugs specifically directed to treating sepsis are currently available. Using human cell genetic depletion, pharmacological inhibition, live-cell microscopy and organelle-targeted molecular sensors we present evidence that the channel TRPC3 is activated intracellularly during macrophage exposure to LPS and is essential for Ca2+ release from internal stores. In this manner, TRPC3 participates in cytosolic Ca2+ elevations, activation of the transcription factor NF-κB and cytokine upregulation. We also report that TRPC3 is activated by diacylglycerol generated by the phosphatidic acid phosphatase lipin-1. In accord with this, lipin-1-deficient cells exhibit reduced Ca2+ responses to LPS challenge. Finally, pharmacological inhibition of TRPC3 reduces systemic inflammation induced by LPS in mice. Collectively, our study unveils a central component of LPS-triggered Ca2+ signaling that involves intracellular sensing of lipin-1-derived DAG by TRPC3, and opens new opportunities for the development of strategies to treat LPS-driven inflammation.

Keywords: Ca2+ release; DAG; Inflammation; Lipin-1; Macrophages; TRPC3.

MeSH terms

  • Animals
  • Cytokines / metabolism*
  • Diglycerides / adverse effects*
  • Humans
  • Inflammation / chemically induced
  • Inflammation / metabolism
  • Inflammation / pathology*
  • Lipopolysaccharides / pharmacology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Phosphatidate Phosphatase / metabolism*
  • TRPC Cation Channels / genetics
  • TRPC Cation Channels / metabolism*

Substances

  • 1,2-diacylglycerol
  • Cytokines
  • Diglycerides
  • Lipopolysaccharides
  • TRPC Cation Channels
  • TRPC3 cation channel
  • LPIN1 protein, human
  • Phosphatidate Phosphatase