Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

Satellite glial cells (SGCs) closely envelop cell bodies of neurons in sensory, sympathetic and parasympathetic ganglia. This unique organization is not found elsewhere in the nervous system. SGCs in sensory ganglia are activated by numerous types of nerve injury and inflammation. The activation includes upregulation of glial fibrillary acidic protein, stronger gap junction-mediated SGC–SGC and neuron–SGC coupling, increased sensitivity to ATP, downregulation of Kir4.1 potassium channels and increased cytokine synthesis and release. There is evidence that these changes in SGCs contribute to chronic pain by augmenting neuronal activity and that these changes are consistent in various rodent pain models and likely also in human pain. Therefore, understanding these changes and the resulting abnormal interactions of SGCs with sensory neurons could provide a mechanistic approach that might be exploited therapeutically in alleviation and prevention of pain. We describe how SGCs are altered in rodent models of four common types of pain: systemic inflammation (sickness behaviour), post-surgical pain, diabetic neuropathic pain and post-herpetic pain.

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“…Neurons in sensory ganglia receive no synapses and are separated from each other by SGCs and the connective tissue space 4 (Fig. 1c ).…”

Section: Characteristics Of Sgcsmentioning

confidence: 99%

“…1c ). In most cases, neurons are wrapped individually with several SGCs, but there is evidence that a small proportion (4–9% depending on the species) of dorsal root ganglia (DRG) neurons share a common glial envelope, forming a ‘cluster’ with one or two other neurons 4 (Fig. 1d ).…”

Section: Introductionmentioning

confidence: 99%

Emerging importance of satellite glia in nervous system function and dysfunction

2020

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“…SGCs share many features with astrocytes, like the expression of glutamine synthetase and various neurotransmitter transporters. They cover axon terminals that make synaptic contacts on, or near, the neuronal somata, wrap around dendrites that emerge from neuronal somata to control the microenvironment and, similarly to astrocytes, influence synaptic transmission [98,99]. SGCs can be considered a substitute of the lacking BBB in sensory ganglia and have been shown to have phagocytic activity [98].…”

Section: Nervous System Cells and Tissues: An Overviewmentioning

confidence: 99%

Extracellular Vesicle-Mediated Cell–Cell Communication in the Nervous System: Focus on Neurological Diseases

Bavisotto

Scalia

Gammazza

et al. 2019

IJMS

120

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Extracellular vesicles (EVs), including exosomes, are membranous particles released by cells into the extracellular space. They are involved in cell differentiation, tissue homeostasis, and organ remodelling in virtually all tissues, including the central nervous system (CNS). They are secreted by a range of cell types and via blood reaching other cells whose functioning they can modify because they transport and deliver active molecules, such as proteins of various types and functions, lipids, DNA, and miRNAs. Since they are relatively easy to isolate, exosomes can be characterized, and their composition elucidated and manipulated by bioengineering techniques. Consequently, exosomes appear as promising theranostics elements, applicable to accurately diagnosing pathological conditions, and assessing prognosis and response to treatment in a variety of disorders. Likewise, the characteristics and manageability of exosomes make them potential candidates for delivering selected molecules, e.g., therapeutic drugs, to specific target tissues. All these possible applications are pertinent to research in neurophysiology, as well as to the study of neurological disorders, including CNS tumors, and autoimmune and neurodegenerative diseases. In this brief review, we discuss what is known about the role and potential future applications of exosomes in the nervous system and its diseases, focusing on cell–cell communication in physiology and pathology.

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“…Sensory neurons are enveloped by satellite glial cells (SGCs) with a gap of only 20 nm between these cells types (Hanani, , ; Pannese, ). Therefore, NO that is produced in the neurons can reach SGCs easily by diffusion and induces cGMP synthesis in them (Morris, Southam, Braid, & Garthwaite, ; Thippeswamy & Morris, ).…”

Section: Introductionmentioning

confidence: 99%

Nitric oxide as a messenger between neurons and satellite glial cells in dorsal root ganglia

Belzer

Hanani

2019

Glia

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Abnormal neuronal activity in sensory ganglia contributes to chronic pain. There is evidence that signals can spread between cells in these ganglia, which may contribute to this activity. Satellite glial cells (SGCs) in sensory ganglia undergo activation following peripheral injury and participate in cellular communication via gap junctions and chemical signaling. Nitric oxide (NO) is released from neurons in dorsal root ganglia (DRG) and induces cyclic GMP (cGMP) production in SCGs, but its role in SGC activation and neuronal excitability has not been explored. It was previously reported that induction of intestinal inflammation with dinitrobenzoate sulfonate (DNBS) increased gap junctional communications among SGCs, which contributed to neuronal excitability and pain. Here we show that DNBS induced SGC activation in mouse DRG, as assayed by glial fibrillary acidic protein upregulation. DNBS also upregulated cGMP level in SGCs, consistent with NO production. In vitro studies on intact ganglia from DNBS‐treated mice showed that blocking NO synthesis inhibited both SGCs activation and cGMP upregulation, indicating an ongoing NO production. Application of NO donor in vitro induced SGC activation, augmented gap junctional communications, and raised neuronal excitability, as assessed by electrical recordings. The cGMP analog 8‐Br‐cGMP mimicked these actions, confirming the role of the NO‐cGMP pathway in intraganglionic communications. NO also augmented Ca2+ waves propagation in DRG cultures. It is proposed that NO synthesis in DRG neurons increases after peripheral inflammation and that NO induces SGC activation, which in turn contributes to neuronal hyperexcitability. Thus, NO plays a major role in neuron–SGC communication.

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Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

Cited by 15 publications

References 316 publications

Emerging importance of satellite glia in nervous system function and dysfunction

Emerging importance of satellite glia in nervous system function and dysfunction

Extracellular Vesicle-Mediated Cell–Cell Communication in the Nervous System: Focus on Neurological Diseases

Nitric oxide as a messenger between neurons and satellite glial cells in dorsal root ganglia

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