Neuroscience
Frontiers in Neuroenergetics ·
Volume 2 - 2010 | https://doi.org/10.3389/fnene.2010.00129
Astroglial Wiring is Adding Complexity to Neuroglial Networking
- Christian Giaume1*corresponding author
- 1 INSERM U840, Collège de France Paris, France
Abstract
Astrocytes are organized as networks of communicating cells due to their high expression level of connexins, the molecular constituents of gap junction channels. Based on their permeability properties for ions and small signaling molecules such astroglial wiring interferes with neuronal activity and survival. In this paper, I identify and discuss which future technical and conceptual progress or advances should be achieved in order to better understand how neuroglial networking contributes to brain functions and dysfunctions.
Keywords
References
- Agulhon C., Fiacco T. A., McCarthy K. D. (2010). Hippocampal short- and long-term plasticity are not modulated by astrocyte Ca 2+ signaling. Science 327, 1250 – 1254. doi:10.1126/science.1184821
- Agulhon C., Petravicz J., McMullen A. B., Sweger E. J., Minton S. K., Taves S. R., Casper K. B., Fiacco T. A., McCarthy K. D. (2008). What is the role of astrocyte calcium in neurophysiology? Neuron 59, 932 – 946. doi:10.1016/j.neuron.2008.09.004
- Ball K. K., Gandhi G. K., Thrash J., Cruz N. F., Dienel G. A. (2007). Astrocytic connexin distributions and rapid, extensive dye transfer via gap junctions in the inferior colliculus: implications for [(14)C]glucose metabolite trafficking. J. Neurosci. Res. 85, 3267 – 3283. doi:10.1002/jnr.21376
- Barres B. A. (2008). The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60, 430 – 440. doi:10.1016/j.neuron.2008.10.013
- Binmoller F. J., Muller C. M. (1992). Postnatal development of dye-coupling among astrocytes in rat visual cortex. Glia 6, 127 – 137.
- Blomstrand F., Giaume C. (2006). Kinetics of endothelin-induced inhibition and glucose permeability of astrocyte gap junctions. J. Neurosci. Res. 83, 996 – 1003. doi:10.1002/jnr.20801
- Blomstrand F., Venance L., Siren A. L., Ezan P., Hanse E., Glowinski J., Ehrenreich H., Giaume C. (2004). Endothelins regulate astrocyte gap junctions in rat hippocampal slices. Eur. J. Neurosci. 19, 1005 – 1015. doi:10.1111/j.0953-816X.2004.03197.x
- Bruzzone R., Barbe M. T., Jakob N. J., Monyer H. (2005). Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J. Neurochem. 92, 1033 – 1043. doi:10.1111/j.1471-4159.2004.02947.x
- Bruzzone R., White T. W., Paul D. L. (1996). Connections with connexins: the molecular basis of direct intercellular signaling. Eur. J. Biochem. 238, 1 – 27. doi:10.1111/j.1432-1033.1996.0001q.x
- Bushong E. A., Martone M. E., Jones Y. Z., Ellisman M. H. (2002). Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci 22, 183 – 192.
- Cina C., Maass K., Theis M., Willecke K., Bechberger J. F., Naus C. C. (2009). Involvement of the cytoplasmic C-terminal domain of connexin43 in neuronal migration. J. Neurosci. 29, 2009 – 2021. doi:10.1523/JNEUROSCI.5025-08.2009
- Colin A., Faideau M., Dufour N., Auregan G., Hassig R., Andrieu T., Brouillet E., Hantraye P., Bonvento G., Deglon N. (2009). Engineered lentiviral vector targeting astrocytes in vivo. Glia 57, 667 – 679.
- Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., Smith S. J. (1990). Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470 – 473. doi:10.1126/science.1967852
- Cruz N. F., Ball K. K., Dienel G. A. (2007). Functional imaging of focal brain activation in conscious rats: impact of [(14)C]glucose metabolite spreading and release. J. Neurosci. Res. 85, 3254 – 3266. doi:10.1002/jnr.21193
- D'Ambrosio R., Wenzel J., Schwartzkroin P. A., McKhann G. M. 2nd, Janigro D. (1998). Functional specialization and topographic segregation of hippocampal astrocytes. J. Neurosci. 18, 4425 – 4438.
- Dermietzel R., Traub O., Hwang T. K., Beyer E., Bennett M. V., Spray D. C., Willecke K. (1989). Differential expression of three gap junction proteins in developing and mature brain tissues. Proc. Natl. Acad. Sci. U.S.A. 86, 10148 – 10152. doi:10.1073/pnas.86.24.10148
- Dobrowolski R., Sasse P., Schrickel J. W., Watkins M., Kim J. S., Rackauskas M., Troatz C., Ghanem A., Tiemann K., Degen J., Bukauskas F. F., Civitelli R., Lewalter T., Fleischmann B. K., Willecke K. (2008). The conditional connexin43G138R mouse mutant represents a new model of hereditary oculodentodigital dysplasia in humans. Hum. Mol. Genet. 17, 539 – 554. doi:10.1093/hmg/ddm329
- Dobrowolski R., Willecke K. (2009). Connexin-caused genetic diseases and corresponding mouse models. Antioxid. Redox Signal. 11, 283 – 295. doi:10.1089/ars.2008.2128
- Elias L. A., Wang D. D., Kriegstein A. R. (2007). Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448, 901 – 907. doi:10.1038/nature06063
- Fiacco T. A., McCarthy K. D. (2006). Astrocyte calcium elevations: properties, propagation, and effects on brain signaling. Glia 54, 676 – 690.
- Figiel M., Allritz C., Lehmann C., Engele J. (2007). Gap junctional control of glial glutamate transporter expression. Mol. Cell. Neurosci. 35, 130 – 137. doi:10.1016/j.mcn.2007.02.009
- Froger N., Orenalla J. A., Calvo C. F., Amigou E., Kozoriz M. G., Naus C. C., Sáez J. C., Giaume C. (2010). Inhibition of cytokine-induced connexin43 hemichannel activity in astrocytes is neuroprotective. Mol. Cell. Neurosci 45, 37 – 46. doi:10.1016/j.mcn.2010.05.007
- Gandhi G. K., Cruz N. F., Ball K. K., Theus S. A., Dienel G. A. (2009). Selective astrocytic gap junctional trafficking of molecules involved in the glycolytic pathway: impact on cellular brain imaging. J. Neurochem. 110, 857 – 869. doi:10.1111/j.1471-4159.2009.06173.x
- Giaume C., Fromaget C., el Aoumari A., Cordier J., Glowinski J., Gros D. (1991). Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron 6, 133 – 143. doi:10.1016/0896-6273(91)90128-M
- Giaume C., Kirchhoff F., Matute C., Reichenbach A., Verkhratsky A. (2007). Glia: the fulcrum of brain diseases. Cell Death Differ. 14, 1324 – 1335. doi:10.1038/sj.cdd.4402144
- Giaume C., Koulakoff A., Roux L., Holcman D., Rouach N. (2010). Astroglial networks: a step further in neuroglial and gliovascular interactions. Nat. Rev. Neurosci. 11, 87 – 99. doi:10.1038/nrn2757
- Giaume C., Maravall M., Welker E., Bonvento G. (2009). The barrel cortex as a model to study dynamic neuroglial interaction. Neuroscientist. 15, 351 – 366. doi:10.1177/1073858409336092
- Giaume C., Tabernero A., Medina J. M. (1997). Metabolic trafficking through astrocytic gap junctions. Glia 21, 114 – 123.
- Giaume C., Theis M. (2010). Pharmacological and genetic approaches to study connexin-mediated channels in glial cells of the central nervous system. Brain Res. Rev. 63, 160 – 176. doi:10.1016/j.brainresrev.2009.11.005
- Giaume C., Venance L. (1998). Intercellular calcium signaling and gap junctional communication in astrocytes. Glia 24, 50 – 64.
- Goldberg G. S., Lampe P. D., Nicholson B. J. (1999). Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat. Cell Biol. 1, 457 – 459. doi:10.1038/15693
- Goldberg G. S., Moreno A. P., Lampe P. D. (2002). Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and ATP. J. Biol. Chem. 277, 36725 – 36730. doi:10.1074/jbc.M109797200
- Grosche J., Matyash V., Moller T., Verkhratsky A., Reichenbach A., Kettenmann H. (1999). Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat. Neurosci. 2, 139 – 143. doi:10.1038/5692
- Harris A. L. (2007). Connexin channel permeability to cytoplasmic molecules. Prog. Biophys. Mol. Biol. 94, 120 – 143. doi:10.1016/j.pbiomolbio.2007.03.011
- Haydon P. G., Carmignoto G. (2006). Astrocyte control of synaptic transmission and neurovascular coupling. Physiol. Rev. 86, 1009 – 1031. doi:10.1152/physrev.00049.2005
- Henneberger C., Papouin T., Oliet S. H., Rusakov D. A. (2010). Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232 – 236. doi:10.1038/nature08673
- Herrero-Gonzalez S., Valle-Casuso J. C., Sanchez-Alvarez R., Giaume C., Medina J. M., Tabernero A. (2009). Connexin43 is involved in the effect of endothelin-1 on astrocyte proliferation and glucose uptake. Glia 57, 222 – 233.
- Hofer T., Venance L., Giaume C. (2002). Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J. Neurosci. 22, 4850 – 4859.
- Houades V., Koulakoff A., Ezan P., Seif I., Giaume C. (2008). Gap junction-mediated astrocytic networks in the mouse barrel cortex. J. Neurosci. 28, 5207 – 5217. doi:10.1523/JNEUROSCI.5100-07.2008
- Houades V., Rouach N., Ezan P., Kirchhoff F., Koulakoff A., Giaume C. (2006). Shapes of astrocyte networks in the juvenile brain. Neuron Glia Biol. 2, 3 – 14. doi:10.1017/S1740925X06000081
- Iacobas D. A., Iacobas S., Spray D. C. (2007). Connexin43 and the brain transcriptome of newborn mice. Genomics 89, 113 – 123. doi:10.1016/j.ygeno.2006.09.007
- Iacobas D. A., Iacobas S., Urban-Maldonado M., Scemes E., Spray D. C. (2008). Similar transcriptomic alterations in Cx43 knockdown and knockout astrocytes. Cell Commun. Adhes. 15, 195 – 206. doi:10.1080/15419060802014222
- Iadecola C., Nedergaard M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369 – 1376. doi:10.1038/nn2003
- Juszczak G. R., Swiergiel A. H. (2009). Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: animal and human studies. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 181 – 198. doi:10.1016/j.pnpbp.2008.12.014
- Kang N., Xu J., Xu Q., Nedergaard M., Kang J. (2005). Astrocytic glutamate release-induced transient depolarization and epileptiform discharges in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 94, 4121 – 4130. doi:10.1152/jn.00448.2005
- Koulakoff A., Ezan P., Giaume C. (2008). Neurons control the expression of connexin 30 and connexin 43 in mouse cortical astrocytes. Glia 56, 1299 – 1311.
- Kuchibhotla K. V., Lattarulo C. R., Hyman B. T., Bacskai B. J. (2009). Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 323, 1211 – 1215. doi:10.1126/science.1169096
- Kunze A., Congreso M. R., Hartmann C., Wallraff-Beck A., Huttmann K., Bedner P., Requardt R., Seifert G., Redecker C., Willecke K., Hofmann A., Pfeifer A., Theis M., Steinhauser C. (2009). Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 106, 11336 – 11341. doi:10.1073/pnas.0813160106
- Malarkey E. B., Parpura V. (2008). Mechanisms of glutamate release from astrocytes. Neurochem. Int. 52, 142 – 154. doi:10.1016/j.neuint.2007.06.005
- Mathiisen T. M., Lehre K. P., Danbolt N. C., Ottersen O. P. (2010). The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia 58, 1094 – 1103.
- Matyash V., Kettenmann H. (2010). Heterogeneity in astrocyte morphology and physiology. Brain Res. Rev. 63, 2 – 10. doi:10.1016/j.brainresrev.2009.12.001
- Meme W., Vandecasteele M., Giaume C., Venance L. (2009). Electrical coupling between hippocampal astrocytes in rat brain slices. Neurosci. Res. 63, 236 – 243. doi:10.1016/j.neures.2008.12.008
- Mugnaini E. (1986). “Cell junctions of astrocytes, ependymal and related cells in the mammal central nervous system, with emphasis on the hypothesis of a generalized syncytium of supporting cells,” in Astrocytes, eds Fedoroff S., Vernadakis A. (New York: Academic Press), 329 – 371.
- Nagy J. I., Dudek F. E., Rash J. E. (2004). Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res. Brain Res. Rev. 47, 191 – 215. doi:10.1016/j.brainresrev.2004.05.005
- Nagy J. I., Rash J. E. (2000). Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res. Brain Res. Rev. 32, 29 – 44. doi:10.1016/S0165-0173(99)00066-1
- Ogata K., Kosaka T. (2002). Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113, 221 – 233. doi:10.1016/S0306-4522(02)00041-6
- Olk S., Zoidl G., Dermietzel R. (2009). Connexins, cell motility, and the cytoskeleton. Cell Motil. Cytoskeleton 66, 1000 – 1016. doi:10.1002/cm.20404
- Orellana J. A., Saez P. J., Shoji K. F., Schalper K. A., Palacios-Prado N., Velarde V., Giaume C., Bennett M. V., Saez J. C. (2009). Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid. Redox Signal. 11, 369 – 399. doi:10.1089/ars.2008.2130
- Orkand R. K., Nicholls J. G., Kuffler S. W. (1966). Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29, 788 – 806.
- Reichenbach A., Derouiche A., Kirchhoff F. (2010). Morphology and dynamics of perisynaptic glia. Brain Res. Rev. 63, 11 – 25. doi:10.1016/j.brainresrev.2010.02.003
- Rela L., Bordey A., Greer C. A. (2009). Olfactory ensheathing cell membrane properties are shaped by connectivity. Glia 58, 665 – 678.
- Roerig B., Feller M. B. (2000). Neurotransmitters and gap junctions in developing neural circuits. Brain Res. Brain Res. Rev. 32, 86 – 114. doi:10.1016/S0165-0173(99)00069-7
- Rohlmann A., Wolff J. R. (1998). “Subcellular topography and plasticity of gap junction distribution in astrocytes,” in Gap Junctions in the Nervous System, eds Spray D. C., Dermietzel R. (Austin, TX: R. G. Landes), 175 – 192.
- Rose C. R., Ransom B. R. (1997). Gap junctions equalize intracellular Na+ concentration in astrocytes. Glia 20, 299 – 307.
- Rouach N., Glowinski J., Giaume C. (2000). Activity-dependent neuronal control of gap-junctional communication in astrocytes. J. Cell Biol. 149, 1513 – 1526. doi:10.1083/jcb.149.7.1513
- Rouach N., Koulakoff A., Abudara V., Willecke K., Giaume C. (2008). Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322, 1551 – 1555. doi:10.1126/science.1164022
- Rouach N., Tence M., Glowinski J., Giaume C. (2002). Costimulation of N -methyl- d -aspartate and muscarinic neuronal receptors modulates gap junctional communication in striatal astrocytes. Proc. Natl. Acad. Sci. U.S.A. 99, 1023 – 1028. doi:10.1073/pnas.022257499
- Roux L., Giaume C. (2009). Two astroglial neworks are differentially regulated by neuronal activity in the olfactory glomerular layer. Glia 57 (Suppl. 13), 57.
- Scemes E. (2008). Modulation of astrocyte P2Y1 receptors by the carboxyl terminal domain of the gap junction protein Cx43. Glia 56, 145 – 153.
- Scemes E., Giaume C. (2006). Astrocyte calcium waves: what they are and what they do. Glia 54, 716 – 725.
- Scemes E., Suadicani S. O., Dahl G., Spray D. C. (2007). Connexin and pannexin mediated cell-cell communication. Neuron Glia Biol. 3, 199 – 208. doi:10.1017/S1740925X08000069
- Serrano A., Haddjeri N., Lacaille J. C., Robitaille R. (2006). GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J. Neurosci. 26, 5370 – 5382. doi:10.1523/JNEUROSCI.5255-05.2006
- Sohl G., Maxeiner S., Willecke K. (2005). Expression and functions of neuronal gap junctions. Nat. Rev. Neurosci. 6, 191 – 200. doi:10.1038/nrn1627
- Spray D. C., Ye Z. C., Ransom B. R. (2006). Functional connexin “hemichannels”: a critical appraisal. Glia 54, 758 – 773.
- Tabernero A., Giaume C., Medina J. M. (1996). Endothelin-1 regulates glucose utilization in cultured astrocytes by controlling intercellular communication through gap junctions. Glia 16, 187 – 195.
- Tabernero A., Medina J. M., Giaume C. (2006). Glucose metabolism and proliferation in glia: role of astrocytic gap junctions. J. Neurochem. 99, 1049 – 1061. doi:10.1111/j.1471-4159.2006.04088.x
- Theis M., Sohl G., Eiberger J., Willecke K. (2005). Emerging complexities in identity and function of glial connexins. Trends Neurosci. 28, 188 – 195. doi:10.1016/j.tins.2005.02.006
- Venance L., Premont J., Glowinski J., Giaume C. (1998). Gap junctional communication and pharmacological heterogeneity in astrocytes cultured from the rat striatum. J. Physiol. (Lond.) 510, 429 – 440. doi:10.1111/j.1469-7793.1998.429bk.x
- Venance L., Stella N., Glowinski J., Giaume C. (1997). Mechanism involved in initiation and propagation of receptor-induced intercellular calcium signaling in cultured rat astrocytes. J. Neurosci. 17, 1981 – 1992.
- Verkhratsky A., Landfield P. W., Thibault O. (2002). Preface. Ca 2+ and neuronal pathology. Eur. J. Pharmacol. 447, 115 – 117. doi:10.1016/S0014-2999(02)01835-6
- Vincent P., Gervasi N., Zhang J. (2008). Real-time monitoring of cyclic nucleotide signaling in neurons using genetically encoded FRET probes. Brain Cell Biol. 36, 3 – 17. doi:10.1007/s11068-008-9035-6
- Volterra A., Bezzi P. (2002). “Release of transmitters from glial cells,” in The Tripartite Synapse: Glial in Synaptic Transmission eds Volterra A., Magistretti P., Haydon P. G. (Oxford: Oxford University Press), 164 – 182.
- Wallraff A., Kohling R., Heinemann U., Theis M., Willecke K., Steinhauser C. (2006). The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci. 26, 5438 – 5447. doi:10.1523/JNEUROSCI.0037-06.2006
- Wang X., Lou N., Xu Q., Tian G. F., Peng W. G., Han X., Kang J., Takano T., Nedergaard M. (2006). Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat. Neurosci. 9, 816 – 823. doi:10.1038/nn1703
- Wiencken-Barger A. E., Djukic B., Casper K. B., McCarthy K. D. (2007). A role for Connexin43 during neurodevelopment. Glia 55, 675 – 686.
- Xu G., Wang W., Kimelberg HK., Zhou M. (2010) Electrical coupling of astrocytes in rat hippocampal slices under physiological and simulated ischemic conditions. Glia. 2010 Mar; 58 (4): 481 – 93.
Citation
Giaume, C. (2010). Astroglial Wiring is Adding Complexity to Neuroglial Networking. Frontiers in Neuroenergetics, Volume 2. https://doi.org/
- Received
- Accepted
- Published
- Volume
- 2 - 2010
Copyright
Copyright © 2010 Giaume.
License: http://www.frontiersin.org/licenseagreement
*Correspondence: Christian Giaume
Article metrics
- Views
- 0
- Downloads
- 0
- Citations
- 0
- Shares
- 0
Related articles
NeuroscienceInduction of ischemic stroke in awake freely moving mice reveals that isoflurane anesthesia can mask the benefits of a neuroprotection therapyAngela Seto, Stephanie Taylor, Dustin Trudeau, Ian Swan, Jay Leung, Patrick Reeson, Kerry R. Delaney, Craig E. BrownNeuroscienceImpaired cortical mitochondrial function following TBI precedes behavioral changesWilliam D. Watson, John E. Buonora, Angela M. Yarnell, Jessica J. Lucky, Michaela I. D’Acchille, David C. McMullen, Andrew G. Boston, Andrew V. Kuczmarski, William S. Kean, Ajay Verma, Neil E. Grunberg, Jeffrey T. ColeNeuroscienceFDG-PET imaging in mild traumatic brain injury: a critical reviewKimberly R. Byrnes, Colin M. Wilson, Fiona Brabazon, Ramona von Leden, Jennifer S. Jurgens, Terrence R. Oakes, Reed G. Selwyn
