Glycine Triggers an Intracellular Calcium Influx in Oligodendrocyte Progenitor Cells Which Is Mediated by the Activation of Both the Ionotropic Glycine Receptor and Na+-Dependent Transporters
[en] Using fluo-3 calcium imaging, we demonstrate that glycine induces an increase in intracellular calcium concentration ([Ca2+]i) in cortical oligodendrocyte progenitor (OP) cells. This effect results from a calcium entry through voltage-gated calcium channels (VGCC), as it is observed only in OP cells expressing such channels, and it is abolished either by removal of calcium from the extracellular medium or by application of an L-type VGCC blocker. Glycine-triggered Ca2+ influx in OP cells actually results from an initial depolarization that is the consequence of the activation of both the ionotropic glycine receptor (GlyR) and Na+-dependent transporters, most probably the glycine transporters 1 (GLYT1) and/or 2 (GLYT2) which are colocalized in these cells. Through this GlyR- and transporter-mediated effect on OP intrcellular calcium concentration [Ca2+]i, glycine released by neurons may, as well as other neurotransmitters, serve as a signal between neurons and OP during development.
Belachew, Shibeshih ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie
Malgrange, Brigitte ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Rigo, Jean-Michel; Universiteit Hasselt - UH
Rogister, Bernard ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Leprince, Pierre ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.
Hans, Grégory ; Centre Hospitalier Universitaire de Liège - CHU > Anesthésie et réanimation
Nguyen, Laurent ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie
Moonen, Gustave ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie - Doyen de la Faculté de Médecine
Language :
English
Title :
Glycine Triggers an Intracellular Calcium Influx in Oligodendrocyte Progenitor Cells Which Is Mediated by the Activation of Both the Ionotropic Glycine Receptor and Na+-Dependent Transporters
Publication date :
June 2000
Journal title :
European Journal of Neuroscience
ISSN :
0953-816X
eISSN :
1460-9568
Publisher :
Blackwell, Oxford, United Kingdom
Volume :
12
Issue :
6
Pages :
1924-30
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Adams, R.H., Sato, K., Shimada, S., Tohyama, M., Pschel, A.W. & Betz, H. (1995) Gene structure and glial expression of the glycine transporter GlyT1 in embryonic and adult rodents. J. Neurosci., 15, 2524-2532.
Aragon, M.C., Gimenez, C. & Mayor, F. (1987) Stoichiometry of sodium-and chloride-coupled glycine transport in synaptic plasma membrane vesicles derived from rat brain. FEBS Lett., 212, 87-90.
Avellana-Adalid, V., Nait Oumesmar, B., Lachapelle, F. & Baron-Van Evercooren, A. (1996) Expansion of rat oligodendrocyte progenitors into proliferative 'oligospheres' that retain differentiation potential. J. Neurosci. Res., 45, 558-570.
Belachew, S., Malgrange, B., Rigo, J.-M., Rogister, B., Coucke, P., Mazy-Servais, C. & Moonen, G. (1998a) Developmental regulation of neuroligand-induced responses in cultured oligodendroglia. Neuroreport, 9, 973-980.
Belachew, S., Register, B., Rigo, J.-M., Malgrange, B., Mazy-Servais, C., Xhauflaire, G., Coucke, P. & Moonen, G. (1998b) Cultured oligodendrocyte progenitors derived from cerebral cortex express a glycine receptor which is pharmacologically distinct from the neuronal isoform. Eur. J. Neurosci., 10, 3556-3564.
Borowsky, B., Mezey, E. & Hoffman, B.J. (1993) Two glycine transporter variants with distinct localization in the CNS and peripheral tissues are encoded by a common gene. Neuron, 10, 851-863.
Calver, A.R., Hall, A.C., Yu, W.P., Walsh, F.S., Heath, J.K., Betsholtz, C. & Richardson, W.D. (1998) Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron, 20, 869-882.
Chattopadhyay, N., Ye, C.P., Yamaguchi, T., Kifor, O., Vassilev, P.M., Nishimura, R. & Brown, E.M. (1998) Extracellular calcium-sensing receptor in rat oligodendrocytes: Expression and potential role in regulation of cellular proliferation and an outward K + channel. Glia, 24, 449-158.
Cohen, R.I. & Almazan, G. (1993) Norepinephrine-stimulated PI hydrolysis in oligodendrocytes is mediated by alpha 1A-adrenoceptors. Neuroreport, 4, 1115-1118.
Cohen, R.I. & Almazan, G. (1994) Rat oligodendrocytes express muscarinic receptors coupled to phosphoinositide hydrolysis and adenylyl cyclase. Eur. J. Neurosci., 6, 1213-1224.
Demerens, C., Stankoff, B., Logak, M., Anglade, P., Allinquant, B., Couraud, F., Zalc, B. & Lubetzki, C. (1996) Induction of myelination in the central nervous system by electrical activity. Proc. Natl Acad. Sci. USA, 93, 9887-9892.
Flint, A.C., Liu, X.L. & Kriegstein, A.R. (1998) Nonsynaptic glycine receptor activation during early neocortical development. Neuron, 20, 43-53.
Gilbert, P., Kettenmann, H. & Schachner, M. (1984) Gamma-aminobutyric acid directly depolarizes cultured oligodendrocytes. J. Neurosci., 4, 561-569.
Guastella, J., Brecha, N., Weigmann, C., Lester, H.A. & Davidson, N. (1992) Cloning, expression, and localization of a rat brain high-affinity glycine transporter. Proc. Natl Acad. Sci. USA, 89, 7189-7193.
He, M.H., Howe, D.G. & McCarthy, K.D. (1996) Oligodendroglial signal transduclion systems are regulated by neuronal contact. J. Neurochem., 67, 1491-1499.
Holtzclaw, L.A., Gallo, V. & Russell, J.T. (1995) AMPA receptors shape calcium responses in cortical oligodendrocyte progenitors and CG-4 cells. J. Neurosci. Res., 42, 124-130.
Hoppe, D. & Kettenmann, H. (1989) GABA triggers a chloride efflux from cultured oligodendrocytes. Neurosci. Lett., 97, 334-339.
Jursky, F. & Nelson, N. (1995) Localization of glycine neurotransmitter transporter (GLYT2) reveals correlation with the distribution of glycine receptor. J. Neurochem., 64, 1026-1033.
Kim, K.M., Kingsmore, S.F., Han, H., Yang-Feng, T.L., Godinot, N., Seldin, M.F., Caron, M.G. & Giros, B. (1994) Cloning of the human glycine transporter type 1: molecular and pharmacological characterization of novel isoform variants and chromosomal localization of the gene in the human and mouse genomes. Mol. Pharmacol., 45, 608-617.
Kirchhoff, F. & Kettenmann, H. (1992) GABA triggers a [Ca 2+]i increase in murinc precursor cells of the oligodendrocyte lineage. Eur. J. Neurosci., 4, 1049-1058.
Kirchhoff, F., Mulhardt, C., Pastor, A., Becker, C.-M. & Kettenmann, H. (1996) Expression of glycine receptor subunits in glial cells of the rat spinal cord. J. Neurochem., 4, 1383-1390.
Kirischuk, S., Scherer, J., Kettenmann, H. & Verkhratsky, A. (1995a) Activation of P2 -purinoreceptors triggered Ca 2+ release from InsP3 -sensitive internal stores in mammalian oligodendrocytes. J. Physiol. (London), 483, 41-57.
Kirischuk, S., Scherer, J., Möller, T., Verkhratsky, A. & Kettenmann, H. (1995b) Subcellular heterogeneity of voltage-gated Ca 2+ channels in cells of the oligodendrocyte lineage. Glia, 13, 1-12.
Knutson, P., Ghiani, C.A., Zhou, J.M., Gallo, V. & McBain, C.J. (1997) K + channel expression and cell proliferation are regulated by intracellular sodium and membrane depolarization in oligodendrocyte progenitor cells. J. Neurosci., 17, 2669-2682.
Liu, Q.R., Löpez-Corcuera, B., Mandiyan, S., Nelson, H. & Nelson, N. (1993) Cloning and expression of a spinal cord-and brain-specific glycine transporter with novel structural features. J. Biol. Chem, 268, 22802-22808.
Liu, Q.R., Nelson, H., Mandiyan, S., Löpez-Corcuera, B. & Nelson, N. (1992) Cloning and expression of a glycine transporter from mouse brain. FEBS Lett., 305, 110-114.
Löpez-Corcuera, B., Martínez-Maza, R., Núnez, E., Roux, M., Supplisson, S. & Aragón, C. (1998) Differential properties of two stably expressed brain-specific glycine transporters. J. Neurochem., 71, 2211-2219.
Luque, J.M., Nelson, N. & Richards, J.G. (1995) Cellular expression of glycine transporter 2 messenger RNA exclusively in rat hindbrain and spinal cord. Neuroscience, 64, 525-535.
Morrow, J.A., Collie, I.T., Dunbar, D.R., Walker, G.B., Shahid, M. & Hill, D.R. (1998) Molecular cloning and functional expression of the human glycine transporter GlyT2 and chromosomal localisation of the gene in the human genome. FEBS Lett., 439, 334-340.
Pende, M., Fisher, T.L., Simpson, P.B., Russell, J.T., Blenis, J. & Gallo, V. (1997) Neurotransmitter-and growth factor-induced cAMP response element binding protein phosphorylalion in glial cell progenitors: role of calcium ions, protein kinase C, and mitogen-activated protein kinase/ ribosomal S6 kinase pathway. J. Neurosci., 17, 1291-1301.
Poyatos, I., Ponce, J., Aragon, C., Gimenez, C. & Zafra, F. (1997) The glycine transporter GLYT2 is a reliable marker for glycine-immunoreactive neurons. Brain Res. Mol. Brain Res., 49, 63-70.
Sato-Bigbee, C., Pal, S. & Chu, A.K. (1999) Different neuroligands and signal transduction pathways stimulate CREB phosphorylation at specific developmental stages along oligodendrocyte differentiation. J. Neurochem., 72, 139-147.
Smith, K.E., Borden, L.A., Hartig, P.R., Branchek, T. & Weinshank, R.L. (1992) Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron, 8, 927-935.
Takeda, M., Nelson, D.J. & Soliven, B. (1995) Calcium signaling in cultured rat oligodendrocytes. Glia, 14, 225-236.
Verkhratsky, A., Orkand, R.K. & Kettenmann, H. (1998) Glial calcium: Homeostasis and signaling function. Physiol. Rev., 78, 99-141.
Von Blankenfeld, G., Verkhratsky, A. & Kettenmann, H. (1992) Calcium channel expression in the oligodendrocyte lineage. Eur. J. Neurosci., 4, 1035-1048.
Zafra, F., Aragon, C., Olivares, L., Danbolt, N.C., Gimenez, C. & Storm-Mathisen, J. (1995a) Glycine transporters are differentially expressed among CNS cells. J. Neurosci., 15, 3952-3969.
Zafra, F., Gomeza, J., Olivares, L., Aragon, C. & Gimenez, C. (1995b) Regional distribution and developmental variation of the glycine transporters GLYT1 and GLYT2 in the rat CNS. Eur J. Neurosci., 7, 1342-1352.
Zafra, F., Poyatos, I. & Gimenez, C. (1997) Neuronal dependency of the glycine transporter GLYT1 expression in glial cells. Glia, 20, 155-162.