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Expression and contribution of satellite glial cells purinoceptors to pain transmission in sensory ganglia: an update

Published online by Cambridge University Press:  06 July 2010

Giovanni Villa ,
Marta Fumagalli ,
Claudia Verderio ,
Maria P. Abbracchio  and
Stefania Ceruti
Giovanni Villa
Affiliation:
Laboratory of Molecular and Cellular, Pharmacology of Purinergic Transmission, Department of Pharmacological Sciences, Università degli Studi di Milano, Milan, Italy
Marta Fumagalli
Affiliation:
Laboratory of Molecular and Cellular, Pharmacology of Purinergic Transmission, Department of Pharmacological Sciences, Università degli Studi di Milano, Milan, Italy
Claudia Verderio
Affiliation:
CNR Institute of Neuroscience, Department of Medical Pharmacology – Università degli Studi di Milano, Milan, Italy
Maria P. Abbracchio*
Affiliation:
Laboratory of Molecular and Cellular, Pharmacology of Purinergic Transmission, Department of Pharmacological Sciences, Università degli Studi di Milano, Milan, Italy
Stefania Ceruti
Affiliation:
Laboratory of Molecular and Cellular, Pharmacology of Purinergic Transmission, Department of Pharmacological Sciences, Università degli Studi di Milano, Milan, Italy
*
Correspondence should be addressed to: Maria P. Abbracchio, Department of Pharmacological Sciences, Università degli Studi di Milano, via Balzaretti, 9-20133 Milan, Italy phone: +39-0250318304 email: [email protected]
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Abstract

The role of adenosine-5′-triphosphate (ATP) and of the ligand-gated P2X3 receptor in neuronal dorsal root ganglia (DRG) pain transmission is relatively well established. Much less is known about the purinergic system in trigeminal ganglia (TG), which are involved in certain types of untreatable neuropathic and inflammatory pain, as well as in migraine. Emerging data suggest that purinergic metabotropic P2Y receptors on both neurons and satellite glial cells (SGCs) may also participate in both physiological and pathological pain development. Here, we provide an updated literature review on the role of purinergic signaling in sensory ganglia, with special emphasis on P2Y receptors on SGCs. We also provide new original data showing a time-dependent downregulation of P2Y2 and P2Y4 receptor expression and function in purified SGCs cultures from TG, in comparison with primary mixed neuron–SGCs cultures. These data highlight the importance of the neuron–glia cross-talk in determining the SGCs phenotype. Finally, we show that, in mixed TG cultures, both adenine and guanosine induce intracellular calcium transients in neurons but not in SGCs, suggesting that also these purinergic-related molecules can participate in pain signaling. These findings may have relevant implications for the development of new therapeutic strategies for chronic pain treatment.

Keywords

Extracellular nucleotidespurinestrigeminal ganglianociceptioncell-to-cell communication
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Special Issue 1: Satellite Glial Cells , February 2010 , pp. 31 - 42
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Abbracchio, M.P., Burnstock, G., Boeynaems, J.M., Barnard, E.A., Boyer, J.L., Kennedy, C. et al. (2006) International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacological Reviews 58, 281–341.CrossRefGoogle ScholarPubMed
Abbracchio, M.P. and Verderio, C. (2006) Pathophysiological roles of P2 receptors in glial cells. Novartis Foundation Symposium 276, 91–103; discussion 103–112, 275–181.CrossRefGoogle ScholarPubMed
Bender, E., Buist, A., Jurzak, M., Langlois, X., Baggerman, G., Verhasselt, P. et al. (2002) Characterization of an orphan G protein-coupled receptor localized in the dorsal root ganglia reveals adenine as a signaling molecule. Proceedings of the National Academy of Sciences of the U.S.A. 99, 8573–8578.CrossRefGoogle ScholarPubMed
Benfenati, V., Caprini, M., Nobile, M., Rapisarda, C. and Ferroni, S. (2006) Guanosine promotes the up-regulation of inward rectifier potassium current mediated by Kir4.1 in cultured rat cortical astrocytes. Journal of Neurochemistry 98, 430–445.CrossRefGoogle ScholarPubMed
Bianchi, B.R., Lynch, K.J., Touma, E., Niforatos, W., Burgard, E.C., Alexander, K.M. et al. (1999) Pharmacological characterization of recombinant human and rat P2X receptor subtypes. European Journal of Pharmacology 376, 127–138.CrossRefGoogle ScholarPubMed
Bianco, F., Colombo, A., Saglietti, L., Lecca, D., Abbracchio, M.P., Matteoli, M. et al. (2009) Different properties of P2X7 receptor in hippocampal and cortical astrocytes. Purinergic Signaling 5, 233–240.CrossRefGoogle ScholarPubMed
Bianco, F., Fumagalli, M., Pravettoni, E., D'Ambrosi, N., Volonte, C., Matteoli, M. et al. (2005a) Pathophysiological roles of extracellular nucleotides in glial cells: differential expression of purinergic receptors in resting and activated microglia. Brain Research and Brain Research Reviews 48, 144–156.CrossRefGoogle ScholarPubMed
Bianco, F., Pravettoni, E., Colombo, A., Schenk, U., Möller, T., Matteoli, M. et al. (2005b) Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. Journal of Immunology 174, 7268–7277.CrossRefGoogle ScholarPubMed
Bleehen, T. and Keele, C.A. (1977) Observations on the algogenic actions of adenosine compounds on the human blister base preparation. Pain 3, 367–377.CrossRefGoogle ScholarPubMed
Burnstock, G. (1996) A unifying purinergic hypothesis for the initiation of pain. The Lancet 347, 1604–1605.CrossRefGoogle ScholarPubMed
Burnstock, G. (2001) Purine-mediated signalling in pain and visceral perception. Trends in Pharmacological Sciences 22, 182–188.CrossRefGoogle ScholarPubMed
Burnstock, G. (2006) Purinergic P2 receptors as targets for novel analgesics. Pharmacology and Therapeutics 110, 433–454.CrossRefGoogle ScholarPubMed
Burnstock, G. (2008) Purinergic signalling and disorders of the central nervous system. Nature Reviews Drug Discovery 7, 575–590.CrossRefGoogle ScholarPubMed
Burnstock, G. (2009a) Purinergic receptors and pain. Current Pharmacological Design 15, 1717–1735.CrossRefGoogle ScholarPubMed
Burnstock, G. (2009b) Purines and sensory nerves. Handbook of Experimental Pharmacology 194, 333–392.CrossRefGoogle Scholar
Capuano, A., De Corato, A., Lisi, L., Tringali, G., Navarra, P. and Dello Russo, C. (2009) Proinflammatory-activated trigeminal satellite cells promote neuronal sensitization: relevance for migraine pathology. Molecular Pain 5, 43.CrossRefGoogle ScholarPubMed
Carruthers, A.M., Sellers, L.A., Jenkins, D.W., Jarvie, E.M., Feniuk, W. and Humphrey, P.P. (2001) Adenosine A1 receptor-mediated inhibition of protein kinase A-induced calcitonin gene-related peptide release from rat trigeminal neurons. Molecular Pharmacology 59, 1533–1541.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, 576–590.CrossRefGoogle ScholarPubMed
Chen, C.C., Akopian, A.N., Sivilotti, L., Colquhoun, D., Burnstock, G. and Wood, J.N. (1995) A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377, 428–431.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, 16773–16778.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, 386–396.CrossRefGoogle ScholarPubMed
Chizh, B.A. and Illes, P. (2001) P2X receptors and nociception. Pharmacology Review 53, 553–568.Google ScholarPubMed
Dolphin, A.C., Forda, S.R. and Scott, R.H. (1986) Calcium-dependent currents in cultured rat dorsal root ganglion neurones are inhibited by an adenosine analogue. Journal of Physiology 373, 47–61.CrossRefGoogle ScholarPubMed
Dong, X., Han, S., Zylka, M.J., Simon, M.I. and Anderson, D.J. (2001) A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 106, 619–632.CrossRefGoogle ScholarPubMed
Donnelly-Roberts, D., McGaraughty, S., Shieh, C.C., Honore, P. and Jarvis, M.F. (2008) Painful purinergic receptors. Journal of Pharmacology and Experimental Therapeutics 324, 409–415.CrossRefGoogle ScholarPubMed
Dunn, P.M., Zhong, Y. and Burnstock, G. (2001) P2X receptors in peripheral neurons. Progress in Neurobiology 65, 107–134.CrossRefGoogle ScholarPubMed
England, S., Heblich, F., James, I.F., Robbins, J. and Docherty, R.J. (2001) Bradykinin evokes a Ca2 +-activated chloride current in non-neuronal cells isolated from neonatal rat dorsal root ganglia. Journal of Physiology 530, 395–403.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, 3877–3883.CrossRefGoogle ScholarPubMed
Fields, R.D. and Stevens, B. (2000) ATP: an extracellular signaling molecule between neurons and glia. Trends in Neuroscience 23, 625–633.CrossRefGoogle ScholarPubMed
Fredholm, B.B., IJzerman, A.P., Jacobson, K.A., Klotz, K.N. and Linden, J. (2001) International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacological Reviews 53, 527–552.Google ScholarPubMed
Gerevich, Z. and Illes, P. (2004) P2Y receptors and pain transmission. Purinergic Signalling 1, 3–10.CrossRefGoogle ScholarPubMed
Gerevich, Z., Muller, C. and Illes, P. (2005) Metabotropic P2Y1 receptors inhibit P2X3 receptor-channels in rat dorsal root ganglion neurons. European Journal of Pharmacology 521, 34–38.CrossRefGoogle ScholarPubMed
Giaume, C. and Venance, L. (1998) Intercellular calcium signaling and gap junctional communication in astrocytes. Glia 24, 50–64.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Gorzalka, S., Vittori, S., Volpini, R., Cristalli, G., von Kugelgen, I. and Muller, C.E. (2005) Evidence for the functional expression and pharmacological characterization of adenine receptors in native cells and tissues. Molecular Pharmacology 67, 955–964.CrossRefGoogle ScholarPubMed
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Brain Research Reviews 48, 457–476.CrossRefGoogle ScholarPubMed
Hanani, M., Huang, T.Y., Cherkas, P.S., Ledda, M. and Pannese, E. (2002) Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience 114, 279–283.CrossRefGoogle ScholarPubMed
Haydon, P.G. (2001) GLIA: listening and talking to the synapse. Nature Reviews Neuroscience 2, 185–193.CrossRefGoogle Scholar
Honore, P., Donnelly-Roberts, D., Namovic, M.T., Hsieh, G., Zhu, C.Z., Mikusa, J.P. et al. (2006) A-740003 [N-(1-{[(cyanoimino)(5-quinolinylamino) methyl]amino}-2,2-dimethylpropyl)-2-(3,4-dimethoxyphenyl)acetamide], a novel and selective P2X7 receptor antagonist, dose-dependently reduces neuropathic pain in the rat. Journal of Pharmacology and Experimental Therapeutics 319, 1376–1385.CrossRefGoogle ScholarPubMed
Huang, T.Y., Belzer, V. and Hanani, M. (2009) Gap junctions in dorsal root ganglia: possible contribution to visceral pain. European Journal of Pain 14, 49.e1–49.e11.Google ScholarPubMed
Huang, H., Wu, X., Nicol, G.D., Meller, S. and Vasko, M.R. (2003) ATP augments peptide release from rat sensory neurons in culture through activation of P2Y receptors. Journal of Pharmacology and Experimental Therapeutics 306, 1137–1144.CrossRefGoogle ScholarPubMed
Illes, P. and Ribeiro, J.A. (2004) Neuronal P2 receptors of the central nervous system. Current Topics in Medicinal Chemistry 4, 831–838.CrossRefGoogle ScholarPubMed
Inoue, K. (2008) Purinergic systems in microglia. Cellular and Molecular Life Sciences 65, 3074–3080.CrossRefGoogle ScholarPubMed
Jacobson, K.A., Jarvis, M.F. and Williams, M. (2002) Purine and pyrimidine (P2) receptors as drug targets. Journal of Medicinal Chemistry 45, 4057–4093.CrossRefGoogle ScholarPubMed
Jarvis, M.F. (2003) Contributions of P2X3 homomeric and heteromeric channels to acute and chronic pain. Expert Opinion on Therapeutic Targets 7, 513–522.CrossRefGoogle ScholarPubMed
Jarvis, M.F. (2010) The neural–glial purinergic receptor ensemble in chronic pain states. Trends in Neurosciences 33, 48–57.CrossRefGoogle ScholarPubMed
Kim, Y.S., Paik, S.K., Cho, Y.S., Shin, H.S., Bae, J.Y., Moritani, M. et al. (2008) Expression of P2X3 receptor in the trigeminal sensory nuclei of the rat. Journal of Comparative Neurology 506, 627–639.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, 377–390.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, 443–454.CrossRefGoogle ScholarPubMed
Krishtal, O.A., Marchenko, S.M. and Pidoplichko, V.I. (1983) Receptor for ATP in the membrane of mammalian sensory neurones. Neuroscience Letters 35, 41–45.CrossRefGoogle ScholarPubMed
Ledda, M., Blum, E., De Palo, S. and Hanani, M. (2009) Augmentation in gap junction-mediated cell coupling in dorsal root ganglia following sciatic nerve neuritis in the mouse. Neuroscience 164, 1538–1545.CrossRefGoogle ScholarPubMed
Li, J., Vause, C.V. and Durham, P.L. (2008) Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Research 1196, 22–32.CrossRefGoogle ScholarPubMed
Liu, X.J. and Salter, M.W. (2005) Purines and pain mechanisms: recent developments. Current Opinion in Investigational Drugs 6, 65–75.Google ScholarPubMed
Malin, S.A., Davis, B.M., Koerber, H.R., Reynolds, I.J., Albers, K.M. and Molliver, D.C. (2008) Thermal nociception and TRPV1 function are attenuated in mice lacking the nucleotide receptor P2Y2. Pain 138, 484–496.CrossRefGoogle ScholarPubMed
Matsuka, Y., Ono, T., Iwase, H., Mitrirattanakul, S., Omoto, K.S., Cho, T. et al. (2008) Altered ATP release and metabolism in dorsal root ganglia of neuropathic rats. Molecular Pain 4, 66.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, 1817–1828.CrossRefGoogle ScholarPubMed
Moriyama, T., Iida, T., Kobayashi, K., Higashi, T., Fukuoka, T., Tsumura, H. et al. (2003) Possible involvement of P2Y2 metabotropic receptors in ATP-induced transient receptor potential vanilloid receptor 1-mediated thermal hypersensitivity. Journal of Neuroscience 23, 6058–6062.CrossRefGoogle ScholarPubMed
Nakayama, S., Yamashita, T., Konishi, M., Kazama, H. and Kokubun, S. (2004) P2Y-mediated Ca2+ response is spatiotemporally graded and synchronized in sensory neurons: a two-photon photolysis study. The Faseb Journal 18, 1562–1564.CrossRefGoogle ScholarPubMed
Neusch, C., Weishaupt, J.H. and Bahr, M. (2003) Kir channels in the CNS: emerging new roles and implications for neurological diseases. Cell and Tissue Research 311, 131–138.CrossRefGoogle ScholarPubMed
North, R.A. (2002) Molecular physiology of P2X receptors. Physiology Reviews 82, 1013–1067.CrossRefGoogle ScholarPubMed
Ohara, P.T., Vit, J.P., Bhargava, A. and Jasmin, L. (2008) Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. Journal of Neurophysiology 100, 3064–3073.CrossRefGoogle ScholarPubMed
Ohara, P.T., Vit, J.P., Bhargava, A., Romero, M., Sundberg, C., Charles, A.C. et al. (2009) Gliopathic pain: when satellite glial cells go bad. Neuroscientist 15, 450–463.CrossRefGoogle ScholarPubMed
Petruska, J.C., Cooper, B.Y., Gu, J.G., Rau, K.K. and Johnson, R.D. (2000) Distribution of P2X1, P2X2, and P2X3 receptor subunits in rat primary afferents: relation to population markers and specific cell types. Journal of Chemical Neuroanatomy 20, 141–162.CrossRefGoogle ScholarPubMed
Rathbone, M.P., Middlemiss, P., Andrew, C., Caciagli, F., Ciccarelli, R., Di Iorio, P. et al. (1998) The trophic effects of purines and purinergic signaling in pathologic reactions of astrocytes. Alzheimer Disease and Associated Disorders 12 Suppl 2, S36–S45.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, 415–426.CrossRefGoogle ScholarPubMed
Sanada, M., Yasuda, H., Omatsu-Kanbe, M., Sango, K., Isono, T., Matsuura, H. et al. (2002) Increase in intracellular Ca2+ and calcitonin gene-related peptide release through metabotropic P2Y receptors in rat dorsal root ganglion neurons. Neuroscience 111, 413–422.CrossRefGoogle ScholarPubMed
Sanz, J.M., Chiozzi, P., Ferrari, D., Colaianna, M., Idzko, M., Falzoni, S. et al. (2009) Activation of microglia by amyloid-beta requires P2X7 receptor expression. Journal of Immunology 182, 4378–4385.CrossRefGoogle ScholarPubMed
Sawynok, J. (1998) Adenosine receptor activation and nociception. European Journal of Pharmacology 347, 1–11.CrossRefGoogle ScholarPubMed
Sawynok, J. (2007) Adenosine and ATP receptors. Handbook of Experimental Pharmacology 177, 309–328.CrossRefGoogle Scholar
Scemes, E. and Giaume, C. (2006) Astrocyte calcium waves: what they are and what they do. Glia 54, 716–725.CrossRefGoogle Scholar
Schmidt, A.P., Paniz, L., Schallenberger, C., Bohmer, A.E., Wofchuk, S.T., Elisabetsky, E. et al. (2010) Guanosine prevents thermal hyperalgesia in a rat model of peripheral mononeuropathy. Journal of Pain 11, 131–141.CrossRefGoogle Scholar
Simonetti, M., Fabbro, A., D'Arco, M., Zweyer, M., Nistri, A., Giniatullin, R. et al. (2006) Comparison of P2X and TRPV1 receptors in ganglia or primary culture of trigeminal neurons and their modulation by NGF or serotonin. Molecular Pain 2, 11.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 6, 1–9.Google ScholarPubMed
Svichar, N., Shmigol, A., Verkhratsky, A. and Kostyuk, P. (1997) ATP induces Ca2+ release from IP3-sensitive Ca2+ stores exclusively in large DRG neurones. Neuroreport 8, 1555–1559.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, 155–166.CrossRefGoogle ScholarPubMed
Takeda, M., Takahashi, M. and Matsumoto, S. (2009) Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neuroscience Biobehavioural Reviews 33, 784–792.CrossRefGoogle ScholarPubMed
Thalakoti, S., Patil, V.V., Damodaram, S., Vause, C.V., Langford, L.E., Freeman, S.E. et al. (2007) Neuron–glia signaling in trigeminal ganglion: implications for migraine pathology. Headache 47, 1008–1023; discussion 1024–1005.CrossRefGoogle ScholarPubMed
Traversa, U., Bombi, G., Camaioni, E., Macchiarulo, A., Costantino, G., Palmieri, C. et al. (2003) Rat brain guanosine binding site. Biological studies and pseudo-receptor construction. Bioorganic Medicinal Chemistry 11, 5417–5425.CrossRefGoogle ScholarPubMed
Traversa, U., Bombi, G., Di Iorio, P., Ciccarelli, R., Werstiuk, E.S. and Rathbone, M.P. (2002) Specific [3H]-guanosine binding sites in rat brain membranes. British Journal of Pharmacology 135, 969–976.CrossRefGoogle ScholarPubMed
Tsuda, M., Kuboyama, K., Inoue, T., Nagata, K., Tozaki-Saitoh, H. and Inoue, K. (2009a) Behavioral phenotypes of mice lacking purinergic P2X4 receptors in acute and chronic pain assays. Molecular Pain 5, 28.CrossRefGoogle ScholarPubMed
Tsuda, M., Tozaki-Saitoh, H. and Inoue, K. (2010) Pain and purinergic signaling. Brain Research Reviews 63, 222–232.CrossRefGoogle ScholarPubMed
Tung, E.K., Choi, R.C., Siow, N.L., Jiang, J.X., Ling, K.K., Simon, J. et al. (2004) P2Y2 receptor activation regulates the expression of acetylcholinesterase and acetylcholine receptor genes at vertebrate neuromuscular junctions. Molecular Pharmacology 66, 794–806.CrossRefGoogle ScholarPubMed
van den Maagdenberg, A.M., Pietrobon, D., Pizzorusso, T., Kaja, S., Broos, L.A., Cesetti, T. et al. (2004) A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 41, 701–710.CrossRefGoogle ScholarPubMed
Vega-Avelaira, D., Géranton, S.M. and Fitzgerald, M. (2009) Differential regulation of immune responses and macrophage/neuron interactions in the dorsal root ganglion in young and adult rats following nerve injury. Molecular Pain 5, 70.CrossRefGoogle Scholar
Verkhratsky, A., Krishtal, O.A. and Burnstock, G. (2009) Purinoceptors on neuroglia. Molecular Neurobiology 39, 190–208.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, 247–257.CrossRefGoogle ScholarPubMed
Vit, J.P., Ohara, P.T., Bhargava, A., Kelley, K. and Jasmin, L. (2008) Silencing the Kir4.1 potassium channel subunit in satellite glial cells of the rat trigeminal ganglion results in pain-like behavior in the absence of nerve injury. Journal of Neuroscience 28, 4161–4171.CrossRefGoogle ScholarPubMed
Vulchanova, L., Riedl, M.S., Shuster, S.J., Buell, G., Surprenant, A., North, R.A. et al. (1997) Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology 36, 1229–1242.CrossRefGoogle 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, 969–977.CrossRefGoogle ScholarPubMed
Willis, W.D. (2001) Role of neurotransmitters in sensitization of pain responses. Annual New York Academy of Sciences 933, 142–156.CrossRefGoogle ScholarPubMed
Xiao, H.S., Huang, Q.H., Zhang, F.X., Bao, L., Lu, Y.J., Guo, C. et al. (2002) Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proceedings of the National Academy of Sciences of the U.S.A. 99, 8360–8365.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, 9864–9869.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, 63–70.CrossRefGoogle ScholarPubMed
Zimmermann, K., Reeh, P.W. and Averbeck, B. (2002) ATP can enhance the proton-induced CGRP release through P2Y receptors and secondary PGE2 release in isolated rat dura mater. Pain 97, 259–265.CrossRefGoogle ScholarPubMed