Brazilian Journal of Anesthesiology
https://bjan-sba.org/article/doi/10.1016/j.bjane.2013.07.013
Brazilian Journal of Anesthesiology
Review Article

Satellite glial cells in sensory ganglia: its role in pain

Células gliais satélite de gânglios sensitivos: o seu papel na dor

Filipa Alexandra Leite Costa; Fani Lourença Moreira Neto

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Abstract

BACKGROUND AND OBJECTIVES: Satellite glial cells in sensory ganglia are a recent subject of research in the field of pain and a possible therapeutic target in the future. Therefore, the aim of this study was to summarize some of the important physiological and morphological characteristics of these cells and gather the most relevant scientific evidence about its possible role in the development of chronic pain. CONTENT: In the sensory ganglia, each neuronal body is surrounded by satellite glial cells forming distinct functional units. This close relationship enables bidirectional communication via a paracrine signaling between those two cell types. There is a growing body of evidence that glial satellite cells undergo structural and biochemical changes after nerve injury, which influence neuronal excitability and consequently the development and/or maintenance of pain in different animal models of chronic pain. CONCLUSIONS: Satellite glial cells are important in the establishment of physiological pain, in addition to being a potential target for the development of new pain treatments.

Keywords

Satellite glial cells, Sensory ganglia, Pain, Intraganglionar communication, Purinergic receptors

Resumo

JUSTIFICATIVA E OBJETIVOS: As células gliais satélite de gânglios sensitivos são um objeto recente de pesquisa na área da dor e um possível alvo terapêutico no futuro. Assim, este trabalho tem como objetivo resumir algumas das características morfológicas e fisiológicas mais importantes destas células e reunir as evidências científicas mais relevantes acerca do seu possível papel no desenvolvimento da dor crônica. CONTEÚDO: Nos gânglios sensitivos cada corpo neuronial é envolvido por células gliais satélite, formando unidades funcionais distintas. Esta íntima relação possibilita a comunicação bidirecional, através de uma sinalização parácrina, entre estes dois tipos de células. Existe um número crescente de evidências de que as células gliais satélite sofrem alterações estruturais e bioquímicas, após lesão nervosa, que influenciam a excitabilidade neuronial e consequentemente o desenvolvimento e/ou manutenção da dor, em diferentes modelos animais de dor crônica. CONCLUSÕES: As células gliais satélite são importantes no estabelecimento da dor não fisiológica e constituem um alvo potencial para o desenvolvimento de novos tratamentos da dor.

Palavras-chave

Células gliais satélite, Gânglio sensitivo, Dor, Comunicação intraganglionar, Receptores purinérgicos

References

Merskey H, Lindblom U, Mumford JM, Nathan PW, Sunderland S. Part III Pain terms: a current list with definitions and notes on usage. Classification of chronic pain. .

McMahon SB, Koltzenburg M. Wall and Melzack's - textbook of pain. .

Scholz J, Woolf CJ. Can we conquer pain?. Nat Neurosci.. ;5 Suppl.:1062-1067.

McMahon SB, Malcangio M. Current challenges in glia-pain biology. Neuron.. ;64:46-54.

Hanani M. Satellite glial cells: more than just 'rings around the neuron'. Neuron Glia Biol.. ;6:1-2.

Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev.. ;48:476-457.

Jessen KR, Mirsky R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci.. ;6:671-682.

Pannese E. The satellite cells of the sensory ganglia. Adv Anat Embryol Cell Biol.. ;65:1-111.

Bunge MB, Bunge RP, Peterson ER. A light and electron microscope study of long-term organized cultures of rat dorsal root ganglia. J Cell Biol.. ;32:466-439.

Pannese E. The structure of the perineuronial sheath of satellite glial cells (SGCs) in sensory ganglia. Neuron Glia Biol.. ;6:10-3.

Pannese E, Ledda M, Arcidiacono G. Clusters of nerve cell bodies enclosed within a common connective tissue envelope in the spinal ganglia of the lizard and rat. Cell Tissue Res.. ;264:209-214.

Hanani M, Huang TY, Cherkas PS. Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience.. ;114:279-283.

Pannese E, Ledda M, Cherkas PS. Satellite cell reactions to axon injury of sensory ganglion neurons: increase in em umber of gap junctions and formation of bridges connecting previously separate perineuronial sheaths. Anat Embryol (Berl).. ;206:337-347.

Pannese E, Procacci P, Ledda M. Age-related reduction of the satellite cell sheath around spinal ganglion neurons in the rabbit. J Neurocytol.. ;25:146-137.

Cherkas PS, Huang TY, Pannicke T. The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain.. ;110:298-290.

Vit JP, Jasmin L, Bhargava A. Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain. Neuron Glia Biol.. ;2:247-257.

Zhang H, Mei X, Zhang P. Altered functional properties of satellite glial cells in compressed spinal ganglia. Glia.. ;57:1588-1599.

Ceruti S, Fumagalli M, Villa G. Purinoceptor-mediated calcium signaling in primary neuron-glia trigeminal cultures. Cell Calcium.. ;43:590-576.

Villa G, Fumagalli M, Verderio C. Expression and contribution of satellite glial cells purinoceptors to pain transmission in sensory ganglia: an update. Neuron Glia Biol.. ;6:31-42.

Zhang X, Chen Y, Wang C. Neuronial somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci U S A.. ;104:9869-9864.

Li J, Vause CV, Durham PL. Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Res.. ;1196:32-22.

Takeda M, Takahashi M, Matsumoto S. Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neurosci Biobehav Rev.. ;33:784-792.

Dubovy P, Jancalek R, Klusakova I. Intra- and extraneuronial changes of immunofluorescence staining for TNF-alpha and TNFR1 in the dorsal root ganglia of rat peripheral neuropathic pain models. Cell Mol Neurobiol.. ;26:1205-1217.

Li M, Shi J, Tang JR. Effects of complete Freund's adjuvant on immunohistochemical distribution of IL-1beta and IL-1R I in neurons and glia cells of dorsal root ganglion. Acta Pharmacol Sin.. ;26:198-192.

Pomonis JD, Rogers SD, Peters CM. Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception. J Neurosci.. ;21:1006-999.

Castillo C, Norcini M, Martin Hernandez LA. Satellite glia cells in dorsal root ganglia express functional NMDA receptors. Neuroscience.. ;240C:146-135.

Shinder V, Devor M. Structural basis of neuron-to-neuron crossexcitation in dorsal root ganglia. J Neurocytol.. ;23:515-531.

Amir R, Devor M. Chemically mediated cross-excitation in rat dorsal root ganglia. J Neurosci.. ;16:4733-4741.

Amir R, Devor M. Functional cross-excitation between afferent A- and C-neurons in dorsal root ganglia. Neuroscience.. ;95:195-189.

Huang LY, Neher E. Ca2+-dependent exocytosis in the somata of dorsal root ganglion neurons. Neuron.. ;17:145-135.

Matsuka Y, Neubert JK, Maidment NT. Concurrent release of ATP and substance P within guinea pig trigeminal ganglia in vivo. Brain Res.. ;915:248-255.

Hayasaki H, Sohma Y, Kanbara K. A local GABAergic system within rat trigeminal ganglion cells. Eur J Neurosci.. ;23:757-745.

McCarthy PW, Lawson SN. Differing action potential shapes in rat dorsal root ganglion neurones related to their substance P and calcitonin gene-related peptide immunoreactivity. J Comp Neurol.. ;388:549-541.

Gu Y, Chen Y, Zhang X. Neuronial soma-satellite glial cell interactions in sensory ganglia and the participation of purinergic receptors. Neuron Glia Biol.. ;6:62-53.

Suadicani SO, Cherkas PS, Zuckerman J. Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. Neuron Glia Biol.. ;6:51-43.

Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev.. ;87:797-659.

Weick M, Cherkas PS, Hartig W. P2 receptors in satellite glial cells in trigeminal ganglia of mice. Neuroscience.. ;120:977-969.

Kobayashi K, Fukuoka T, Yamanaka H. Neurons and glial cells differentially express P2Y receptor mRNAs in the rat dorsal root ganglion and spinal cord. J Comp Neurol.. ;498:443-454.

Kobayashi K, Fukuoka T, Yamanaka H. Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. J Comp Neurol.. ;481:390-377.

Chen Y, Zhang X, Wang C. Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proc Natl Acad Sci U S A.. ;105:16778-16773.

Kushnir R, Cherkas PS, Hanani M. Peripheral inflammation upregulates P2X receptor expression in satellite glial cells of mouse trigeminal ganglia: a calcium imaging study. Neuropharmacology.. ;61:739-746.

Scemes E, Giaume C. Astrocyte calcium waves: what they are and what they do. Glia.. ;54:716-725.

Neubert JK, Maidment NT, Matsuka Y. Inflammationinduced changes in primary afferent-evoked release of substance P within trigeminal ganglia in vivo. Brain Res.. ;871:181-191.

Takeda M, Tanimoto T, Ikeda M. Temporomandibular joint inflammation potentiates the excitability of trigeminal root ganglion neurons innervating the facial skin in rats. J Neurophysiol.. ;93:2738-2723.

Takeda M, Tanimoto T, Nasu M. Activation of NK1 receptor of trigeminal root ganglion via substance P paracrine mechanism contributes to the mechanical allodynia in the temporomandibular joint inflammation in rats. Pain.. ;116:375-385.

Marriott I. The role of tachykinins in central nervous system inflammatory responses. Front Biosci.. ;9:2165-2153.

Zhang Z, Winborn CS, Marquez de Prado B. Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J Neurosci.. ;27:2693-2703.

Thalakoti S, Patil VV, Damodaram S. Neuron-glia signaling in trigeminal ganglion: implications for migraine pathology. Headache.. ;47:1025-1008.

Thippeswamy T, Morris R. The roles of nitric oxide in dorsal root ganglion neurons. Ann N Y Acad Sci.. ;962:103-110.

Feldman-Goriachnik R, Hanani M. Functional study of endothelin B receptors in satellite glial cells in trigeminal ganglia. Neuroreport.. ;22:465-469.

Giaid A, Gibson SJ, Ibrahim BN. Endothelin 1, an endothelium-derived peptide, is expressed in neurons of the human spinal cord and dorsal root ganglia. Proc Natl Acad Sci U S A.. ;86:7638-7634.

Willcockson H, Valtschanoff J. AMPA and NMDA glutamate receptors are found in both peptidergic and non-peptidergic primary afferent neurons in the rat. Cell Tissue Res.. ;334:17-23.

Brumovsky P, Watanabe M, Hokfelt T. Expression of the vesicular glutamate transporters-1 and -2 in adult mouse dorsal root ganglia and spinal cord and their regulation by nerve injury. Neuroscience.. ;147:490-469.

Ohara PT, Vit JP, Bhargava A. Gliopathic pain: when satellite glial cells go bad. Neuroscientist.. ;15:450-463.

Jasmin L, Vit JP, Bhargava A. Can satellite glial cells be therapeutic targets for pain control?. Neuron Glia Biol.. ;6:63-71.

Amir R, Michaelis M, Devor M. Membrane potential oscillations in dorsal root ganglion neurons: role in normal electrogenesis and neuropathic pain. J Neurosci.. ;19:8589-8596.

Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol.. ;429:37-23.

Liu FY, Sun YN, Wang FT. Activation of satellite glial cells in lumbar dorsal root ganglia contributes to neuropathic pain after spinal nerve ligation. Brain Res.. ;1427:77-65.

Xie W, Strong JA, Meij JT. Neuropathic pain: early spontaneous afferent activity is the trigger. Pain.. ;116:256-243.

Xie W, Strong JA, Zhang JM. Early blockade of injured primary sensory afferents reduces glial cell activation in two rat neuropathic pain models. Neuroscience.. ;160:847-857.

Hanani M. Intercellular communication in sensory ganglia by purinergic receptors and gap junctions: implications for chronic pain. Brain Res.. ;1487:183-191.

Ohara PT, Vit JP, Bhargava A. Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. J Neurophysiol.. ;100:3073-3064.

Huang TY, Belzer V, Hanani M. Gap junctions in dorsal root ganglia: possible contribution to visceral pain. Eur J Pain.. ;14:49.11-49.e1.

Stephenson JL, Byers MR. GFAP immunoreactivity in trigeminal ganglion satellite cells after tooth injury in rats. Exp Neurol.. ;131:11-22.

Chudler EH, Anderson LC, Byers MR. Trigeminal ganglion neuronial activity and glial fibrillary acidic protein immunoreactivity after inferior alveolar nerve crush in the adult rat. Pain.. ;73:149-141.

Ohtori S, Takahashi K, Moriya H. TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord. Spine (Phila Pa 1976).. ;29:1082-1088.

Miyagi M, Ohtori S, Ishikawa T. Up-regulation of TNFalpha in DRG satellite cells following lumbar facet joint injury in rats. Eur Spine J.. ;15:958-953.

Siemionow K, Klimczak A, Brzezicki G. The effects of inflammation on glial fibrillary acidic protein expression in satellite cells of the dorsal root ganglion. Spine (Phila Pa 1976).. ;34:1631-1637.

Sullivan SM, Lee A, Bjorkman ST. Cytoskeletal anchoring of GLAST determines susceptibility to brain damage: an identified role for GFAP. J Biol Chem.. ;282:29423-29414.

Romao LF, Sousa VdeO, Neto VM. Glutamate activates GFAP gene promoter from cultured astrocytes through TGFbeta1 pathways. J Neurochem.. ;106:756-746.

Dublin P, Hanani M. Satellite glial cells in sensory ganglia: their possible contribution to inflammatory pain. Brain Behav Immun.. ;21:598-592.

Ledda M, Blum E, De Palo S. Augmentation in gap junctionmediated cell coupling in dorsal root ganglia following sciatic nerve neuritis in the mouse. Neuroscience.. ;164:1545-1538.

Garrett FG, Durham PL. Differential expression of connexins in trigeminal ganglion neurons and satellite glial cells in response to chronic or acute joint inflammation. Neuron Glia Biol.. ;4:295-306.

Chessell IP, Hatcher JP, Bountra C. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain.. ;114:396-386.

LaMotte RH, Ma C. Hyperexcitable neurons and altered nonneuronial cells in the compressed spinal ganglion. Sheng Li Xue Bao.. ;60:597-602.

Huang TY, Cherkas PS, Rosenthal DW. Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Res.. ;1036:42-49.

Takeda M, Tanimoto T, Kadoi J. Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain.. ;129:166-155.

Dubovy P, Klusakova I, Svizenska I. Satellite glial cells express IL-6 and corresponding signal-transducing receptors in the dorsal root ganglia of rat neuropathic pain model. Neuron Glia Biol.. ;6:83-73.

Takahashi N, Kikuchi S, Shubayev VI. TNF-alpha and phosphorylation of ERK in DRG and spinal cord: insights into mechanisms of sciatica. Spine (Phila Pa 1976).. ;31:529-523.

Doya H, Ohtori S, Takahashi K. Extracellular signalregulated kinase mitogen-activated protein kinase activation in the dorsal root ganglion (DRG) and spinal cord after DRG injury in rats. Spine (Phila Pa 1976).. ;30:2256-2252.

Takeda M, Takahashi M, Matsumoto S. Contribution of activated interleukin receptors in trigeminal ganglion neurons to hyperalgesia via satellite glial interleukin-1beta paracrine mechanism. Brain Behav Immun.. ;22:1016-1023.

Takeda M, Kitagawa J, Takahashi M. Activation of interleukin-1beta receptor suppresses the voltage-gated potassium currents in the small-diameter trigeminal ganglion neurons following peripheral inflammation. Pain.. ;139:594-602.

White FA, Jung H, Miller RJ. Chemokines and the pathophysiology of neuropathic pain. Proc Natl Acad Sci U S A.. ;104:20151-20158.

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