Abstract
The purine adenosine 5′-triphosphate (ATP) and its breakdown products, ADP and adenosine, act as intercellular messenger molecules throughout the nervous system. While ATP contributes to fast synaptic transmission via activation of ionotropic P2X receptors as well as neuromodulation via metabotropic P2Y receptors, ADP and adenosine only stimulate P2Y and P1 receptors, respectively, thereby adjusting neuronal performance. Often glial cells are recipient as well as source for extracellular ATP. Hence, purinergic neuron-glia signalling contributes bidirectionally to information processing in the nervous system, including sensory organs and brain areas computing sensory information. In this review, we summarize recent data of purinergic neuron-glia communication in two sensory systems, the visual and the olfactory systems. In both retina and olfactory bulb, ATP is released by neurons and evokes Ca2+ transients in glial cells, viz. Müller cells, astrocytes and olfactory ensheathing cells. Glial Ca2+ signalling, in turn, affects homeostasis of the nervous tissue such as volume regulation and control of blood flow. In addition, ‘gliotransmitter’ release upon Ca2+ signalling—evoked by purinoceptor activation—modulates neuronal activity, thus contributing to the processing of sensory information.
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References
Abe M, Endoh T, Suzuki T (2003) Extracellular ATP-induced calcium channel inhibition mediated by P1/P2Y purinoceptors in hamster submandibular ganglion neurons. Br J Pharmacol 138:1535–1543
Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232–243
Au WW, Treloar HB, Greer CA (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68–80
Berkowicz DA, Trombley PQ, Shepherd GM (1994) Evidence for glutamate as the olfactory receptor cell neurotransmitter. J Neurophysiol 71:2557–2561
Boehm S (1998) Selective inhibition of M-type potassium channels in rat sympathetic neurons by uridine nucleotide preferring receptors. Br J Pharmacol 124:1261–1269
Bringmann A, Pannicke T, Weick M, Biedermann B, Uhlmann S, Kohen L, Wiedemann P, Reichenbach A (2002) Activation of P2Y receptors stimulates potassium and cation currents in acutely isolated human Müller (glial) cells. Glia 37:139–152
Brückner E, Grosche A, Pannicke T, Wiedemann P, Reichenbach A, Bringmann A (2012) Mechanisms of VEGF- and glutamate-induced inhibition of osmotic swelling of murine retinal glial (Müller) cells: indications for the involvement of vesicular glutamate release and connexin-mediated ATP release. Neurochem Res 37:268–278
Burnstock G (2006) Historical review: ATP as a neurotransmitter. Trends Pharmacol Sci 27:166–176
Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797
Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483
Cai Z, Schools GP, Kimelberg HK (2000) Metabotropic glutamate receptors in acutely isolated hippocampal astrocytes: developmental changes of mGluR5 mRNA and functional expression. Glia 29:70–80
Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D (1996) Cell fate determination in the vertebrate retina. Proc Natl Acad Sci U S A 93:589–595
Clemow DB, Brunjes PC (1996) Development of 5′-nucleotidase staining in the olfactory bulbs of normal and naris-occluded rats. Int J Dev Neurosci 14:901–911
Collo G, North RA, Kawashima E, Merlo-Pich E, Neidhart S, Surprenant A, Buell G (1996) Cloning OF P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J Neurosci 16:2495–2507
Cunha RA (2001) Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: different roles, different sources and different receptors. Neurochem Int 38:107–125
Cunha RA, Vizi ES, Ribeiro JA, Sebastião AM (1996) Preferential release of ATP and its extracellular catabolism as a source of adenosine upon high- but not low-frequency stimulation of rat hippocampal slices. J Neurochem 67:2180–2187
De Saint JD, Westbrook GL (2005) Detecting activity in olfactory bulb glomeruli with astrocyte recording. J Neurosci 25:2917–2924
De Saint JD, Hirnet D, Westbrook GL, Charpak S (2009) External tufted cells drive the output of olfactory bulb glomeruli. J Neurosci 29:2043–2052
Dilip R, Ishii T, Imada H, Wada-Kiyama Y, Kiyama R, Miyachi E, Kaneda M (2013) Distribution and development of P2Y1-purinoceptors in the mouse retina. J Mol Hist 44:639–644
Dittrich K, Sansone A, Hassenklöver T, Manzini I (2013) Purinergic receptor-induced Ca2+ signaling in the neuroepithelium of the vomeronasal organ of larval Xenopus laevis. Purin Signal. doi:10.1007/s11302-013-9402-3
Dixon AK, Gubitz AK, Sirinathsinghji DJ, Richardson PJ, Freeman TC (1996) Tissue distribution of adenosine receptor mRNAs in the rat. Br J Pharmacol 118:1461–1468
Doengi M, Deitmer JW, Lohr C (2008) New evidence for purinergic signaling in the olfactory bulb: A2A and P2Y1 receptors mediate intracellular calcium release in astrocytes. FASEB J 22:2368–2378
Doengi M, Hirnet D, Coulon P, Pape H, Deitmer JW, Lohr C (2009) GABA uptake-dependent Ca2+ signaling in developing olfactory bulb astrocytes. Proc Natl Acad Sci U S A 106:17570–17575
Doucette JR (1984) The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat Rec 210:385–391
Doucette R (1990) Glial influences on axonal growth in the primary olfactory system. Glia 3:433–449
Ennis M, Zimmer LA, Shipley MT (1996) Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. Neuroreport 7:989–992
Famiglietti EV Jr, Kolb H (1976) Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194:193–195
Filippov AK, Webb TE, Barnard EA, Brown DA (1999) Dual coupling of heterologously-expressed rat P2Y6 nucleotide receptors to N-type Ca2+ and M-type K+ currents in rat sympathetic neurones. Br J Pharmacol 126:1009–1017
Filippov AK, Simon J, Barnard EA, Brown DA (2003) Coupling of the nucleotide P2Y4 receptor to neuronal ion channels. Br J Pharmacol 138:400–406
Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310:1495–1499
Fischer T, Rotermund N, Lohr C, Hirnet D (2012) P2Y1 receptor activation by photolysis of caged ATP enhances neuronal network activity in the developing olfactory bulb. Purinergic Signal 8:191–198
Fries JE, Wheeler-Schilling TH, Guenther E, Kohler K (2004) Expression of P2Y1, P2Y2, P2Y4, and P2Y6 receptor subtypes in the rat retina. Invest Ophthalmol Vis Sci 45:3410–3417
Geiger JD, Nagy JI (1987) Ontogenesis of adenosine deaminase activity in rat brain. J Neurochem 48:147–153
Gerevich Z, Borvendeg SJ, Schroder W, Franke H, Wirkner K, Norenberg W, Furst S, Gillen C, Illes P (2004) Inhibition of N-type voltage-activated calcium channels in rat dorsal root ganglion neurons by P2Y receptors is a possible mechanism of ADP-induced analgesia. J Neurosci 24:797–807
Grosche A, Reichenbach A (2013) Developmental refining of neuroglial signaling? Science 339:152–153
Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A, Kettenmann H (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci 2:139–143
Guo W, Xu X, Gao X, Burnstock G, He C, Xiang Z (2008) Expression of P2X5 receptors in the mouse CNS. Neuroscience 156:673–692
Hagins WA, Penn RD, Yoshikami S (1970) Dark current and photocurrent in retinal rods. Biophys J 10:380–412
Hansel DE, Eipper BA, Ronnett GV (2001) Neuropeptide Y functions as a neuroproliferative factor. Nature 410:940–944
Hassenklöver T, Kurtanska S, Bartoszek I, Junek S, Schild D, Manzini I (2008) Nucleotide-induced Ca2+ signaling in sustentacular supporting cells of the olfactory epithelium. Glia 56:1614–1624
Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009–1031
Hayoz S, Jia C, Hegg CC (2012) Mechanisms of constitutive and ATP-evoked ATP release in neonatal mouse olfactory epithelium. BMC Neurosci 13:53
Hegg CC, Greenwood D, Huang W, Han P, Lucero MT (2003) Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 23:8291–8301
Hegg CC, Irwin M, Lucero MT (2009) Calcium store-mediated signaling in sustentacular cells of the mouse olfactory epithelium. Glia 57:634–644
Holton P (1959) The liberation of adenosine triphosphate on antidromic stimulation of sensory nerves. J Physiol 145:494–504
Housley GD, Marcotti W, Navaratnam D, Yamoah EN (2006) Hair cells—beyond the transducer. J Membr Biol 209:89–118
Housley GD, Bringmann A, Reichenbach A (2009) Purinergic signaling in special senses. Trends Neurosci 32:128–141
Iandiev I, Wurm A, Pannicke T, Wiedemann P, Reichenbach A, Robson SC, Zimmermann H, Bringmann A (2007) Ectonucleotidases in Müller glial cells of the rodent retina: involvement in inhibition of osmotic cell swelling. Purinergic Signal 3:423–433
Je H, Zhou J, Yang F, Lu B (2005) Distinct mechanisms for neurotrophin-3-induced acute and long-term synaptic potentiation. J Neurosci 25:11719–11729
Jia C, Doherty J, Crudgington S, Hegg C (2009) Activation of purinergic receptors induces proliferation and neuronal differentiation in Swiss Webster mouse olfactory epithelium. Neuroscience 163:120–128
Jia C, Roman C, Hegg CC (2010) Nickel sulfate induces location-dependent atrophy of mouse olfactory epithelium: protective and proliferative role of purinergic receptor activation. Toxicol Sci 115:547–556
Johansson B, Georgiev V, Fredholm BB (1997) Distribution and postnatal ontogeny of adenosine A2A receptors in rat brain: comparison with dopamine receptors. Neuroscience 80:1187–1207
Jonzon B, Fredholm BB (1985) Release of purines, noradrenaline, and GABA from rat hippocampal slices by field stimulation. J Neurochem 44:217–224
Jung J, Shin YH, Konishi H, Lee SJ, Kiyama H (2013) Possible ATP release through lysosomal exocytosis from primary sensory neurons. Biochem Biophys Res Commun 430:488–493
Kaelin-Lang A, Lauterburg T, Burgunder JM (1999) Expression of adenosine A2a receptors gene in the olfactory bulb and spinal cord of rat and mouse. Neurosci Lett 261:189–191
Kaneda M, Ishii T, Hosoya T (2008) Pathway-dependent modulation by P2-purinoceptors in the mouse retina. Eur J Neurosci 28:128–136
Kaneda M, Ito K, Shigematsu Y, Shimoda Y (2010) The OFF-pathway dominance of P2X2-purinoceptors is formed without visual experience. Neurosci Res 66:86–91
Kanekar S, Jia C, Hegg CC (2009) Purinergic receptor activation evokes neurotrophic factor neuropeptide Y release from neonatal mouse olfactory epithelial slices. J Neurosci Res 87:1424–1434
Kanjhan R, Housley GD, Burton LD, Christie DL, Kippenberger A, Thorne PR, Luo L, Ryan AF (1999) Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407:11–32
Karwoski CJ, Lu HK, Newman EA (1989) Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells. Science 244:578–580
Khakh BS, North RA (2012) Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 76:51–69
Klyuch BP, Dale N, Wall MJ (2012) Deletion of ecto-5′-nucleotidase (CD73) reveals direct action potential-dependent adenosine release. J Neurosci 32:3842–3847
Kofuji P, Biedermann B, Siddharthan V, Raap M, Iandiev I, Milenkovic I, Thomzig A, Veh RW, Bringmann A, Reichenbach A (2002) Kir potassium channel subunit expression in retinal glial cells: implications for spatial potassium buffering. Glia 39:292–303
Köles L, Leichsenring A, Rubini P, Illes P (2011) P2 receptor signaling in neurons and glial cells of the central nervous system. Adv Pharmacol 61:441–493
Kozlov AS, Angulo MC, Audinat E, Charpak S (2006) Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci U S A 103:10058–10063
Krügel K, Wurm A, Linnertz R, Pannicke T, Wiedemann P, Reichenbach A, Bringmann A (2010) Erythropoietin inhibits osmotic swelling of retinal glial cells by Janus kinase- and extracellular signal-regulated kinases1/2-mediated release of vascular endothelial growth factor. Neuroscience 165:1147–1158
Kur J, Newman EA (2014) Purinergic control of vascular tone in the retina. J Physiol 592:491–504
Langer D, Hammer K, Koszalka P, Schrader J, Robson S, Zimmermann H (2008) Distribution of ectonucleotidases in the rodent brain revisited. Cell Tissue Res 334:199–217
Larsson M, Sawada K, Morland C, Hiasa M, Ormel L, Moriyama Y, Gundersen V (2012) Functional and anatomical identification of a vesicular transporter mediating neuronal ATP release. Cereb Cortex 22:1203–1214
Lê KT, Villeneuve P, Ramjaun AR, McPherson PS, Beaudet A, Séguéla P (1998) Sensory presynaptic and widespread somatodendritic immunolocalization of central ionotropic P2X ATP receptors. Neuroscience 83:177–190
Li Y, Holtzclaw LA, Russell JT (2001) Müller cell Ca2+ waves evoked by purinergic receptor agonists in slices of rat retina. J Neurophysiol 85:986–994
Li H, Zhang Z, Blackburn MR, Wang SW, Ribelayga CP, O’Brien J (2013) Adenosine and dopamine receptors coregulate photoreceptor coupling via gap junction phosphorylation in mouse retina. J Neurosci 33:3135–3150
Liou GI, Auchampach JA, Hillard CJ, Zhu G, Yousufzai B, Mian S, Khan S, Khalifa Y (2008) Mediation of cannabidiol anti-inflammation in the retina by equilibrative nucleoside transporter and A2A adenosine receptor. Invest Ophthalmol Vis Sci 49:5526–5531
Lohr C, Thyssen A, Hirnet D (2011) Extrasynaptic neuron-glia communication: the how and why. Commun Integr Biol 4:109–111
Lovatt D, Xu Q, Liu W, Takano T, Smith NA, Schnermann J, Tieu K, Nedergaard M (2012) Neuronal adenosine release, and not astrocytic ATP release, mediates feedback inhibition of excitatory activity. Proc Natl Acad Sci U S A 109:6265–6270
Luthardt J, Borvendeg SJ, Sperlagh B, Poelchen W, Wirkner K, Illes P (2003) P2Y(1) receptor activation inhibits NMDA receptor-channels in layer V pyramidal neurons of the rat prefrontal and parietal cortex. Neurochem Int 42:161–172
Mahan LC, McVittie LD, Smyk-Randall EM, Nakata H, Monsma FJ, Gerfen CR, Sibley DR (1991) Cloning and expression of an A1 adenosine receptor from rat brain. Mol Pharmacol 40:1–7
Martín-Peña A, Acebes A, Rodríguez J, Sorribes A, de Polavieja GG, Fernández-Fúnez P, Ferrús A (2006) Age-independent synaptogenesis by phosphoinositide 3 kinase. J Neurosci 26:10199–10208
Martins RA, Pearson RA (2008) Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Res 1192:37–60
Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26:2862–2870
Mishra A, Newman EA (2010) Inhibition of inducible nitric oxide synthase reverses the loss of functional hyperemia in diabetic retinopathy. Glia 58:1996–2004
Neumann F, Wurm A, Linnertz R, Pannicke T, Iandiev I, Wiedemann P, Reichenbach A, Bringmann A (2010) Sex steroids inhibit osmotic swelling of retinal glial cells. Neurochem Res 35:522–530
Newman EA (2003) Glial cell inhibition of neurons by release of ATP. J Neurosci 23:1659–1666
Newman EA (2004) A dialogue between glia and neurons in the retina: modulation of neuronal excitability. Neuron Glia Biol 1:245–252
Newman EA (2004) Glial modulation of synaptic transmission in the retina. Glia 47:268–274
Newman EA (2005) Calcium increases in retinal glial cells evoked by light-induced neuronal activity. J Neurosci 25:5502–5510
Newman EA, Zahs KR (1997) Calcium waves in retinal glial cells. Science 275:844–847
Notomi S, Hisatomi T, Kanemaru T, Takeda A, Ikeda Y, Enaida H, Kroemer G, Ishibashi T (2011) Critical involvement of extracellular ATP acting on P2RX7 purinergic receptors in photoreceptor cell death. Am J Pathol 179:2798–2809
Oku H, Goto W, Kobayashi T, Okuno T, Hirao M, Sugiyama T, Yoneda S, Hara H, Ikeda T (2004) Adenosine protects cultured retinal neurons against NMDA-induced cell death through A1 receptors. Curr Eye Res 29:449–455
Pannicke T, Iandiev I, Uckermann O, Biedermann B, Kutzera F, Wiedemann P, Wolburg H, Reichenbach A, Bringmann A (2004) A potassium channel-linked mechanism of glial cell swelling in the postischemic retina. Mol Cell Neurosci 26:493–502
Parpura V, Heneka MT, Montana V, Oliet SHR, Schousboe A, Haydon PG, Stout RF, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A (2012) Glial cells in (patho)physiology. J Neurochem 121:4–27
Petzold GC, Murthy VN (2011) Role of astrocytes in neurovascular coupling. Neuron 71:782–797
Petzold GC, Albeanu DF, Sato TF, Murthy VN (2008) Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways. Neuron 58:897–910
Puthussery T, Fletcher EL (2004) Synaptic localization of P2X7 receptors in the rat retina. J Comp Neurol 472:13–23
Puthussery T, Fletcher EL (2006) P2X2 receptors on ganglion and amacrine cells in cone pathways of the rat retina. J Comp Neurol 496:595–609
Puthussery T, Yee P, Vingrys AJ, Fletcher EL (2006) Evidence for the involvement of purinergic P2X receptors in outer retinal processing. Eur J Neurosci 24:7–19
Reichenbach A, Bringmann A (2013) New functions of Müller cells. Glia 61:651–678
Reichenbach A, Derouiche A, Kirchhoff F (2010) Morphology and dynamics of perisynaptic glia. Brain Res Rev 63:11–25
Rieger A, Deitmer JW, Lohr C (2007) Axon-glia communication evokes calcium signaling in olfactory ensheathing cells of the developing olfactory bulb. Glia 55:352–359
Rillich K, Gentsch J, Reichenbach A, Bringmann A, Weick M (2009) Light stimulation evokes two different calcium responses in Müller glial cells of the guinea pig retina. Eur J Neurosci 29:1165–1176
Rosin DL, Robeva A, Woodard RL, Guyenet PG, Linden J (1998) Immunohistochemical localization of adenosine A2A receptors in the rat central nervous system. J Comp Neurol 401:163–186
Roux L, Benchenane K, Rothstein JD, Bonvento G, Giaume C (2011) Plasticity of astroglial networks in olfactory glomeruli. Proc Natl Acad Sci U S A 108:18442–18446
Schoen SW, Kreutzberg GW (1995) Evidence that 5′-nucleotidase is associated with malleable synapses—an enzyme cytochemical investigation of the olfactory bulb of adult rats. Neuroscience 65:37–50
Schoen SW, Kreutzberg GW (1997) 5′-Nucleotidase enzyme cytochemistry as a tool for revealing activated glial cells and malleable synapses in CNS development and regeneration. Brain Res Brain Res Protoc 1:33–43
Schubert P, Ogata T, Marchini C, Ferroni S, Rudolphi K (1997) Protective mechanisms of adenosine in neurons and glial cells. Ann N Y Acad Sci 825:1–10
Shigemoto R, Nakanishi S, Mizuno N (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322:121–135
Sholl-Franco A, Fragel-Madeira L, Macama Ada C, Linden R, Ventura AL (2010) ATP controls cell cycle and induces proliferation in the mouse developing retina. Int J Dev Neurosci 28:63–73
Simon J, Webb TE, Barnard EA (1997) Distribution of [35S]dATP alpha S binding sites in the adult rat neuraxis. Neuropharmacology 36:1243–1251
Singaravelu K, Lohr C, Deitmer JW (2006) Regulation of store-operated calcium entry by calcium-independent phospholipase A2 in rat cerebellar astrocytes. J Neurosci 26:9579–9592
Slezak M, Grosche A, Niemiec A, Tanimoto N, Pannicke T, Münch TA, Crocker B, Isope P, Härtig W, Beck SC, Huber G, Ferracci G, Perraut M, Reber M, Miehe M, Demais V, Lévêque C, Metzger D, Szklarczyk K, Przewlocki R, Seeliger MW, Sage-Ciocca D, Hirrlinger J, Reichenbach A, Reibel S, Pfrieger FW (2012) Relevance of exocytotic glutamate release from retinal glia. Neuron 74:504–516
Stavermann M, Buddrus K, St John JA, Ekberg JA, Nilius B, Deitmer JW, Lohr C (2012) Temperature-dependent calcium-induced calcium release via InsP3 receptors in mouse olfactory ensheathing glial cells. Cell Calcium 52:113–123
Su Z, He C (2010) Olfactory ensheathing cells: biology in neural development and regeneration. Prog Neurobiol 92:517–532
Sun W, McConnell E, Pare J, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M (2013) Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339:197–200
Taruno A, Vingtdeux V, Ohmoto M, Ma Z, Dvoryanchikov G, Li A, Adrien L, Zhao H, Leung S, Abernethy M, Koppel J, Davies P, Civan MM, Chaudhari N, Matsumoto I, Hellekant G, Tordoff MG, Marambaud P, Foskett JK (2013) CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature 495:223–226
Thyssen A, Hirnet D, Wolburg H, Schmalzing G, Deitmer JW, Lohr C (2010) Ectopic vesicular neurotransmitter release along sensory axons mediates neurovascular coupling via glial calcium signaling. Proc Natl Acad Sci U S A 107:15258–15263
Thyssen A, Stavermann M, Buddrus K, Doengi M, Ekberg JA, St John JA, Deitmer JW, Lohr C (2013) Spatial and developmental heterogeneity of calcium signaling in olfactory ensheathing cells. Glia 61:327–337
Tian N (2004) Visual experience and maturation of retinal synaptic pathways. Vis Res 44:3307–3316
Tian G, Takano T, Lin JH, Wang X, Bekar L, Nedergaard M (2006) Imaging of cortical astrocytes using 2-photon laser scanning microscopy in the intact mouse brain. Adv Drug Deliv Rev 58:773–787
Tohda C, Nakanishi R, Kadowaki M (2006) Learning deficits and agenesis of synapses and myelinated axons in phosphoinositide-3 kinase-deficient mice. Neurosignals 15:293–306
Uckermann O, Grosche J, Reichenbach A, Bringmann A (2002) ATP-evoked calcium responses of radial glial (Müller) cells in the postnatal rabbit retina. J Neurosci Res 70:209–218
Uckermann O, Kutzera F, Wolf A, Pannicke T, Reichenbach A, Wiedemann P, Wolf S, Bringmann A (2005) The glucocorticoid triamcinolone acetonide inhibits osmotic swelling of retinal glial cells via stimulation of endogenous adenosine signaling. J Pharmacol Exp Ther 315:1036–1045
Valverde F, Lopez-Mascaraque L (1991) Neuroglial arrangements in the olfactory glomeruli of the hedgehog. J Comp Neurol 307:658–674
van den Pol AN (1995) Presynaptic metabotropic glutamate receptors in adult and developing neurons: autoexcitation in the olfactory bulb. J Comp Neurol 359:253–271
Verkhratsky A, Krishtal OA, Burnstock G (2009) Purinoceptors on neuroglia. Mol Neurobiol 39:190–208
Vessey KA, Fletcher EL (2012) Rod and cone pathway signalling is altered in the P2X7 receptor knock out mouse. PLoS ONE 7:e29990
Vogalis F, Hegg CC, Lucero MT (2005) Electrical coupling in sustentacular cells of the mouse olfactory epithelium. J Neurophysiol 94:1001–1012
Vogler S, Grosche A, Pannicke T, Ulbricht E, Wiedemann P, Reichenbach A, Bringmann A (2013) Hypoosmotic and glutamate-induced swelling of bipolar cells in the rat retina: comparison with swelling of Müller glial cells. J Neurochem 126:372–381
Vulchanova L, Arvidsson U, Riedl M, Wang J, Buell G, Surprenant A, North RA, Elde R (1996) Differential distribution of two ATP-gated channels (P2X receptors) determined by immunocytochemistry. Proc Natl Acad Sci U S A 93:8063–8067
Wahl V, Vogler S, Grosche A, Pannicke T, Ueffing M, Wiedemann P, Reichenbach A, Hauck S, Bringmann A (2013) Osteopontin inhibits osmotic swelling of retinal glial (Müller) cells by inducing release of VEGF. Neuroscience 246:59–72
Wall MJ, Dale N (2013) Neuronal transporter and astrocytic ATP exocytosis underlie activity-dependent adenosine release in the hippocampus. J Physiol Lond 591:3853–3871
Wang Q, Liu L, Pei L, Ju W, Ahmadian G, Lu J, Wang Y, Liu F, Wang YT (2003) Control of synaptic strength, a novel function of Akt. Neuron 38:915–928
Ward MM, Fletcher EL (2009) Subsets of retinal neurons and glia express P2Y1 receptors. Neuroscience 160:555–566
Ward MM, Puthussery T, Fletcher EL (2008) Localization and possible function of P2Y4 receptors in the rodent retina. Neuroscience 155:1262–1274
Weuste M, Wurm A, Iandiev I, Wiedemann P, Reichenbach A, Bringmann A (2006) HB-EGF: increase in the ischemic rat retina and inhibition of osmotic glial cell swelling. Biochem Biophys Res Commun 347:310–318
Wirkner K, Koles L, Thummler S, Luthardt J, Poelchen W, Franke H, Furst S, Illes P (2002) Interaction between P2Y and NMDA receptors in layer V pyramidal neurons of the rat prefrontal cortex. Neuropharmacology 42:476–488
Wirkner K, Sperlagh B, Illes P (2007) P2X3 receptor involvement in pain states. Mol Neurobiol 36:165–183
Wong ROL, Ghosh A (2002) Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3:803–812
Wurm A, Pannicke T, Iandiev I, Bühner E, Pietsch U, Reichenbach A, Wiedemann P, Uhlmann S, Bringmann A (2006) Changes in membrane conductance play a pathogenic role in osmotic glial cell swelling in detached retinas. Am J Pathol 169:1990–1998
Wurm A, Pannicke T, Iandiev I, Wiedemann P, Reichenbach A, Bringmann A (2006) The developmental expression of K+ channels in retinal glial cells is associated with a decrease of osmotic cell swelling. Glia 54:411–423
Wurm A, Iandiev I, Hollborn M, Wiedemann P, Reichenbach A, Zimmermann H, Bringmann A, Pannicke T (2008) Purinergic receptor activation inhibits osmotic glial cell swelling in the diabetic rat retina. Exp Eye Res 87:385–393
Wurm A, Erdmann I, Bringmann A, Reichenbach A, Pannicke T (2009) Expression and function of P2Y receptors on Müller cells of the postnatal rat retina. Glia 57:1680–1690
Wurm A, Lipp S, Pannicke T, Linnertz R, Färber K, Wiedemann P, Reichenbach A, Bringmann A (2009) Involvement of A1 adenosine receptors in osmotic volume regulation of retinal glial cells in mice. Mol Vis 15:1858–1867
Wurm A, Lipp S, Pannicke T, Linnertz R, Krügel U, Schulz A, Färber K, Zahn D, Grosse J, Wiedemann P, Chen J, Schöneberg T, Illes P, Reichenbach A, Bringmann A (2010) Endogenous purinergic signaling is required for osmotic volume regulation of retinal glial cells. J Neurochem 112:1261–1272
Wurm A, Pannicke T, Iandiev I, Francke M, Hollborn M, Wiedemann P, Reichenbach A, Osborne NN, Bringmann A (2011) Purinergic signaling involved in Müller cell function in the mammalian retina. Prog Retin Eye Res 30:324–342
Young RW (1984) Cell death during differentiation of the retina in the mouse. J Comp Neurol 229:362–373
Zhang X, Zhang M, Laties AM, Mitchell CH (2006) Balance of purines may determine life or death of retinal ganglion cells as A3 adenosine receptors prevent loss following P2X7 receptor stimulation. J Neurochem 98:566–575
Zhang X, Chen Y, Wang C, Huang LM (2007) Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci U S A 104:9864–9869
Zhang PP, Yang XL, Zhong YM (2012) Cellular localization of P2Y6 receptor in rat retina. Neuroscience 220:62–69
Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflugers Arch 452:573–588
Acknowledgments
Financial support by the Deutsche Forschungsgemeinschaft (LO779/3 and GRK845 to C.L.; LO779/6 to C.L. and D.H.; RE849/12, RE 849/16, GRK 1097 and SPP 1172 to A.R.; FOR 748 to A.G. and A.R.; GR4403/1-1 to A.G.), the EU FP 7 Program EduGlia 237956 to A.R. and the PRO RETINA-Stiftung to A.G. is gratefully acknowledged.
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Lohr, C., Grosche, A., Reichenbach, A. et al. Purinergic neuron-glia interactions in sensory systems. Pflugers Arch - Eur J Physiol 466, 1859–1872 (2014). https://doi.org/10.1007/s00424-014-1510-6
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DOI: https://doi.org/10.1007/s00424-014-1510-6