Satellite Glial Cells: Morphology, functional heterogeneity, and role in pain

Andreeva, Daria; Мурашова, Лада; Burzak, Nikita; Dyachuk, Vyacheslav

doi:10.3389/fncel.2022.1019449

Cited by 13 publications

(9 citation statements)

References 99 publications

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“…This was directly detected by Yoda1-induced calcium transients in this type of glia and further confirmed by the depressant effect of the nonspecific blocker of Piezo1 channels, Gd 3+ , on FM1-43- plus Yoda1-induced transient fluorescence peaks. Our proposal on the functional involvement of Piezo1-expressing SGCs in trigeminal nociception is consistent with the recent hypothesis that glial cells, apart from their supportive role, also functionally modulate neuronal activity [ 26 , 27 , 28 ]. Therefore, the SGCs surrounding the bodies of trigeminal neurons represent a new target for blocking the pro-nociceptive activity of Piezo channels in the trigeminovascular system.…”

Section: Discussionsupporting

confidence: 91%

FM1-43 Dye Memorizes Piezo1 Activation in the Trigeminal Nociceptive System Implicated in Migraine Pain

Pietra¹,

Mikhailov²,

Giniatullin³

2023

IJMS

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It has been proposed that mechanosensitive Piezo1 channels trigger migraine pain in trigeminal nociceptive neurons, but the mechanosensitivity of satellite glial cells (SGCs) supporting neuronal sensitization has not been tested before. Moreover, tools to monitor previous Piezo1 activation are not available. Therefore, by using live calcium imaging with Fluo-4 AM and labeling with FM1-43 dye, we explored a new strategy to identify Piezo channels’ activity in mouse trigeminal neurons, SGCs, and isolated meninges. The specific Piezo1 agonist Yoda1 induced calcium transients in both neurons and SGCs, suggesting the functional expression of Piezo1 channels in both types of cells. In Piezo1-transfected HEK cells, FM1-43 produced only a transient fluorescent response, whereas co-application with Yoda1 provided higher transient signals and a remarkable long-lasting FM1-43 ‘tail response’. A similar Piezo1-related FM1-43 trapping was observed in neurons and SGCs. The non-specific Piezo channel blocker, Gadolinium, inhibited the transient peak, confirming the involvement of Piezo1 receptors. Finally, FM1-43 labeling demonstrated previous activity in meningeal tissues 3.5 h after Yoda1 washout. Our data indicated that trigeminal neurons and SGCs express functional Piezo channels, and their activation provides sustained labeling with FM1-43. This long-lasting labelling can be used to monitor the ongoing and previous activation of Piezo1 channels in the trigeminal nociceptive system, which is implicated in migraine pain.

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Section: Discussionsupporting

confidence: 91%

FM1-43 Dye Memorizes Piezo1 Activation in the Trigeminal Nociceptive System Implicated in Migraine Pain

Pietra¹,

Mikhailov²,

Giniatullin³

2023

IJMS

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“…Other evidence on the role of SGCs in cross-organ sensitization includes that targeting glutamate transporter (GLT-1) blocks colon-to-bladder cross sensitization (Yang et al, 2011), with a speculation that GLT-1 may be expressed by SGCs due to glutamate as a major signaling system in sensory neuron-SGC communication (Andreeva et al, 2022). In patients with irritable bowel syndrome, nucleotide polymorphisms within the 3'UTR region of the TrkB.T1 isoform is associated with worsened somatic symptoms, including headache, back pain, joint pain, muscle pain, and somatization as well as diminished sleep quality, energy level and overall quality of life (Hong et al, 2023).…”

Section: Sgcs Regulate the Activity Of Uninjured Drg Neurons And Cros...mentioning

confidence: 99%

“…Other Transmitters in sensory neuron-SGC communications include NO, glutamate, interleukins, chemokines, and Fasn, etc (Dubovy et al, 2010;Belzer and Hanani, 2019;Lin et al, 2019;Andreeva et al, 2022). NO is released from DRG neurons and induces cyclic GMP production in SCGs (Belzer and Hanani, 2019;Hanani, 2022).…”

Section: Couplingmentioning

confidence: 99%

“…Accumulating evidence reveals a critical role of SGCs in association with a variety of chronic pain modalities, sensory axon regeneration, and stem cell-like properties (Wu et al, 2016;Avraham et al, 2020;Hanani and Spray, 2020;Wang et al, 2021;Qiu et al, 2024). Several recent review articles have summarized a series of molecules present in SGCs, such as connexin 43 (Cx43), pannexin1 (Panx1), potassium channels and purinergic systems, and the upregulation of glia fibrillary acidic protein (GFAP) and proinflammatory cytokines in SGCs in pain (Hanani and Spray, 2020;Andreeva et al, 2022;McGinnis and Ji, 2023;Estivill-Torrus et al, 2024;Qiu et al, 2024). Modern techniques continue identifying novel factors that are expressed by SGCs.…”

Section: Introductionmentioning

confidence: 99%

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Satellite Glial Cells Bridge Sensory Neuron Crosstalk in Visceral Pain and Cross-Organ Sensitization

Qiao

2024

J Pharmacol Exp Ther

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Following colonic inflammation, the uninjured bladder afferent neurons are also activated.The mechanisms and pathways underlying this sensory neuron cross-activation (from injured neurons to uninjured neurons) are not fully understood. Colonic and bladder afferent neurons reside in the same spinal segments and are separated by satellite glial cells (SGCs) and extracellular matrix in dorsal root ganglia (DRG). SGCs communicate with sensory neurons in a bidirectional fashion. In this review, I summarize the differentially regulated genes/proteins in the injured and uninjured DRG neurons and explore the role of SGCs in regulation of sensory neuron crosstalk in visceral cross-organ sensitization. I also highlight the paracrine pathways in mediating neuron-SGC and SGC-neuron coupling with an emphasis on the neurotrophins and purinergic systems. Finally, I discuss the results from recent RNAseq profiling of SGCs to reveal useful molecular markers for characterization, functional study, and therapeutic targets of SGCs.Keywords: satellite glial cells; dorsal root ganglia; crosstalk; colon; bladder; pain Significant Statements: Satellite glial cells (SGCs) are the largest glial subtypes in sensory ganglia and play a critical role in mediating sensory neuron crosstalk, an underlying mechanism in colon-bladder cross-sensitization. Identification of novel and unique molecular markers of SGCs can advance the discovery of therapeutics targets in treatment of chronic pain including visceral pain comorbidity.

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“…While there is a growing consensus that SGCs play a role in important physiological and pathological pain mechanisms ( Hanani and Spray, 2020 ; Gazerani, 2021 ; Andreeva et al, 2022 ) and may provide new therapeutic targets for pain relief, our knowledge of SGC biology is still limited because of the lack of techniques to study these cells in vitro. Previous protocols for the dissociation and culture of SGCs have been generated from neonatal and immature tissues, contained neuronal and non-neuronal cells, or mostly used rats ( Chen et al, 2008 ; Belzer et al, 2010 ; de Corato et al, 2011 ; Poulsen et al, 2014 ; Wang et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

Dissociation and Culture of Adult Mouse Satellite Glial Cells

Tonello,

Davidson,

Berta

2023

BIO-PROTOCOL

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Satellite glial cells (SGCs) are a type of glial cell population that originates from neural crest cells. They ultimately migrate to surround the cell bodies of neurons in the ganglia of the peripheral nervous system. Under physiological conditions, SGCs perform homeostatic functions by modifying the microenvironment around nearby neurons and provide nutrients, structure, and protection. In recent years, they have gained considerable attention due to their involvement in peripheral nerve regeneration and pain. Although methods for culturing neonatal or rat SGCs have long existed, a well-characterized method for dissociating and culturing adult SGCs from mouse tissues has been lacking until recently. This has impeded further studies of their function and the testing of new therapeutics. This protocol provides a detailed description of how to obtain primary cultures of adult SGCs from mouse dorsal root ganglia in approximately two weeks with over 90% cell purity. We also demonstrate cell purity of these cultures using quantitative real-time RT-PCR and their functional integrity using calcium imaging. Key features • Detailed and simplified protocol to dissociate and culture primary satellite glial cells (SGCs) from adult mice. • Cells are dissociated in approximately 2–3 h and cultured for approximately two weeks. • These SGC cultures allow both molecular and functional studies.

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Satellite Glial Cells: Morphology, functional heterogeneity, and role in pain

Cited by 13 publications

References 99 publications

FM1-43 Dye Memorizes Piezo1 Activation in the Trigeminal Nociceptive System Implicated in Migraine Pain

FM1-43 Dye Memorizes Piezo1 Activation in the Trigeminal Nociceptive System Implicated in Migraine Pain

Satellite Glial Cells Bridge Sensory Neuron Crosstalk in Visceral Pain and Cross-Organ Sensitization

Dissociation and Culture of Adult Mouse Satellite Glial Cells

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