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Academia Mexicana de Neurologνa, A.C.

2017, Number 4

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Rev Mex Neuroci 2017; 18 (4)

Cellular aspects and considerations from the study of ca2+ excitability in astrocytes

Montes BP

Language: Spanish
References: 88
Page: 57-69
PDF size: 277.11 Kb.


ABSTRACT

Introduction: For more than a century the Nervous System (NS) function was studied from a neurocentric perspective, considering the electric neuronal activity, the function of their circuits and their cellular responses as the only substrate for information flow and handling. In this perspective astrocytes, the most abundant cells of the CNS, had assigned connective, homeostatic and metabolic roles that enabled neuronal function. However, today we known that astroglial cells actively participate in information flow and handling, mediated by their neurotransmitter receptor expression, their neurotransmitter secretion, their Ca2+ excitability, their network formation and their close interaction with the synapse. These characteristics together originated the tripartite synapse hypothesis more than fifteen years ago. Objective: In the present work, astrocytes’ mechanism of Ca2+ mediated excitability, its molecular actors, the cellular organelles involved and the Ca2+ wave properties are reviewed. In addition some considerations, mainly methodological, are recapitulated that emanated from the study of these cells in the last decades. Conclusions: The role of astrocytes in information handling within the brain represents with no doubt a paradigmatic advance for the understanding of NS, and its apparent contradictions are slowly being solved. The study of astrocytes’ Ca2+ excitability has generated a reassessment of their functions, that gradually is accompanied by a more integrated view of the NS.


REFERENCES

  1. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science. (80-. ). 1990;247(4941):470–473.

  2. Giaume C, McCarthy KD. Control of gap-junctional communication in astrocytic networks. Trends Neurosci. 1996;19(8):319–325.

  3. Araque A, Parpura V, Sanzgiri RP, Haydon PG. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 1999;22(5):208–215.

  4. Volterra A, Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci. 2005;6(8):626–640.

  5. Volterra A, Liaudet N, Savtchouk I. Astrocyte Ca2+ signalling: an unexpected complexity. Nat. Rev. Neurosci. 2014;15(5):327–35.

  6. De Pitt?? M, Brunel N, Volterra A. Astrocytes: Orchestrating synaptic plasticity? Neuroscience. 2015;

  7. Bernardinelli Y, Randall J, Janett E, et al. Activity-Dependent Structural Plasticity of Perisynaptic Astrocytic Domains Promotes Excitatory Synapse Stability. Curr. Biol. 2014;24(15):1679–1688.

  8. Di Castro MA, Chuquet J, Liaudet N, et al. Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat. Neurosci. 2011;14(10):1276–84.

  9. Srinivasan R, Huang BS, Venugopal S, et al. Ca2+ signaling in astrocytes from Ip3r2-/- mice in brain slices and during startle responses in vivo. Nat. Neurosci. 2015;18(5):708–717.

  10. Nedergaard M, Rodr??guez JJ, Verkhratsky A. Glial calcium and diseases of the nervous system. Cell Calcium. 2010;47(2):140–149.

  11. Robertson JM. The Astrocentric Hypothesis: proposed role of astrocytes in consciousness and memory formation. J Physiol Paris. 2002;96(3–4):251–255.

  12. Porter JT, McCarthy KD. GFAP-positive hippocampal astrocytes in situ respond to glutamatergic neuroligands with increases in [Ca2+]i. Glia. 1995;13(2):101–12.

  13. Pasti L, Zonta M, Pozzan T, Vicini S, Carmignoto G. Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. J. Neurosci. 2001;21(2):477–484.

  14. Dani JW, Smith SJ. The triggering of astrocytic calcium waves by NMDA-induced neuronal activation. Ciba Found. Symp. 1995;188:195-205–9.

  15. Di Castro MA, Chuquet J, Liaudet N, et al. Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat. Neurosci. 2011;14(10):1276–1284.

  16. Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y. Large-Scale Calcium Waves Traveling through Astrocytic Networks In Vivo. J. Neurosci. 2011;31(7):2607–2614.

  17. Scemes E, Giaume C. Astrocyte calcium waves: what they are and what they do. Glia. 2006;54(7):716–25.

  18. Bushong EA, Martone ME, Jones YZ, Ellisman MH. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 2002;22(1):183–92.

  19. Ogata K, Kosaka T. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience. 2002;113(1):221–33.

  20. Koizumi S. Synchronization of Ca2+ oscillations: involvement of ATP release in astrocytes. Febs J. 2010;277(2):286–292.

  21. Khakh BS, McCarthy KD. Astrocyte calcium signaling: from observations to functions and the challenges therein. Cold Spring Harb. Perspect. Biol. 2015;7(4):a020404.

  22. Verkhratsky A, Parpura V. Calcium Signaling in Neuroglia. Neuroglia. 2013;320–332.

  23. Glial physiology and pathophysiology: a handbook. Chichester: Wiley-Blackwell; 2013.

  24. Hashioka S, Wang YF, Little JP, et al. Purinergic responses of calcium-dependent signaling pathways in cultured adult human astrocytes. BMC Neurosci. 2014;15:18.

  25. Lalo U, Pankratov Y, Wichert SP, et al. P2X1 and P2X5 subunits form the functional P2X receptor in mouse cortical astrocytes. J. Neurosci. 2008;28(21):5473–5480.

  26. Pan H-C, Chou Y-C, Sun SH. P2X7 R-mediated Ca(2+) -independent d-serine release via pannexin-1 of the P2X7 R-pannexin-1 complex in astrocytes. Glia. 2015;63(5):877–93.

  27. Kettenman H, Zorec R. Release of Gliotransmitters and Transmitter Receptors in Astrocytes. Neuroglia. 2013;197–211.

  28. Sharma G, Vijayaraghavan S. Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc. Natl. Acad. Sci. U. S. A. 2001;98(7):4148–4153.

  29. Montes de Oca Balderas P, Aguilera P. A Metabotropic-Like Flux-Independent NMDA Receptor Regulates Ca2+ Exit from Endoplasmic Reticulum and Mitochondrial Membrane Potential in Cultured Astrocytes. PLoS One. 2015;10(5):e0126314.

  30. Rodrνguez-Moreno A, Sihra TS. Kainate receptors with a metabotropic modus operandi. Trends Neurosci. 2007;30(12):630–7.

  31. D’Ascenzo M, Vairano M, Andreassi C, et al. Electrophysiological and Molecular Evidence of L-(Cav1), N- (Cav2.2), and R- (Cav2.3) Type Ca2+ Channels in Rat Cortical Astrocytes. Glia. 2004;45(4):354–363.

  32. Latour I, Hamid J, Beedle AM, Zamponi GW, Macvicar BA. Expression of voltage-gated Ca2+ channel subtypes in cultured astrocytes. Glia. 2003;41(4):347–353.

  33. Barres BA, Koroshetz WJ, Chun LL, Corey DP. Ion channel expression by white matter glia: the type- 1 astrocyte. Neuron. 1990;5(4):527–44.

  34. Ransom B, Giaume C. Gap Junctions and Hemichannels. Neuroglia. 2013;292–305.

  35. Reyes RC, Parpura V. The trinity of Ca2+ sources for the exocytotic glutamate release from astrocytes. Neurochem Int. 2009;55(1–3):2–8.

  36. Golovina V a. Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J. Physiol. 2005;564(Pt 3):737–749.

  37. Malarkey EB, Ni Y, Parpura V. Ca2+ entry through TRPC1 channels contributes to intracellular Ca2+ dynamics and consequent glutamate release from rat astrocytes. Glia. 2008;56(8):821–835.

  38. Reyes RC, Verkhratsky A, Parpura V. TRPC1-mediated Ca2+ and Na+ signalling in astroglia: differential filtering of extracellular cations. Cell Calcium. 2013;54(2):120–5.

  39. Streifel KM, Miller J, Mouneimne R, Tjalkens RB. Manganese inhibits ATP-induced calcium entry through the transient receptor potential channel TRPC3 in astrocytes. Neurotoxicology. 2013;34:160–6.

  40. Liang C, Du T, Zhou J, Verkhratsky A, Peng L. Ammonium increases Ca(2+) signalling and upregulates expression of TRPC1 gene in astrocytes in primary cultures and in the in vivo brain. Neurochem. Res. 2014;39(11):2127–35.

  41. Ronco V, Grolla AA, Glasnov TN, et al. Differential deregulation of astrocytic calcium signalling by amyloid-β, TNFα, IL-1β and LPS. Cell Calcium. 2014;55(4):219–29.

  42. Shibasaki K, Ikenaka K, Tamalu F, Tominaga M, Ishizaki Y. A novel subtype of astrocytes expressing TRPV4 (transient receptor potential vanilloid 4) regulates neuronal excitability via release of gliotransmitters. J. Biol. Chem. 2014;289(21):14470–80.

  43. Dunn KM, Hill-Eubanks DC, Liedtke WB, Nelson MT. TRPV4 channels stimulate Ca2+-induced Ca2+ release in astrocytic endfeet and amplify neurovascular coupling responses. Proc. Natl. Acad. Sci. U.S.A. 2013;110(15):6157–62.

  44. Shibasaki K, Ishizaki Y, Mandadi S. Astrocytes express functional TRPV2 ion channels. Biochem. Biophys. Res. Commun. 2013;441(2):327–32.

  45. Shigetomi E, Tong X, Kwan KY, Corey DP, Khakh BS. TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat. Neurosci. 2012;15(1):70–80.

  46. Shigetomi E, Jackson-Weaver O, Huckstepp RT, O’Dell TJ, Khakh BS. TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J. Neurosci. 2013;33(24):10143–53.

  47. Barajas M, Andrade A, Hernandez-Hernandez O, Felix R, Arias-Montaρo JA. Histamine-induced Ca21 entry in human astrocytoma U373 MG cells: Evidence for involvement of store-operated channels. J. Neurosci. Res. 2008;86(15):3456–3468.

  48. Moreno C, Sampieri A, Vivas O, Peρa-Segura C, Vaca L. STIM1 and Orai1 mediate thrombin-induced Ca(2+) influx in rat cortical astrocytes. Cell Calcium. 2012;52(6):457–67.

  49. Putney JW. Recent breakthroughs in the molecular mechanism of capacitative calcium entry (with thoughts on how we got here). Cell Calcium. 2007;42(2):103–10.

  50. Minelli A, Castaldo P, Gobbi P, et al. Cellular and subcellular localization of Na+-Ca2+ exchanger protein isoforms, NCX1, NCX2, and NCX3 in cerebral cortex and hippocampus of adult rat. Cell Calcium. 2007;41(3):221–234.

  51. Kirischuk S, Ketfenmann H. Na+/ Ca2+exchanger modulates Ca2+ signaling in Bergmann glial cells in situ. Fed. Am. Soc. Exp. Biol. 2007;7(566):566–572.

  52. Goldman WF, Yarowsky PJ, Juhaszova M, Krueger BK, Blaustein MP. Sodium/calcium exchange in rat cortical astrocytes. J. Neurosci. 1994;14(10):5834–5843.

  53. Reyes RC, Verkhratsky A, Parpura V. Plasmalemmal Na+/Ca2+ exchanger modulates Ca2+- dependent exocytotic release of glutamate from rat cortical astrocytes. ASN Neuro. 2012;4(1):33–45.

  54. Paluzzi S, Alloisio S, Zappettini S, et al. Adult astroglia is competent for Na+/Ca2+ exchangeroperated exocytotic glutamate release triggered by mild depolarization. J. Neurochem. 2007;103(3):1196–1207.

  55. Kamer KJ, Mootha VK. The molecular era of the mitochondrial calcium uniporter. Nat. Rev. Mol. Cell Biol. 2015;16(9):545–53.

  56. Rizzuto R. Microdomains of Intracellular Ca2+: Molecular Determinants and Functional Consequences. Physiol. Rev. 2006;86(1):369–408.

  57. Parnis J, Montana V, Delgado-Martinez I, et al. Mitochondrial exchanger NCLX plays a major role in the intracellular Ca2+ signaling, gliotransmission, and proliferation of astrocytes. J. Neurosci. 2013;33(17):7206–19.

  58. Vardjan N, Parpura V, Zorec R. Loose excitation-secretion coupling in astrocytes. Glia. 2016;May 64(5):655–67.

  59. Sahlender DA, Savtchouk I, Volterra A. What do we know about gliotransmitter release from astrocytes? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2014;369(1654):20130592.

  60. Neuroglia. New York: Oxford; 2013.

  61. Golovina VA, Blaustein MP. Unloading and refilling of two classes of spatially resolved endoplasmic reticulum Ca(2+) stores in astrocytes. Glia. 2000;31(1):15–28.

  62. Hua X, Malarkey EB, Sunjara V, et al. Ca2+-Dependent Glutamate Release Involves Two Classes of Endoplasmic Reticulum Ca2+ Stores in Astrocytes. J. Neurosci. Res. 2004;76(1):86–97.

  63. Rusakov DA, Bard L, Stewart MG, Henneberger C. Diversity of astroglial functions alludes to subcellular specialisation. Trends Neurosci. 2014;37(4):228–42.

  64. Petravicz J, Boyt KM, McCarthy KD. Astrocyte IP3R2-dependent Ca(2+) signaling is not a major modulator of neuronal pathways governing behavior. Front. Behav. Neurosci. 2014;8(November):384.

  65. Fiacco TA, Agulhon C, Taves SR, et al. Selective Stimulation of Astrocyte Calcium In??Situ??Does Not Affect Neuronal Excitatory??Synaptic Activity. Neuron. 2007;54(4):611–626.

  66. Petravicz J, Fiacco TA, McCarthy KD. Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J. Neurosci. 2008;28(19):4967–73.

  67. Agulhon C, Fiacco TA, McCarthy KD. Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science. (80-. ). 2010;327(5970):1250–1254.

  68. Reichenbach A, Derouiche A, Kirchhoff F. Morphology and dynamics of perisynaptic glia. Brain Res. Rev. 2010;63(1–2):11–25.

  69. Patrushev I, Gavrilov N, Turlapov V, Semyanov A. Subcellular location of astrocytic calcium stores favors extrasynaptic neuron-astrocyte communication. Cell Calcium. 2013;54(5):343–9.

  70. Jackson JG, Robinson MB. Reciprocal Regulation of Mitochondrial Dynamics and Calcium Signaling in Astrocyte Processes. J. Neurosci. 2015;35(45):15199–213.

  71. Peng TI, Greenamyre JT. Privileged access to mitochondria of calcium influx through N-methyl-Daspartate receptors. Mol. Pharmacol. 1998;53(6):974–80.

  72. Hur YS, Kim KD, Paek SH, Yoo SH. Evidence for the existence of secretory granule (dense-core vesicle)-based inositol 1,4,5-trisphosphate-dependent Ca2+ signaling system in astrocytes. PLoS One. 2010;5(8):e11973.

  73. Barcelσ-Torns M, Lewis AM, Gubern A, et al. NAADP mediates ATP-induced Ca2+ signals in astrocytes. FEBS Lett. 2011;585(14):2300–6.

  74. Heidemann AC, Schipke CG, Kettenmann H. Extracellular application of nicotinic acid adenine dinucleotide phosphate induces Ca2+ signaling in astrocytes in situ. J. Biol. Chem. 2005;280(42):35630–40.

  75. Gomes DA, Leite MF, Bennett AM, Nathanson MH. Calcium signaling in the nucleus. Can. J. Physiol. Pharmacol. 2006;84(3–4):325–32.

  76. Hardingham GE, Arnold FJ, Bading H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 2001;4(3):261–7.

  77. Zhao L, Brinton RD. Vasopressin-induced cytoplasmic and nuclear calcium signaling in embryonic cortical astrocytes: dynamics of calcium and calcium-dependent kinase translocation. J. Neurosci. 2003;23(10):4228–39.

  78. Zheng K, Bard L, Reynolds JP, et al. Time-Resolved Imaging Reveals Heterogeneous Landscapes of Nanomolar Ca2+ in Neurons and Astroglia. Neuron. 2015;88(2):277–288.

  79. Smith K. Neuroscience: Settling the great glia debate. Nature. 2010;468(7321):160–162.

  80. Panatier A, Vallιe J, Haber M, et al. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell. 2011;146(5):785–98.

  81. Croft W, Dobson KL, Bellamy TC. Plasticity of Neuron-Glial Transmission: Equipping Glia for Long- Term Integration of Network Activity. Neural Plast. 2015;2015:1–11.

  82. Dombeck DA, Khabbaz AN, Collman F, Adelman TL, Tank DW. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron. 2007;56(1):43–57.

  83. Howarth C. The contribution of astrocytes to the regulation of cerebral blood flow. Front. Neurosci. 2014;8:103.

  84. Anderson MA, Ao Y, Sofroniew M V. Heterogeneity of reactive astrocytes. Neurosci. Lett. 2014;565:23–29.

  85. Matyash V, Kettenmann H. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev. 2010;63(1–2):2–10.

  86. Sun W, McConnell E, Pare J-F, et al. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science. 2013;339(6116):197–200.

  87. Thrane AS, Rangroo Thrane V, Zeppenfeld D, et al. General anesthesia selectively disrupts astrocyte calcium signaling in the awake mouse cortex. Proc. Natl. Acad. Sci. U. S. A. 2012;109(46):18974–9.

  88. Rusakov D a. Disentangling calcium-driven astrocyte physiology. Nat. Rev. Neurosci. 2015;16(March):1–8.




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