Elongator controls cortical interneuron migration by regulating actomyosin dynamics.

[en] The migration of cortical interneurons is a fundamental process for the establishment of cortical connectivity and its impairment underlies several neurological disorders. During development, these neurons are born in the ganglionic eminences and they migrate tangentially to populate the cortical layers. This process relies on various morphological changes that are driven by dynamic cytoskeleton remodelings. By coupling time lapse imaging with molecular analyses, we show that the Elongator complex controls cortical interneuron migration in mouse embryos by regulating nucleokinesis and branching dynamics. At the molecular level, Elongator fine-tunes actomyosin forces by regulating the distribution and turnover of actin microfilaments during cell migration. Thus, we demonstrate that Elongator cell-autonomously promotes cortical interneuron migration by controlling actin cytoskeletal dynamics.Cell Research advance online publication 27 September 2016; doi:10.1038/cr.2016.112.

Disciplines :

Neurology

Author, co-author :

Tielens, Sylvia ^✱; Université de Liège > GIGA - Neurosciences

Huysseune, Sandra ^✱

Godin, Juliette D.

Chariot, Alain ; Université de Liège > Département de pharmacie > Chimie médicale

Malgrange, Brigitte ; Université de Liège > GIGA - Neurosciences

Nguyen, Laurent ; Université de Liège > GIGA - Neurosciences

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Elongator controls cortical interneuron migration by regulating actomyosin dynamics.

Publication date :

2016

Journal title :

Cell Research

ISSN :

1001-0602

eISSN :

1748-7838

Publisher :

Institute of Biochemistry and Cell Biology, Shanghai, China

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 29 September 2016

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Bibliography

Rash BG, Grove EA. Area and layer patterning in the developing cerebral cortex. Curr Opin Neurobiol 2006; 16: 25-34
Gupta A, Tsai LH, Wynshaw-Boris A. Life is a journey: a genetic look at neocortical development. Nat Rev Genet 2002; 3: 342-355
Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 1997; 278: 474-476
Gelman DM, Martini FJ, Nobrega-Pereira S, Pierani A, Kessaris N, Marin O. The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci 2009; 29: 9380-9389
Wonders CP, Anderson SA. The origin and specification of cortical interneurons. Nat Rev Neurosci 2006; 7: 687-696
Metin C, Baudoin JP, Rakic S, Parnavelas JG. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur J Neurosci 2006; 23: 894-900
Tanaka DH, Maekawa K, Yanagawa Y, Obata K, Murakami F. Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex. Development 2006; 133: 2167-2176
Marin O, Plump AS, Flames N, Sanchez-Camacho C, Tessier-Lavigne M, Rubenstein JL. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction. Development 2003; 130: 1889-1901
Marin O, Valiente M, Ge XC, Tsai LH. Guiding neuronal cell migrations. Cold Spring Harb Perspect Biol 2010; 2: a001834
Bellion A, Baudoin JP, Alvarez C, Bornens M, Metin 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 2005; 25: 5691-5699
Godin JD, Thomas N, Laguesse S, et al. p27(Kip1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration. Dev Cell 2012; 23: 729-744
Etienne-Manneville S. Microtubules in cell migration. Annu Rev Cell Dev Biol 2013; 29: 471-499
Heng JI, Chariot A, Nguyen L. Molecular layers underlying cytoskeletal remodelling during cortical development. Trends Neurosci 2010; 33: 38-47
Poirier K, Lebrun N, Broix L, et al. Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat Genet 2013; 45: 639-647
Creppe C, Malinouskaya L, Volvert ML, et al. Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 2009; 136: 551-564
Anderson SL, Coli R, Daly IW, et al. Familial dysautonomia is caused by mutations of the IKAP gene. Am J Hum Genet 2001; 68: 753-758
Nguyen L, Humbert S, Saudou F, Chariot A. Elongator - an emerging role in neurological disorders. Trends Mol Med 2010; 16: 1-6
Simpson CL, Lemmens R, Miskiewicz K, et al. Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration. Hum Mol Genet 2009; 18: 472-481
Slaugenhaupt SA, Blumenfeld A, Gill SP, et al. Tissue-specific expression of a splicing mutation in the IKBKAP gene causes familial dysautonomia. Am J Hum Genet 2001; 68: 598-605
Hawkes NA, Otero G, Winkler GS, et al. Purification and characterization of the human elongator complex. J Biol Chem 2002; 277: 3047-3052
Kim JH, Lane WS, Reinberg D. Human elongator facilitates RNA polymerase II transcription through chromatin. Proc Natl Acad Sci USA 2002; 99: 1241-1246
Winkler GS, Kristjuhan A, Erdjument-Bromage H, Tempst P, Svejstrup JQ. Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc Natl Acad Sci USA 2002; 99: 3517-3522
Okada Y, Yamagata K, Hong K, Wakayama T, Zhang Y. A role for the elongator complex in zygotic paternal genome demethylation. Nature 2010; 463: 554-558
Close P, Hawkes N, Cornez I, et al. Transcription impairment and cell migration defects in elongator-depleted cells: implication for familial dysautonomia. Mol Cell 2006; 22: 521-531
Kristjuhan A, Svejstrup JQ. Evidence for distinct mechanisms facilitating transcript elongation through chromatin in vivo. Embo J 2004; 23: 4243-4252
Esberg A, Huang B, Johansson MJ, Bystrom AS. Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol Cell 2006; 24: 139-148
Nedialkova DD, Leidel SA. Optimization of codon translation rates via tRNA modifications maintains proteome integrity. Cell 2015; 161: 1606-1618
Rahl PB, Chen CZ, Collins RN. Elp1p, the yeast homolog of the FD disease syndrome protein, negatively regulates exocytosis independently of transcriptional elongation. Mol Cell 2005; 17: 841-853
Laguesse S, Creppe C, Nedialkova DD, et al. A dynamic unfolded protein response contributes to the control of cortical neurogenesis. Dev Cell 2015; 35: 553-567
Karlsborn T, Tukenmez H, Mahmud AK, Xu F, Xu H, Bystrom AS. Elongator, a conserved complex required for wobble uridine modifications in eukaryotes. RNA Biol 2014; 11: 1519-1528
Ladang A, Rapino F, Heukamp LC, et al. Elp3 drives Wnt-dependent tumor initiation and regeneration in the intestine. J Exp Med 2015; 212: 2057-2075
Miskiewicz K, Jose LE, Bento-Abreu A, et al. ELP3 controls active zone morphology by acetylating the ELKS family member Bruchpilot. Neuron 2011; 72: 776-788
George L, Chaverra M, Wolfe L, et al. Familial dysautonomia model reveals Ikbkap deletion causes apoptosis of Pax3+ progenitors and peripheral neurons. Proc Natl Acad Sci USA 2013; 110: 18698-18703
Jackson MZ, Gruner KA, Qin C, Tourtellotte WG. A neuron autonomous role for the familial dysautonomia gene ELP1 in sympathetic and sensory target tissue innervation. Development 2014; 141: 2452-2461
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 2003; 23: 167-174
Wittschieben BO, Fellows J, Du W, Stillman DJ, Svejstrup JQ. Overlapping roles for the histone acetyltransferase activities of SAGA and elongator in vivo. Embo J 2000; 19: 3060-3068
Saez PJ, Villalobos-Labra R, Westermeier F, Sobrevia L, Farias-Jofre M. Modulation of endothelial cell migration by ER stress and insulin resistance: a role during maternal obesity? Front Pharmacol 2014; 5: 189
Chrzanowska-Wodnicka M, Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol 1996; 133: 1403-1415
Burkel BM, von Dassow G, Bement WM. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil Cytoskeleton 2007; 64: 822-832
Johansen LD, Naumanen T, Knudsen A, et al. IKAP localizes to membrane ruffles with filamin A and regulates actin cytoskeleton organization and cell migration. J Cell Sci 2008; 121: 854-864
Nakamura F, Osborn TM, Hartemink CA, Hartwig JH, Stossel TP. Structural basis of filamin A functions. J Cell Biol 2007; 179: 1011-1025
Marin O. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 2012; 13: 107-120
Chenn A, Walsh CA. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 2002; 297: 365-369
Rakic P, Knyihar-Csillik E, Csillik B. Polarity of microtubule assemblies during neuronal cell migration. Proc Natl Acad Sci USA 1996; 93: 9218-9222
Rivas RJ, Hatten ME. Motility and cytoskeletal organization of migrating cerebellar granule neurons. J Neurosci 1995; 15: 981-989
Schaar BT, McConnell SK. Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci USA 2005; 102: 13652-13657
Xie Z, Samuels BA, Tsai LH. Cyclin-dependent kinase 5 permits efficient cytoskeletal remodeling-a hypothesis on neuronal migration. Cereb Cortex 2006; 16 Suppl 1: i64-i68
Akella JS, Wloga D, Kim J, et al. MEC-17 is an alpha-tubulin acetyltransferase. Nature 2010; 467: 218-222
Shinohara R, Thumkeo D, Kamijo H, et al. A role for mDia, a Rho-regulated actin nucleator, in tangential migration of interneuron precursors. Nat Neurosci 2012; 15: 373-380
Jaglin XH, Chelly J. Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects. Trends Genet 2009; 25: 555-566
Kappeler C, Saillour Y, Baudoin JP, et al. Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum Mol Genet 2006; 15: 1387-1400
McManus MF, Nasrallah IM, Pancoast MM, Wynshaw-Boris A, Golden JA. Lis1 is necessary for normal non-radial migration of inhibitory interneurons. Am J Pathol 2004; 165: 775-784
Avila A, Vidal PM, Dear TN, Harvey RJ, Rigo JM, Nguyen L. Glycine receptor alpha2 subunit activation promotes cortical interneuron migration. Cell Rep 2013; 4: 738-750
Bellenchi GC, Gurniak CB, Perlas E, Middei S, Ammassari-Teule M, Witke W. N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev 2007; 21: 2347-2357
Wang JT, Song LZ, Li LL, et al. Src controls neuronal migration by regulating the activity of FAK and cofilin. Neuroscience 2015; 292: 90-100
Gleeson JG, Lin PT, Flanagan LA, Walsh CA. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999; 23: 257-271
Volvert ML, Prevot PP, Close P, et al. MicroRNA targeting of CoREST controls polarization of migrating cortical neurons. Cell Rep 2014; 7: 1168-1183
Martini FJ, Valdeolmillos M. Actomyosin contraction at the cell rear drives nuclear translocation in migrating cortical interneurons. J Neurosci 2010; 30: 8660-8670
Martini FJ, Valiente M, Lopez Bendito G, et al. Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration. Development 2009; 136: 41-50
Nagano T, Morikubo S, Sato M. Filamin A and FILIP (Filamin A-Interacting Protein) regulate cell polarity and motility in neocortical subventricular and intermediate zones during radial migration. J Neurosci 2004; 24: 9648-9657
Kuhn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science 1995; 269: 1427-1429
Tielens S, Godin JD, Nguyen L. Real-time recordings of migrating cortical neurons from GFP and Cre recombinase expressing mice. Curr Protoc Neurosci 2016; 74: 3.29.1-23