Cell-Intrinsic Control of Interneuron Migration Drives Cortical Morphogenesis

[en] Interneurons navigate along multiple tangential paths to settle into appropriate cortical layers. They undergo a saltatory migration paced by intermittent nuclear jumps whose regulation relies on interplay between extracellular cues and genetic-encoded information. It remains unclear how cycles of pause and movement are coordinated at the molecular level. Post-translational modification of proteins contributes to cell migration regulation. The present study uncovers that carboxypeptidase 1, which promotes post-translational protein deglutamylation, controls the pausing of migrating cortical interneurons. Moreover, we demonstrate that pausing during migration attenuates movement simultaneity at the population level, thereby controlling the flow of interneurons invading the cortex. Interfering with the regulation of pausing not only affects the size of the cortical interneuron cohort but also impairs the generation of age-matched projection neurons of the upper layers. The “stop and go” movement of individual migrating cortical interneurons is critical for ensuring a proper rate of cortical invasion for the entire population. © 2018 The Authors

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Gomes Da Silva, Carla ; Université de Liège > GIGA - Neurosciences

Peyre, Elise ; Université de Liège - ULiège > GIGA - Neurosciences

Adhikari, M. H.; Center for Brain and Cognition, Department of Information and Technology, Universitat Pompeu Fabra, Calle Ramon Trias Fargas 25-27Barcelona, Spain

Tielens, Sylvia ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale

Tanco, S.; VIB-UGent Center for Medical Biotechnologie, VIB, Ghent, Belgium, Department of Biochemistry, Ghent University, Ghent, Belgium

Van Damme, P.; VIB-UGent Center for Medical Biotechnologie, VIB, Ghent, Belgium, Department of Biochemistry, Ghent University, Ghent, Belgium

Magno, L.; Wolfson Institute for Biomedical Research and Department of Cell and Developmental Biology, University College London, London, United Kingdom

Krusy, Nathalie ; Université de Liège - ULiège > GIGA - Neurosciences

Agirman, Gulistan ; Université de Liège - ULiège > GIGA - Neurosciences

Magiera, M. M.; Institut Curie, CNRS UMR3348, PSL Research University, Centre UniversitaireOrsay, France

More authors (5 more)

Language :

English

Title :

Cell-Intrinsic Control of Interneuron Migration Drives Cortical Morphogenesis

Publication date :

2018

Journal title :

Cell

ISSN :

0092-8674

eISSN :

1097-4172

Publisher :

Cell Press

Volume :

172

Issue :

Pages :

1063-1067.e19

Peer reviewed :

Peer Reviewed verified by ORBi

Name of the research project :

108726/Z/15/Z; 2013-1-PLBIO-02-ICR-1; 2014-PLBIO-11-ICR-1; ANR-10-IDEX-0001-02 PSL; ANR-10-LBX-0038; ANR-12-BSV2-0007; ARC11/16-01,

Funders :

Wellcome Trust
F.R.S.-FNRS - Fonds de la Recherche Scientifique
INCa - Institut National du Cancer
ANR - Agence Nationale de la Recherche
CNRS - Centre National de la Recherche Scientifique
Fonds Léon Fredericq

Available on ORBi :

since 09 May 2018

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Bibliography

Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., Kaibuchi, K., Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271 (1996), 20246–20249.
Barber, M., Arai, Y., Morishita, Y., Vigier, L., Causeret, F., Borello, U., Ledonne, F., Coppola, E., Contremoulins, V., Pfrieger, F.W., et al. Migration speed of Cajal-Retzius cells modulated by vesicular trafficking controls the size of higher-order cortical areas. Curr. Biol. 25 (2015), 2466–2478.
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. J. Neurosci. 25 (2005), 5691–5699.
Bortone, D., Polleux, F., KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 62 (2009), 53–71.
Butt, S.J., Sousa, V.H., Fuccillo, M.V., Hjerling-Leffler, J., Miyoshi, G., Kimura, S., Fishell, G., The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59 (2008), 722–732.
Courchesne, E., Mouton, P.R., Calhoun, M.E., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M.J., Barnes, C.C., Pierce, K., Neuron number and size in prefrontal cortex of children with autism. JAMA 306 (2011), 2001–2010.
Creppe, C., Malinouskaya, L., Volvert, M.L., Gillard, M., Close, P., Malaise, O., Laguesse, S., Cornez, I., Rahmouni, S., Ormenese, S., et al. Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136 (2009), 551–564.
Firth, H.V., Richards, S.M., Bevan, A.P., Clayton, S., Corpas, M., Rajan, D., Van Vooren, S., Moreau, Y., Pettett, R.M., Carter, N.P., DECIPHER: database of chromosomal imbalance and phenotype in humans using Ensembl resources. Am. J. Hum. Genet. 84 (2009), 524–533.
Flames, N., Long, J.E., Garratt, A.N., Fischer, T.M., Gassmann, M., Birchmeier, C., Lai, C., Rubenstein, J.L., Marín, O., Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44 (2004), 251–261.
Fogarty, M., Grist, M., Gelman, D., Marín, O., Pachnis, V., Kessaris, N., Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27 (2007), 10935–10946.
Gluska, S., Chein, M., Rotem, N., Ionescu, A., Perlson, E., Tracking Quantum-Dot labeled neurotropic factors transport along primary neuronal axons in compartmental microfluidic chambers. Methods Cell Biol. 131 (2016), 365–387.
Godin, J.D., Thomas, N., Laguesse, S., Malinouskaya, L., Close, P., Malaise, O., Purnelle, A., Raineteau, O., Campbell, K., Fero, M., et al. p27(Kip1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration. Dev. Cell 23 (2012), 729–744.
Hahn, M.A., Qiu, R., Wu, X., Li, A.X., Zhang, H., Wang, J., Jui, J., Jin, S.G., Jiang, Y., Pfeifer, G.P., Lu, Q., Dynamics of 5-hydroxymethylcytosine and chromatin marks in Mammalian neurogenesis. Cell Rep. 3 (2013), 291–300.
Hevner, R.F., Daza, R.A., Rubenstein, J.L., Stunnenberg, H., Olavarria, J.F., Englund, C., Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev. Neurosci. 25 (2003), 139–151.
Janke, C., The tubulin code: molecular components, readout mechanisms, and functions. J. Cell Biol. 206 (2014), 461–472.
Janke, C., Rogowski, K., Wloga, D., Regnard, C., Kajava, A.V., Strub, J.M., Temurak, N., van Dijk, J., Boucher, D., van Dorsselaer, A., et al. Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science 308 (2005), 1758–1762.
Javaherian, A., Kriegstein, A., A stem cell niche for intermediate progenitor cells of the embryonic cortex. Cereb. Cortex 19:Suppl 1 (2009), i70–i77.
Kappeler, C., Saillour, Y., Baudoin, J.P., Tuy, F.P., Alvarez, C., Houbron, C., Gaspar, P., Hamard, G., Chelly, J., Métin, C., Francis, F., Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum. Mol. Genet. 15 (2006), 1387–1400.
Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., et al. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273 (1996), 245–248.
Komada, M., Saitsu, H., Kinboshi, M., Miura, T., Shiota, K., Ishibashi, M., Hedgehog signaling is involved in development of the neocortex. Development 135 (2008), 2717–2727.
Kusakabe, T., Hoshi, N., Kimura, S., Origin of the ultimobranchial body cyst: T/ebp/Nkx2.1 expression is required for development and fusion of the ultimobranchial body to the thyroid. Dev. Dyn. 235 (2006), 1300–1309.
Lange, C., Turrero Garcia, M., Decimo, I., Bifari, F., Eelen, G., Quaegebeur, A., Boon, R., Zhao, H., Boeckx, B., Chang, J., et al. Relief of hypoxia by angiogenesis promotes neural stem cell differentiation by targeting glycolysis. EMBO J. 35 (2016), 924–941.
Marín, O., Yaron, A., Bagri, A., Tessier-Lavigne, M., Rubenstein, J.L., Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 293 (2001), 872–875.
Ponti, G., Obernier, K., Guinto, C., Jose, L., Bonfanti, L., Alvarez-Buylla, A., Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc. Natl. Acad. Sci. USA 110 (2013), E1045–E1054.
Rogowski, K., van Dijk, J., Magiera, M.M., Bosc, C., Deloulme, J.C., Bosson, A., Peris, L., Gold, N.D., Lacroix, B., Bosch Grau, M., et al. A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell 143 (2010), 564–578.
Sessa, A., Mao, C.A., Colasante, G., Nini, A., Klein, W.H., Broccoli, V., Tbr2-positive intermediate (basal) neuronal progenitors safeguard cerebral cortex expansion by controlling amplification of pallial glutamatergic neurons and attraction of subpallial GABAergic interneurons. Genes Dev. 24 (2010), 1816–1826.
Solecki, D.J., Trivedi, N., Govek, E.E., Kerekes, R.A., Gleason, S.S., Hatten, M.E., Myosin II motors and F-actin dynamics drive the coordinated movement of the centrosome and soma during CNS glial-guided neuronal migration. Neuron 63 (2009), 63–80.
Somlyo, A.P., Somlyo, A.V., Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83 (2003), 1325–1358.
Southwell, D.G., Paredes, M.F., Galvao, R.P., Jones, D.L., Froemke, R.C., Sebe, J.Y., Alfaro-Cervello, C., Tang, Y., Garcia-Verdugo, J.M., Rubenstein, J.L., et al. Intrinsically determined cell death of developing cortical interneurons. Nature 491 (2012), 109–113.
Stenman, J., Toresson, H., Campbell, K., Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 23 (2003), 167–174.
Sussel, L., Marin, O., Kimura, S., Rubenstein, J.L., Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126 (1999), 3359–3370.
Tanco, S., Lorenzo, J., Garcia-Pardo, J., Degroeve, S., Martens, L., Aviles, F.X., Gevaert, K., Van Damme, P., Proteome-derived peptide libraries to study the substrate specificity profiles of carboxypeptidases. Mol. Cell. Proteomics 12 (2013), 2096–2110.
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. J. Neurosci. 26 (2006), 13273–13278.
Tort, O., Tanco, S., Rocha, C., Bièche, I., Seixas, C., Bosc, C., Andrieux, A., Moutin, M.J., Avilés, F.X., Lorenzo, J., Janke, C., The cytosolic carboxypeptidases CCP2 and CCP3 catalyze posttranslational removal of acidic amino acids. Mol. Biol. Cell 25 (2014), 3017–3027.
Vaccarino, F.M., Grigorenko, E.L., Smith, K.M., Stevens, H.E., Regulation of cerebral cortical size and neuron number by fibroblast growth factors: implications for autism. J. Autism Dev. Disord. 39 (2009), 511–520.
van Dijk, J., Rogowski, K., Miro, J., Lacroix, B., Eddé B., Janke, C., A targeted multienzyme mechanism for selective microtubule polyglutamylation. Mol. Cell 26 (2007), 437–448.
van Dijk, J., Miro, J., Strub, J.M., Lacroix, B., van Dorsselaer, A., Edde, B., Janke, C., Polyglutamylation is a post-translational modification with a broad range of substrates. J. Biol. Chem. 283 (2008), 3915–3922.
Vasudevan, A., Long, J.E., Crandall, J.E., Rubenstein, J.L., Bhide, P.G., Compartment-specific transcription factors orchestrate angiogenesis gradients in the embryonic brain. Nat. Neurosci. 11 (2008), 429–439.
Villar-Cerviño, V., Molano-Mazón, M., Catchpole, T., Valdeolmillos, M., Henkemeyer, M., Martínez, L.M., Borrell, V., Marín, O., Contact repulsion controls the dispersion and final distribution of Cajal-Retzius cells. Neuron 77 (2013), 457–471.
Yang, N., Higuchi, O., Ohashi, K., Nagata, K., Wada, A., Kangawa, K., Nishida, E., Mizuno, K., Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393 (1998), 809–812.
Zielinski, B.A., Prigge, M.B., Nielsen, J.A., Froehlich, A.L., Abildskov, T.J., Anderson, J.S., Fletcher, P.T., Zygmunt, K.M., Travers, B.G., Lange, N., et al. Longitudinal changes in cortical thickness in autism and typical development. Brain 137 (2014), 1799–1812.