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

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. K E Y W O R D S connexin, dual whole cell recording, dye coupling, electrical coupling, glia-neuron communication

Cross-talk signaling in the trigeminal ganglion: role of neuropeptides and other mediators

“…Similarly, after inferior alveolar nerve injury mechanical allodynia in the whisker pad was accompanied by an enhanced expression of connexin 43 in trigeminal ganglion SGCs, suggesting that glia activation has significant impact on the excitability of nociceptive trigeminal ganglion neurons (Kaji et al 2016). Functional gap junctions between cultured mouse trigeminal ganglion neurons and glial cells have also been substantiated by recording bidirectional electrical responses with patch clamp techniques (Spray et al 2019).…”

“…1a). Results from a retrograde labeling study provided some of the first evidences of cross-excitation from V3 to V1 and V2 within the ganglion, including communication between neurons and satellite glial cells (SGCs) discussed below (Thalakoti et al 2007;Durham and Garrett 2010;Spray et al 2019). The central processes of the trigeminal afferents arise from the trigeminal ganglion forming the trigeminal nerve that enters the brainstem at the pontine level.…”

Changes in the transcriptional fingerprint of satellite glial cells following peripheral nerve injury

“…An increasing number of studies describe how nerve injury induces changes in the SGC‐neuron interplay. At the structural level, SGCs appear to change morphology (Pannese, ) and to undergo proliferation (Donegan, Kernisant, Cua, Jasmin, & Ohara, ; Friede & Johnstone, ; Lu & Richardson, ; Shinder et al, ; Vit, Jasmin, Bhargava, & Ohara, ), as well as to increase inter‐SGC coupling via gap junctions (Cherkas et al, ; Hanani, Huang, Cherkas, Ledda, & Pannese, ; Huang, Cherkas, Rosenthal, & Hanani, ; Pannese, Ledda, Cherkas, Huang, & Hanani, ; Spray et al, ; Suadicani et al, ). Upregulation of glial fibrillary acidic protein (GFAP) is also described (Liu et al, ; Vit et al, ; Woodham, Anderson, Nadim, & Turmaine, ), which is often used as a marker for activated SGCs (Blum, Procacci, Conte, Sartori, & Hanani, ; Gunjigake, Goto, Nakao, Kobayashi, & Yamaguchi, ; Hanani, Blum, Liu, Peng, & Liang, ; Nadeau, Wilson‐Gerwing, & Verge, ; Ohara et al, ; Ohtori, Takahashi, Moriya, & Myers, ).…”

Oligodendrocytes Remodel the Genomic Fabrics of Functional Pathways in Astrocytes

“…Until now, no gap junction channel was found between neurons and astrocytes or oligodendrocytes in the mouse brain. However, formation of functional neuron-glia gap junction channels has so far been identified between somata of peripheral sensory ganglia neurons and surrounding satellite glial cells [54]. There are also reports of glia-neuronal gap junctions in C.…”