Gap junction mediated signaling between satellite glia and neurons in trigeminal ganglia

Glia. 2019 May;67(5):791-801. doi: 10.1002/glia.23554. Epub 2019 Feb 4.

Abstract

Peripheral sensory ganglia contain the somata of neurons mediating mechanical, thermal, and painful sensations from somatic, visceral, and oro-facial organs. Each neuronal cell body is closely surrounded by satellite glial cells (SGCs) that have properties and functions similar to those of central astrocytes, including expression of gap junction proteins and functional dye coupling. As shown in other pain models, after systemic pain induction by intra-peritoneal injection of lipopolysaccharide, dye coupling among SGCs in intact trigeminal ganglion was enhanced. Moreover, neuron-neuron and neuron-SGC coupling was also detected. To verify the presence of gap junction-mediated coupling between SGCs and sensory neurons, we performed dual whole cell patch clamp recordings from both freshly isolated and short term cultured cell pairs dissociated from mouse trigeminal ganglia. Bidirectional gap junction mediated electrical responses were frequently recorded between SGCs, between neurons and between neurons and SGCs. Polarization of SGC altered neuronal excitability, providing evidence that gap junction-mediated interactions between neurons and glia within sensory ganglia may contribute to integration of peripheral sensory responses, and to the modulation and coordinaton of neuronal activity.

Keywords: connexin; dual whole cell recording; dye coupling; electrical coupling; glia-neuron communication.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Boron Compounds / pharmacology
  • Carbenoxolone / pharmacology
  • Cells, Cultured
  • Disease Models, Animal
  • Female
  • Flufenamic Acid / pharmacology
  • Gap Junctions / drug effects
  • Gap Junctions / physiology*
  • Heptanol / pharmacology
  • Inflammation / chemically induced
  • Inflammation / drug therapy
  • Inflammation / pathology
  • Isoquinolines / metabolism
  • Lipopolysaccharides / pharmacology
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Mice
  • Mice, Inbred C57BL
  • Neuroglia / physiology*
  • Neurons / physiology*
  • Probenecid / pharmacology
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology*
  • Trigeminal Ganglion / cytology*

Substances

  • Boron Compounds
  • Isoquinolines
  • Lipopolysaccharides
  • Flufenamic Acid
  • Heptanol
  • lucifer yellow
  • 2-aminoethoxydiphenyl borate
  • Carbenoxolone
  • Probenecid