SpringerLink
Log in

Purinergic and Glutamatergic Receptors on Astroglia

  • Chapter
  • First Online:
Glutamate and ATP at the Interface of Metabolism and Signaling in the Brain

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 11))

Abstract

Astroglial cells express many neurotransmitter receptors; the receptors to glutamate and ATP being the most abundant. Here, we provide a concise overview on the expression and main properties of astroglial glutamate receptors (ionotropic receptors represented by AMPA and NMDA subtypes) and metabotropic (mainly mGluR5 and mGluR3 subtypes) and purinoceptors (adenosine receptors of A1, A2A, A2B, and A3 types, ionotropic P2X1/5 and P2X7 subtypes, and metabotropic P2Y purinoceptors). We also discuss the role of these receptors in glial physiology and pathophysiology.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abbracchio MP, Ceruti S, Langfelder R, Cattabeni F, Saffrey MJ, Burnstock G (1995) Effects of ATP analogues and basic fibroblast growth factor on astroglial cell differentiation in primary cultures of rat striatum. Int J Dev Neurosci 13:685–693

    PubMed  CAS  Google Scholar 

  • Abbracchio MP, Ceruti S, Brambilla R, Franceschi C, Malorni W, Jacobson KA, von Lubitz DK, Cattabeni F (1997) Modulation of apoptosis by adenosine in the central nervous system: a possible role for the A3 receptor. Pathophysiological significance and therapeutic implications for neurodegenerative disorders. Ann N Y Acad Sci 825:11–22

    PubMed  CAS  PubMed Central  Google Scholar 

  • Abbracchio MP, Cerut S, Brambilla R, Barbieri D, Camurri A, Franceschi C, Giammarioli AM, Jacobson KA, Cattabeni F, Malorni W (1998) Adenosine A3 receptors and viability of astrocytes. Drug Dev Res 45:379–386

    CAS  Google Scholar 

  • Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19–29

    PubMed  CAS  Google Scholar 

  • Abdipranoto A, Liu GJ, Werry EL, Bennett MR (2003) Mechanisms of secretion of ATP from cortical astrocytes triggered by uridine triphosphate. Neuroreport 14:2177–2181

    PubMed  CAS  Google Scholar 

  • Alberdi E, Sanchez-Gomez MV, Matute C (2005) Calcium and glial cell death. Cell Calcium 38:417–425

    PubMed  CAS  Google Scholar 

  • Alloisio S, Cugnoli C, Ferroni S, Nobile M (2004) Differential modulation of ATP-induced calcium signalling by A1 and A2 adenosine receptors in cultured cortical astrocytes. Br J Pharmacol 141:935–942

    PubMed  CAS  PubMed Central  Google Scholar 

  • Anderson CM, Bergher JP, Swanson RA (2004) ATP-induced ATP release from astrocytes. J Neurochem 88:246–256

    PubMed  CAS  Google Scholar 

  • Appel E, Kazimirsky G, Ashkenazi E, Kim SG, Jacobson KA, Brodie C (2001) Roles of BCL-2 and caspase 3 in the adenosine A3 receptor-induced apoptosis. J Mol Neurosci 17:285–292

    PubMed  CAS  Google Scholar 

  • Aronica E, van Vliet EA, Mayboroda OA, Troost D, da Silva FH, Gorter JA (2000) Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur J Neurosci 12:2333–2344

    PubMed  CAS  Google Scholar 

  • Ashour F, Deuchars J (2004) Electron microscopic localisation of P2X4 receptor subunit immunoreactivity to pre- and post-synaptic neuronal elements and glial processes in the dorsal vagal complex of the rat. Brain Res 1026:44–55

    PubMed  CAS  Google Scholar 

  • Ballerini P, Rathbone MP, Di Iorio P, Renzetti A, Giuliani P, D’Alimonte I, Trubiani O, Caciagli F, Ciccarelli R (1996) Rat astroglial P2Z (P2X7) receptors regulate intracellular calcium and purine release. Neuroreport 7:2533–2537

    PubMed  CAS  Google Scholar 

  • Ballerini P, Ciccarelli R, Caciagli F, Rathbone MP, Werstiuk ES, Traversa U, Buccella S, Giuliani P, Jang S, Nargi E, Visini D, Santavenere C, Di Iorio P (2005) P2X7 receptor activation in rat brain cultured astrocytes increases the biosynthetic release of cysteinyl leukotrienes. Int J Immunopathol Pharmacol 18:417–430

    PubMed  CAS  Google Scholar 

  • Bennett GC, Ford AP, Smith JA, Emmett CJ, Webb TE, Boarder MR (2003) P2Y receptor regulation of cultured rat cerebral cortical cells: calcium responses and mRNA expression in neurons and glia. Br J Pharmacol 139:279–288

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bennett MR, Buljan V, Farnell L, Gibson WG (2006) Purinergic junctional transmission and propagation of calcium waves in spinal cord astrocyte networks. Biophys J 91:3560–3571

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bergles DE, Roberts JD, Somogyi P, Jahr CE (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187–191

    PubMed  CAS  Google Scholar 

  • Biber K, Klotz KN, Berger M, Gebicke-Harter PJ, van Calker D (1997) Adenosine A1 receptor-mediated activation of phospholipase C in cultured astrocytes depends on the level of receptor expression. J Neurosci 17:4956–4964

    PubMed  CAS  Google Scholar 

  • Biber K, Fiebich BL, Gebicke-Harter P, van Calker D (1999) Carbamazepine-induced upregulation of adenosine A1-receptors in astrocyte cultures affects coupling to the phosphoinositol signaling pathway. Neuropsychopharmacology 20:271–278

    PubMed  CAS  Google Scholar 

  • Biber K, Lubrich B, Fiebich BL, Boddeke HW, van Calker D (2001) Interleukin-6 enhances expression of adenosine A(1) receptor mRNA and signaling in cultured rat cortical astrocytes and brain slices. Neuropsychopharmacology 24:86–96

    PubMed  CAS  Google Scholar 

  • Bjorklund O, Shang M, Tonazzini I, Dare E, Fredholm BB (2008) Adenosine A1 and A3 receptors protect astrocytes from hypoxic damage. Eur J Pharmacol 596:6–13

    PubMed  Google Scholar 

  • Bolego C, Ceruti S, Brambilla R, Puglisi L, Cattabeni F, Burnstock G, Abbracchio MP (1997) Characterization of the signalling pathways involved in ATP and basic fibroblast growth factor-induced astrogliosis. Br J Pharmacol 121:1692–1699

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bowie D (2012) Redefining the classification of AMPA-selective ionotropic glutamate receptors. J Physiol 590:49–61

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bowser DN, Khakh BS (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J Neurosci 24:8606–8620

    PubMed  CAS  Google Scholar 

  • Bowser DN, Khakh BS (2007) Vesicular ATP is the predominant cause of intercellular calcium waves in astrocytes. J Gen Physiol 129:485–491

    PubMed  CAS  PubMed Central  Google Scholar 

  • Brambilla R, Burnstock G, Bonazzi A, Ceruti S, Cattabeni F, Abbracchio MP (1999) Cyclo-oxygenase-2 mediates P2Y receptor-induced reactive astrogliosis. Br J Pharmacol 126:563–567

    PubMed  CAS  PubMed Central  Google Scholar 

  • Brambilla R, Ceruti S, Malorni W, Cattabeni F, Abbracchio MP (2000) A novel gliotic P2 receptor mediating cyclooxygenase-2 induction in rat and human astrocytes. J Auton Nerv Syst 81:3–9

    PubMed  CAS  Google Scholar 

  • Brambilla R, Neary JT, Cattabeni F, Cottini L, D’Ippolito G, Schiller PC, Abbracchio MP (2002) Induction of COX-2 and reactive gliosis by P2Y receptors in rat cortical astrocytes is dependent on ERK1/2 but independent of calcium signalling. J Neurochem 83:1285–1296

    PubMed  CAS  Google Scholar 

  • Brambilla R, Cottini L, Fumagalli M, Ceruti S, Abbracchio MP (2003) Blockade of A2A adenosine receptors prevents basic fibroblast growth factor-induced reactive astrogliosis in rat striatal primary astrocytes. Glia 43:190–194

    PubMed  Google Scholar 

  • Brand-Schieber E, Lowery SL, Werner P (2004) Select ionotropic glutamate AMPA/kainate receptors are expressed at the astrocyte-vessel interface. Brain Res 1007:178–182

    PubMed  CAS  Google Scholar 

  • Bringmann A, Pannicke T, Moll V, Milenkovic I, Faude F, Enzmann V, Wolf S, Reichenbach A (2001) Upregulation of P2X(7) receptor currents in Muller glial cells during proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 42:860–867

    PubMed  CAS  Google Scholar 

  • 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 Muller (glial) cells. Glia 37:139–152

    PubMed  Google Scholar 

  • Brodie C, Blumberg PM, Jacobson KA (1998) Activation of the A2A adenosine receptor inhibits nitric oxide production in glial cells. FEBS Lett 429:139–142

    PubMed  CAS  Google Scholar 

  • Bruner G, Murphy S (1990) ATP-evoked arachidonic acid mobilization in astrocytes is via a P2Y-purinergic receptor. J Neurochem 55:1569–1575

    PubMed  CAS  Google Scholar 

  • Bruner G, Murphy S (1993a) Purinergic P2Y receptors on astrocytes are directly coupled to phospholipase A2. Glia 7:219–224

    PubMed  CAS  Google Scholar 

  • Bruner G, Murphy S (1993b) UTP activates multiple second messenger systems in cultured rat astrocytes. Neurosci Lett 162:105–108

    PubMed  CAS  Google Scholar 

  • Burnashev N, Khodorova A, Jonas P, Helm PJ, Wisden W, Monyer H, Seeburg PH, Sakmann B (1992) Calcium-permeable AMPA-kainate receptors in fusiform cerebellar glial cells. Science 256:1566–1570

    PubMed  CAS  Google Scholar 

  • Burnstock G (1996) Purinoceptors: ontogeny and phylogeny. Drug Dev Res 39:204–242

    CAS  Google Scholar 

  • Burnstock G (2007a) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483

    PubMed  CAS  Google Scholar 

  • Burnstock G (2007b) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797

    PubMed  CAS  Google Scholar 

  • Burnstock G, Kennedy C (1985) Is there a basis for distinguishing two types of P2-purinoceptor? Gen Pharmacol 16:433–440

    PubMed  CAS  Google Scholar 

  • Burnstock G, Verkhratsky A (2009) Evolutionary origins of the purinergic signalling system. Acta Physiol (Oxf) 195:415–447

    CAS  Google Scholar 

  • Burnstock G, Verkhratsky A (2012) Purinergic signalling and the nervous system. Springer, Heidelberg

    Google Scholar 

  • Burnstock G, Fredholm BB, North RA, Verkhratsky A (2010) The birth and postnatal development of purinergic signalling. Acta Physiol (Oxf) 199:93–147

    CAS  Google Scholar 

  • Burnstock G, Fredholm BB, Verkhratsky A (2011) Adenosine and ATP receptors in the brain. Curr Top Med Chem 11:973–1011

    PubMed  CAS  Google Scholar 

  • Centemeri C, Bolego C, Abbracchio MP, Cattabeni F, Puglisi L, Burnstock G, Nicosia S (1997) Characterization of the Ca2+ responses evoked by ATP and other nucleotides in mammalian brain astrocytes. Br J Pharmacol 121:1700–1706

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chen CC, Chen WC (1996) ATP-evoked inositol phosphates formation through activation of P2U purinergic receptors in cultured astrocytes: regulation by PKC subtypes alpha, delta, and theta. Glia 17:63–71

    PubMed  CAS  Google Scholar 

  • Chen Y, Rathbone MP, Hertz L (2001) Guanosine-induced increase in free cytosolic calcium concentration in mouse astrocytes in primary cultures: does it act on an A3 adenosine receptor? J Neurosci Res 65:184–189

    PubMed  CAS  Google Scholar 

  • Choi JW, Yoo BK, Ryu MK, Choi MS, Park GH, Ko KH (2005) Adenosine and purine nucleosides prevent the disruption of mitochondrial transmembrane potential by peroxynitrite in rat primary astrocytes. Arch Pharm Res 28:810–815

    PubMed  CAS  Google Scholar 

  • Ciccarelli R, Di Iorio P, Ballerini P, Ambrosini G, Giuliani P, Tiboni GM, Caciagli F (1994) Effects of exogenous ATP and related analogues on the proliferation rate of dissociated primary cultures of rat astrocytes. J Neurosci Res 39:556–566

    PubMed  CAS  Google Scholar 

  • Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278:1354–1362

    PubMed  CAS  Google Scholar 

  • Condorelli DF, Conti F, Gallo V, Kirchhoff F, Seifert G, Steinhauser C, Verkhratsky A, Yuan X (1999) Expression and functional analysis of glutamate receptors in glial cells. Adv Exp Med Biol 468:49–67

    PubMed  CAS  Google Scholar 

  • Conti F, DeBiasi S, Minelli A, Melone M (1996) Expression of NR1 and NR2A/B subunits of the NMDA receptor in cortical astrocytes. Glia 17:254–258

    PubMed  CAS  Google Scholar 

  • Conti F, Minelli A, DeBiasi S, Melone M (1997) Neuronal and glial localization of NMDA receptors in the cerebral cortex. Mol Neurobiol 14:1–18

    PubMed  CAS  Google Scholar 

  • Cotrina ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M (1998) Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci U S A 95:15735–15740

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cotrina ML, Lin JH, Lopez-Garcia JC, Naus CC, Nedergaard M (2000) ATP-mediated glia signaling. J Neurosci 20:2835–2844

    PubMed  CAS  Google Scholar 

  • D’Alimonte I, Ballerini P, Nargi E, Buccella S, Giuliani P, Di Iorio P, Caciagli F, Ciccarelli R (2007a) Staurosporine-induced apoptosis in astrocytes is prevented by A1 adenosine receptor activation. Neurosci Lett 418:66–71

    PubMed  Google Scholar 

  • D’Alimonte I, Ciccarelli R, Di Iorio P, Nargi E, Buccella S, Giuliani P, Rathbone MP, Jiang S, Caciagli F, Ballerini P (2007b) Activation of P2X(7) receptors stimulates the expression of P2Y(2) receptor mRNA in astrocytes cultured from rat brain. Int J Immunopathol Pharmacol 20:301–316

    PubMed  Google Scholar 

  • Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105

    PubMed  CAS  Google Scholar 

  • Dave V, Gordon GW, McCarthy KD (1991) Cerebral type 2 astroglia are heterogeneous with respect to their ability to respond to neuroligands linked to calcium mobilization. Glia 4:440–447

    PubMed  CAS  Google Scholar 

  • Dixon SJ, Yu R, Panupinthu N, Wilson JX (2004) Activation of P2 nucleotide receptors stimulates acid efflux from astrocytes. Glia 47:367–376

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Domercq M, Brambilla L, Pilati E, Marchaland J, Volterra A, Bezzi P (2006) P2Y1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-alpha and prostaglandins. J Biol Chem 281:30684–30696

    PubMed  CAS  Google Scholar 

  • Duan S, Neary JT (2006) P2X7 receptors: properties and relevance to CNS function. Glia 54:738–746

    PubMed  Google Scholar 

  • Duan S, Anderson CM, Keung EC, Chen Y, Swanson RA (2003) P2X7 receptor-mediated release of excitatory amino acids from astrocytes. J Neurosci 23:1320–1328

    PubMed  CAS  Google Scholar 

  • Enkvist MO, Holopainen I, Akerman KE (1989) Glutamate receptor-linked changes in membrane potential and intracellular Ca2+ in primary rat astrocytes. Glia 2:397–402

    PubMed  CAS  Google Scholar 

  • Fam SR, Gallagher CJ, Salter MW (2000) P2Y(1) purinoceptor-mediated Ca(2+) signaling and Ca(2+) wave propagation in dorsal spinal cord astrocytes. J Neurosci 20:2800–2808

    PubMed  CAS  Google Scholar 

  • Fellin T, Pozzan T, Carmignoto G (2006) Purinergic receptors mediate two distinct glutamate release pathways in hippocampal astrocytes. J Biol Chem 281:4274–4284

    PubMed  CAS  Google Scholar 

  • Ferroni S, Marchini C, Ogata T, Schubert P (2002) Recovery of deficient cholinergic calcium signaling by adenosine in cultured rat cortical astrocytes. J Neurosci Res 68:615–621

    PubMed  CAS  Google Scholar 

  • Francke M, Uhlmann S, Pannicke T, Goczalik I, Uckermann O, Weick M, Hartig W, Wiedemann P, Reichenbach A, Bringmann A (2003) Experimental dispase-induced retinopathy causes up-regulation of P2Y receptor-mediated calcium responses in Muller glial cells. Ophthalmic Res 35:30–41

    PubMed  CAS  Google Scholar 

  • Franke H, Grosche J, Schadlich H, Krugel U, Allgaier C, Illes P (2001a) P2X receptor expression on astrocytes in the nucleus accumbens of rats. Neuroscience 108:421–429

    PubMed  CAS  Google Scholar 

  • Franke H, Krugel U, Schmidt R, Grosche J, Reichenbach A, Illes P (2001b) P2 receptor-types involved in astrogliosis in vivo. Br J Pharmacol 134:1180–1189

    PubMed  CAS  PubMed Central  Google Scholar 

  • Franke H, Gunther A, Grosche J, Schmidt R, Rossner S, Reinhardt R, Faber-Zuschratter H, Schneider D, Illes P (2004) P2X7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 63:686–699

    PubMed  CAS  Google Scholar 

  • Franke H, Verkhratsky A, Burnstock G, Illes P (2012) Pathophysiology of astroglial purinergic signalling. Purinergic Signal 8:629–657

    PubMed  CAS  PubMed Central  Google Scholar 

  • Fries JE, Wheeler-Schilling TH, Kohler K, Guenther E (2004) Distribution of metabotropic P2Y receptors in the rat retina: a single-cell RT-PCR study. Brain Res Mol Brain Res 130:1–6

    PubMed  CAS  Google Scholar 

  • Fries JE, Goczalik IM, Wheeler-Schilling TH, Kohler K, Guenther E, Wolf S, Wiedemann P, Bringmann A, Reichenbach A, Francke M, Pannicke T (2005) Identification of P2Y receptor subtypes in human muller glial cells by physiology, single cell RT-PCR, and immunohistochemistry. Invest Ophthalmol Vis Sci 46:3000–3007

    PubMed  Google Scholar 

  • Fumagalli M, Brambilla R, D’Ambrosi N, Volonte C, Matteoli M, Verderio C, Abbracchio MP (2003) Nucleotide-mediated calcium signaling in rat cortical astrocytes: role of P2X and P2Y receptors. Glia 43:218–230

    PubMed  Google Scholar 

  • Gallagher CJ, Salter MW (2003) Differential properties of astrocyte calcium waves mediated by P2Y1 and P2Y2 receptors. J Neurosci 23:6728–6739

    PubMed  CAS  Google Scholar 

  • Gallo V, Ghiani CA (2000) Glutamate receptors in glia: new cells, new inputs and new functions. Trends Pharmacol Sci 21:252–258

    PubMed  CAS  Google Scholar 

  • Garcia-Barcina JM, Matute C (1996) Expression of kainate-selective glutamate receptor subunits in glial cells of the adult bovine white matter. Eur J Neurosci 8:2379–2387

    PubMed  CAS  Google Scholar 

  • Gebicke-Haerter PJ, Wurster S, Schobert A, Hertting G (1988) P2-purinoceptor induced prostaglandin synthesis in primary rat astrocyte cultures. Naunyn Schmiedebergs Arch Pharmacol 338:704–707

    PubMed  CAS  Google Scholar 

  • Gerard F, Hansson E (2012) Inflammatory activation enhances NMDA-triggered Ca2+ signalling and IL-1beta secretion in primary cultures of rat astrocytes. Brain Res 1473:1–8

    PubMed  CAS  Google Scholar 

  • Haas B, Schipke CG, Peters O, Sohl G, Willecke K, Kettenmann H (2006) Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb Cortex 16:237–246

    PubMed  Google Scholar 

  • Hamilton N, Vayro S, Kirchhoff F, Verkhratsky A, Robbins J, Gorecki DC, Butt AM (2008) Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 56:734–749

    PubMed  Google Scholar 

  • Hindley S, Herman MA, Rathbone MP (1994) Stimulation of reactive astrogliosis in vivo by extracellular adenosine diphosphate or an adenosine A2 receptor agonist. J Neurosci Res 38:399–406

    PubMed  CAS  Google Scholar 

  • Hosli L, Hosli E, Uhr M, Della Briotta G (1987) Electrophysiological evidence for adenosine receptors on astrocytes of cultured rat central nervous system. Neurosci Lett 79:108–112

    PubMed  CAS  Google Scholar 

  • Illes P, Verkhratsky A, Burnstock G, Franke H (2012) P2X receptors and their roles in astroglia in the central and peripheral nervous system. Neuroscientist 18:422–438

    PubMed  CAS  Google Scholar 

  • Ishimoto H, Nakahata N, Matsuoka I, Nakanishi H (1997) Effects of ATP on phosphoinositide hydrolysis and prostaglandin E2 generation in rabbit astrocytes. J Pharm Pharmacol 49:520–524

    PubMed  CAS  Google Scholar 

  • Jabs R, Kirchhoff F, Kettenmann H, Steinhauser C (1994) Kainate activates Ca(2+)-permeable glutamate receptors and blocks voltage-gated K+ currents in glial cells of mouse hippocampal slices. Pflugers Arch 426:310–319

    PubMed  CAS  Google Scholar 

  • Jabs R, Guenther E, Marquordt K, Wheeler-Schilling TH (2000) Evidence for P2X(3), P2X(4), P2X(5) but not for P2X(7) containing purinergic receptors in Muller cells of the rat retina. Brain Res Mol Brain Res 76:205–210

    PubMed  CAS  Google Scholar 

  • James G, Butt AM (2001) P2X and P2Y purinoreceptors mediate ATP-evoked calcium signalling in optic nerve glia in situ. Cell Calcium 30:251–259

    PubMed  CAS  Google Scholar 

  • James G, Butt AM (2002) P2Y and P2X purinoceptor mediated Ca2+ signalling in glial cell pathology in the central nervous system. Eur J Pharmacol 447:247–260

    PubMed  CAS  Google Scholar 

  • Jeremic A, Jeftinija K, Stevanovic J, Glavaski A, Jeftinija S (2001) ATP stimulates calcium-dependent glutamate release from cultured astrocytes. J Neurochem 77:664–675

    PubMed  CAS  Google Scholar 

  • Jimenez AI, Castro E, Mirabet M, Franco R, Delicado EG, Miras-Portugal MT (1999) Potentiation of ATP calcium responses by A2B receptor stimulation and other signals coupled to Gs proteins in type-1 cerebellar astrocytes. Glia 26:119–128

    PubMed  CAS  Google Scholar 

  • Jimenez AI, Castro E, Communi D, Boeynaems JM, Delicado EG, Miras-Portugal MT (2000) Coexpression of several types of metabotropic nucleotide receptors in single cerebellar astrocytes. J Neurochem 75:2071–2079

    PubMed  CAS  Google Scholar 

  • John GR, Simpson JE, Woodroofe MN, Lee SC, Brosnan CF (2001) Extracellular nucleotides differentially regulate interleukin-1beta signaling in primary human astrocytes: implications for inflammatory gene expression. J Neurosci 21:4134–4142

    PubMed  CAS  Google Scholar 

  • Kanjhan R, Housley GD, Thorne PR, Christie DL, Palmer DJ, Luo L, Ryan AF (1996) Localization of ATP-gated ion channels in cerebellum using P2x2R subunit-specific antisera. Neuroreport 7:2665–2669

    PubMed  CAS  Google Scholar 

  • Karadottir R, Cavelier P, Bergersen LH, Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162–1166

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kastritsis CH, Salm AK, McCarthy K (1992) Stimulation of the P2Y purinergic receptor on type 1 astroglia results in inositol phosphate formation and calcium mobilization. J Neurochem 58:1277–1284

    PubMed  CAS  Google Scholar 

  • Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91:461–553

    PubMed  CAS  Google Scholar 

  • Kirchhoff F, Mulhardt C, Pastor A, Becker CM, Kettenmann H (1996) Expression of glycine receptor subunits in glial cells of the rat spinal cord. J Neurochem 66:1383–1390

    PubMed  CAS  Google Scholar 

  • Kirischuk S, Moller T, Voitenko N, Kettenmann H, Verkhratsky A (1995) ATP-induced cytoplasmic calcium mobilization in Bergmann glial cells. J Neurosci 15:7861–7871

    PubMed  CAS  Google Scholar 

  • Kirischuk S, Tuschick S, Verkhratsky A, Kettenmann H (1996a) Calcium signalling in mouse Bergmann glial cells mediated by α1-adrenoreceptors and H1 histamine receptors. Eur J Neurosci 8:1198–1208

    PubMed  CAS  Google Scholar 

  • Kirischuk S, Matiash V, Kulik A, Voitenko N, Kostyuk P, Verkhratsky A (1996b) Activation of P2-purino-, α1-adreno and H1-histamine receptors triggers cytoplasmic calcium signalling in cerebellar Purkinje neurons. Neuroscience 73:643–647

    PubMed  CAS  Google Scholar 

  • Kirischuk S, Kirchhoff F, Matyash V, Kettenmann H, Verkhratsky A (1999) Glutamate-triggered calcium signalling in mouse bergmann glial cells in situ: role of inositol-1,4,5-trisphosphate-mediated intracellular calcium release. Neuroscience 92:1051–1059

    PubMed  CAS  Google Scholar 

  • Kirischuk S, Parpura V, Verkhratsky A (2012) Sodium dynamics: another key to astroglial excitability? Trends Neurosci 35:497–506

    PubMed  CAS  Google Scholar 

  • Kucher BM, Neary JT (2005) Bi-functional effects of ATP/P2 receptor activation on tumor necrosis factor-alpha release in lipopolysaccharide-stimulated astrocytes. J Neurochem 92:525–535

    PubMed  CAS  Google Scholar 

  • Kukley M, Barden JA, Steinhauser C, Jabs R (2001) Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 36:11–21

    PubMed  CAS  Google Scholar 

  • Lalo U, Pankratov Y, Kirchhoff F, North RA, Verkhratsky A (2006) NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. J Neurosci 26:2673–2683

    PubMed  CAS  Google Scholar 

  • Lalo U, Pankratov Y, Wichert SP, Rossner MJ, North RA, Kirchhoff F, Verkhratsky A (2008) P2X1 and P2X5 subunits form the functional P2X receptor in mouse cortical astrocytes. J Neurosci 28:5473–5480

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lalo U, Verkhratsky A, Pankratov Y (2011a) Ionotropic ATP receptors in neuronal-glial communication. Semin Cell Dev Biol 22:220–228

    PubMed  CAS  Google Scholar 

  • Lalo U, Pankratov Y, Parpura V, Verkhratsky A (2011b) Ionotropic receptors in neuronal-astroglial signalling: what is the role of “excitable” molecules in non-excitable cells. Biochim Biophys Acta 1813:992–1002

    PubMed  CAS  Google Scholar 

  • Lee M, Lee SJ, Choi HJ, Jung YW, Frokiaer J, Nielsen S, Kwon TH (2008) Regulation of AQP4 protein expression in rat brain astrocytes: role of P2X7 receptor activation. Brain Res 1195:1–11

    PubMed  CAS  Google Scholar 

  • Lee MC, Ting KK, Adams S, Brew BJ, Chung R, Guillemin GJ (2010) Characterisation of the expression of NMDA receptors in human astrocytes. PLoS One 5:e14123

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lin SC, Bergles DE (2002) Physiological characteristics of NG2-expressing glial cells. J Neurocytol 31:537–549

    PubMed  CAS  Google Scholar 

  • Loesch A, Burnstock G (1998) Electron-immunocytochemical localization of P2X1 receptors in the rat cerebellum. Cell Tissue Res 294:253–260

    PubMed  CAS  Google Scholar 

  • Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C (2003) Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23:1750–1758

    PubMed  CAS  Google Scholar 

  • Mayer ML (2005) Glutamate receptor ion channels. Curr Opin Neurobiol 15:282–288

    PubMed  CAS  Google Scholar 

  • McCarthy KD, Salm AK (1991) Pharmacologically-distinct subsets of astroglia can be identified by their calcium response to neuroligands. Neuroscience 41:325–333

    PubMed  CAS  Google Scholar 

  • McDougal DH, Hermann GE, Rogers RC (2011) Vagal afferent stimulation activates astrocytes in the nucleus of the solitary tract via AMPA receptors: evidence of an atypical neural-glial interaction in the brainstem. J Neurosci 31:14037–14045

    PubMed  CAS  PubMed Central  Google Scholar 

  • Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, Yin X, Trapp BD, McRory JE, Rehak R, Zamponi GW, Wang W, Stys PK (2006) NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439:988–992

    PubMed  CAS  Google Scholar 

  • Miyazaki I, Asanuma M, Diaz-Corrales FJ, Miyoshi K, Ogawa N (2004) Direct evidence for expression of dopamine receptors in astrocytes from basal ganglia. Brain Res 1029:120–123

    PubMed  CAS  Google Scholar 

  • Muller T, Moller T, Berger T, Schnitzer J, Kettenmann H (1992) Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells. Science 256: 1563–1566

    PubMed  CAS  Google Scholar 

  • Narcisse L, Scemes E, Zhao Y, Lee SC, Brosnan CF (2005) The cytokine IL-1β transiently enhances P2X7 receptor expression and function in human astrocytes. Glia 49:245–258

    PubMed  PubMed Central  Google Scholar 

  • Nishizaki T, Nagai K, Nomura T, Tada H, Kanno T, Tozaki H, Li XX, Kondoh T, Kodama N, Takahashi E, Sakai N, Tanaka K, Saito N (2002) A new neuromodulatory pathway with a glial contribution mediated via A(2a) adenosine receptors. Glia 39:133–147

    PubMed  CAS  Google Scholar 

  • Nobile M, Monaldi I, Alloisio S, Cugnoli C, Ferroni S (2003) ATP-induced, sustained calcium signalling in cultured rat cortical astrocytes: evidence for a non-capacitative, P2X7-like-mediated calcium entry. FEBS Lett 538:71–76

    PubMed  CAS  Google Scholar 

  • Noda M, Nakanishi H, Nabekura J, Akaike N (2000) AMPA-kainate subtypes of glutamate receptor in rat cerebral microglia. J Neurosci 20:251–258

    PubMed  CAS  Google Scholar 

  • Norenberg W, Schunk J, Fischer W, Sobottka H, Riedel T, Oliveira JF, Franke H, Illes P (2010) Electrophysiological classification of P2X7 receptors in rat cultured neocortical astroglia. Br J Pharmacol 160:1941–1952

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ogata T, Nakamura Y, Tsuji K, Shibata T, Kataoka K, Schubert P (1994) Adenosine enhances intracellular Ca2+ mobilization in conjunction with metabotropic glutamate receptor activation by t-ACPD in cultured hippocampal astrocytes. Neurosci Lett 170:5–8

    PubMed  CAS  Google Scholar 

  • Oliveira JF, Riedel T, Leichsenring A, Heine C, Franke H, Krugel U, Norenberg W, Illes P (2011) Rodent cortical astroglia express in situ functional P2X7 receptors sensing pathologically high ATP concentrations. Cereb Cortex 21:806–820

    PubMed  Google Scholar 

  • Palygin O, Lalo U, Verkhratsky A, Pankratov Y (2010) Ionotropic NMDA and P2X1/5 receptors mediate synaptically induced Ca2+ signalling in cortical astrocytes. Cell Calcium 48:225–231

    PubMed  CAS  Google Scholar 

  • Palygin O, Lalo U, Pankratov Y (2011) Distinct pharmacological and functional properties of NMDA receptors in mouse cortical astrocytes. Br J Pharmacol 163:1755–1766

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pankratov Y, Lalo U, Verkhratsky A, North RA (2006) Vesicular release of ATP at central synapses. Pflugers Arch 452:589–597

    PubMed  CAS  Google Scholar 

  • Pannicke T, Fischer W, Biedermann B, Schadlich H, Grosche J, Faude F, Wiedemann P, Allgaier C, Illes P, Burnstock G, Reichenbach A (2000) P2X7 receptors in Muller glial cells from the human retina. J Neurosci 20:5965–5972

    PubMed  CAS  Google Scholar 

  • Parfenova H, Tcheranova D, Basuroy S, Fedinec AL, Liu J, Leffler CW (2012) Functional role of astrocyte glutamate receptors and carbon monoxide in cerebral vasodilation response to glutamate. Am J Physiol Heart Circ Physiol 302:H2257–H2266

    PubMed  CAS  PubMed Central  Google Scholar 

  • Parpura V, Verkhratsky A (2012) Homeostatic function of astrocytes: Ca(2+) and Na(+) signalling. Transl Neurosci 3:334–344

    PubMed  PubMed Central  Google Scholar 

  • Parpura V, Verkhratsky A (2013) Astroglial amino acid-based transmitter receptors. Amino Acids 44:1151–1158

    PubMed  CAS  Google Scholar 

  • Parpura V, Grubisic V, Verkhratsky A (2011) Ca2+ sources for the exocytotic release of glutamate from astrocytes. Biochim Biophys Acta 1813:984–991

    PubMed  CAS  Google Scholar 

  • Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, 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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Peakman MC, Hill SJ (1994) Adenosine A2B-receptor-mediated cyclic AMP accumulation in primary rat astrocytes. Br J Pharmacol 111:191–198

    PubMed  CAS  PubMed Central  Google Scholar 

  • Peakman MC, Hill SJ (1995) Adenosine A1 receptor-mediated changes in basal and histamine-stimulated levels of intracellular calcium in primary rat astrocytes. Br J Pharmacol 115:801–810

    PubMed  CAS  PubMed Central  Google Scholar 

  • Peakman MC, Hill SJ (1996) Adenosine A1 receptor-mediated inhibition of cyclic AMP accumulation in type-2 but not type-1 rat astrocytes. Eur J Pharmacol 306:281–289

    PubMed  CAS  Google Scholar 

  • Pearce B, Langley D (1994) Purine- and pyrimidine-stimulated phosphoinositide breakdown and intracellular calcium mobilisation in astrocytes. Brain Res 660:329–332

    PubMed  CAS  Google Scholar 

  • Pearce B, Murphy S, Jeremy J, Morrow C, Dandona P (1989) ATP-evoked Ca2+ mobilisation and prostanoid release from astrocytes: P2-purinergic receptors linked to phosphoinositide hydrolysis. J Neurochem 52:971–977

    PubMed  CAS  Google Scholar 

  • Perrais D, Veran J, Mulle C (2010) Gating and permeation of kainate receptors: differences unveiled. Trends Pharmacol Sci 31:516–522

    PubMed  CAS  Google Scholar 

  • Petralia RS, Wang YX, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71:949–976

    PubMed  CAS  Google Scholar 

  • Piet R, Jahr CE (2007) Glutamatergic and purinergic receptor-mediated calcium transients in Bergmann glial cells. J Neurosci 27:4027–4035

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pilitsis JG, Kimelberg HK (1998) Adenosine receptor mediated stimulation of intracellular calcium in acutely isolated astrocytes. Brain Res 798:294–303

    PubMed  CAS  Google Scholar 

  • Porter JT, McCarthy KD (1995a) Adenosine receptors modulate [Ca2+]i in hippocampal astrocytes in situ. J Neurochem 65:1515–1523

    PubMed  CAS  Google Scholar 

  • Porter JT, McCarthy KD (1995b) GFAP-positive hippocampal astrocytes in situ respond to glutamatergic neuroligands with increases in [Ca2+]i. Glia 13:101–112

    PubMed  CAS  Google Scholar 

  • Reifel Saltzberg JM, Garvey KA, Keirstead SA (2003) Pharmacological characterization of P2Y receptor subtypes on isolated tiger salamander Muller cells. Glia 42:149–159

    PubMed  Google Scholar 

  • Salter MG, Fern R (2005) NMDA receptors are expressed in develo** oligodendrocyte processes and mediate injury. Nature 438:1167–1171

    PubMed  CAS  Google Scholar 

  • Salter MW, Hicks JL (1994) ATP-evoked increases in intracellular calcium in neurons and glia from the dorsal spinal cord. J Neurosci 14:1563–1575

    PubMed  CAS  Google Scholar 

  • Salter MW, Hicks JL (1995) ATP causes release of intracellular Ca2+ via the phospholipase C beta/IP3 pathway in astrocytes from the dorsal spinal cord. J Neurosci 15:2961–2971

    PubMed  CAS  Google Scholar 

  • Schipke CG, Ohlemeyer C, Matyash M, Nolte C, Kettenmann H, Kirchhoff F (2001) Astrocytes of the mouse neocortex express functional N-methyl-D-aspartate receptors. FASEB J 15:1270–1272

    PubMed  CAS  Google Scholar 

  • Seifert G, Steinhauser C (2001) Ionotropic glutamate receptors in astrocytes. Prog Brain Res 132:287–299

    PubMed  CAS  Google Scholar 

  • Shao Y, McCarthy KD (1994) Plasticity of astrocytes. Glia 11:147–155

    PubMed  CAS  Google Scholar 

  • Striedinger K, Meda P, Scemes E (2007) Exocytosis of ATP from astrocyte progenitors modulates spontaneous Ca2+ oscillations and cell migration. Glia 55:652–662

    PubMed  PubMed Central  Google Scholar 

  • Suadicani SO, Brosnan CF, Scemes E (2006) P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 26:1378–1385

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sun W, McConnell E, Pare JF, 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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106:481–503

    PubMed  CAS  Google Scholar 

  • Toms NJ, Roberts PJ (1999) Group 1 mGlu receptors elevate [Ca2+]i in rat cultured cortical type 2 astrocytes: [Ca2+]i synergy with adenosine A1 receptors. Neuropharmacology 38:1511–1517

    PubMed  CAS  Google Scholar 

  • Tran MD, Neary JT (2006) Purinergic signaling induces thrombospondin-1 expression in astrocytes. Proc Natl Acad Sci U S A 103:9321–9326

    PubMed  CAS  PubMed Central  Google Scholar 

  • Troadec JD, Thirion S, Petturiti D, Bohn MT, Poujeol P (1999) ATP acting on P2Y receptors triggers calcium mobilization in primary cultures of rat neurohypophysial astrocytes (pituicytes). Pflugers Arch 437:745–753

    PubMed  CAS  Google Scholar 

  • Uchiyama M, Nakajima Y, Sakuma Y, Kato M (2001) Purinergic regulation of intracellular Ca2+ concentration of rat pituitary folliculo-stellate cells in primary culture. J Neuroendocrinol 13:378–385

    PubMed  CAS  Google Scholar 

  • Uckermann O, Uhlmann S, Weick M, Pannicke T, Francke M, Reichenbach A, Wiedemann P, Bringmann A (2003) Upregulation of purinergic P2Y receptor-mediated calcium responses in glial cells during experimental detachment of the rabbit retina. Neurosci Lett 338:131–134

    PubMed  CAS  Google Scholar 

  • Vargas JR, Takahashi DK, Thomson KE, Wilcox KS (2013) The expression of kainate receptor subunits in hippocampal astrocytes after experimentally induced status epilepticus. J Neuropathol Exp Neurol 72:919–932

    PubMed  CAS  Google Scholar 

  • Verkhratsky A (2010) Physiology of neuronal-glial networking. Neurochem Int 57:332–343

    PubMed  CAS  Google Scholar 

  • Verkhratsky A, Kirchhoff F (2007a) NMDA receptors in glia. Neuroscientist 13:28–37

    PubMed  CAS  Google Scholar 

  • Verkhratsky A, Kirchhoff F (2007b) Glutamate-mediated neuronal-glial transmission. J Anat 210:651–660

    PubMed  CAS  PubMed Central  Google Scholar 

  • Verkhratsky A, Shmigol A (1996) Calcium-induced calcium release in neurones. Cell Calcium 19:1–14

    PubMed  CAS  Google Scholar 

  • Verkhratsky A, Steinhauser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380–412

    PubMed  CAS  Google Scholar 

  • Verkhratsky A, Orkand RK, Kettenmann H (1998) Glial calcium: homeostasis and signaling function. Physiol Rev 78:99–141

    PubMed  CAS  Google Scholar 

  • Verkhratsky A, Krishtal OA, Burnstock G (2009) Purinoceptors on neuroglia. Mol Neurobiol 39:190–208

    PubMed  CAS  Google Scholar 

  • Verkhratsky A, Parpura V, Rodriguez JJ (2011) Where the thoughts dwell: the physiology of neuronal-glial “diffuse neural net”. Brain Res Rev 66:133–151

    PubMed  Google Scholar 

  • Verkhratsky A, Rodriguez JJ, Parpura V (2012a) Calcium signalling in astroglia. Mol Cell Endocrinol 353:45–56

    PubMed  CAS  Google Scholar 

  • Verkhratsky A, Rodriguez JJ, Parpura V (2012b) Neurotransmitters and integration in neuronal-astroglial networks. Neurochem Res 37:2326–2338

    PubMed  CAS  Google Scholar 

  • Walter L, Dinh T, Stella N (2004) ATP induces a rapid and pronounced increase in 2-arachidonoylglycerol production by astrocytes, a response limited by monoacylglycerol lipase. J Neurosci 24:8068–8074

    PubMed  CAS  Google Scholar 

  • Wirkner K, Gunther A, Weber M, Guzman SJ, Krause T, Fuchs J, Koles L, Norenberg W, Illes P (2007) Modulation of NMDA receptor current in layer V pyramidal neurons of the rat prefrontal cortex by P2Y receptor activation. Cereb Cortex 17:621–631

    PubMed  Google Scholar 

  • Wisden W, Seeburg PH (1993) Mammalian ionotropic glutamate receptors. Curr Opin Neurobiol 3:291–298

    PubMed  CAS  Google Scholar 

  • Wittendorp MC, Boddeke HW, Biber K (2004) Adenosine A3 receptor-induced CCL2 synthesis in cultured mouse astrocytes. Glia 46:410–418

    PubMed  Google Scholar 

  • Woods MD, Freshney RI, Ball SG, Vaughan PF (1989) Regulation of cyclic AMP formation in cultures of human foetal astrocytes by beta 2-adrenergic and adenosine receptors. J Neurochem 53:864–869

    PubMed  CAS  Google Scholar 

  • Zhou Y, Li HL, Zhao R, Yang LT, Dong Y, Yue X, Ma YY, Wang Z, Chen J, Cui CL, Yu AC (2010) Astrocytes express N-methyl-D-aspartate receptor subunits in development, ischemia and post-ischemia. Neurochem Res 35:2124–2134

    PubMed  CAS  Google Scholar 

  • Zhu Y, Kimelberg HK (2004) Cellular expression of P2Y and beta-AR receptor mRNAs and proteins in freshly isolated astrocytes and tissue sections from the CA1 region of P8-12 rat hippocampus. Brain Res Dev Brain Res 148:77–87

    PubMed  CAS  Google Scholar 

  • Ziak D, Chvatal A, Sykova E (1998) Glutamate-, kainate- and NMDA-evoked membrane currents in identified glial cells in rat spinal cord slice. Physiol Res 47:365–375

    PubMed  CAS  Google Scholar 

Download references

Conflict of Interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Faculty of Life Sciences, School of Biological Sciences, The University of Manchester, 1.124 Stopford Building, Oxford Road, Manchester, M13 9PT, UK

    Alexei Verkhratsky M.D., Ph.D., D.Sc.

  2. Achucarro Center for Neuroscience, IKERBASQUE, Basque Foundation for Science, 48011, Bilbao, Spain

    Alexei Verkhratsky M.D., Ph.D., D.Sc.

  3. Department of Neurosciences, University of the Basque Country UPV/EHU, 48940, Leioa, Spain

    Alexei Verkhratsky M.D., Ph.D., D.Sc.

  4. Autonomic Neuroscience Centre, Royal Free and University College Medical School, Rowland Hill Street, London, NW3 2PF, UK

    Geoffrey Burnstock

  5. Department of Pharmacology and Therapeutics, The University of Melbourne, Melbourne, Australia

    Geoffrey Burnstock

Authors
  1. Alexei Verkhratsky M.D., Ph.D., D.Sc.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geoffrey Burnstock
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Alexei Verkhratsky M.D., Ph.D., D.Sc. or Geoffrey Burnstock .

Editor information

Editors and Affiliations

  1. Department of Neurobiology CIRC 429, University of Alabama, Birmingham, Alabama, USA

    Vladimir Parpura

  2. Faculty of Health and Medical Sciences, Department of Drug Design and Pharmacology, University of Copenhagen, Copenhagen, Denmark

    Arne Schousboe

  3. Faculty of Life Sciences, The University of Manchester, Manchester, United Kingdom

    Alexei Verkhratsky

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Verkhratsky, A., Burnstock, G. (2014). Purinergic and Glutamatergic Receptors on Astroglia. In: Parpura, V., Schousboe, A., Verkhratsky, A. (eds) Glutamate and ATP at the Interface of Metabolism and Signaling in the Brain. Advances in Neurobiology, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-319-08894-5_4

Download citation

Publish with us

Policies and ethics

Search

Navigation