Pflügers Archiv - European Journal of Physiology

, Volume 466, Issue 10, pp 1859–1872 | Cite as

Purinergic neuron-glia interactions in sensory systems

Invited Review


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.


ATP Adenosine Purinoceptors Retina Olfactory bulb Müller cells Ensheathing cells Astrocytes 


  1. 1.
    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 138:1535–1543PubMedPubMedCentralGoogle Scholar
  2. 2.
    Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232–243PubMedPubMedCentralGoogle Scholar
  3. 3.
    Au WW, Treloar HB, Greer CA (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68–80PubMedGoogle Scholar
  4. 4.
    Berkowicz DA, Trombley PQ, Shepherd GM (1994) Evidence for glutamate as the olfactory receptor cell neurotransmitter. J Neurophysiol 71:2557–2561PubMedGoogle Scholar
  5. 5.
    Boehm S (1998) Selective inhibition of M-type potassium channels in rat sympathetic neurons by uridine nucleotide preferring receptors. Br J Pharmacol 124:1261–1269PubMedPubMedCentralGoogle Scholar
  6. 6.
    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 37:139–152PubMedGoogle Scholar
  7. 7.
    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 37:268–278PubMedGoogle Scholar
  8. 8.
    Burnstock G (2006) Historical review: ATP as a neurotransmitter. Trends Pharmacol Sci 27:166–176PubMedGoogle Scholar
  9. 9.
    Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797PubMedGoogle Scholar
  10. 10.
    Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483PubMedGoogle Scholar
  11. 11.
    Cai Z, Schools GP, Kimelberg HK (2000) Metabotropic glutamate receptors in acutely isolated hippocampal astrocytes: developmental changes of mGluR5 mRNA and functional expression. Glia 29:70–80PubMedGoogle Scholar
  12. 12.
    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 93:589–595PubMedPubMedCentralGoogle Scholar
  13. 13.
    Clemow DB, Brunjes PC (1996) Development of 5′-nucleotidase staining in the olfactory bulbs of normal and naris-occluded rats. Int J Dev Neurosci 14:901–911PubMedGoogle Scholar
  14. 14.
    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 16:2495–2507PubMedGoogle Scholar
  15. 15.
    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 38:107–125PubMedGoogle Scholar
  16. 16.
    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 67:2180–2187PubMedGoogle Scholar
  17. 17.
    De Saint JD, Westbrook GL (2005) Detecting activity in olfactory bulb glomeruli with astrocyte recording. J Neurosci 25:2917–2924Google Scholar
  18. 18.
    De Saint JD, Hirnet D, Westbrook GL, Charpak S (2009) External tufted cells drive the output of olfactory bulb glomeruli. J Neurosci 29:2043–2052Google Scholar
  19. 19.
    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 44:639–644Google Scholar
  20. 20.
    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 Google Scholar
  21. 21.
    Dixon AK, Gubitz AK, Sirinathsinghji DJ, Richardson PJ, Freeman TC (1996) Tissue distribution of adenosine receptor mRNAs in the rat. Br J Pharmacol 118:1461–1468PubMedPubMedCentralGoogle Scholar
  22. 22.
    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 22:2368–2378PubMedGoogle Scholar
  23. 23.
    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 106:17570–17575PubMedPubMedCentralGoogle Scholar
  24. 24.
    Doucette JR (1984) The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat Rec 210:385–391PubMedGoogle Scholar
  25. 25.
    Doucette R (1990) Glial influences on axonal growth in the primary olfactory system. Glia 3:433–449PubMedGoogle Scholar
  26. 26.
    Ennis M, Zimmer LA, Shipley MT (1996) Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. Neuroreport 7:989–992PubMedGoogle Scholar
  27. 27.
    Famiglietti EV Jr, Kolb H (1976) Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194:193–195PubMedGoogle Scholar
  28. 28.
    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 126:1009–1017PubMedPubMedCentralGoogle Scholar
  29. 29.
    Filippov AK, Simon J, Barnard EA, Brown DA (2003) Coupling of the nucleotide P2Y4 receptor to neuronal ion channels. Br J Pharmacol 138:400–406PubMedPubMedCentralGoogle Scholar
  30. 30.
    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 310:1495–1499PubMedGoogle Scholar
  31. 31.
    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 8:191–198PubMedPubMedCentralGoogle Scholar
  32. 32.
    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 45:3410–3417PubMedGoogle Scholar
  33. 33.
    Geiger JD, Nagy JI (1987) Ontogenesis of adenosine deaminase activity in rat brain. J Neurochem 48:147–153PubMedGoogle Scholar
  34. 34.
    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 24:797–807PubMedGoogle Scholar
  35. 35.
    Grosche A, Reichenbach A (2013) Developmental refining of neuroglial signaling? Science 339:152–153PubMedGoogle Scholar
  36. 36.
    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 2:139–143PubMedGoogle Scholar
  37. 37.
    Guo W, Xu X, Gao X, Burnstock G, He C, Xiang Z (2008) Expression of P2X5 receptors in the mouse CNS. Neuroscience 156:673–692PubMedGoogle Scholar
  38. 38.
    Hagins WA, Penn RD, Yoshikami S (1970) Dark current and photocurrent in retinal rods. Biophys J 10:380–412PubMedPubMedCentralGoogle Scholar
  39. 39.
    Hansel DE, Eipper BA, Ronnett GV (2001) Neuropeptide Y functions as a neuroproliferative factor. Nature 410:940–944PubMedGoogle Scholar
  40. 40.
    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 56:1614–1624PubMedGoogle Scholar
  41. 41.
    Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009–1031PubMedGoogle Scholar
  42. 42.
    Hayoz S, Jia C, Hegg CC (2012) Mechanisms of constitutive and ATP-evoked ATP release in neonatal mouse olfactory epithelium. BMC Neurosci 13:53PubMedPubMedCentralGoogle Scholar
  43. 43.
    Hegg CC, Greenwood D, Huang W, Han P, Lucero MT (2003) Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 23:8291–8301PubMedPubMedCentralGoogle Scholar
  44. 44.
    Hegg CC, Irwin M, Lucero MT (2009) Calcium store-mediated signaling in sustentacular cells of the mouse olfactory epithelium. Glia 57:634–644PubMedPubMedCentralGoogle Scholar
  45. 45.
    Holton P (1959) The liberation of adenosine triphosphate on antidromic stimulation of sensory nerves. J Physiol 145:494–504PubMedPubMedCentralGoogle Scholar
  46. 46.
    Housley GD, Marcotti W, Navaratnam D, Yamoah EN (2006) Hair cells—beyond the transducer. J Membr Biol 209:89–118PubMedGoogle Scholar
  47. 47.
    Housley GD, Bringmann A, Reichenbach A (2009) Purinergic signaling in special senses. Trends Neurosci 32:128–141PubMedGoogle Scholar
  48. 48.
    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 3:423–433PubMedPubMedCentralGoogle Scholar
  49. 49.
    Je H, Zhou J, Yang F, Lu B (2005) Distinct mechanisms for neurotrophin-3-induced acute and long-term synaptic potentiation. J Neurosci 25:11719–11729PubMedGoogle Scholar
  50. 50.
    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 163:120–128PubMedPubMedCentralGoogle Scholar
  51. 51.
    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 115:547–556PubMedPubMedCentralGoogle Scholar
  52. 52.
    Johansson B, Georgiev V, Fredholm BB (1997) Distribution and postnatal ontogeny of adenosine A2A receptors in rat brain: comparison with dopamine receptors. Neuroscience 80:1187–1207PubMedGoogle Scholar
  53. 53.
    Jonzon B, Fredholm BB (1985) Release of purines, noradrenaline, and GABA from rat hippocampal slices by field stimulation. J Neurochem 44:217–224PubMedGoogle Scholar
  54. 54.
    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 430:488–493PubMedGoogle Scholar
  55. 55.
    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 261:189–191PubMedGoogle Scholar
  56. 56.
    Kaneda M, Ishii T, Hosoya T (2008) Pathway-dependent modulation by P2-purinoceptors in the mouse retina. Eur J Neurosci 28:128–136PubMedGoogle Scholar
  57. 57.
    Kaneda M, Ito K, Shigematsu Y, Shimoda Y (2010) The OFF-pathway dominance of P2X2-purinoceptors is formed without visual experience. Neurosci Res 66:86–91PubMedGoogle Scholar
  58. 58.
    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 87:1424–1434PubMedPubMedCentralGoogle Scholar
  59. 59.
    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 407:11–32PubMedGoogle Scholar
  60. 60.
    Karwoski CJ, Lu HK, Newman EA (1989) Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells. Science 244:578–580PubMedPubMedCentralGoogle Scholar
  61. 61.
    Khakh BS, North RA (2012) Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 76:51–69PubMedPubMedCentralGoogle Scholar
  62. 62.
    Klyuch BP, Dale N, Wall MJ (2012) Deletion of ecto-5′-nucleotidase (CD73) reveals direct action potential-dependent adenosine release. J Neurosci 32:3842–3847PubMedGoogle Scholar
  63. 63.
    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 39:292–303PubMedGoogle Scholar
  64. 64.
    Köles L, Leichsenring A, Rubini P, Illes P (2011) P2 receptor signaling in neurons and glial cells of the central nervous system. Adv Pharmacol 61:441–493PubMedGoogle Scholar
  65. 65.
    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 103:10058–10063PubMedPubMedCentralGoogle Scholar
  66. 66.
    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 165:1147–1158PubMedGoogle Scholar
  67. 67.
    Kur J, Newman EA (2014) Purinergic control of vascular tone in the retina. J Physiol 592:491–504PubMedGoogle Scholar
  68. 68.
    Langer D, Hammer K, Koszalka P, Schrader J, Robson S, Zimmermann H (2008) Distribution of ectonucleotidases in the rodent brain revisited. Cell Tissue Res 334:199–217PubMedGoogle Scholar
  69. 69.
    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 22:1203–1214PubMedGoogle Scholar
  70. 70.
    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 83:177–190PubMedGoogle Scholar
  71. 71.
    Li Y, Holtzclaw LA, Russell JT (2001) Müller cell Ca2+ waves evoked by purinergic receptor agonists in slices of rat retina. J Neurophysiol 85:986–994PubMedGoogle Scholar
  72. 72.
    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 33:3135–3150PubMedPubMedCentralGoogle Scholar
  73. 73.
    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 49:5526–5531PubMedPubMedCentralGoogle Scholar
  74. 74.
    Lohr C, Thyssen A, Hirnet D (2011) Extrasynaptic neuron-glia communication: the how and why. Commun Integr Biol 4:109–111PubMedPubMedCentralGoogle Scholar
  75. 75.
    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 109:6265–6270PubMedPubMedCentralGoogle Scholar
  76. 76.
    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 42:161–172PubMedGoogle Scholar
  77. 77.
    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 40:1–7PubMedGoogle Scholar
  78. 78.
    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 26:10199–10208PubMedGoogle Scholar
  79. 79.
    Martins RA, Pearson RA (2008) Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Res 1192:37–60PubMedGoogle Scholar
  80. 80.
    Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26:2862–2870PubMedPubMedCentralGoogle Scholar
  81. 81.
    Mishra A, Newman EA (2010) Inhibition of inducible nitric oxide synthase reverses the loss of functional hyperemia in diabetic retinopathy. Glia 58:1996–2004PubMedPubMedCentralGoogle Scholar
  82. 82.
    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 35:522–530PubMedGoogle Scholar
  83. 83.
    Newman EA (2003) Glial cell inhibition of neurons by release of ATP. J Neurosci 23:1659–1666PubMedPubMedCentralGoogle Scholar
  84. 84.
    Newman EA (2004) A dialogue between glia and neurons in the retina: modulation of neuronal excitability. Neuron Glia Biol 1:245–252PubMedPubMedCentralGoogle Scholar
  85. 85.
    Newman EA (2004) Glial modulation of synaptic transmission in the retina. Glia 47:268–274PubMedPubMedCentralGoogle Scholar
  86. 86.
    Newman EA (2005) Calcium increases in retinal glial cells evoked by light-induced neuronal activity. J Neurosci 25:5502–5510PubMedPubMedCentralGoogle Scholar
  87. 87.
    Newman EA, Zahs KR (1997) Calcium waves in retinal glial cells. Science 275:844–847PubMedPubMedCentralGoogle Scholar
  88. 88.
    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 179:2798–2809PubMedPubMedCentralGoogle Scholar
  89. 89.
    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 29:449–455PubMedGoogle Scholar
  90. 90.
    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 26:493–502PubMedGoogle Scholar
  91. 91.
    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 121:4–27PubMedPubMedCentralGoogle Scholar
  92. 92.
    Petzold GC, Murthy VN (2011) Role of astrocytes in neurovascular coupling. Neuron 71:782–797PubMedGoogle Scholar
  93. 93.
    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 58:897–910PubMedPubMedCentralGoogle Scholar
  94. 94.
    Puthussery T, Fletcher EL (2004) Synaptic localization of P2X7 receptors in the rat retina. J Comp Neurol 472:13–23PubMedGoogle Scholar
  95. 95.
    Puthussery T, Fletcher EL (2006) P2X2 receptors on ganglion and amacrine cells in cone pathways of the rat retina. J Comp Neurol 496:595–609PubMedGoogle Scholar
  96. 96.
    Puthussery T, Yee P, Vingrys AJ, Fletcher EL (2006) Evidence for the involvement of purinergic P2X receptors in outer retinal processing. Eur J Neurosci 24:7–19PubMedGoogle Scholar
  97. 97.
    Reichenbach A, Bringmann A (2013) New functions of Müller cells. Glia 61:651–678PubMedGoogle Scholar
  98. 98.
    Reichenbach A, Derouiche A, Kirchhoff F (2010) Morphology and dynamics of perisynaptic glia. Brain Res Rev 63:11–25PubMedGoogle Scholar
  99. 99.
    Rieger A, Deitmer JW, Lohr C (2007) Axon-glia communication evokes calcium signaling in olfactory ensheathing cells of the developing olfactory bulb. Glia 55:352–359PubMedGoogle Scholar
  100. 100.
    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 29:1165–1176PubMedGoogle Scholar
  101. 101.
    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 401:163–186PubMedGoogle Scholar
  102. 102.
    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 108:18442–18446PubMedPubMedCentralGoogle Scholar
  103. 103.
    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 65:37–50PubMedGoogle Scholar
  104. 104.
    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 1:33–43PubMedGoogle Scholar
  105. 105.
    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 825:1–10PubMedGoogle Scholar
  106. 106.
    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 322:121–135PubMedGoogle Scholar
  107. 107.
    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 28:63–73PubMedGoogle Scholar
  108. 108.
    Simon J, Webb TE, Barnard EA (1997) Distribution of [35S]dATP alpha S binding sites in the adult rat neuraxis. Neuropharmacology 36:1243–1251PubMedGoogle Scholar
  109. 109.
    Singaravelu K, Lohr C, Deitmer JW (2006) Regulation of store-operated calcium entry by calcium-independent phospholipase A2 in rat cerebellar astrocytes. J Neurosci 26:9579–9592PubMedGoogle Scholar
  110. 110.
    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 74:504–516PubMedGoogle Scholar
  111. 111.
    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 52:113–123PubMedGoogle Scholar
  112. 112.
    Su Z, He C (2010) Olfactory ensheathing cells: biology in neural development and regeneration. Prog Neurobiol 92:517–532PubMedGoogle Scholar
  113. 113.
    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 339:197–200PubMedPubMedCentralGoogle Scholar
  114. 114.
    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 495:223–226PubMedPubMedCentralGoogle Scholar
  115. 115.
    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 107:15258–15263PubMedPubMedCentralGoogle Scholar
  116. 116.
    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 61:327–337PubMedGoogle Scholar
  117. 117.
    Tian N (2004) Visual experience and maturation of retinal synaptic pathways. Vis Res 44:3307–3316PubMedGoogle Scholar
  118. 118.
    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 58:773–787PubMedGoogle Scholar
  119. 119.
    Tohda C, Nakanishi R, Kadowaki M (2006) Learning deficits and agenesis of synapses and myelinated axons in phosphoinositide-3 kinase-deficient mice. Neurosignals 15:293–306PubMedGoogle Scholar
  120. 120.
    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 70:209–218PubMedGoogle Scholar
  121. 121.
    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 315:1036–1045PubMedGoogle Scholar
  122. 122.
    Valverde F, Lopez-Mascaraque L (1991) Neuroglial arrangements in the olfactory glomeruli of the hedgehog. J Comp Neurol 307:658–674PubMedGoogle Scholar
  123. 123.
    van den Pol AN (1995) Presynaptic metabotropic glutamate receptors in adult and developing neurons: autoexcitation in the olfactory bulb. J Comp Neurol 359:253–271PubMedGoogle Scholar
  124. 124.
    Verkhratsky A, Krishtal OA, Burnstock G (2009) Purinoceptors on neuroglia. Mol Neurobiol 39:190–208PubMedGoogle Scholar
  125. 125.
    Vessey KA, Fletcher EL (2012) Rod and cone pathway signalling is altered in the P2X7 receptor knock out mouse. PLoS ONE 7:e29990PubMedPubMedCentralGoogle Scholar
  126. 126.
    Vogalis F, Hegg CC, Lucero MT (2005) Electrical coupling in sustentacular cells of the mouse olfactory epithelium. J Neurophysiol 94:1001–1012PubMedGoogle Scholar
  127. 127.
    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 126:372–381PubMedGoogle Scholar
  128. 128.
    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 93:8063–8067PubMedPubMedCentralGoogle Scholar
  129. 129.
    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 246:59–72PubMedGoogle Scholar
  130. 130.
    Wall MJ, Dale N (2013) Neuronal transporter and astrocytic ATP exocytosis underlie activity-dependent adenosine release in the hippocampus. J Physiol Lond 591:3853–3871PubMedPubMedCentralGoogle Scholar
  131. 131.
    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 38:915–928PubMedGoogle Scholar
  132. 132.
    Ward MM, Fletcher EL (2009) Subsets of retinal neurons and glia express P2Y1 receptors. Neuroscience 160:555–566PubMedGoogle Scholar
  133. 133.
    Ward MM, Puthussery T, Fletcher EL (2008) Localization and possible function of P2Y4 receptors in the rodent retina. Neuroscience 155:1262–1274PubMedGoogle Scholar
  134. 134.
    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 347:310–318PubMedGoogle Scholar
  135. 135.
    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 42:476–488PubMedGoogle Scholar
  136. 136.
    Wirkner K, Sperlagh B, Illes P (2007) P2X3 receptor involvement in pain states. Mol Neurobiol 36:165–183PubMedGoogle Scholar
  137. 137.
    Wong ROL, Ghosh A (2002) Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3:803–812PubMedGoogle Scholar
  138. 138.
    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 169:1990–1998PubMedPubMedCentralGoogle Scholar
  139. 139.
    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 54:411–423PubMedGoogle Scholar
  140. 140.
    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 87:385–393PubMedGoogle Scholar
  141. 141.
    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 57:1680–1690PubMedGoogle Scholar
  142. 142.
    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 15:1858–1867PubMedPubMedCentralGoogle Scholar
  143. 143.
    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 112:1261–1272PubMedGoogle Scholar
  144. 144.
    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 30:324–342PubMedGoogle Scholar
  145. 145.
    Young RW (1984) Cell death during differentiation of the retina in the mouse. J Comp Neurol 229:362–373PubMedGoogle Scholar
  146. 146.
    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 98:566–575PubMedGoogle Scholar
  147. 147.
    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 104:9864–9869PubMedPubMedCentralGoogle Scholar
  148. 148.
    Zhang PP, Yang XL, Zhong YM (2012) Cellular localization of P2Y6 receptor in rat retina. Neuroscience 220:62–69PubMedGoogle Scholar
  149. 149.
    Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflugers Arch 452:573–588PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Division of Neurophysiology, Biocenter GrindelUniversity of HamburgHamburgGermany
  2. 2.Institute of Human Genetics, Faculty of MedicineUniversity of RegensburgRegensburgGermany
  3. 3.Paul Flechsig Institute of Brain Research, Faculty of MedicineUniversity of LeipzigLeipzigGermany

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