Skip to main content
SpringerLink
Log in

Components of astrocytic intercellular calcium signaling

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

It has become evident that astrocytes play major roles in central nervous system (CNS) function. Because they are endowed with ion channels, transport pathways, and enzymatic intermediates optimized for ionic uptake, degradation of metabolic products, and inactivation of numerous substances, they are able to sense and correct for changes in neural microenvironment. Besides this housekeeping role, astrocytes modulate neuronal activity either by direct communication through gap junctions or through the release of neurotransmitters and/or nucleotides affecting nearby receptors. One prominent mode by which astrocytes regulate their own activity and influence neuronal behavior is via Ca2+ signals, which may be restricted within one cell or be transmitted throughout the interconnected syncytium through the propagation of intercellular calcium waves. This review aims to outline the most recent advances regarding the active communication of astrocytes that is encoded by intracellular calcium variation.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kater S. B., Matson M. P., Cohen C., and Connor J. (1988) Calcium regulation of the neuronal growth cone. Trends Neurosci. 11, 315–321.

    PubMed  CAS  Google Scholar 

  2. Lo Turco J. J., Owens D. F., Heath M. J. S., Davis B. E. M., and Kriegstein A. R. (1995) GABA and glutamate depolarize cortical progenitor cells and inhibits DNA synthesis. Neuron 15, 1287–1298.

    Google Scholar 

  3. Gosh A. and Greenberg M. E. (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268, 239–247.

    Google Scholar 

  4. Komuro H. and Rakic P. (1996) Intracellular Ca2+ fluctuations modulates the rate of neuronal migration. Neuron 17, 275–285.

    Google Scholar 

  5. Gu X. and Spitzer N. C. (1997) Breaking the code: regulation of neuronal differentiation by spontaneous calcium transients. Dev. Neurosci. 19, 33–41.

    PubMed  CAS  Google Scholar 

  6. Galli I. and Maffe L. (1988) Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 272, 90–91.

    Google Scholar 

  7. Meister M., Wong R. O. I., Baylor D. A., and Shatz C. J. (1991) Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943.

    PubMed  CAS  Google Scholar 

  8. Feller M. B., Wellis D. P., Stellwagen D., Werblin E. S., and Shatz C. J. (1996) Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272, 1182–1187.

    Google Scholar 

  9. Yuste R., Peinado A., and Katz L. C. (1992) Neuronal domains in developing neocortex. Science 257, 665–669.

    PubMed  CAS  Google Scholar 

  10. Kandler K. and Katz L. C. (1998) Coordination of neuronal activity in developing visual cortex by gap junction-mediated biochemical communication. J. Neurosci. 18, 1419–1427.

    PubMed  CAS  Google Scholar 

  11. Garaschuck O., Linn J., Eilers J., and Konnerth A. (2000) Large-scale oscillatory calcium waves in the immature cortex. Nat. Neurosci. 3, 452–459.

    Google Scholar 

  12. Harris-White M. E., Zanotti A. S., Frautschy A. S., and Charles A. C. (1998) Spiral intercellular calcium waves in hippocampal slice cultures J. Neurophysiol. 79, 1045–1052.

    PubMed  CAS  Google Scholar 

  13. Weliky M. and Katz L. C. (1997) Disruption of orientation tuning in visual cortex by artificaially correlated neuronal activity. Nature 386, 680–685.

    PubMed  CAS  Google Scholar 

  14. Penn A. A., Riquelme P. A., Feller M. B., and Shatz C. L. (1998) Competition in retinogeniculate pattering driven by spontaneous activity. Science 279, 2108–2112.

    PubMed  CAS  Google Scholar 

  15. Shatz C. J. and Stryker M. P. (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculae afferents. Science 242, 87–89.

    PubMed  CAS  Google Scholar 

  16. Sanderson M. J., Charles A. C., Boitano S., and Dirksen E. R. (1994) Mechanisms and function of intercellular calcium signaling. Mol. Cell. Endocrinol. 98, 173–197.

    PubMed  CAS  Google Scholar 

  17. Newman E. A. and Zahs K. R. (1997) Calcium waves in retinal glial cells. Science 275, 844–847.

    PubMed  CAS  Google Scholar 

  18. Newman E. A. and Zahs K. R. (1998) Modulation of neuronal activity by glial cells in the retina. J. Neurosci. 18, 4022–4028.

    PubMed  CAS  Google Scholar 

  19. Araque A., Sanzgiri R. P., Parpura V., and Haydon P. G. (1998) Calcium elevation in astrocytes causes and NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J. Neurosci. 18, 6822–6829.

    PubMed  CAS  Google Scholar 

  20. Araque A., Parpura V., Sanzgiri R. P., and Haydon P. G. (1998) Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10, 2129–2142.

    PubMed  CAS  Google Scholar 

  21. Araque A., Parpura V., Sanzgiri R. P., and Haydon P. G. (1999) Tripartite synapses: glia, the uncknowledged partner. Trends Neurosci. Sci. 22, 208–215.

    CAS  Google Scholar 

  22. Cornell-Bell A. H. and Finkbeiner S. M. (1991) Ca2+ waves in astrocytes. Cell Calcium 12, 185–204.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  24. Martins-Ferreira H. and Ribeiro L. J. (1995) Biphasic effect of gap junctional uncoupling agents on the propagation of retinal spreading depression. Braz. J. Med. Biol. Res. 28, 991–994.

    PubMed  CAS  Google Scholar 

  25. Nedergaard M., Cooper A. J., and Goodman S. A. (1995) Gap junctions are required for the propagation of spreading depression. J. Neurobiol. 28, 433–444.

    PubMed  CAS  Google Scholar 

  26. Lauritzen M. (1994) Pathophysiology of the migraine aura. The spreading depression theory. Brain 117, 199–210.

    PubMed  Google Scholar 

  27. Martins-Ferreira H., Nedergaard M., and Nicholson C. (2000) Perspectives on spreading depression. Brain Res. Rev. 32, 203–214.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  29. Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., and Smith S. J. (1990) Glutamate induces calcium waves in cultured astrocytes: longrange glial signalling. Science 247, 470–473.

    PubMed  CAS  Google Scholar 

  30. Kim W. T., Rioult M. G., and Cornell-Bell A. H. (1994) Glutamate-induced calcium signaling in astrocytes. Glia 11, 173–184.

    PubMed  CAS  Google Scholar 

  31. Charles A. C., Merrill J. E., Dirksen E. R., and Sanderson M. J. (1991) Intercellular signaling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6, 983–992.

    PubMed  CAS  Google Scholar 

  32. Charles A. C., Kodali S. K., and Tyndale R. F. (1996) Intercellular calcium waves in neurons. Mol. Cell. Neurosci. 7, 337–353.

    Google Scholar 

  33. Venance L., Piomelli D., Glowinski J., and Giaume C. (1995) Inhibition by anandamide of gap junctions and intercellular calcium signaling in striatal astrocytes. Nature 376, 590–594.

    PubMed  CAS  Google Scholar 

  34. Venance L., Stella N., Glowinski J., and Giaume C. (1997) Mechaism involved in initiation and propagation of receptor-induced intercellular calcium signaling in cultured rat astrocytes. J. Neurosci. 17, 1981–1992.

    PubMed  CAS  Google Scholar 

  35. Muyderman H., Nilsson M., Blomstrand F., Khatibi S., Olsson T., Hansson E., and Ronnback L. (1998) Modulation of mechanically induced calcium waves in hippocampal astroglial cells. Inhibitory effects of alpha 1-adrenergic stimulation. Brain Res. 793, 127–135.

    PubMed  CAS  Google Scholar 

  36. Strahonja-Packard A. and Sanderson M. J. (1999) Intercellular Ca2+ waves induce temporally and spatially distinct intracellular Ca2+ oscillations in glia. Glia 28, 97–113.

    PubMed  CAS  Google Scholar 

  37. Scemes E., Dermietzel R., and Spray D. C. (1998) Calcium waves between astrocytes from Cx43 knock-out mice. Glia 24, 65–73.

    PubMed  CAS  Google Scholar 

  38. Scemes E., Suadicani S. O., and Spray D. C. (2000a) Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation. J. Neurosci. 20, 1435–1445.

    PubMed  CAS  Google Scholar 

  39. Finkbeiner S. (1992) Calcium waves in astrocytes: filling in the gaps. Neuron. 8, 1101–1108.

    PubMed  CAS  Google Scholar 

  40. Enkvist M. O. and McCarthy K. D. (1992) Activation of protein kinase C blocks astroglial gap junction communication and inhibits the spread of calcium waves. J. Neurochem. 59, 519–526.

    PubMed  CAS  Google Scholar 

  41. Yagodin S., Holtzclaw L. A., and Russell J. T. (1995) Subcellular calcium oscillators and calcium influx support agonist-induced calcium waves in cultured astrocytes. Mol. Cell Biochem. 149–150, 137–144.

    PubMed  Google Scholar 

  42. Blomstrand F., Aberg N. D., Eriksson P. S., Hansson E., and Ronnback L. (1999a) Extent of intercellular calcium wave propagation is related to gap junction permeability and level of connexin43 expression in astrocytes in primary cultures from four brain regions. Neuroscience 92, 255–265.

    PubMed  CAS  Google Scholar 

  43. Blomstrand F., Khatibi S., Muyderman H., Hansson E., Olsson T., and Ronnback L. (1999b) 5-Hydroxytryptamine and glutamate modulate velocity and extent of intercellular calcium signalling in hippocampal astroglial cells in primary cultures. Neuroscience 88, 1241–1253.

    PubMed  CAS  Google Scholar 

  44. Dani J. W., Chernjavsky A., and Smith S. J. (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8, 429–440.

    PubMed  CAS  Google Scholar 

  45. Porter J. T. and McCarthy K. D. (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16, 5073–5081.

    Google Scholar 

  46. Bacci A., Verderio C., Pravetonni E., and Matteoli M. (1999) The role of glial cells in synaptic function. Phil. Trans. R. Soc. Lond. 354, 403–409.

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  48. Kang J., Jiang L., Goldman A. S., and Nedergaard M. (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1, 683–692.

    PubMed  CAS  Google Scholar 

  49. Parpura V., Basarsky T. A., Liu F., Jeftinija S., and Haydon P. G. (1994) Glutamate-mediated astrocyte-neuron signaling. Nature 369, 744–747.

    PubMed  CAS  Google Scholar 

  50. Parpura V., Doyle R. T., Basarsky T. A., Henderson E., and Haydon P. G. (1995) Dynamic imaging of purified individual synaptic vesicles. Neuroimage 2(1), 3–7.

    PubMed  CAS  Google Scholar 

  51. Hassinger T. D., Atkinson P. B., Strecker G. J., Whalen I. R., Dudek F. E., Koseel A. H., and Kater S. B. (1996) Evidence for glutamate-mediated activation of hippocampal neurons by glial calcium waves. J. Neurobiol. 28, 159–170.

    Google Scholar 

  52. Bezzi P., Carmignoto G., Pasti L., Vesce S., Rossi D., Rizzini B. L., Pozzan T., and Volterra A. (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 281–285.

  53. Innocenti B., Parpura V., and Haydon P. G. (2000) Imaging extracellular waves of glutamate during calcium signaling in cultured astrocytes. J. Neurosci. 20, 1800–1808.

    PubMed  CAS  Google Scholar 

  54. Parpura V. and Haydon P. G. (2000) Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. Proc. Natl. Acad. Sci. USA 97, 8629–8634.

    PubMed  CAS  Google Scholar 

  55. Grundfest H. (1959) Synaptic and ephatic transmission, in Handbook of Physiology (Field J., Magoun H-. W-., and Hall V. E., eds), vol. 1, pp. 147–197, Williams & Wilkins Co., Baltimore, MD.

    Google Scholar 

  56. Giaume C. and Venance L. (1998) Intercellular calcium signaling and gap junction communication in astrocytes. Glia 24, 50–64.

    PubMed  CAS  Google Scholar 

  57. Scemes E., Suadicani S. O., and Spray D. C. (2000b) Intercellular calcium wave communication via gap junction dependent and independent mechanisms. Curr. Topics Membr. 49, 145–173.

    CAS  Google Scholar 

  58. Parker I. and Yao Y. (1994) Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate. Proc. R. Soc. Lond. 246, 269–274.

    Google Scholar 

  59. Bootman M. D. and Berridge M. J. (1995) The elemental principal of calcium signalling. Cell 83, 675–678.

    PubMed  CAS  Google Scholar 

  60. Berridge M. J. (1997) Elementary and global aspects of calcium signalling. J. Physiol. 499, 291–306.

    PubMed  CAS  Google Scholar 

  61. Berridge M. J., Bootman M. D., and Lipp P. (1998) Calcium: a life and death signal. Curr. Biol. 9, 157–159.

    Google Scholar 

  62. Sheppard C. A., Simpson P. B., Sharp A. H., Nucifora F. C., Ross C. A., Lange G. D., and Russell J. T. (1997) Comparison of type 2 inositol 1,4,5-trisphosphate receptor distribution and subcellular Ca2+ release sites that support Ca2+ waves in cultured astrocytes. J. Neurochem. 68, 2317–2327.

    Article  PubMed  CAS  Google Scholar 

  63. Rooney T. A., Sass E. J., and Thomas A. P. (1990) Agonist-induced cytosolic calcium oscillations originate from a specific locus in single hepatocytes. J. Biol. Chem. 265, 10792–10796.

    PubMed  CAS  Google Scholar 

  64. Thomas A. P., Renard D. C., and Rooney T. A. (1991) Spatial and temporal organization of calcium signalling in hepatocytes. Cell Calcium 12, 111–126.

    PubMed  CAS  Google Scholar 

  65. Simpson P. B. and Russell J. T. (1996) Mitochondria support inositol 1,4,5 trisphosphate-mediated Ca2+ waves in cultured olygodendrocytes. J. Biol. Chem. 271, 33493–33501.

    Google Scholar 

  66. Thomas D., Lipp P., Tovey S. C., Berridge M. J., Li W., Tsien R. Y., and Bootman M. D. (2000) Microscopic properties of elementary Ca2+ release sites in non-excitable cells. Cur. Biol. 10, 8–15.

    CAS  Google Scholar 

  67. Bezprozvanny I. and Ehrlich B. E. (1995) The inositol 1,4,5-trisphosphate receptors. J. Membr. Biol. 145, 205–216.

    PubMed  CAS  Google Scholar 

  68. Finch E. A., Turner T. J., and Goldin S. M. (1991) Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252, 443–446.

    PubMed  CAS  Google Scholar 

  69. Yao Y., Choi J., and Parker I. (1995) Quantal puffs of intracellular Ca2+ evoked by inositol trisphosphate in Xenopus oocytes. J. Physiol. 482, 533–553.

    PubMed  CAS  Google Scholar 

  70. Berridge M. J. (1993) Inositol trisphosphate and calcium signalling. Nature 361, 315–325.

    PubMed  CAS  Google Scholar 

  71. Golovina V. A. and Blaustein M. P. (2000) Unloading and refilling of two classes of spatially resolved endoplasmic reticulum Ca2+ stores in astrocytes. Glia 31, 15–28.

    PubMed  CAS  Google Scholar 

  72. Taylor C. W. (1998) Inositol trisphosphate receptors: Ca2+-modulated intracellular Ca2+ channels. Biochim. Biophys Acta 1436, 19–33.

    PubMed  CAS  Google Scholar 

  73. Joseph S. K. (1996) The inositol triphosphate receptor family. Cell. Signal. 8, 1–7.

    Google Scholar 

  74. Yamamoto-Hino M., Miyawaki A., Kawano H., Sugiyama T., Furuichi T., Hasegawa M., and Mikoshiba K. (1995) Immunohistochemical study of inositol 1,4,5-trisphosphate receptor type 3 in rat central nervous system. Neuroreport 26, 273–276.

    Article  Google Scholar 

  75. Yakel J. L. (1997) Calcineurin regulation of synaptic function: from ion channels to transmitter release and gene transcription. Trends Pharmacol. Sci. 18, 124–134.

    PubMed  CAS  Google Scholar 

  76. Cameron A. M., Steiner J. P., Roskams A. J., Ali S. M., Ronnett G. V., and Snyder S. H. (1995) Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell 83, 463–472.

    PubMed  CAS  Google Scholar 

  77. Simpson P. B., Holtzclaw L. A., Langley D. B., and Russell J. T. (1998a) Characterization of ryanodine receptors in oligodendrocytes, type 2 astrocytes and O-2A progenitors. J. Neurosci. Res. 52, 468–482.

    PubMed  CAS  Google Scholar 

  78. Simpson P. B., Mehotra S., Langley D., Sheppard C. A., and Russell J. T. (1998b) Specialized distributions of mitochondria and endoplasmic reticulum proteins define Ca2+ wave amplification sites in cultured astrocytes. J. Neurosci. Res. 52, 672–683.

    PubMed  CAS  Google Scholar 

  79. Boitier E., Rea R., and Duchen M. R. (1999) Mitochondria exert a negative feedback on the propagation of intracellular Ca2+ waves in rat cortical astrocytes. J. Cell Biol. 145, 795–808.

    PubMed  CAS  Google Scholar 

  80. Charles A. C. (1998) Intercellular calcium waves in glia. Glia 24, 39–49.

    PubMed  CAS  Google Scholar 

  81. Charles A. C., Naus C. C., Kidder G. M., Dirksen E. R., and Sanderson M. (1992) Intercellular calcium signaling via gap junctions in glioma cells. J. Cell Biol. 118, 195–201.

    PubMed  CAS  Google Scholar 

  82. Hassinger T. D., Guthrie P. B., Atkinson P. B., Bennett M. V. L., and Kater S. B. (1996) An extracellular component in propagation of astrocytic calcium waves. Proc. Natl. Acad. Sci. USA 93, 13268–13273.

    Google Scholar 

  83. Guan X., Cravatt B. F., Ehring G. R., Hall J. E., Boger D. L., Lerner R. A., and Gilula N. B. (1997) The sleep-inducing lipid oleomide deconvolutes gap junctions communication and calcium wave transmission in glial cells. J. Cell Biol. 139, 1785–1792.

    PubMed  CAS  Google Scholar 

  84. Zanotti S. and Charles A. (1997) Extracellular calcium sensing by glial cells: low extracellular calcium induces intracellular calcium release and intracellular signaling. J. Neurochem. 69, 594–602.

    Article  PubMed  CAS  Google Scholar 

  85. Cotrina M. L., Lin J. H. C., and Nedergaard M. (1998) Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling. J. Neurosci. 18, 8794–8804.

    PubMed  CAS  Google Scholar 

  86. Wang Z., Haydon P. G., and Yeung E. S. (2000) Direct observation of Calcium-independent intercellular ATP signaling in astrocytes. Anal. Chem. 72, 2001–2007.

    PubMed  CAS  Google Scholar 

  87. Batter D. K., Corpina R. A., Roy C., Spray D. C., Hertzberg E. L., and Kessler J. A. (1992) Heterogeneity in gap junction expression in astrocytes cultured from different brain regions. Glia 6, 213–221.

    PubMed  CAS  Google Scholar 

  88. Lee S. H., Kim W. T., Cornell-Bell A. H., and Sontheimer H. (1994) Astrocytes exhibits regional specificity in gap junction coupling. Glia 11, 315–325.

    PubMed  CAS  Google Scholar 

  89. Spray D. C., Vink M. J., Scemes E., Suadicani S. O., Fishman G. I., and Dermietzel R. (1998) Characteristics of coupling in cardiac myocytes and CNS astrocytes cultured from wild-type and Cx43-null mice, in Gap Junctions (Werner R., ed.), IOS, Netherlands, pp. 281–285.

    Google Scholar 

  90. Kunzelman P., Schroder W., Traub O., Steinhauser C., Dermietzel R., and Willecke K. (1999) Late onset and increasing expression of the gap junction protein connexin30 in adult murine brain and long-term cultured astrocytes. Glia 25, 111–119.

    Google Scholar 

  91. Dermietzel R., Gao Y., Scemes E., Vieira D., Urban M., Kremer M., et al. (2000) Connexin43 null [Cx43(−/−)] mice reveal that astrocytes express multiple connexins. Brain Res. Rev. 32, 45–56.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  93. Ho C., Hicks J., and Salter M. W. (1995) A novel P2 purinoceptor expressed by a subpopulation of astrocytes from the dorsal spinal cord of the rat. Br. J. Pharmacol. 116, 2909–2918.

    PubMed  CAS  Google Scholar 

  94. King B. F., Neary J. T., Zhu Q., Wang S., Norenberg M. D., and Burnstock G. (1996) P2 purinoceptors in rat cortical astrocytes: expression, calcium imaging, and signaling studies. Neuroscience 74, 1187–1196.

    Google Scholar 

  95. John G. R., Scemes E., Suadicani S. O., Liu J. S., Charles P. C., Lee S. C., et al. (1999) Inter-leukin-1β differentially regulates calcium wave propagation between primary human fetal astrocytes via pathways involving P2 receptors and gap junction channels. Proc. Natl. Acad. Sci. USA 98, 11613–11618.

    Google Scholar 

  96. Suadicani S. O., Urban M., Spray D. C., and Scemes E. (2000) Astrocytic signaling: interplay between connexin43 (Cx43) and P2Y receptor subtypes. Rev. Neurol. 30(6), 32 (abstract).

    Google Scholar 

  97. Nagy J. I. and Rash J. E. (2000) Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res. Rev. 32, 29–44.

    PubMed  CAS  Google Scholar 

  98. Dermietzel R., Hertzberg E. L., Kessler J. A., and Spray D. C. (1991) Gap junctions between cultured astrocytes: immunocytochemical, molecular and electrophysiological analysis. J. Neurosci. 11, 1421–1432.

    PubMed  CAS  Google Scholar 

  99. Dermietzel R. (1996) Molecular diversity and plasticity of gap junctions in the nervous system, in Gap Junctions in the Nervous System (Spray D. C. and Dermietzel R., eds.), Landes, Houston, pp. 39–60.

    Google Scholar 

  100. Spray D. C. (1996) Physiological properties of gap junction channels, in Gap Junctions in the Nervous Systems (Spray D. C. and Dermietzel R., eds.), Landes, Houston, pp. 39–60.

    Google Scholar 

  101. Ochalski P. A., Frankenstein U. N., Hertzberg E. L., and Nagy J. I. (1997) Connexin43 rat spinal cord: localization and identification of heterotypic astro-oligodendrocytic gap junctions. Neuroscience 76, 931–945.

    PubMed  CAS  Google Scholar 

  102. Theriault E., Frankenstein U. N., Hertzberg E. L., and Nagy J. I. (1997) Connexin43 and astrocytic gap junctions in the rat spinal cord after acute compression injury. J. Comp. Neurol. 328, 199–214.

    Google Scholar 

  103. Rash J. K. and Yasumura T. (1999) Direct immunogold labeling of connexin and aquaporin-4 in freeze fracture replicas of liver, brain, and spinal cord: factors limiting quantitative analysis. Cell Tissue Res. 296, 307–321.

    PubMed  CAS  Google Scholar 

  104. Veenstra R. D., Wang H. Z., Beyer E. C., and Brink P. R. (1994) selective dye and ionic permeability of gap junction channels formed by connexin45. Circ. Res. 75, 483–490.

    PubMed  CAS  Google Scholar 

  105. Beblo D. A., Wang H. Z., Beyer E. C., Westphale E. M., and Veenstra R. D. (1995) Unique conductance, gating, and selective permeability properties of gap junction channels formed by connexin40. Circ. Res. 77, 813–822.

    PubMed  CAS  Google Scholar 

  106. Beblo D. A. and Veenstra R. D. (1997) Monovalent cation permeation through the connexin40 gap junction channels, Cs+, Rb+, K+, Li+, TEA, TMA, TBA and effects of anions Br−, Cl−, F−, acetate, aspartate, glutamate and NO3. J. Gen. Physiol. 109, 509–522.

    PubMed  CAS  Google Scholar 

  107. Wang H. Z. and Veenstra R. D. (1997) Monovalent ion selectivity sequences of rat connexin43 gap junction channel. J. Gen. Physiol. 109, 491–507.

    PubMed  CAS  Google Scholar 

  108. Niessen H., Harz H., Bedner P., Kramer K., and Willecke K. (2000) Selective permeability of different connexin channels to the second messenger inositol 1,4,5-trisphosphate. J. Cell Sci. 113, 1365–1372.

    PubMed  CAS  Google Scholar 

  109. Paemeleire K., Martin P. E. M., Coleman S. L., Fogarty K. E., Carrington W. A., Leybaert L., et al. (2000) Intercellular calcium waves in HeLa cells expressing GFP-labeled connexin 43, 32, or 26. Mol. Biol. Cell 11, 1815–1827.

    PubMed  CAS  Google Scholar 

  110. Saez J. C., Connor J. A., Spray D. C., and Bennett M. V. L. (1989) Hepatocyte gap junctions are permeable to second messenger, inositol 1,4,5 trisphosphate, and to calcium ions. Proc. Natl. Acad. Sci. USA 86, 2708–2712.

    PubMed  CAS  Google Scholar 

  111. Galione A., Lee H. C., and Busa W. B. (1991) Ca2+-induced Ca2+ release in sea urchin egg homogenates: Modulation by cyclic ADP-ribose. Science, 253, 1143–1146.

    PubMed  CAS  Google Scholar 

  112. Galione A. (1992) Ca2+-induced Ca2+ release and its modulation by cyclic ADP-ribose. Trends Pharmacol. Sci. 13, 304–306.

    PubMed  CAS  Google Scholar 

  113. D’Andrea P. and Vittur F. (1997) Propagation of intercellular Ca2+ waves in mechanically stimulated articular chondrocytes. FEBES Lett. 400, 58–64.

    CAS  Google Scholar 

  114. Miura M., Boyden P. A., and ter Keurs H. E. D. J. (1998) Ca2+ waves during triggered propagated contractions in intact trabeculae. Am. J. Physiol. 274, H266-H276.

    PubMed  CAS  Google Scholar 

  115. Churchill G. and Louis C. (1998) Role of Ca2+, inositol trisphosphate, and cyclic ADP ribose in mediating intercellular Ca2+ signaling in sheep lens cells. J. Cell Sci. 111, 1217–1225.

    PubMed  CAS  Google Scholar 

  116. Lamont C., Luther P. W., Bakle C. W., and Wier W. G. (1998) Intercellular Ca2+ waves in rat heart muscle. J. Physiol. 512, 157–167.

    Google Scholar 

  117. Leybaert L., Paemeleire K., Strahonja A., and Sanderson M. J. (1998) Inositol-trisphosphate-dependent intercellular calcium signaling in and between astrocytes and endothelial cells. Glia 24, 398–407.

    PubMed  CAS  Google Scholar 

  118. Allbritton N. L., Meyer T., and Stryer L. (1992) Range of messenger action of calcium ions and inositol 1,4,5-trisphosphate. Science 258, 1812–1815.

    PubMed  CAS  Google Scholar 

  119. Sneyd J., Wetton B. T. R., Charles A. C., and Sanderson M. J. (1995) Intercellular calcium waves mediated by diffusion of inositol trisphosphate: a two-dimensional model. Am. J. Physiol. 268, C1537-C1545.

    PubMed  CAS  Google Scholar 

  120. Osipchuk Y. and Cahalan M. (1992) Cell-to-cell spread of calcium signals mediated by ATP receptors in mast cells. Nature 359, 241–244.

    PubMed  CAS  Google Scholar 

  121. Guthrie P. B., Knappenberger J., Segal M., Bennett M. V. L., Charles A. C., and Kater S. B. (1999) ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520–528.

    PubMed  CAS  Google Scholar 

  122. Queiroz G., Gebicke-Haerter P. J., Schobert A., Starke K., and von Kegelgen I. (1997) Release of ATP from cultured rat astrocytes elicited by glutamate receptor activation. Neuroscience 78, 1203–1208.

    PubMed  CAS  Google Scholar 

  123. Pasti I., Volterra A., Pozzan T., and Carmignoto G. (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J. Neurosci. 17, 7817–7830.

    PubMed  CAS  Google Scholar 

  124. Cotrina M. L., Lin J. H. C., Lopez-Garcia J. C., Naus C. C. G., and Nedergaard M. (2000) ATP-mediated glia signaling. J. Neurosci. 20, 2835–2844.

    PubMed  CAS  Google Scholar 

  125. Li H., Liu T. F., Lazrak A., Peracchia C., Goldberg G. S., Lampe P. D., and Johnson R. G. (1996) Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J. Cell Biol. 134, 1019–1030.

    Google Scholar 

  126. John S. A., Kondo R., Wang S. Y., Goldhaber J. I., and Weiss J. N. (1999) Connexin-43 hemichannels opened by metabolic inhibition. J. Biol. Chem. 274, 236–240.

    PubMed  CAS  Google Scholar 

  127. Condorelli D. F., Conti F., Gallo V., Kirchhoff F., Seifer G., Steinhauser C., et al. (1999) Expression and functional analysis of glutamate receptors in glial cells. Adv. Exp. Med. Biol. 468, 49–67.

    PubMed  CAS  Google Scholar 

  128. Gallagher C. J. and Salter M. W. (1999) Nucleotide receptor signalling in spinal cord astrocytes: findings and functional implications. Prog. Brain Res. 120, 311–322.

    Article  PubMed  CAS  Google Scholar 

  129. Motin L. and Bennett M. R. (1995) Effect of P2-purinoceptor antagonists on glutamatergic transmission in the rat hippocampus. Br. J. Pharmacol. 115, 1276–1280.

    PubMed  CAS  Google Scholar 

  130. Wierasko A. and Ehrlich Y. H. (1994) On the role of extracellular ATP in the induction of long-term potentiation in the hippocampus. J. Neurochem 63, 1731–1737.

    Article  Google Scholar 

  131. Fujii S., Kato H., Furuse H., Ito K., Osada H., Hamaguchi T., and Kuroda Y. (1995) The mechanism of ATP-induced long-term potentiation involves extracellular phosphorylation of membrane proteins in guinea pig hippocampal CA1 neurons. Neurosci. Lett. 187, 130–132.

    PubMed  CAS  Google Scholar 

  132. Fujii S., Kato H., and Kuroda Y. (1999) Extracellular adenosine 5′-triphosphate plus activation of glutamatergic receptors induces long-term potentiation in CA1 neurons of guinea pig hippocampal slices. Neurosci. Lett. 276, 21–24.

    PubMed  CAS  Google Scholar 

  133. Sykova E. (1997) Extracellular space volume and geometry of the brain after ischemia and central injury. Adv. Neurol. 73, 121–135.

    PubMed  CAS  Google Scholar 

  134. Schmitt F. O. (1984) Molecular regulator of brain function: a new view. Neuroscience 13, 991–1001.

    PubMed  CAS  Google Scholar 

  135. Nicholson C. and Sykova E. (1998) Extracellular structure revealed by diffusion analysis. Trends Neurosci. 21, 207–215.

    PubMed  CAS  Google Scholar 

  136. Froes M. M., Correia A. H., Garcia-Abreu J., Spray D. C., Campos de Carvalho A. C., and Neto M. V. (1999) Gap-junctional coupling between neurons and astrocytes in primary central nervous system cultures. Proc. Natl. Acad. Sci. 96, 7541–7546.

    PubMed  CAS  Google Scholar 

  137. Alvarez-Maubecin V., Garcia-Hernandez F., Williams J. T., and Van Bockstaele E. J. (2000) Functional coupling between neurons and glia. J. Neurosci. 20, 4091–4098.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, Kennedy Center, Rm 924, Albert Einstein College of Medicine, 1410 Pelham Parkway South, 10461, Bronx, NY

    Eliana Scemes

Authors
  1. Eliana Scemes
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scemes, E. Components of astrocytic intercellular calcium signaling. Mol Neurobiol 22, 167–179 (2000). https://doi.org/10.1385/MN:22:1-3:167

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/MN:22:1-3:167

Index Entries

Search

Navigation