Glycine Receptor α2 Subunit Activation Promotes Cortical Interneuron Migration

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Interneuron; glycine receptors; GlyR; time-lapse; Development; migration; patch-clamp; glycine

Abstract :

[en] Glycine receptors (GlyRs) are detected in the developing CNS before synaptogenesis, but their function remains elusive. This study demonstrates that functional GlyRs are expressed by embryonic cortical interneurons in vivo. Furthermore, genetic disruption of these receptors leads to interneuron migration defects. We discovered that extrasynaptic activation of GlyRs containing the α2 subunit in cortical interneurons by endogenous glycine activates voltage-gated calcium channels and promotes calcium influx, which further modulates actomyosin contractility to fine-tune nuclear translocation during migration. Taken together, our data highlight the molecular events triggered by GlyR α2 activation that control cortical tangential migration during embryogenesis.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Avila Macaya, Ariel Salvatore ; Université de Liège - ULiège > Form. doc. sc. bioméd. & pharma.

Vidal, Pia M; Universiteit Hasselt - UH > Morphology

Dear, T Neil; University of Leeds

Harvey, Robert J; University College London - UCL > UCL Shool of Pharmacy

Rigo, Jean-Michel; Universiteit Hasselt - UH > Cell Physiology

Nguyen, Laurent ; Université de Liège - ULiège > GIGA - Neurosciences

Language :

English

Title :

Glycine Receptor α2 Subunit Activation Promotes Cortical Interneuron Migration

Publication date :

29 August 2013

Journal title :

Cell Reports

eISSN :

2211-1247

Publisher :

Elsevier

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.cell.com/cell-reports/fulltext/S2211-1247(13)00378-1?switch=standard
http://reflexions.ulg.ac.be/RecepteurGlycine

Available on ORBi :

since 16 August 2013

Statistics

Number of views

118 (13 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Anderson, S.A., Eisenstat, D.D., Shi, L., Rubenstein, J.L., Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes (1997) Science, 278, pp. 474-476
Ayala, R., Shu, T., Tsai, L.H., Trekking across the brain: the journey of neuronal migration (2007) Cell, 128, pp. 29-43
Baev, K.V., Rusin, K.I., Safronov, B.V., Development of L-glutamate- and glycine-activated currents in spinal cord neurones during early chick embryogenesis (1990) J.Physiol., 423, pp. 381-395
Becker, C.M., Hoch, W., Betz, H., Glycine receptor heterogeneity in rat spinal cord during postnatal development (1988) EMBO J., 7, pp. 3717-3726
Behar, T.N., Li, Y.X., Tran, H.T., Ma, W., Dunlap, V., Scott, C., Barker, J.L., GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms (1996) J.Neurosci., 16, pp. 1808-1818
Bellion, A., Baudoin, J.P., Alvarez, C., Bornens, M., Métin, C., Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear (2005) J.Neurosci., 25, pp. 5691-5699
Benítez-Diaz, P., Miranda-Contreras, L., Mendoza-Briceño, R.V., Peña-Contreras, Z., Palacios-Prü, E., Prenatal and postnatal contents of amino acid neurotransmitters in mouse parietal cortex (2003) Dev. Neurosci., 25, pp. 366-374
Bortone, D., Polleux, F., KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner (2009) Neuron, 62, pp. 53-71
Burkel, B.M., von Dassow, G., Bement, W.M., Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin (2007) Cell Motil. Cytoskeleton, 64, pp. 822-832
Bystron, I., Blakemore, C., Rakic, P., Development of the human cerebral cortex: Boulder Committee revisited (2008) Nat. Rev. Neurosci., 9, pp. 110-122
Caronia-Brown, G., Grove, E.A., Timing of cortical interneuron migration is influenced by the cortical hem (2011) Cereb. Cortex, 21, pp. 748-755
Cobos, I., Calcagnotto, M.E., Vilaythong, A.J., Thwin, M.T., Noebels, J.L., Baraban, S.C., Rubenstein, J.L., Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy (2005) Nat. Neurosci., 8, pp. 1059-1068
Cuzon Carlson, V.C., Yeh, H.H., GABAA receptor subunit profiles of tangentially migrating neurons derived from the medial ganglionic eminence (2011) Cereb. Cortex, 21, pp. 1792-1802
Cuzon, V.C., Yeh, P.W., Cheng, Q., Yeh, H.H., Ambient GABA promotes cortical entry of tangentially migrating cells derived from the medial ganglionic eminence (2006) Cereb. Cortex, 16, pp. 1377-1388
Emmert, D.A., Fee, J.A., Goeckeler, Z.M., Grojean, J.M., Wakatsuki, T., Elson, E.L., Herring, B.P., Wysolmerski, R.B., Rho-kinase-mediated Ca2+-independent contraction in rat embryo fibroblasts (2004) Am. J. Physiol. Cell Physiol., 286, pp. C8-C21
Flint, A.C., Liu, X., Kriegstein, A.R., Nonsynaptic glycine receptor activation during early neocortical development (1998) Neuron, 20, pp. 43-53
Godin, J.D., Thomas, N., Laguesse, S., Malinouskaya, L., Close, P., Malaise, O., Purnelle, A., Fero, M., P27(Kip1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration (2012) Dev. Cell, 23, pp. 729-744
Harvey, R.J., Depner, U.B., Wässle, H., Ahmadi, S., Heindl, C., Reinold, H., Smart, T.G., Abo-Salem, O.M., GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization (2004) Science, 304, pp. 884-887
Heng, J.I., Moonen, G., Nguyen, L., Neurotransmitters regulate cell migration in the telencephalon (2007) Eur. J. Neurosci., 26, pp. 537-546
Hussy, N., Deleuze, C., Pantaloni, A., Desarménien, M.G., Moos, F., Agonist action of taurine on glycine receptors in rat supraoptic magnocellular neurones: possible role in osmoregulation (1997) J.Physiol., 502, pp. 609-621
Inoue, K., Furukawa, T., Kumada, T., Yamada, J., Wang, T., Inoue, R., Fukuda, A., Taurine inhibits K+-Cl- cotransporter KCC2 to regulate embryonic Cl- homeostasis via with-no-lysine (WNK) protein kinase signaling pathway (2012) J.Biol. Chem., 287, pp. 20839-20850
Kilb, W., Ikeda, M., Uchida, K., Okabe, A., Fukuda, A., Luhmann, H.J., Depolarizing glycine responses in Cajal-Retzius cells of neonatal rat cerebral cortex (2002) Neuroscience, 112, pp. 299-307
Kilb, W., Hanganu, I.L., Okabe, A., Sava, B.A., Shimizu-Okabe, C., Fukuda, A., Luhmann, H.J., Glycine receptors mediate excitation of subplate neurons in neonatal rat cerebral cortex (2008) J.Neurophysiol., 100, pp. 698-707
Komuro, H., Rakic, P., Modulation of neuronal migration by NMDA receptors (1993) Science, 260, pp. 95-97
Kühn, R., Schwenk, F., Aguet, M., Rajewsky, K., Inducible gene targeting in mice (1995) Science, 269, pp. 1427-1429
López-Bendito, G., Luján, R., Shigemoto, R., Ganter, P., Paulsen, O., Molnár, Z., Blockade of GABA(B) receptors alters the tangential migration of cortical neurons (2003) Cereb. Cortex, 13, pp. 932-942
Lynch, J.W., Native glycine receptor subtypes and their physiological roles (2009) Neuropharmacology, 56, pp. 303-309
Lynch, J.W., Rajendra, S., Barry, P.H., Schofield, P.R., Mutations affecting the glycine receptor agonist transduction mechanism convert thecompetitive antagonist, picrotoxin, into an allosteric potentiator (1995) J.Biol. Chem., 270, pp. 13799-13806
Malosio, M.L., Marquèze-Pouey, B., Kuhse, J., Betz, H., Widespread expression of glycine receptor subunit mRNAs in the adult anddeveloping rat brain (1991) EMBO J., 10, pp. 2401-2409
Manent, J.B., Jorquera, I., Ben-Ari, Y., Aniksztejn, L., Represa, A., Glutamate acting on AMPA but not NMDA receptors modulates the migration of hippocampal interneurons (2006) J.Neurosci., 26, pp. 5901-5909
Mangin, J.M., Nguyen, L., Gougnard, C., Hans, G., Rogister, B., Belachew, S., Moonen, G., Rigo, J.M., Developmental regulation of beta-carboline-induced inhibition of glycine-evoked responses depends on glycine receptor beta subunit expression (2005) Mol. Pharmacol., 67, pp. 1783-1796
Manzke, T., Niebert, M., Koch, U.R., Caley, A., Vogelgesang, S., Hülsmann, S., Ponimaskin, E., Richter, D.W., Serotonin receptor 1A-modulated phosphorylation of glycine receptor α3 controls breathing in mice (2010) J.Clin. Invest., 120, pp. 4118-4128
Marín, O., Rubenstein, J.L., A long, remarkable journey: tangential migration in the telencephalon (2001) Nat. Rev. Neurosci., 2, pp. 780-790
Martini, F.J., Valdeolmillos, M., Actomyosin contraction at the cellrear drives nuclear translocation in migrating cortical interneurons (2010) J.Neurosci., 30, pp. 8660-8670
Meijering, E., Dzyubachyk, O., Smal, I., Methods for cell and particle tracking (2012) Methods Enzymol., 504, pp. 183-200
Métin, C., Denizot, J.P., Ropert, N., Intermediate zone cells express calcium-permeable AMPA receptors and establish close contact with growing axons (2000) J.Neurosci., 20, pp. 696-708
Métin, C., Baudoin, J.P., Rakić, S., Parnavelas, J.G., Cell and molecular mechanisms involved in the migration of cortical interneurons (2006) Eur. J. Neurosci., 23, pp. 894-900
Nguyen, L., Rigo, J.M., Rocher, V., Belachew, S., Malgrange, B., Rogister, B., Leprince, P., Moonen, G., Neurotransmitters as early signals for central nervous system development (2001) Cell Tissue Res., 305, pp. 187-202
Nguyen, L., Malgrange, B., Belachew, S., Rogister, B., Rocher, V., Moonen, G., Rigo, J.M., Functional glycine receptors are expressed by postnatal nestin-positive neural stem/progenitor cells (2002) Eur. J. Neurosci., 15, pp. 1299-1305
Nimmervoll, B., Denter, D.G., Sava, I., Kilb, W., Luhmann, H.J., Glycine receptors influence radial migration in the embryonic mouse neocortex (2011) Neuroreport, 22, pp. 509-513
O'Gorman, S., Dagenais, N.A., Qian, M., Marchuk, Y., Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells (1997) Proc. Natl. Acad. Sci. USA, 94, pp. 14602-14607
Okabe, A., Kilb, W., Shimizu-Okabe, C., Hanganu, I.L., Fukuda, A., Luhmann, H.J., Homogenous glycine receptor expression in cortical plate neurons and Cajal-Retzius cells of neonatal rat cerebral cortex (2004) Neuroscience, 123, pp. 715-724
Pla, R., Borrell, V., Flames, N., Marin, O., Layer acquisition bycortical GABAergic interneurons is independent of Reelin signaling (2006) J.Neurosci., 26, pp. 6924-6934
Pribilla, I., Takagi, T., Langosch, D., Bormann, J., Betz, H., The atypical M2 segment of the beta subunit confers picrotoxinin resistance to inhibitory glycine receptor channels (1992) EMBO J., 11, pp. 4305-4311
Scain, A.L., Le Corronc, H., Allain, A.E., Muller, E., Rigo, J.M., Meyrand, P., Branchereau, P., Legendre, P., Glycine release from radial cells modulates the spontaneous activity and its propagation during early spinal cord development (2010) J.Neurosci., 30, pp. 390-403
Schaar, B.T., McConnell, S.K., Cytoskeletal coordination during neuronal migration (2005) Proc. Natl. Acad. Sci. USA, 102, pp. 13652-13657
Schmieden, V., Kuhse, J., Betz, H., Agonist pharmacology of neonatal and adult glycine receptor alpha subunits: identification of amino acid residues involved in taurine activation (1992) EMBO J., 11, pp. 2025-2032
Seybold, B.A., Stanco, A., Cho, K.K., Potter, G.B., Kim, C., Sohal, V.S., Rubenstein, J.L., Schreiner, C.E., Chronic reduction in inhibition reduces receptive field size in mouse auditory cortex (2012) Proc. Natl. Acad. Sci. USA, 109, pp. 13829-13834
Soria, J.M., Valdeolmillos, M., Receptor-activated calcium signals in tangentially migrating cortical cells (2002) Cereb. Cortex, 12, pp. 831-839
Stenman, J., Toresson, H., Campbell, K., Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis (2003) J.Neurosci., 23, pp. 167-174
Stühmer, T., Anderson, S.A., Ekker, M., Rubenstein, J.L., Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression (2002) Development, 129, pp. 245-252
Sturman, J.A., Taurine in development (1988) J.Nutr., 118, pp. 1169-1176
Tiveron, M.C., Rossel, M., Moepps, B., Zhang, Y.L., Seidenfaden, R., Favor, J., König, N., Cremer, H., Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone (2006) J.Neurosci., 26, pp. 13273-13278
Wang, F., Xiao, C., Ye, J.H., Taurine activates excitatory non-synaptic glycine receptors on dopamine neurones in ventral tegmental area of young rats (2005) J.Physiol., 565, pp. 503-516
Wang, D.S., Buckinx, R., Lecorronc, H., Mangin, J.M., Rigo, J.M., Legendre, P., Mechanisms for picrotoxinin and picrotin blocks of alpha2 homomeric glycine receptors (2007) J.Biol. Chem., 282, pp. 16016-16035
Watanabe, E., Akagi, H., Distribution patterns of mRNAs encoding glycine receptor channels in the developing rat spinal cord (1995) Neurosci. Res., 23, pp. 377-382
Wonders, C.P., Anderson, S.A., The origin and specification of cortical interneurons (2006) Nat. Rev. Neurosci., 7, pp. 687-696
Yang, Z., Cromer, B.A., Harvey, R.J., Parker, M.W., Lynch, J.W., Aproposed structural basis for picrotoxinin and picrotin binding in the glycine receptor pore (2007) J.Neurochem., 103, pp. 580-589
Yoshida, M., Fukuda, S., Tozuka, Y., Miyamoto, Y., Hisatsune, T., Developmental shift in bidirectional functions of taurine-sensitive chloride channels during cortical circuit formation in postnatal mouse brain (2004) J.Neurobiol., 60, pp. 166-175
Young-Pearse, T.L., Ivic, L., Kriegstein, A.R., Cepko, C.L., Characterization of mice with targeted deletion of glycine receptor alpha 2 (2006) Mol. Cell. Biol., 26, pp. 5728-5734
Young, T.L., Cepko, C.L., A role for ligand-gated ion channels in rodphotoreceptor development (2004) Neuron, 41, pp. 867-879