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TRP Channels Coordinate Ion Signalling in Astroglia

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Part of the book series: Reviews of Physiology, Biochemistry and Pharmacology ((REVIEWS,volume 166))

Abstract

Astroglial excitability is based on highly spatio-temporally coordinated fluctuations of intracellular ion concentrations, among which changes in Ca2+ and Na+ take the leading role. Intracellular signals mediated by Ca2+ and Na+ target numerous molecular cascades that control gene expression, energy production and numerous homeostatic functions of astrocytes. Initiation of Ca2+ and Na+ signals relies upon plasmalemmal and intracellular channels that allow fluxes of respective ions down their concentration gradients. Astrocytes express several types of TRP channels of which TRPA1 channels are linked to regulation of functional expression of GABA transporters, whereas TRPV4 channels are activated following osmotic challenges and are up-regulated in ischaemic conditions. Astrocytes also ubiquitously express several isoforms of TRPC channels of which heteromers assembled from TRPC1, 4 and/or 5 subunits that likely act as stretch-activated channels and are linked to store-operated Ca2+ entry. The TRPC channels mediate large Na+ fluxes that are associated with the endoplasmic reticulum Ca2+ signalling machinery and hence coordinate Na+ and Ca2+ signalling in astroglia.

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References

  • Akita T, Okada Y (2011) Regulation of bradykinin-induced activation of volume-sensitive outwardly rectifying anion channels by Ca2+ nanodomains in mouse astrocytes. J Physiol 589:3909–3927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14

    Article  CAS  PubMed  Google Scholar 

  • Bai JZ, Lipski J (2010) Differential expression of TRPM2 and TRPV4 channels and their potential role in oxidative stress-induced cell death in organotypic hippocampal culture. Neurotoxicology 31:204–214

    Article  CAS  PubMed  Google Scholar 

  • Benfenati V, Ferroni S (2010) Water transport between CNS compartments: functional and molecular interactions between aquaporins and ion channels. Neuroscience 168:926–940

    Article  CAS  PubMed  Google Scholar 

  • Benfenati V, Amiry-Moghaddam M, Caprini M, Mylonakou MN, Rapisarda C, Ottersen OP, Ferroni S (2007) Expression and functional characterization of transient receptor potential vanilloid-related channel 4 (TRPV4) in rat cortical astrocytes. Neuroscience 148:876–892

    Article  CAS  PubMed  Google Scholar 

  • Benfenati V, Caprini M, Dovizio M, Mylonakou MN, Ferroni S, Ottersen OP, Amiry-Moghaddam M (2011) An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc Natl Acad Sci USA 108:2563–2568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beskina O, Miller A, Mazzocco-Spezzia A, Pulina MV, Golovina VA (2007) Mechanisms of interleukin-1β-induced Ca2+ signals in mouse cortical astrocytes: roles of store- and receptor-operated Ca2+ entry. Am J Physiol Cell Physiol 293:C1103–C1111

    Article  CAS  PubMed  Google Scholar 

  • Black JA, Newcombe J, Waxman SG (2010) Astrocytes within multiple sclerosis lesions upregulate sodium channel Nav1.5. Brain 133:835–846

    Article  PubMed  Google Scholar 

  • Boison D, Chen JF, Fredholm BB (2010) Adenosine signaling and function in glial cells. Cell Death Differ 17:1071–1082

    Article  CAS  PubMed  Google Scholar 

  • Broer S, Brookes N (2001) Transfer of glutamine between astrocytes and neurons. J Neurochem 77:705–719

    Article  CAS  PubMed  Google Scholar 

  • Burdakov D, Petersen OH, Verkhratsky A (2005) Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium 38:303–310

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Butenko O, Dzamba D, Benesova J, Honsa P, Benfenati V, Rusnakova V, Ferroni S, Anderova M (2012) The increased activity of TRPV4 channel in the astrocytes of the adult rat hippocampus after cerebral hypoxia/ischemia. PLoS One 7:e39959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cahalan MD (2009) STIMulating store-operated Ca2+ entry. Nat Cell Biol 11:669–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carmignoto G, Gomez-Gonzalo M (2010) The contribution of astrocyte signalling to neurovascular coupling. Brain Res Rev 63:138–148

    Article  CAS  PubMed  Google Scholar 

  • Carrasco S, Meyer T (2011) STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu Rev Biochem 80:973–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cebolla B, Fernandez-Perez A, Perea G, Araque A, Vallejo M (2008) DREAM mediates cAMP-dependent, Ca2+-induced stimulation of GFAP gene expression and regulates cortical astrogliogenesis. J Neurosci 28:6703–6713

    Article  CAS  PubMed  Google Scholar 

  • Charles AC, Merrill JE, Dirksen ER, Sanderson MJ (1991) Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6:983–992

    Article  CAS  PubMed  Google Scholar 

  • Conner MT, Conner AC, Bland CE, Taylor LH, Brown JE, Parri HR, Bill RM (2012) Rapid aquaporin translocation regulates cellular water flow: mechanism of hypotonicity-induced subcellular localization of aquaporin 1 water channel. J Biol Chem 287:11516–11525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conti F, Minelli A, Melone M (2004) GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications. Brain Res Brain Res Rev 45:196–212

    Article  CAS  PubMed  Google Scholar 

  • Cornell Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long- range glial signaling. Science 247:470–473

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • De Keyser J, Mostert JP, Koch MW (2008) Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders. J Neurol Sci 267:3–16

    Article  PubMed  CAS  Google Scholar 

  • Deitmer JW, Rose CR (2010) Ion changes and signalling in perisynaptic glia. Brain Res Rev 63:113–129

    Article  CAS  PubMed  Google Scholar 

  • Eder P, Poteser M, Romanin C, Groschner K (2005) Na+ entry and modulation of Na+/Ca2+ exchange as a key mechanism of TRPC signaling. Pflugers Arch 451:99–104

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Fernandez S, Almeida A, Bolanos JP (2012) Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochem J 443:3–11

    Article  CAS  PubMed  Google Scholar 

  • Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185

    Article  CAS  PubMed  Google Scholar 

  • Finkbeiner SM (1993) Glial calcium. Glia 9:83–104

    Article  CAS  PubMed  Google Scholar 

  • Giaume C, Kirchhoff F, Matute C, Reichenbach A, Verkhratsky A (2007) Glia: the fulcrum of brain diseases. Cell Death Differ 14:1324–1335

    Article  CAS  PubMed  Google Scholar 

  • Golovina VA (2005) Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J Physiol 564:737–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomeza J, Hulsmann S, Ohno K, Eulenburg V, Szoke K, Richter D, Betz H (2003) Inactivation of the glycine transporter 1 gene discloses vital role of glial glycine uptake in glycinergic inhibition. Neuron 40:785–796

    Article  CAS  PubMed  Google Scholar 

  • Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S (2010) Astrocytes control breathing through pH-dependent release of ATP. Science 329:571–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimaldi M, Maratos M, Verma A (2003) Transient receptor potential channel activation causes a novel form of [Ca2+]i oscillations and is not involved in capacitative Ca2+ entry in glial cells. J Neurosci 23:4737–4745

    CAS  PubMed  Google Scholar 

  • Haj-Yasein NN, Jensen V, Ostby I, Omholt SW, Voipio J, Kaila K, Ottersen OP, Hvalby O, Nagelhus EA (2012) Aquaporin-4 regulates extracellular space volume dynamics during high-frequency synaptic stimulation: a gene deletion study in mouse hippocampus. Glia 60:867–874

    Article  PubMed  Google Scholar 

  • Hardie RC (2011) A brief history of TRP: commentary and personal perspective. Pflugers Arch 461:493–498

    Article  CAS  PubMed  Google Scholar 

  • Hartmann J, Verkhratsky A (1998) Relations between intracellular Ca2+ stores and store-operated Ca2+ entry in primary cultured human glioblastoma cells. J Physiol 513(Pt 2):411–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463:232–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hertz L (1979) Functional interactions between neurons and astrocytes I. Turnover and metabolism of putative amino acid transmitters. Prog Neurobiol 13:277–323

    Article  CAS  PubMed  Google Scholar 

  • Hertz L, Zielke HR (2004) Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci 27:735–743

    Article  CAS  PubMed  Google Scholar 

  • Hertz L, Dringen R, Schousboe A, Robinson SR (1999) Astrocytes: glutamate producers for neurons. J Neurosci Res 57:417–428

    Article  CAS  PubMed  Google Scholar 

  • Hofmann T, Schaefer M, Schultz G, Gudermann T (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci USA 99:7461–7466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iadecola C, Nedergaard M (2007) Glial regulation of the cerebral microvasculature. Nat Neurosci 10:1369–1376

    Article  CAS  PubMed  Google Scholar 

  • Kettenmann H, Ransom BR (eds) (2013) Neuroglia. Oxford University Press, Oxford, 864 pp

    Google Scholar 

  • Kintner DB, Look A, Shull GE, Sun D (2005) Stimulation of astrocyte Na+/H+ exchange activity in response to in vitro ischemia depends in part on activation of ERK1/2. Am J Physiol Cell Physiol 289:C934–C945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirischuk S, Kettenmann H, Verkhratsky A (1997) Na+/Ca2+ exchanger modulates kainate-triggered Ca2+ signaling in Bergmann glial cells in situ. FASEB J 11:566–572

    CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Kirischuk S, Kettenmann H, Verkhratsky A (2007) Membrane currents and cytoplasmic sodium transients generated by glutamate transport in Bergmann glial cells. Pflugers Arch 454:245–252

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kresse W, Sekler I, Hoffmann A, Peters O, Nolte C, Moran A, Kettenmann H (2005) Zinc ions are endogenous modulators of neurotransmitter-stimulated capacitative Ca2+ entry in both cultured and in situ mouse astrocytes. Eur J Neurosci 21:1626–1634

    Article  PubMed  Google Scholar 

  • Kucheryavykh YV, Antonov SM, Shuba YM, Rivera Y, Inyushin MY, Veh RW, Verkhratsky A, Nichols CG, Eaton MJ, Skatchkov SN (2012) Sodium accumulated in glia during glutamate transport increases polyamine dependent block of Kir4.1 channels. 2012 Neuroscience Meeting Planner. Society for Neuroscience, New Orleans. Abstract #236.05/C15 Online

    Google Scholar 

  • Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y (2011) Large-scale calcium waves traveling through astrocytic networks in vivo. J Neurosci 31:2607–2614

    Article  CAS  PubMed  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

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langer J, Rose CR (2009) Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol 587:5859–5877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langer J, Stephan J, Theis M, Rose CR (2012) Gap junctions mediate intercellular spread of sodium between Hippocampal astrocytes in situ. Glia 60:239–252

    Article  PubMed  Google Scholar 

  • Lascola C, Kraig RP (1997) Astroglial acid–base dynamics in hyperglycemic and normoglycemic global ischemia. Neurosci Biobehav Rev 21:143–150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SM, Cho YS, Kim TH, Jin MU, Ahn DK, Noguchi K, Bae YC (2012) An ultrastructural evidence for the expression of transient receptor potential ankyrin 1 (TRPA1) in astrocytes in the rat trigeminal caudal nucleus. J Chem Neuroanat 45:45–49

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dong L, Fu H, Wang B, Hertz L, Peng L (2011) Effects of chronic treatment with fluoxetine on receptor-stimulated increase of [Ca2+]i in astrocytes mimic those of acute inhibition of TRPC1 channel activity. Cell Calcium 50:42–53

    Article  CAS  PubMed  Google Scholar 

  • Linde CI, Baryshnikov SG, Mazzocco-Spezzia A, Golovina VA (2011) Dysregulation of Ca2+ signaling in astrocytes from mice lacking amyloid precursor protein. Am J Physiol Cell Physiol 300:C1502–C1512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Bandyopadhyay BC, Nakamoto T, Singh B, Liedtke W, Melvin JE, Ambudkar I (2006) A role for AQP5 in activation of TRPV4 by hypotonicity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 281:15485–15495

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Singh BB, Ambudkar IS (2003) TRPC1 is required for functional store-operated Ca2+ channels. Role of acidic amino acid residues in the S5-S6 region. J Biol Chem 278:11337–11343.

    Article  CAS  PubMed  Google Scholar 

  • MacVicar BA, Feighan D, Brown A, Ransom B (2002) Intrinsic optical signals in the rat optic nerve: role for K+ uptake via NKCC1 and swelling of astrocytes. Glia 37:114–123

    Article  PubMed  Google Scholar 

  • Magistretti PJ (2011) Neuron-glia metabolic coupling and plasticity. Exp Physiol 96:407–410

    Article  CAS  PubMed  Google Scholar 

  • Malarkey EB, Ni Y, Parpura V (2008) Ca2+ entry through TRPC1 channels contributes to intracellular Ca2+ dynamics and consequent glutamate release from rat astrocytes. Glia 56:821–835

    Article  PubMed  Google Scholar 

  • Mannari T, Morita S, Furube E, Tominaga M, Miyata S (2013) Astrocytic TRPV1 ion channels detect blood-borne signals in the sensory circumventricular organs of adult mouse brains. Glia 61:957–971

    Article  PubMed  Google Scholar 

  • Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP (2005) TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7:179–185

    Article  CAS  PubMed  Google Scholar 

  • Minke B (2010) The history of the drosophila TRP channel: the birth of a new channel superfamily. J Neurogenet 24:216–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittelsteadt T, Seifert G, Alvarez-Baron E, Steinhauser C, Becker AJ, Schoch S (2009) Differential mRNA expression patterns of the synaptotagmin gene family in the rodent brain. J Comp Neurol 512:514–528

    Article  CAS  PubMed  Google Scholar 

  • Miyano K, Morioka N, Sugimoto T, Shiraishi S, Uezono Y, Nakata Y (2010) Activation of the neurokinin-1 receptor in rat spinal astrocytes induces Ca2+ release from IP3-sensitive Ca2+ stores and extracellular Ca2+ influx through TRPC3. Neurochem Int 57:923–934

    Article  CAS  PubMed  Google Scholar 

  • Moller T, Nolte C, Burger R, Verkhratsky A, Kettenmann H (1997) Mechanisms of C5a and C3a complement fragment-induced [Ca2+]i signaling in mouse microglia. J Neurosci 17:615–624

    CAS  PubMed  Google Scholar 

  • Montell C (2011) The history of TRP channels, a commentary and reflection. Pflugers Arch 461:499–506

    Article  CAS  PubMed  Google Scholar 

  • Moreno C, Sampieri A, Vivas O, Pena-Segura C, Vaca L (2012) STIM1 and Orai1 mediate thrombin-induced Ca2+ influx in rat cortical astrocytes. Cell Calcium 52:457–467

    Article  CAS  PubMed  Google Scholar 

  • Motiani RK, Hyzinski-Garcia MC, Zhang X, Henkel MM, Abdullaev IF, Kuo YH, Matrougui K, Mongin AA, Trebak M (2013) STIM1 and Orai1 mediate CRAC channel activity and are essential for human glioblastoma invasion. Pflugers Arch, in press doi:10.1007/s00424-013-1254-8

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Muller MS, Obel LF, Waagepetersen HS, Schousboe A, Bak LK (2013) Complex actions of ionomycin in cultured cerebellar astrocytes affecting both calcium-induced calcium release and store-operated calcium entry. Neurochem Res

    Google Scholar 

  • Nagelhus EA, Mathiisen TM, Ottersen OP (2004) Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129:905–913

    Article  CAS  PubMed  Google Scholar 

  • Nakao K, Shirakawa H, Sugishita A, Matsutani I, Niidome T, Nakagawa T, Kaneko S (2008) Ca2+ mobilization mediated by transient receptor potential canonical 3 is associated with thrombin-induced morphological changes in 1321N1 human astrocytoma cells. J Neurosci Res 86:2722–2732

    Article  CAS  PubMed  Google Scholar 

  • Nedergaard M (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263:1768–1771

    Article  CAS  PubMed  Google Scholar 

  • Nedergaard M, Verkhratsky A (2012) Artifact versus reality – how astrocytes contribute to synaptic events. Glia 60:1013–1023

    Article  PubMed  PubMed Central  Google Scholar 

  • Nilius B (2012) Transient receptor potential (TRP) channels in the brain: the good and the ugly. Eur Review 20:343–355

    Article  Google Scholar 

  • Nilius B, Appendino G (2013) Spices: The savory and beneficial science of pungency. Rev Physiol Biochem Pharmacol doi:10.4103/0974-8490.105636

  • Nilius B, Honore E (2012) Sensing pressure with ion channels. Trends Neurosci 35:477–486

    Article  CAS  PubMed  Google Scholar 

  • Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12:218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilius B, Owsianik G, Voets T, Peters JA (2007) Transient receptor potential cation channels in disease. Physiol Rev 87:165–217

    Article  CAS  PubMed  Google Scholar 

  • Nilius B, Prenen J, Owsianik G (2011) Irritating channels: the case of TRPA1. J Physiol 589:1543–1549

    Article  CAS  PubMed  Google Scholar 

  • Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch 464:425–458

    Article  CAS  PubMed  Google Scholar 

  • Olsen ML, Sontheimer H (2008) Functional implications for Kir4.1 channels in glial biology: from K+ buffering to cell differentiation. J Neurochem 107:589–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Owsianik G, Talavera K, Voets T, Nilius B (2006) Permeation and selectivity of TRP channels. Annu Rev Physiol 68:685–717

    Article  CAS  PubMed  Google Scholar 

  • Paez PM, Fulton DJ, Spreuer V, Handley V, Campagnoni CW, Campagnoni AT (2009) Regulation of store-operated and voltage-operated Ca2+ channels in the proliferation and death of oligodendrocyte precursor cells by golli proteins. ASN Neuro 1

    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

    Article  CAS  PubMed  Google Scholar 

  • Pankratov Y, Lalo U, Krishtal OA, Verkhratsky A (2009) P2X receptors and synaptic plasticity. Neuroscience 158:137–148

    Article  CAS  PubMed  Google Scholar 

  • Parekh AB (2010) Store-operated CRAC channels: function in health and disease. Nat Rev Drug Discov 9:399–410

    Article  CAS  PubMed  Google Scholar 

  • Parekh AB, Penner R (1997) Store depletion and calcium influx. Physiol Rev 77:901–930

    CAS  PubMed  Google Scholar 

  • Parnis J, Montana V, Delgado-Martinez I, Matyash V, Parpura V, Kettenmann H, Sekler I, Nolte C (2013) Mitochondrial exchanger NCLX plays a major role in the intracellular Ca2+ signaling, gliotransmission, and proliferation of astrocytes. J Neurosci 33:7206–7219

    Article  CAS  PubMed  Google Scholar 

  • Parpura V, Verkhratsky A (2012) Homeostatic function of astrocytes: Ca2+ and Na+ signalling. Transl Neurosci 3:334–344

    Article  PubMed  PubMed Central  Google Scholar 

  • Parpura V, Zorec R (2010) Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63:83–92

    Article  CAS  PubMed  Google Scholar 

  • Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369:744–747

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233–252

    Article  CAS  PubMed  Google Scholar 

  • Pelizzoni I, Zacchetti D, Campanella A, Grohovaz F, Codazzi F (2013) Iron uptake in quiescent and inflammation-activated astrocytes: A potentially neuroprotective control of iron burden. Biochim Biophys Acta 1832:1326–1333

    Google Scholar 

  • Pellerin L, Magistretti PJ (1996) Excitatory amino acids stimulate aerobic glycolysis in astrocytes via an activation of the Na+/K+ ATPase. Dev Neurosci 18:336–342

    Article  CAS  PubMed  Google Scholar 

  • Pellerin L, Magistretti PJ (2012) Sweet sixteen for ANLS. J Cereb Blood Flow Metab. doi:E-pub ahead of print: 10.1038/jcbfm.2011.149

    PubMed  Google Scholar 

  • Pivneva T, Haas B, Reyes-Haro D, Laube G, Veh RW, Nolte C, Skibo G, Kettenmann H (2008) Store-operated Ca2+ entry in astrocytes: different spatial arrangement of endoplasmic reticulum explains functional diversity in vitro and in situ. Cell Calcium 43:591–601

    Article  CAS  PubMed  Google Scholar 

  • Pizzo P, Burgo A, Pozzan T, Fasolato C (2001) Role of capacitative calcium entry on glutamate-induced calcium influx in type-I rat cortical astrocytes. J Neurochem 79:98–109

    Article  CAS  PubMed  Google Scholar 

  • Poskanzer KE, Yuste R (2011) Astrocytic regulation of cortical UP states. Proc Natl Acad Sci USA 108:18453–18458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poteser M, Schleifer H, Lichtenegger M, Schernthaner M, Stockner T, Kappe CO, Glasnov TN, Romanin C, Groschner K (2011) PKC-dependent coupling of calcium permeation through transient receptor potential canonical 3 (TRPC3) to calcineurin signaling in HL-1 myocytes. Proc Natl Acad Sci USA 108:10556–10561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Putney JW Jr (1990) Capacitative calcium entry revisited. Cell Calcium 11:611–624

    Article  CAS  PubMed  Google Scholar 

  • Putney JW Jr (2007) Recent breakthroughs in the molecular mechanism of capacitative calcium entry (with thoughts on how we got here). Cell Calcium 42:103–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes RC, Parpura V (2008) Mitochondria modulate Ca2+-dependent glutamate release from rat cortical astrocytes. J Neurosci 28:9682–9691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes RC, Parpura V (2009) The trinity of Ca2+ sources for the exocytotic glutamate release from astrocytes. Neurochem Int 55:2–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes RC, Perry G, Lesort M, Parpura V (2011) Immunophilin deficiency augments Ca2+-dependent glutamate release from mouse cortical astrocytes. Cell Calcium 49:23–34

    Article  CAS  PubMed  Google Scholar 

  • Reyes RC, Verkhratsky A, Parpura V (2012) Plasmalemmal Na+/Ca2+ exchanger modulates Ca2+-dependent exocytotic release of glutamate from rat cortical astrocytes. ASN Neuro 4

    Google Scholar 

  • Reyes RC, Verkhratsky A, Parpura V (2013) TRPC1-mediated Ca2+ and Na+ signalling in astroglia: differential filtering of extracellular cations. Cell Calcium, in press, http://dx.doi.org/10.1016/j.ceca.2013.05.005

  • Rose CR, Karus C (2013) Two sides of the same coin: sodium homeostasis and signaling in astrocytes under physiological and pathophysiological conditions. Glia, in press doi: 10.1002/glia.22492

  • Rose CR, Ransom BR (1996) Intracellular sodium homeostasis in rat hippocampal astrocytes. J Physiol 491:291–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rose CR, Ransom BR (1997) Gap junctions equalize intracellular Na+ concentration in astrocytes. Glia 20:299–307

    Article  CAS  PubMed  Google Scholar 

  • Sharma G, Vijayaraghavan S (2001) Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci USA 98:4148–4153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen JX, Yakel JL (2012) Functional α7 nicotinic ACh receptors on astrocytes in rat hippocampal CA1 slices. J Mol Neurosci 48:14–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigetomi E, Tong X, Kwan KY, Corey DP, Khakh BS (2012) TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat Neurosci 15:70–80

    Article  CAS  Google Scholar 

  • Shirakawa H (2012) Pathophysiological significance of the canonical transient receptor potential (TRPC) subfamily in astrocyte activation. Yakugaku Zasshi 132:587–593

    Article  CAS  PubMed  Google Scholar 

  • Soboloff J, Rothberg BS, Madesh M, Gill DL (2012) STIM proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol 13:549–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638–647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song X, Zhao Y, Narcisse L, Duffy H, Kress Y, Lee S, Brosnan CF (2005) Canonical transient receptor potential channel 4 (TRPC4) co-localizes with the scaffolding protein ZO-1 in human fetal astrocytes in culture. Glia 49:418–429

    Article  PubMed  Google Scholar 

  • Steinhauser C, Gallo V (1996) News on glutamate receptors in glial cells. Trends Neurosci 19:339–345

    Article  CAS  PubMed  Google Scholar 

  • Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2001) TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29:645–655

    Article  CAS  PubMed  Google Scholar 

  • Struys-Ponsar C, Guillard O, van den Bosch de Aguilar P (2000) Effects of aluminum exposure on glutamate metabolism: a possible explanation for its toxicity. Exp Neurol 163:157–164

    Article  CAS  PubMed  Google Scholar 

  • Suarez-Fernandez MB, Soldado AB, Sanz-Medel A, Vega JA, Novelli A, Fernandez-Sanchez MT (1999) Aluminum-induced degeneration of astrocytes occurs via apoptosis and results in neuronal death. Brain Res 835:125–136

    Article  CAS  PubMed  Google Scholar 

  • Swanson RA, Ying W, Kauppinen TM (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205

    Article  CAS  PubMed  Google Scholar 

  • Tarasov AI, Griffiths EJ, Rutter GA (2012) Regulation of ATP production by mitochondrial Ca2+. Cell Calcium 52:28–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toescu EC, Moller T, Kettenmann H, Verkhratsky A (1998) Long-term activation of capacitative Ca2+ entry in mouse microglial cells. Neuroscience 86:925–935

    Article  CAS  PubMed  Google Scholar 

  • Tuschick S, Kirischuk S, Kirchhoff F, Liefeldt L, Paul M, Verkhratsky A, Kettenmann H (1997) Bergmann glial cells in situ express endothelin B receptors linked to cytoplasmic calcium signals. Cell Calcium 21:409–419

    Article  CAS  PubMed  Google Scholar 

  • Unichenko P, Myakhar O, Kirischuk S (2012) Intracellular Na+ concentration influences short-term plasticity of glutamate transporter-mediated currents in neocortical astrocytes. Glia 60:605–614

    Article  PubMed  Google Scholar 

  • Uwechue NM, Marx MC, Chevy Q, Billups B (2012) Activation of glutamate transport evokes rapid glutamine release from perisynaptic astrocytes. J Physiol 590:2317–2331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vennekens R, Menigoz A, Nilius B (2012) TRPs in the brain. Rev Physiol Biochem Pharmacol 163:27–64

    PubMed  Google Scholar 

  • Verkhratsky A, Butt AM (2013) Glial physiology and pathophysiology. Wiley-Blackwell, Chichester, 560 pp

    Book  Google Scholar 

  • Verkhratsky A, Kettenmann H (1996) Calcium signalling in glial cells. Trends Neurosci 19:346–352

    Article  CAS  PubMed  Google Scholar 

  • Verkhratsky A, Parpura V (2013) Store-operated calcium entry in neuroglia. Neurosci Bull, in press doi:10.1007/s12264-013-1343-x

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Verkhratsky A, Noda M, Parpura V, Kirischuk S (2013a) Sodium fluxes and astroglial function. Adv Exp Med Biol 961:295–305

    Article  CAS  PubMed  Google Scholar 

  • Verkhratsky A, Rodriguez JJ, Parpura V (2013b) Astroglia in neurological diseases. Future Neurol 8:149–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walz W, Hertz L (1984) Sodium transport in astrocytes. J Neurosci Res 11:231–239

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Lou N, Xu Q, Tian GF, Peng WG, Han X, Kang J, Takano T, Nedergaard M (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9:816–823

    Article  CAS  PubMed  Google Scholar 

  • Weerth SH, Holtzclaw LA, Russell JT (2007) Signaling proteins in raft-like microdomains are essential for Ca2+ wave propagation in glial cells. Cell Calcium 41:155–167

    Article  CAS  PubMed  Google Scholar 

  • Yin Z, Milatovic D, Aschner JL, Syversen T, Rocha JB, Souza DO, Sidoryk M, Albrecht J, Aschner M (2007) Methylmercury induces oxidative injury, alterations in permeability and glutamine transport in cultured astrocytes. Brain Res 1131:1–10

    Article  CAS  PubMed  Google Scholar 

  • Zeng W, Yuan JP, Kim MS, Choi YJ, Huang GN, Worley PF, Muallem S (2008) STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell 32:439–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Fukuda M, Van Bockstaele E, Pascual O, Haydon PG (2004) Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci USA 101:9441–9446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Brinton RD (2004) Suppression of proinflammatory cytokines interleukin-1β and tumor necrosis factor-alpha in astrocytes by a V1 vasopressin receptor agonist: a cAMP response element-binding protein-dependent mechanism. J Neurosci 24:2226–2235

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Authors’ research was supported by Alzheimer’s Research Trust (UK) Programme Grant (ART/PG2004A/1) to A.V. and by National Science Foundation (CBET 0943343) grant to V.P. R.C.R. was additionally funded by UCSF Neuroscience and Schizophrenia T32 (MH 089920).

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The authors declare that they have no conflict of interest.

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Verkhratsky, A., Reyes, R.C., Parpura, V. (2013). TRP Channels Coordinate Ion Signalling in Astroglia. In: Nilius, B., Gudermann, T., Jahn, R., Lill, R., Offermanns, S., Petersen, O.H. (eds) Reviews of Physiology, Biochemistry and Pharmacology 166. Reviews of Physiology, Biochemistry and Pharmacology, vol 166. Springer, Cham. https://doi.org/10.1007/112_2013_15

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