Development of functional units within trigeminal ganglia correlates with increased expression of proteins involved in neuron–glia interactions

Cell bodies of trigeminal nerves, which are located in the trigeminal ganglion, are completely surrounded by satellite glial cells and together form a functional unit that regulates neuronal excitability. The goals of this study were to investigate the cellular organization of the rat trigeminal ganglia during postnatal development and correlate those findings with expression of proteins implicated in neuron–glia interactions. During postnatal development there was an increase in the volume of the neuronal cell body, which correlated with a steady increase in the number of glial cells associated with an individual neuron from an average of 2.16 at birth to 7.35 on day 56 in young adults. Interestingly, while the levels of the inwardly rectifying K+ channel Kir4.1 were barely detectable during the first week, its expression in satellite glial cells increased by day 9 and correlated with initial formation of functional units. Similarly, expression of the vesicle docking protein SNAP-25 and neuropeptide calcitonin gene-related peptide was readily detected beginning on day 9 and remained elevated throughout postnatal development. Based on our findings, we propose that the expression of proteins involved in facilitating neuron–glia interactions temporally correlates with the formation of mature functional units during postnatal development of trigeminal ganglion.

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Quiescent satellite glial cells of the adult trigeminal ganglion

Open Medicine ◽

10.2478/s11536-013-0285-z ◽

2014 ◽

Vol 9 (3) ◽

pp. 500-504 ◽

Cited By ~ 1

Author(s):

Mugurel Rusu ◽

Valentina Mănoiu ◽

Nicolae Mirancea ◽

Gheorghe Nini

Keyword(s):

Electron Microscopy ◽

Glial Cells ◽

Trigeminal Ganglion ◽

Membrane Trafficking ◽

Animal Species ◽

Trigeminal Ganglia ◽

Sensory Ganglia ◽

Satellite Glial Cells ◽

Transmission Electron ◽

Immune Phenotypes

AbstractSensory ganglia comprise functional units built up by neurons and satellite glial cells (SGCs). In animal species there was proven the presence of neuronoglial progenitor cells in adult samples. Such neural crest-derived progenitors were found in immunohistochemistry (IHC). These findings were not previously documented in transmission electron microscopy (TEM). It was thus aimed to assess in TEM if cells of the human adult trigeminal ganglion indeed have ultrastructural features to qualify for a progenitor, or quiescent phenotype. Trigeminal ganglia were obtained from fifteen adult donor cadavers. In TEM, cells with heterochromatic nuclei, a pancytoplasmic content of free ribosomes, few perinuclear mitochondria, poor developed endoplasmic reticulum, lack of Golgi complexes and membrane trafficking specializations, were found included in the neuronal envelopes built-up by SGCs. The ultrastructural pattern was strongly suggestive for these cells being quiescent progenitors. However, further experiments should correlate the morphologic and immune phenotypes of such cells.

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Novel theory about radiosurgery’s action mechanisms on trigeminal ganglion for idiopathic trigeminal neuralgia: Role of the satellite glial cells

Surgical Neurology International ◽

10.25259/sni_484_2019 ◽

2020 ◽

Vol 11 ◽

pp. 412

Author(s):

Salvador Somaza ◽

Eglee M. Montilla

Keyword(s):

Trigeminal Neuralgia ◽

Glial Cells ◽

Trigeminal Ganglion ◽

Neuronal Excitability ◽

Single Layer ◽

Painful Condition ◽

Satellite Glial Cells ◽

Beneficial Effects ◽

Idiopathic Trigeminal Neuralgia ◽

Novel Theory

Background: There are many theories about the cause of trigeminal neuralgia (TN). None of them satisfactorily explains how demyelination alone through the ephaptic mechanism can contribute to the development of the TN crisis. The main characteristic of TN pain is its dynamic nature, which is difficult to explain based only on anatomical findings. With these antecedents, the exact mechanism by which radiosurgery produces pain relief in TN is unknown. Methods: It is based on the trigeminal ganglion (TG) cytoarchitecture and the pathophysiological findings observed after an injury to a trigeminal branch. TG seems to have a predominant role given its cellular structure. The neuronal component in sensory ganglia is generally surrounded by a single layer of satellite glial cells (SGC), which forms a sheath around each body cell. There is increasing evidence that SGCs play a key role in nociception. This depends on their ability to influence the neuronal excitability that occurs in conditions of neuropathic and inflammatory pain; contributing to both the generation and maintenance of pain. Results: We have already published the beneficial effects of radiosurgery on the TG for the treatment of idiopathic TN and secondary to vertebrobasilar ectasia. Now, we are investigating the functioning of the TG and how radiosurgery could act on the SGC, deactivating them, and contributing to the decrease or disappearance of the painful condition. Conclusion: We are postulating a theory on how radiosurgery in TG produces changes in the SGC, with implications in the pathological mechanisms initiated by the alteration caused in the neuron after a nerve injury.

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Glutamate Signaling, Associated With Satellite Glial Cells That Envelop Small Trigeminal Ganglion Neurons Is Highly Involved in the Neuropathic Pain

10.21203/rs.3.rs-445113/v1 ◽

2021 ◽

Author(s):

Yi Sul Cho ◽

Hyoung-Gon Ko ◽

Won Mah ◽

Yu Shin Kim ◽

Jin Young Bae ◽

...

Keyword(s):

Neuropathic Pain ◽

Glial Cells ◽

Trigeminal Ganglion ◽

Glutamate Release ◽

Inferior Alveolar Nerve ◽

Neuronal Cell ◽

Satellite Glial Cells ◽

Glutamate Signaling ◽

Trigeminal Neurons ◽

Ganglion Neurons

Abstract Recent studies implicate glutamate release from satellite glial cells (SGCs) surrounding the primary sensory neurons in the mechanisms of pathologic pain. However, little is known about the population of SGCs in the trigeminal ganglion that is involved in glutamate signaling associated with craniofacial neuropathic pain. To address this issue, we used quantitative analysis of electron microscopic immunogold labeling to investigate the changes in glutamate levels in trigeminal neurons and their enveloping SGCs in a rat model of craniofacial neuropathic pain, chronic constriction injury of inferior alveolar nerve (CCI-ION). The density of immunogold, a measure for glutamate concentration, in the neuronal cell bodies of all sizes, and in the SGCs surrounding them, was significantly higher in rats with CCI-ION than in sham-operated rats. This effect was more pronounced for the small neurons (2.2 times higher) and their SGCs (1.8 times higher) than for the medium and the large neurons and their SGCs, respectively. These findings suggest that each populations of SGCs and their surrounding trigeminal neurons of different type are involved in the glutamate signaling associated with neuropathic pain at a different level.

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Nitric oxide-proton stimulation of trigeminal ganglion neurons increases mitogen-activated protein kinase and phosphatase expression in neurons and satellite glial cells

Neuroscience ◽

10.1016/j.neuroscience.2008.09.035 ◽

2008 ◽

Vol 157 (3) ◽

pp. 542-555 ◽

Cited By ~ 25

Author(s):

S.E. Freeman ◽

V.V. Patil ◽

P.L. Durham

Keyword(s):

Nitric Oxide ◽

Protein Kinase ◽

Glial Cells ◽

Trigeminal Ganglion ◽

Mitogen Activated Protein Kinase ◽

Satellite Glial Cells ◽

Mitogen Activated Protein ◽

Trigeminal Ganglion Neurons ◽

Ganglion Neurons ◽

Stimulation Of

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Morphological and electrophysiological changes in mouse dorsal root ganglia after partial colonic obstruction

AJP Gastrointestinal and Liver Physiology ◽

10.1152/ajpgi.00028.2005 ◽

2005 ◽

Vol 289 (4) ◽

pp. G670-G678 ◽

Cited By ~ 36

Author(s):

Tian-Ying Huang ◽

Menachem Hanani

Keyword(s):

Glial Cells ◽

Dorsal Root Ganglia ◽

Dorsal Root ◽

Neuronal Excitability ◽

Colonic Obstruction ◽

Resting Potential ◽

Dye Coupling ◽

Drg Neurons ◽

Satellite Glial Cells ◽

Colon Wall

There is evidence that sensitization of neurons in dorsal root ganglia (DRG) may contribute to pain induced by intestinal injury. We hypothesized that obstruction-induced pain is related to changes in DRG neurons and satellite glial cells (SGCs). In this study, partial colonic obstruction was induced by ligation. The neurons projecting to the colon were traced by an injection of 1,1′-dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate into the colon wall. The electrophysiological properties of DRG neurons were determined using intracellular electrodes. Dye coupling was examined with an intracellular injection of Lucifer yellow (LY). Morphological changes in the colon and DRG were examined. Pain was assessed with von Frey hairs. Partial colonic obstruction caused the following changes. First, coupling between SGCs enveloping different neurons increased 18-fold when LY was injected into SGCs near neurons projecting to the colon. Second, neurons were not coupled to other neurons or SGCs. Third, the firing threshold of neurons projecting to the colon decreased by more than 40% ( P < 0.01), and the resting potential was more positive by 4–6 mV ( P < 0.05). Finally, the number of neurons displaying spontaneous spikes increased eightfold, and the number of neurons with subthreshold voltage oscillations increased over threefold. These changes are consistent with augmented neuronal excitability. The pain threshold to abdominal stimulation decreased by 70.2%. Inflammatory responses were found in the colon wall. We conclude that obstruction increased neuronal excitability, which is likely to be a major factor in the pain behavior observed. The augmented dye coupling between glial cells may contribute to the neuronal hyperexcitability.

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Purinergic signaling between neurons and satellite glial cells of mouse dorsal root ganglia modulates neuronal excitability in vivo

Pain ◽

10.1097/j.pain.0000000000002556 ◽

2021 ◽

Vol Publish Ahead of Print ◽

Author(s):

Zhiyong Chen ◽

Qian Huang ◽

Xiaodan Song ◽

Neil C. Ford ◽

Chi Zhang ◽

...

Keyword(s):

Glial Cells ◽

Dorsal Root Ganglia ◽

Dorsal Root ◽

Neuronal Excitability ◽

Purinergic Signaling ◽

Satellite Glial Cells

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Hemokinin-1 Gene Expression Is Upregulated in Trigeminal Ganglia in an Inflammatory Orofacial Pain Model: Potential Role in Peripheral Sensitization

International Journal of Molecular Sciences ◽

10.3390/ijms21082938 ◽

2020 ◽

Vol 21 (8) ◽

pp. 2938

Author(s):

Timea Aczél ◽

Angéla Kecskés ◽

József Kun ◽

Kálmán Szenthe ◽

Ferenc Bánáti ◽

...

Keyword(s):

Gene Expression ◽

Glial Cells ◽

Orofacial Pain ◽

Model Potential ◽

Trigeminal System ◽

Trigeminal Ganglia ◽

Peripheral Sensitization ◽

Satellite Glial Cells ◽

Pain Model ◽

Nociceptive Neurons

A large percentage of primary sensory neurons in the trigeminal ganglia (TG) contain neuropeptides such as tachykinins or calcitonin gene-related peptide. Neuropeptides released from the central terminals of primary afferents sensitize the secondary nociceptive neurons in the trigeminal nucleus caudalis (TNC), but also activate glial cells contributing to neuroinflammation and consequent sensitization in chronic orofacial pain and migraine. In the present study, we investigated the newest member of the tachykinin family, hemokinin-1 (HK-1) encoded by the Tac4 gene in the trigeminal system. HK-1 had been shown to participate in inflammation and hyperalgesia in various models, but its role has not been investigated in orofacial pain or headache. In the complete Freund’s adjuvant (CFA)-induced inflammatory orofacial pain model, we showed that Tac4 expression increased in the TG in response to inflammation. Duration-dependent Tac4 upregulation was associated with the extent of the facial allodynia. Tac4 was detected in both TG neurons and satellite glial cells (SGC) by the ultrasensitive RNAscope in situ hybridization. We also compared gene expression changes of selected neuronal and glial sensitization and neuroinflammation markers between wild-type and Tac4-deficient (Tac4-/-) mice. Expression of the SGC/astrocyte marker in the TG and TNC was significantly lower in intact and saline/CFA-treated Tac4-/- mice. The procedural stress-related increase of the SGC/astrocyte marker was also strongly attenuated in Tac4-/- mice. Analysis of TG samples with a mouse neuroinflammation panel of 770 genes revealed that regulation of microglia and cytotoxic cell-related genes were significantly different in saline-treated Tac4-/- mice compared to their wild-types. It is concluded that HK-1 may participate in neuron-glia interactions both under physiological and inflammatory conditions and mediate pain in the trigeminal system.

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