Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-14T17:24:35.396Z Has data issue: false hasContentIssue false

Neuronal soma–satellite glial cell interactions in sensory ganglia and the participation of purinergic receptors

Published online by Cambridge University Press:  06 July 2010

Yanping Gu
Affiliation:
Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, TX, USA
Yong Chen
Affiliation:
Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, TX, USA
Xiaofei Zhang
Affiliation:
Department of Cell Biology, Institute for Childhood and Neglected Diseases, The Scripps Research Institute, La Jolla, CA, USA
Guang-Wen Li
Affiliation:
Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, TX, USA
Congying Wang
Affiliation:
Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, TX, USA
Li-Yen Mae Huang*
Affiliation:
Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, TX, USA
*
Correspondence should be addressed to: Li-Yen Mae Huang, Department of Neuroscience and Cell Biology, University of Texas Medical Branch, 301 University Blvd, Galveston, TX 77555-1069, USAphone:409-772-6555email:LmHuang@utmb.edu

Abstract

It has been known for some time that the somata of neurons in sensory ganglia respond to electrical or chemical stimulation and release transmitters in a Ca2+-dependent manner. The function of the somatic release has not been well delineated. A unique characteristic of the ganglia is that each neuronal soma is tightly enwrapped by satellite glial cells (SGCs). The somatic membrane of a sensory neuron rarely makes synaptic contact with another neuron. As a result, the influence of somatic release on the activity of adjacent neurons is likely to be indirect and/or slow. Recent studies of neuron–SGC interactions have demonstrated that ATP released from the somata of dorsal root ganglion neurons activates SGCs. They in turn exert complex excitatory and inhibitory modulation of neuronal activity. Thus, SGCs are actively involved in the processing of afferent information. In this review, we summarize our understanding of bidirectional communication between neuronal somata and SGCs in sensory ganglia and its possible role in afferent signaling under normal and injurious conditions. The participation of purinergic receptors is emphasized because of their dominant roles in the communication.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amir, R. and Devor, M. (2003a) Electrical excitability of the soma of sensory neurons is required for spike invasion of the soma, but not for through-conduction. Biophysical Journal 84, 21812191.CrossRefGoogle Scholar
Amir, R. and Devor, M. (2003b) Extra spike formation in sensory neurons and the disruption of afferent spike patterning. Biophysical Journal 84, 27002708.CrossRefGoogle ScholarPubMed
Bardoni, R., Goldstein, P.A., Lee, C.J., Gu, J.G. and MacDermott, A.B. (1997) ATP P2X receptors mediate fast synaptic transmission in the dorsal horn of the rat spinal cord. Journal of Neuroscience 17, 52975304.CrossRefGoogle ScholarPubMed
Beggs, S. and Salter, M.W. (2007) Stereological and somatotopic analysis of the spinal microglial response to peripheral nerve injury. Brain, Behavior, and Immunity 21, 624633.CrossRefGoogle ScholarPubMed
Bianco, F., Pravettoni, E., Colombo, A., Schenk, U., Moller, T., Matteoli, M. et al. (2005) Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. Journal of Immunology 174, 72687277.CrossRefGoogle ScholarPubMed
Burgard, E.C., Niforatos, W., van Biesen, T., Lynch, K.J., Touma, E., Metzger, R.E. et al. (1999) P2X receptor-mediated ionic currents in dorsal root ganglion neurons. Journal of Neurophysiology 82, 15901598.CrossRefGoogle ScholarPubMed
Burnstock, G. (2000) P2X receptors in sensory neurones. British Journal of Anaesthesia 84, 476488.CrossRefGoogle ScholarPubMed
Ceruti, S., Fumagalli, M., Villa, G., Verderio, C. and Abbracchio, M.P. (2008) Purinoceptor-mediated calcium signaling in primary neuron-glia trigeminal cultures. Cell Calcium 43, 576590.CrossRefGoogle ScholarPubMed
Chen, Y., Zhang, X., Wang, C., Li, G., Gu, Y. and Huang, L.Y. (2008) Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proceedings of the National Academy of Sciences of the U.S.A. 105, 1677316778.CrossRefGoogle ScholarPubMed
Cherkas, P.S., Huang, T.Y., Pannicke, T., Tal, M., Reichenbach, A. and Hanani, M. (2004) The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain 110, 290298.CrossRefGoogle ScholarPubMed
Chessell, I.P., Hatcher, J.P., Bountra, C., Michel, A.D., Hughes, J.P., Green, P. et al. (2005) Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114, 386396.CrossRefGoogle ScholarPubMed
Clark, A.K., Staniland, A.A., Marchand, F., Kaan, T.K., McMahon, S.B. and Malcangio, M. (2010) P2X7-dependent release of interleukin-1beta and nociception in the spinal cord following lipopolysaccharide. Journal of Neuroscience 30, 573582.CrossRefGoogle ScholarPubMed
Colomar, A., Marty, V., Medina, C., Combe, C., Parnet, P. and Amedee, T. (2003) Maturation and release of interleukin-1beta by lipopolysaccharide-primed mouse Schwann cells require the stimulation of P2X7 receptors. Journal of Biological Chemistry 278, 3073230740.CrossRefGoogle ScholarPubMed
Cook, S.P. and McCleskey, E.W. (2002) Cell damage excites nociceptors through release of cytosolic ATP. Pain 95, 4147.CrossRefGoogle ScholarPubMed
Cotrina, M.L., Lin, J.H., Lopez-Garcia, J.C., Naus, C.C. and Nedergaard, M. (2000) ATP-mediated glia signaling. Journal of Neuroscience 20, 28352844.CrossRefGoogle ScholarPubMed
Coull, J.A., Beggs, S., Boudreau, D., Boivin, D., Tsuda, M., Inoue, K. et al. (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438, 10171021.CrossRefGoogle ScholarPubMed
Devor, M. (2009) Ectopic discharge in Abeta afferents as a source of neuropathic pain. Experimental Brain Research 196, 115128.CrossRefGoogle ScholarPubMed
Diem, R., Meyer, R., Weishaupt, J.H. and Bahr, M. (2001) Reduction of potassium currents and phosphatidylinositol 3-kinase-dependent AKT phosphorylation by tumor necrosis factor-(alpha) rescues axotomized retinal ganglion cells from retrograde cell death in vivo. Journal of Neuroscience 21, 20582066.CrossRefGoogle ScholarPubMed
Duan, S. and Neary, J.T. (2006) P2X(7) receptors: properties and relevance to CNS function. Glia 54, 738746.CrossRefGoogle ScholarPubMed
Duan, S., Anderson, C.M., Keung, E.C., Chen, Y. and Swanson, R.A. (2003) P2X7 receptor-mediated release of excitatory amino acids from astrocytes. Journal of Neuroscience 23, 13201328.CrossRefGoogle ScholarPubMed
Dublin, P. and Hanani, M. (2007) Satellite glial cells in sensory ganglia: their possible contribution to inflammatory pain. Brain, Behavior, and Immunity 21, 592598.CrossRefGoogle ScholarPubMed
Fehrenbacher, J.C., Burkey, T.H., Nicol, G.D. and Vasko, M.R. (2005) Tumor necrosis factor alpha and interleukin-1beta stimulate the expression of cyclooxygenase II but do not alter prostaglandin E2 receptor mRNA levels in cultured dorsal root ganglia cells. Pain 113, 113122.CrossRefGoogle Scholar
Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P.G. and Carmignoto, G. (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729743.CrossRefGoogle ScholarPubMed
Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R.M., Curti, A., Idzko, M. et al. (2006) The P2X7 receptor: a key player in IL-1 processing and release. Journal of Immunology 176, 38773883.CrossRefGoogle ScholarPubMed
Fields, R.D. and Burnstock, G. (2006) Purinergic signalling in neuron–glia interactions. Nature Reviews. Neuroscience 7, 423436.CrossRefGoogle ScholarPubMed
Franke, H., Krugel, U. and Illes, P. (2006) P2 receptors and neuronal injury. Pflugers ArchivEuropean. Journal of Physiology 452, 622644.Google Scholar
Grubb, B.D. and Evans, R.J. (1999) Characterization of cultured dorsal root ganglion neuron P2X receptors. European Journal of Neuroscience 11, 149154.CrossRefGoogle ScholarPubMed
Gu, J.G. (2003) P2X receptor-mediated modulation of sensory transmission to the spinal cord dorsal horn. Neuroscientist 9, 370378.CrossRefGoogle Scholar
Guthrie, P.B., Knappenberger, J., Segal, M., Bennett, M.V., Charles, A.C. and Kater, S.B. (1999) ATP released from astrocytes mediates glial calcium waves. Journal of Neuroscience 19, 520528.CrossRefGoogle ScholarPubMed
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Review 48, 457476.CrossRefGoogle ScholarPubMed
Haydon, P.G. and Carmignoto, G. (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiological Reviews 86, 10091031.CrossRefGoogle ScholarPubMed
Hingtgen, C.M. and Vasko, M.R. (1994) Prostacyclin enhances the evoked-release of substance P and calcitonin gene-related peptide from rat sensory neurons. Brain Research 655, 5160.CrossRefGoogle ScholarPubMed
Huang, L.Y. and Neher, E. (1996) Ca2+-dependent exocytosis in the somata of dorsal root ganglion neurons. Neuron 17, 135145.CrossRefGoogle Scholar
Huang, T.Y., Cherkas, P.S., Rosenthal, D.W. and Hanani, M. (2005) Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Research 1036, 4249.CrossRefGoogle ScholarPubMed
Iglesias, R., Dahl, G., Qiu, F., Spray, D.C. and Scemes, E. (2009) Pannexin 1: the molecular substrate of astrocyte “hemichannels”. Journal of Neuroscience 29, 70927097.CrossRefGoogle ScholarPubMed
Iglesias, R., Locovei, S., Roque, A., Alberto, A.P., Dahl, G., Spray, D.C. et al. (2008) P2X7 receptor–Pannexin1 complex: pharmacology and signaling. American Journal of Physiology: Cell Physiology 295, C752C760.CrossRefGoogle ScholarPubMed
Inglis, J.J., Nissim, A., Lees, D.M., Hunt, S.P., Chernajovsky, Y. and Kidd, B.L. (2005) The differential contribution of tumour necrosis factor to thermal and mechanical hyperalgesia during chronic inflammation. Arthritis Research & Therapy 7, R807R816.CrossRefGoogle ScholarPubMed
Ishibashi, T., Dakin, K.A., Stevens, B., Lee, P.R., Kozlov, S.V., Stewart, C.L. et al. (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49, 823832.CrossRefGoogle ScholarPubMed
Jarvis, M.F. and Khakh, B.S. (2009) ATP-gated P2X cation-channels. Neuropharmacology 56, 208215.CrossRefGoogle ScholarPubMed
Jennings, E.A., Christie, M.J. and Sessle, B.J. (2006) ATP potentiates neurotransmission in the rat trigeminal subnucleus caudalis. Neuroreport 17, 15071510.CrossRefGoogle ScholarPubMed
Khakh, B.S. and North, R.A. (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527532.CrossRefGoogle ScholarPubMed
Kobayashi, K., Fukuoka, T., Yamanaka, H., Dai, Y., Obata, K., Tokunaga, A. et al. (2005) Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. Journal of Comparative Neurology 481, 377390.CrossRefGoogle ScholarPubMed
Kobayashi, K., Fukuoka, T., Yamanaka, H., Dai, Y., Obata, K., Tokunaga, A. et al. (2006) Neurons and glial cells differentially express P2Y receptor mRNAs in the rat dorsal root ganglion and spinal cord. Journal of Comparative Neurology 498, 443454.CrossRefGoogle ScholarPubMed
Labasi, J.M., Petrushova, N., Donovan, C., McCurdy, S., Lira, P., Payette, M.M. et al. (2002) Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. Journal of Immunology 168, 64366445.CrossRefGoogle ScholarPubMed
Le Feuvre, R., Brough, D. and Rothwell, N. (2002) Extracellular ATP and P2X7 receptors in neurodegeneration. European Journal of Pharmacology 447, 261269.CrossRefGoogle ScholarPubMed
Liu, B., Li, H., Brull, S.J. and Zhang, J.M. (2002) Increased sensitivity of sensory neurons to tumor necrosis factor alpha in rats with chronic compression of the lumbar ganglia. Journal of Neurophysiology 88, 13931399.CrossRefGoogle ScholarPubMed
Liu, C.N., Wall, P.D., Ben-Dor, E., Michaelis, M., Amir, R. and Devor, M. (2000) Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 85, 503521.CrossRefGoogle ScholarPubMed
Liu, X., Chung, K. and Chung, J.M. (1999) Ectopic discharges and adrenergic sensitivity of sensory neurons after spinal nerve injury. Brain Research 849, 244247.CrossRefGoogle ScholarPubMed
Ma, C. and LaMotte, R.H. (2005) Enhanced excitability of dissociated primary sensory neurons after chronic compression of the dorsal root ganglion in the rat. Pain 113, 106112.CrossRefGoogle ScholarPubMed
MacKenzie, A., Wilson, H.L., Kiss-Toth, E., Dower, S.K., North, R.A. and Surprenant, A. (2001) Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 15, 825835.CrossRefGoogle ScholarPubMed
Malarkey, E.B. and Parpura, V. (2008) Mechanisms of glutamate release from astrocytes. Neurochemistry International 52, 142154.CrossRefGoogle ScholarPubMed
Marchand, F., Perretti, M. and McMahon, S.B. (2005) Role of the immune system in chronic pain. Nature Reviews. Neuroscience 6, 521532.CrossRefGoogle ScholarPubMed
Marty, V., Medina, C., Combe, C., Parnet, P. and Amedee, T. (2005) ATP binding cassette transporter ABC1 is required for the release of interleukin-1beta by P2X7-stimulated and lipopolysaccharide-primed mouse Schwann cells. Glia 49, 511519.CrossRefGoogle ScholarPubMed
Mason, R.T., Peterfreund, R.A., Sawchenko, P.E., Corrigan, A.Z., Rivier, J.E. and Vale, W.W. (1984) Release of the predicted calcitonin gene-related peptide from cultured rat trigeminal ganglion cells. Nature 308, 653655.CrossRefGoogle ScholarPubMed
Matsui, K. and Jahr, C.E. (2004) Differential control of synaptic and ectopic vesicular release of glutamate. Journal of Neuroscience 24, 89328939.CrossRefGoogle ScholarPubMed
Matsuka, Y., Neubert, J.K., Maidment, N.T. and Spigelman, I. (2001) Concurrent release of ATP and substance P within guinea pig trigeminal ganglia in vivo. Brain Research 915, 248255.CrossRefGoogle ScholarPubMed
McGaraughty, S., Chu, K.L., Namovic, M.T., Donnelly-Roberts, D.L., Harris, R.R., Zhang, X.F. et al. (2007) P2X7-related modulation of pathological nociception in rats. Neuroscience 146, 18171828.CrossRefGoogle ScholarPubMed
McMahon, S.B., Cafferty, W.B. and Marchand, F. (2005) Immune and glial cell factors as pain mediators and modulators. Experimental Neurology 192, 444462.CrossRefGoogle ScholarPubMed
Miller, R.J., Jung, H., Bhangoo, S.K. and White, F.A. (2009) Cytokine and chemokine regulation of sensory neuron function. Handbook of Experimental Pharmacology 194, 417449.CrossRefGoogle Scholar
Miyagi, M., Ohtori, S., Ishikawa, T., Aoki, Y., Ozawa, T., Doya, H. et al. (2006) Up-regulation of TNFalpha in DRG satellite cells following lumbar facet joint injury in rats. European Spine Journal 15, 953958.CrossRefGoogle ScholarPubMed
Moqbel, R. and Coughlin, J.J. (2006) Differential secretion of cytokines. Science's STKE: Signal Transduction Knowledge Environment 338, pe26.Google Scholar
Nakatsuka, T. and Gu, J.G. (2006) P2X purinoceptors and sensory transmission. Pflügers Archiv European Journal of Physiology 452, 598607.CrossRefGoogle ScholarPubMed
Nicol, G.D., Lopshire, J.C. and Pafford, C.M. (1997) Tumor necrosis factor enhances the capsaicin sensitivity of rat sensory neurons. Journal of Neuroscience 17, 975982.CrossRefGoogle ScholarPubMed
North, R.A. (2002) Molecular physiology of P2X receptors. Physiological Reviews 82, 10131067.CrossRefGoogle ScholarPubMed
Ohtori, S., Takahashi, K., Moriya, H. and Myers, R.R. (2004) 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 29, 10821088.CrossRefGoogle ScholarPubMed
Pankratov, Y., Lalo, U., Verkhratsky, A. and North, R.A. (2006) Vesicular release of ATP at central synapses. Pflügers Archiv European Journal of Physiology 452, 589597.CrossRefGoogle ScholarPubMed
Pannese, E. (1981) The satellite cells of the sensory ganglia. Advances in Anatomy, Embryology and Cell Biology 65, 1111.CrossRefGoogle ScholarPubMed
Pannese, E., Ledda, M., Cherkas, P.S., Huang, T.Y. and Hanani, M. (2003) Satellite cell reactions to axon injury of sensory ganglion neurons: increase in number of gap junctions and formation of bridges connecting previously separate perineuronal sheaths. Anatomy and Embryology 206, 337347.CrossRefGoogle ScholarPubMed
Papp, L., Vizi, E.S. and Sperlagh, B. (2004) Lack of ATP-evoked GABA and glutamate release in the hippocampus of P2X7 receptor-/- mice. Neuroreport 15, 23872391.CrossRefGoogle ScholarPubMed
Pascual, O., Casper, K.B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J.Y. et al. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113116.CrossRefGoogle ScholarPubMed
Pelegrin, P. and Surprenant, A. (2006) Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. The EMBO Journal 25, 50715082.CrossRefGoogle ScholarPubMed
Pelegrin, P. and Surprenant, A. (2009) The P2X(7) receptor-pannexin connection to dye uptake and IL-1beta release. Purinergic Signal 5, 129137.CrossRefGoogle ScholarPubMed
Perea, G. and Araque, A. (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 10831086.CrossRefGoogle ScholarPubMed
Perea, G. and Araque, A. (2010) GLIA modulates synaptic transmission. Brain Research Review 63, 93102.CrossRefGoogle ScholarPubMed
Perea, G., Navarrete, M. and Araque, A. (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends in Neurosciences 32, 421431.CrossRefGoogle ScholarPubMed
Pollock, J., McFarlane, S.M., Connell, M.C., Zehavi, U., Vandenabeele, P., MacEwan, D.J. et al. (2002) TNF-alpha receptors simultaneously activate Ca2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 42, 93106.CrossRefGoogle ScholarPubMed
Raghavendra, V., Tanga, F.Y. and DeLeo, J.A. (2004) Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. European Journal of Neuroscience 20, 467473.CrossRefGoogle ScholarPubMed
Ruan, H.Z. and Burnstock, G. (2003) Localisation of P2Y1 and P2Y4 receptors in dorsal root, nodose and trigeminal ganglia of the rat. Histochemistry and Cell Biology 120, 415426.CrossRefGoogle ScholarPubMed
Sachs, D., Cunha, F.Q., Poole, S. and Ferreira, S.H. (2002) Tumour necrosis factor-alpha, interleukin-1beta and interleukin-8 induce persistent mechanical nociceptor hypersensitivity. Pain 96, 8997.CrossRefGoogle ScholarPubMed
Scemes, E., Suadicani, S.O., Dahl, G. and Spray, D.C. (2007) Connexin and pannexin mediated cell–cell communication. Neuron Glia Biology 3, 199208.CrossRefGoogle ScholarPubMed
Schafers, M., Lee, D.H., Brors, D., Yaksh, T.L. and Sorkin, L.S. (2003) Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. Journal of Neuroscience 23, 30283038.CrossRefGoogle ScholarPubMed
Skaper, S.D., Debetto, P. and Giusti, P. (2010) The P2X7 purinergic receptor: from physiology to neurological disorders. The FASEB Journal 24, 337345.CrossRefGoogle ScholarPubMed
Solle, M., Labasi, J., Perregaux, D.G., Stam, E., Petrushova, N., Koller, B.H. et al. (2001) Altered cytokine production in mice lacking P2X(7) receptors. Journal of Biological Chemistry 276, 125132.CrossRefGoogle ScholarPubMed
Sperlagh, B., Kofalvi, A., Deuchars, J., Atkinson, L., Milligan, C.J., Buckley, N.J. et al. (2002) Involvement of P2X7 receptors in the regulation of neurotransmitter release in the rat hippocampus. Journal of Neurochemistry 81, 11961211.CrossRefGoogle ScholarPubMed
Sperlagh, B., Vizi, E.S., Wirkner, K. and Illes, P. (2006) P2X7 receptors in the nervous system. Progress in Neurobiology 78, 327346.CrossRefGoogle ScholarPubMed
Stevens, B. and Fields, R.D. (2000) Response of Schwann cells to action potentials in development. Science 287, 22672271.CrossRefGoogle ScholarPubMed
Suadicani, S.O., Cherkas, P.S., Zuckerman, J., Smith, D.N., Spray, D.C. and Hanani, M. (2009) Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. Neuron Glia Biology (Epub) November 6, 19.Google Scholar
Sukhotinsky, I., Ben-Dor, E., Raber, P. and Devor, M. (2004) Key role of the dorsal root ganglion in neuropathic tactile hypersensibility. European Journal of Pain 8, 135143.CrossRefGoogle ScholarPubMed
Surprenant, A. and North, R.A. (2009) Signaling at purinergic P2X receptors. Annual Review of Physiology 71, 333359.CrossRefGoogle ScholarPubMed
Suzuki, T., Hide, I., Ido, K., Kohsaka, S., Inoue, K. and Nakata, Y. (2004) Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. Journal of Neuroscience 24, 17.CrossRefGoogle ScholarPubMed
Takeda, M., Kitagawa, J., Takahashi, M. and Matsumoto, S. (2008a) Activation of interleukin-1beta receptor suppresses the voltage-gated potassium currents in the small-diameter trigeminal ganglion neurons following peripheral inflammation. Pain 139, 594602.CrossRefGoogle ScholarPubMed
Takeda, M., Takahashi, M. and Matsumoto, S. (2009) Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neuroscience and Biobehavioral Reviews 33, 784792.CrossRefGoogle ScholarPubMed
Takeda, M., Tanimoto, T., Kadoi, J., Nasu, M., Takahashi, M., Kitagawa, J. et al. (2007) Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain 129, 155166.CrossRefGoogle ScholarPubMed
Takeda, M., Tanimoto, T., Nasu, M. and Matsumoto, S. (2008b) Temporomandibular joint inflammation decreases the voltage-gated K+ channel subtype 1.4-immunoreactivity of trigeminal ganglion neurons in rats. European Journal of Pain 12, 189195.CrossRefGoogle ScholarPubMed
Trang, T., Beggs, S. and Salter, M.W. (2006) Purinoceptors in microglia and neuropathic pain. Pflügers Archiv European Journal of Physiology 452, 645652.CrossRefGoogle ScholarPubMed
Tsuda, M., Shigemoto-Mogami, Y., Koizumi, S., Mizokoshi, A., Kohsaka, S., Salter, M.W. et al. (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424, 778783.CrossRefGoogle ScholarPubMed
Ulrich-Lai, Y.M., Flores, C.M., Harding-Rose, C.A., Goodis, H.E. and Hargreaves, K.M. (2001) Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from rat trigeminal ganglion: evidence for intraganglionic neurotransmission. Pain 91, 219226.CrossRefGoogle ScholarPubMed
Virginio, C., MacKenzie, A., North, R.A. and Surprenant, A. (1999) Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. Journal of Physiology 519, 335346.CrossRefGoogle ScholarPubMed
Vit, J.P., Jasmin, L., Bhargava, A. and Ohara, P.T. (2006) Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain. Neuron Glia Biology 2, 247257.CrossRefGoogle ScholarPubMed
Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews. Neuroscience 6, 626640.CrossRefGoogle ScholarPubMed
Walter, L., Dinh, T. and Stella, N. (2004) ATP induces a rapid and pronounced increase in 2-arachidonoylglycerol production by astrocytes, a response limited by monoacylglycerol lipase. Journal of Neuroscience 24, 80688074.CrossRefGoogle ScholarPubMed
Wang, X., Arcuino, G., Takano, T., Lin, J., Peng, W.G., Wan, P. et al. (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nature Medicine 10, 821827.CrossRefGoogle ScholarPubMed
Wang, X., Lou, N., Xu, Q., Tian, G.F., Peng, W.G., Han, X. et al. (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nature Neuroscience 9, 816823.CrossRefGoogle ScholarPubMed
Watkins, L.R., Milligan, E.D. and Maier, S.F. (2003) Glial proinflammatory cytokines mediate exaggerated pain states: implications for clinical pain. Advances in Experimental Medicine and Biology 521, 121.Google ScholarPubMed
Weick, M., Cherkas, P.S., Hartig, W., Pannicke, T., Uckermann, O., Bringmann, A. et al. (2003) P2 receptors in satellite glial cells in trigeminal ganglia of mice. Neuroscience 120, 969977.CrossRefGoogle ScholarPubMed
Wieseler-Frank, J., Maier, S.F. and Watkins, L.R. (2005) Immune-to-brain communication dynamically modulates pain: physiological and pathological consequences. Brain, Behavior, and Immunity 19, 104111.CrossRefGoogle ScholarPubMed
Willis, W.D. and Coggeshall, R.E. (2004) Dorsal root ganglion cells and their processes. In Sensory Mechanisms of the Spinal Cord. New York: Kluwer Academic/Plenum Publishers, pp. 91101.Google Scholar
Wilson, H.L., Wilson, S.A., Surprenant, A., North, R.A. (2002) Epithelial membrane proteins induce membrane blebbing and interact with the P2X7 receptor C terminus. Journal of Biological Chemistry 277, 3401734023.CrossRefGoogle ScholarPubMed
Xu, G.Y. and Huang, L.Y. (2002) Peripheral inflammation sensitizes P2X receptor-mediated responses in rat dorsal root ganglion neurons. Journal of Neuroscience 22, 93102.CrossRefGoogle ScholarPubMed
Xu, J.T., Xin, W.J., Zang, Y., Wu, C.Y. and Liu, X.G. (2006) The role of tumor necrosis factor-alpha in the neuropathic pain induced by Lumbar 5 ventral root transection in rat. Pain 123, 306321.CrossRefGoogle ScholarPubMed
Yang, Y., Ge, W., Chen, Y., Zhang, Z., Shen, W., Wu, C. et al. (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proceedings of the National Academy of Sciences of the U.S.A. 100, 1519415199.CrossRefGoogle ScholarPubMed
Zhang, C. and Zhou, Z. (2002) Ca2+-independent but voltage-dependent secretion in mammalian dorsal root ganglion neurons. Nature Neuroscience 5, 425430.CrossRefGoogle Scholar
Zhang, H., Mei, X., Zhang, P., Ma, C., White, F.A., Donnelly, D.F. et al. (2009) Altered functional properties of satellite glial cells in compressed spinal ganglia. Glia 57, 15881599.CrossRefGoogle ScholarPubMed
Zhang, J.M., Song, X.J. and LaMotte, R.H. (1999) Enhanced excitability of sensory neurons in rats with cutaneous hyperalgesia produced by chronic compression of the dorsal root ganglion. Journal of Neurophysiology 82, 33593366.CrossRefGoogle ScholarPubMed
Zhang, J.M., Wang, H.K., Ye, C.Q., Ge, W., Chen, Y., Jiang, Z.L. et al. (2003) ATP released by astrocytes mediates glutamatergic activity-dependent heterosynaptic suppression. Neuron 40, 971982.CrossRefGoogle ScholarPubMed
Zhang, X., Chen, Y., Wang, C. and Huang, L.Y. (2007) Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proceedings of the National Academy of Sciences of the U.S.A. 104, 98649869.CrossRefGoogle ScholarPubMed
Zhang, X.F., Han, P., Faltynek, C.R., Jarvis, M.F. and Shieh, C.C. (2005) Functional expression of P2X7 receptors in non-neuronal cells of rat dorsal root ganglia. Brain Research 1052, 6370.CrossRefGoogle ScholarPubMed
Zhuang, Z.Y., Gerner, P., Woolf, C.J. and Ji, R.R. (2005) ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114, 149159.CrossRefGoogle ScholarPubMed