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TRP Channels Coordinate Ion Signalling in Astroglia

  • Alexei Verkhratsky
  • Reno C. Reyes
  • Vladimir Parpura
Chapter
Part of the Reviews of Physiology, Biochemistry and Pharmacology book series (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.

Keywords

Astrocyte Ca2+ signalling Na+ signalling Metabotropic receptors, endoplasmic reticulum TRPC channels TRPCA1 TRPV4 Store-operated Ca2+ entry Stretch-activated channels Mechanosensitivity Volume regulation Plasticity Brain homeostasis 

Notes

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).

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 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 589:3909–3927PubMedPubMedCentralCrossRefGoogle Scholar
  2. Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1–14PubMedCrossRefGoogle Scholar
  3. 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 31:204–214PubMedCrossRefGoogle Scholar
  4. Benfenati V, Ferroni S (2010) Water transport between CNS compartments: functional and molecular interactions between aquaporins and ion channels. Neuroscience 168:926–940PubMedCrossRefGoogle Scholar
  5. 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 148:876–892PubMedCrossRefGoogle Scholar
  6. 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 108:2563–2568PubMedPubMedCentralCrossRefGoogle Scholar
  7. 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–C1111PubMedCrossRefGoogle Scholar
  8. Black JA, Newcombe J, Waxman SG (2010) Astrocytes within multiple sclerosis lesions upregulate sodium channel Nav1.5. Brain 133:835–846PubMedCrossRefGoogle Scholar
  9. Boison D, Chen JF, Fredholm BB (2010) Adenosine signaling and function in glial cells. Cell Death Differ 17:1071–1082PubMedCrossRefGoogle Scholar
  10. Broer S, Brookes N (2001) Transfer of glutamine between astrocytes and neurons. J Neurochem 77:705–719PubMedCrossRefGoogle Scholar
  11. Burdakov D, Petersen OH, Verkhratsky A (2005) Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium 38:303–310PubMedCrossRefGoogle Scholar
  12. 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 256:1566–1570PubMedCrossRefGoogle Scholar
  13. 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:e39959PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cahalan MD (2009) STIMulating store-operated Ca2+ entry. Nat Cell Biol 11:669–677PubMedPubMedCentralCrossRefGoogle Scholar
  15. Carmignoto G, Gomez-Gonzalo M (2010) The contribution of astrocyte signalling to neurovascular coupling. Brain Res Rev 63:138–148PubMedCrossRefGoogle Scholar
  16. Carrasco S, Meyer T (2011) STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu Rev Biochem 80:973–1000PubMedPubMedCentralCrossRefGoogle Scholar
  17. 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 28:6703–6713PubMedCrossRefGoogle Scholar
  18. 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 6:983–992PubMedCrossRefGoogle Scholar
  19. 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 287:11516–11525PubMedPubMedCentralCrossRefGoogle Scholar
  20. Conti F, Minelli A, Melone M (2004) GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications. Brain Res Brain Res Rev 45:196–212PubMedCrossRefGoogle Scholar
  21. Cornell Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long- range glial signaling. Science 247:470–473PubMedCrossRefGoogle Scholar
  22. Danbolt NC (2001) Glutamate uptake. Progr Neurobiol 65:1–105CrossRefGoogle Scholar
  23. De Keyser J, Mostert JP, Koch MW (2008) Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders. J Neurol Sci 267:3–16PubMedCrossRefGoogle Scholar
  24. Deitmer JW, Rose CR (2010) Ion changes and signalling in perisynaptic glia. Brain Res Rev 63:113–129PubMedCrossRefGoogle Scholar
  25. 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 451:99–104PubMedCrossRefGoogle Scholar
  26. Fernandez-Fernandez S, Almeida A, Bolanos JP (2012) Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochem J 443:3–11PubMedCrossRefGoogle Scholar
  27. 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 441:179–185PubMedCrossRefGoogle Scholar
  28. Finkbeiner SM (1993) Glial calcium. Glia 9:83–104PubMedCrossRefGoogle Scholar
  29. Giaume C, Kirchhoff F, Matute C, Reichenbach A, Verkhratsky A (2007) Glia: the fulcrum of brain diseases. Cell Death Differ 14:1324–1335PubMedCrossRefGoogle Scholar
  30. Golovina VA (2005) Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J Physiol 564:737–749PubMedPubMedCentralCrossRefGoogle Scholar
  31. 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 40:785–796PubMedCrossRefGoogle Scholar
  32. 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 329:571–575PubMedPubMedCentralCrossRefGoogle Scholar
  33. 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 23:4737–4745PubMedGoogle Scholar
  34. 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 60:867–874PubMedCrossRefGoogle Scholar
  35. Hardie RC (2011) A brief history of TRP: commentary and personal perspective. Pflugers Arch 461:493–498PubMedCrossRefGoogle Scholar
  36. 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):411–424PubMedPubMedCentralCrossRefGoogle Scholar
  37. Henneberger C, Papouin T, Oliet SH, Rusakov DA (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463:232–236PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hertz L (1979) Functional interactions between neurons and astrocytes I. Turnover and metabolism of putative amino acid transmitters. Prog Neurobiol 13:277–323PubMedCrossRefGoogle Scholar
  39. Hertz L, Zielke HR (2004) Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci 27:735–743PubMedCrossRefGoogle Scholar
  40. Hertz L, Dringen R, Schousboe A, Robinson SR (1999) Astrocytes: glutamate producers for neurons. J Neurosci Res 57:417–428PubMedCrossRefGoogle Scholar
  41. 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 99:7461–7466PubMedPubMedCentralCrossRefGoogle Scholar
  42. Iadecola C, Nedergaard M (2007) Glial regulation of the cerebral microvasculature. Nat Neurosci 10:1369–1376PubMedCrossRefGoogle Scholar
  43. Kettenmann H, Ransom BR (eds) (2013) Neuroglia. Oxford University Press, Oxford, 864 ppGoogle Scholar
  44. 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–C945PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kirischuk S, Kettenmann H, Verkhratsky A (1997) Na+/Ca2+ exchanger modulates kainate-triggered Ca2+ signaling in Bergmann glial cells in situ. FASEB J 11:566–572PubMedGoogle Scholar
  46. 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 92:1051–1059PubMedCrossRefGoogle Scholar
  47. Kirischuk S, Kettenmann H, Verkhratsky A (2007) Membrane currents and cytoplasmic sodium transients generated by glutamate transport in Bergmann glial cells. Pflugers Arch 454:245–252PubMedCrossRefGoogle Scholar
  48. Kirischuk S, Parpura V, Verkhratsky A (2012) Sodium dynamics: another key to astroglial excitability? Trends Neurosci 35:497–506PubMedCrossRefGoogle Scholar
  49. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045–1056PubMedPubMedCentralCrossRefGoogle Scholar
  50. 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 21:1626–1634PubMedCrossRefGoogle Scholar
  51. 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 OnlineGoogle Scholar
  52. Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y (2011) Large-scale calcium waves traveling through astrocytic networks in vivo. J Neurosci 31:2607–2614PubMedCrossRefGoogle Scholar
  53. Lalo U, Pankratov Y, Kirchhoff F, North RA, Verkhratsky A (2006) NMDA receptors mediate neuron-to-glia signaling in mouse cortical astrocytes. J Neurosci 26:2673–2683PubMedCrossRefGoogle Scholar
  54. 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 28:5473–5480PubMedPubMedCentralCrossRefGoogle Scholar
  55. Langer J, Rose CR (2009) Synaptically induced sodium signals in hippocampal astrocytes in situ. J Physiol 587:5859–5877PubMedPubMedCentralCrossRefGoogle Scholar
  56. Langer J, Stephan J, Theis M, Rose CR (2012) Gap junctions mediate intercellular spread of sodium between Hippocampal astrocytes in situ. Glia 60:239–252PubMedCrossRefGoogle Scholar
  57. Lascola C, Kraig RP (1997) Astroglial acid–base dynamics in hyperglycemic and normoglycemic global ischemia. Neurosci Biobehav Rev 21:143–150PubMedPubMedCentralCrossRefGoogle Scholar
  58. 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 45:45–49PubMedCrossRefGoogle Scholar
  59. 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 50:42–53PubMedCrossRefGoogle Scholar
  60. 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–C1512PubMedPubMedCentralCrossRefGoogle Scholar
  61. 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 281:15485–15495PubMedCrossRefGoogle Scholar
  62. 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.PubMedCrossRefGoogle Scholar
  63. 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 37:114–123PubMedCrossRefGoogle Scholar
  64. Magistretti PJ (2011) Neuron-glia metabolic coupling and plasticity. Exp Physiol 96:407–410PubMedCrossRefGoogle Scholar
  65. 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 56:821–835PubMedCrossRefGoogle Scholar
  66. 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 61:957–971PubMedCrossRefGoogle Scholar
  67. 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 7:179–185PubMedCrossRefGoogle Scholar
  68. Minke B (2010) The history of the drosophila TRP channel: the birth of a new channel superfamily. J Neurogenet 24:216–233PubMedPubMedCentralCrossRefGoogle Scholar
  69. 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 512:514–528PubMedCrossRefGoogle Scholar
  70. 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 57:923–934PubMedCrossRefGoogle Scholar
  71. 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 17:615–624PubMedGoogle Scholar
  72. Montell C (2011) The history of TRP channels, a commentary and reflection. Pflugers Arch 461:499–506PubMedCrossRefGoogle Scholar
  73. 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 52:457–467PubMedCrossRefGoogle Scholar
  74. 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
  75. 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 256:1563–1566PubMedCrossRefGoogle Scholar
  76. 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 ResGoogle Scholar
  77. Nagelhus EA, Mathiisen TM, Ottersen OP (2004) Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129:905–913PubMedCrossRefGoogle Scholar
  78. 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 86:2722–2732PubMedCrossRefGoogle Scholar
  79. Nedergaard M (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263:1768–1771PubMedCrossRefGoogle Scholar
  80. Nedergaard M, Verkhratsky A (2012) Artifact versus reality – how astrocytes contribute to synaptic events. Glia 60:1013–1023PubMedPubMedCentralCrossRefGoogle Scholar
  81. Nilius B (2012) Transient receptor potential (TRP) channels in the brain: the good and the ugly. Eur Review 20:343–355CrossRefGoogle Scholar
  82. Nilius B, Appendino G (2013) Spices: The savory and beneficial science of pungency. Rev Physiol Biochem Pharmacol doi: 10.4103/0974-8490.105636
  83. Nilius B, Honore E (2012) Sensing pressure with ion channels. Trends Neurosci 35:477–486PubMedCrossRefGoogle Scholar
  84. Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12:218PubMedPubMedCentralCrossRefGoogle Scholar
  85. Nilius B, Owsianik G, Voets T, Peters JA (2007) Transient receptor potential cation channels in disease. Physiol Rev 87:165–217PubMedCrossRefGoogle Scholar
  86. Nilius B, Prenen J, Owsianik G (2011) Irritating channels: the case of TRPA1. J Physiol 589:1543–1549PubMedCrossRefGoogle Scholar
  87. Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch 464:425–458PubMedCrossRefGoogle Scholar
  88. Olsen ML, Sontheimer H (2008) Functional implications for Kir4.1 channels in glial biology: from K+ buffering to cell differentiation. J Neurochem 107:589–601PubMedPubMedCentralCrossRefGoogle Scholar
  89. Owsianik G, Talavera K, Voets T, Nilius B (2006) Permeation and selectivity of TRP channels. Annu Rev Physiol 68:685–717PubMedCrossRefGoogle Scholar
  90. 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 1Google Scholar
  91. 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 48:225–231PubMedCrossRefGoogle Scholar
  92. Pankratov Y, Lalo U, Krishtal OA, Verkhratsky A (2009) P2X receptors and synaptic plasticity. Neuroscience 158:137–148PubMedCrossRefGoogle Scholar
  93. Parekh AB (2010) Store-operated CRAC channels: function in health and disease. Nat Rev Drug Discov 9:399–410PubMedCrossRefGoogle Scholar
  94. Parekh AB, Penner R (1997) Store depletion and calcium influx. Physiol Rev 77:901–930PubMedGoogle Scholar
  95. 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 33:7206–7219PubMedCrossRefGoogle Scholar
  96. Parpura V, Verkhratsky A (2012) Homeostatic function of astrocytes: Ca2+ and Na+ signalling. Transl Neurosci 3:334–344PubMedPubMedCentralCrossRefGoogle Scholar
  97. Parpura V, Zorec R (2010) Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63:83–92PubMedCrossRefGoogle Scholar
  98. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369:744–747PubMedCrossRefGoogle Scholar
  99. Parpura V, Grubisic V, Verkhratsky A (2011) Ca2+ sources for the exocytotic release of glutamate from astrocytes. Biochim Biophys Acta 1813:984–991PubMedCrossRefGoogle Scholar
  100. Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233–252PubMedCrossRefGoogle Scholar
  101. 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 1832:1326–1333Google Scholar
  102. Pellerin L, Magistretti PJ (1996) Excitatory amino acids stimulate aerobic glycolysis in astrocytes via an activation of the Na+/K+ ATPase. Dev Neurosci 18:336–342PubMedCrossRefGoogle Scholar
  103. Pellerin L, Magistretti PJ (2012) Sweet sixteen for ANLS. J Cereb Blood Flow Metab. doi:E-pub ahead of print: 10.1038/jcbfm.2011.149PubMedGoogle Scholar
  104. 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 43:591–601PubMedCrossRefGoogle Scholar
  105. 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 79:98–109PubMedCrossRefGoogle Scholar
  106. Poskanzer KE, Yuste R (2011) Astrocytic regulation of cortical UP states. Proc Natl Acad Sci USA 108:18453–18458PubMedPubMedCentralCrossRefGoogle Scholar
  107. 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 108:10556–10561PubMedPubMedCentralCrossRefGoogle Scholar
  108. Putney JW Jr (1990) Capacitative calcium entry revisited. Cell Calcium 11:611–624PubMedCrossRefGoogle Scholar
  109. Putney JW Jr (2007) Recent breakthroughs in the molecular mechanism of capacitative calcium entry (with thoughts on how we got here). Cell Calcium 42:103–110PubMedPubMedCentralCrossRefGoogle Scholar
  110. Reyes RC, Parpura V (2008) Mitochondria modulate Ca2+-dependent glutamate release from rat cortical astrocytes. J Neurosci 28:9682–9691PubMedPubMedCentralCrossRefGoogle Scholar
  111. Reyes RC, Parpura V (2009) The trinity of Ca2+ sources for the exocytotic glutamate release from astrocytes. Neurochem Int 55:2–8PubMedPubMedCentralCrossRefGoogle Scholar
  112. Reyes RC, Perry G, Lesort M, Parpura V (2011) Immunophilin deficiency augments Ca2+-dependent glutamate release from mouse cortical astrocytes. Cell Calcium 49:23–34PubMedCrossRefGoogle Scholar
  113. Reyes RC, Verkhratsky A, Parpura V (2012) Plasmalemmal Na+/Ca2+ exchanger modulates Ca2+-dependent exocytotic release of glutamate from rat cortical astrocytes. ASN Neuro 4Google Scholar
  114. 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
  115. 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
  116. Rose CR, Ransom BR (1996) Intracellular sodium homeostasis in rat hippocampal astrocytes. J Physiol 491:291–305PubMedPubMedCentralCrossRefGoogle Scholar
  117. Rose CR, Ransom BR (1997) Gap junctions equalize intracellular Na+ concentration in astrocytes. Glia 20:299–307PubMedCrossRefGoogle Scholar
  118. Sharma G, Vijayaraghavan S (2001) Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci USA 98:4148–4153PubMedPubMedCentralCrossRefGoogle Scholar
  119. Shen JX, Yakel JL (2012) Functional α7 nicotinic ACh receptors on astrocytes in rat hippocampal CA1 slices. J Mol Neurosci 48:14–21PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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 15:70–80CrossRefGoogle Scholar
  121. Shirakawa H (2012) Pathophysiological significance of the canonical transient receptor potential (TRPC) subfamily in astrocyte activation. Yakugaku Zasshi 132:587–593PubMedCrossRefGoogle Scholar
  122. Soboloff J, Rothberg BS, Madesh M, Gill DL (2012) STIM proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol 13:549–565PubMedPubMedCentralCrossRefGoogle Scholar
  123. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638–647PubMedPubMedCentralCrossRefGoogle Scholar
  124. 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 49:418–429PubMedCrossRefGoogle Scholar
  125. Steinhauser C, Gallo V (1996) News on glutamate receptors in glial cells. Trends Neurosci 19:339–345PubMedCrossRefGoogle Scholar
  126. Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2001) TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29:645–655PubMedCrossRefGoogle Scholar
  127. 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 163:157–164PubMedCrossRefGoogle Scholar
  128. 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 835:125–136PubMedCrossRefGoogle Scholar
  129. Swanson RA, Ying W, Kauppinen TM (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205PubMedCrossRefGoogle Scholar
  130. Tarasov AI, Griffiths EJ, Rutter GA (2012) Regulation of ATP production by mitochondrial Ca2+. Cell Calcium 52:28–35PubMedPubMedCentralCrossRefGoogle Scholar
  131. Toescu EC, Moller T, Kettenmann H, Verkhratsky A (1998) Long-term activation of capacitative Ca2+ entry in mouse microglial cells. Neuroscience 86:925–935PubMedCrossRefGoogle Scholar
  132. 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 21:409–419PubMedCrossRefGoogle Scholar
  133. Unichenko P, Myakhar O, Kirischuk S (2012) Intracellular Na+ concentration influences short-term plasticity of glutamate transporter-mediated currents in neocortical astrocytes. Glia 60:605–614PubMedCrossRefGoogle Scholar
  134. Uwechue NM, Marx MC, Chevy Q, Billups B (2012) Activation of glutamate transport evokes rapid glutamine release from perisynaptic astrocytes. J Physiol 590:2317–2331PubMedPubMedCentralCrossRefGoogle Scholar
  135. Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417PubMedPubMedCentralCrossRefGoogle Scholar
  136. Vennekens R, Menigoz A, Nilius B (2012) TRPs in the brain. Rev Physiol Biochem Pharmacol 163:27–64PubMedGoogle Scholar
  137. Verkhratsky A, Butt AM (2013) Glial physiology and pathophysiology. Wiley-Blackwell, Chichester, 560 ppCrossRefGoogle Scholar
  138. Verkhratsky A, Kettenmann H (1996) Calcium signalling in glial cells. Trends Neurosci 19:346–352PubMedCrossRefGoogle Scholar
  139. Verkhratsky A, Parpura V (2013) Store-operated calcium entry in neuroglia. Neurosci Bull, in press doi: 10.1007/s12264-013-1343-x
  140. Verkhratsky A, Steinhauser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380–412PubMedCrossRefGoogle Scholar
  141. Verkhratsky A, Orkand RK, Kettenmann H (1998) Glial calcium: homeostasis and signaling function. Physiol Rev 78:99–141PubMedGoogle Scholar
  142. Verkhratsky A, Rodriguez JJ, Parpura V (2012) Calcium signalling in astroglia. Mol Cell Endocrinol 353:45–56PubMedCrossRefGoogle Scholar
  143. Verkhratsky A, Noda M, Parpura V, Kirischuk S (2013a) Sodium fluxes and astroglial function. Adv Exp Med Biol 961:295–305PubMedCrossRefGoogle Scholar
  144. Verkhratsky A, Rodriguez JJ, Parpura V (2013b) Astroglia in neurological diseases. Future Neurol 8:149–158PubMedPubMedCentralCrossRefGoogle Scholar
  145. Walz W, Hertz L (1984) Sodium transport in astrocytes. J Neurosci Res 11:231–239PubMedCrossRefGoogle Scholar
  146. 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 9:816–823PubMedCrossRefGoogle Scholar
  147. Weerth SH, Holtzclaw LA, Russell JT (2007) Signaling proteins in raft-like microdomains are essential for Ca2+ wave propagation in glial cells. Cell Calcium 41:155–167PubMedCrossRefGoogle Scholar
  148. 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 1131:1–10PubMedCrossRefGoogle Scholar
  149. 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 32:439–448PubMedPubMedCentralCrossRefGoogle Scholar
  150. Zhang Q, Fukuda M, Van Bockstaele E, Pascual O, Haydon PG (2004) Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci USA 101:9441–9446PubMedPubMedCentralCrossRefGoogle Scholar
  151. 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 24:2226–2235PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Faculty of Life SciencesThe University of ManchesterManchesterUK
  2. 2.Achucarro Center for NeuroscienceIKERBASQUE, Basque Foundation for ScienceBilbaoSpain
  3. 3.Department of Neurobiology, Center for Glial Biology in Medicine, Atomic Force Microscopy & Nanotechnology Laboratories, Civitan International Research Center, Evelyn F. McKnight Brain InstituteUniversity of Alabama at BirminghamBirminghamUSA
  4. 4.Department of Psychiatry, Langley Porter Psychiatric InstituteUniversity of California San FranciscoSan FranciscoUSA
  5. 5.Department of BiotechnologyUniversity or RijekaRijekaCroatia

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