Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration

Martini, Francisco J.; Valiente, Manuel; López‐Bendito, Guillermina; Szabó, Gábor; Moya, Fernando; Valdeolmillos, Miguel; Marı́n, Oscar

doi:10.1242/dev.025502

Cited by 124 publications

(159 citation statements)

References 36 publications

(23 reference statements)

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“…Previous in vitro studies indicated that selection of a LP branch leads to changes in direction of neuronal migration (14,16,28). We found that the LP was usually branched either in the vicinity of or away from the soma (Fig.…”

Section: Multidirectional Migration Of Cortical Interneurons In Livinmentioning

confidence: 57%

“…Thus, the Golgi apparatus appears to pilot the nucleus to the LP branch. on 2D substrates (1), neurons emigrating from an explant (2), and those migrating within a slice culture (14,17,29) or explant (15,16,21,30). However, as informative as those studies are, their conclusions would not be supported if they were found to disagree with in vivo results.…”

Section: Branch Rather Than the Turning Of A Lp Tip Is Critical Formentioning

confidence: 99%

“…Real-time imaging has also helped reveal the dynamics and roles of cytoplasmic organelles and cytoskeletal components, such as the centrosome (5-9), microtubules (9), and even of some molecules like calcium (10) and actin (7,11,12) during migration. In addition, slice and explant preparations have demonstrated aspects of migratory behaviors, including locomotion and translocation (13), branch-induced changes in migratory direction (14), multidirectional migration (15), random-walk-like behavior (16), pausing behavior, and the transition from tangential to radial migration (17).…”

mentioning

confidence: 99%

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Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos

Yanagida

Miyoshi

Toyokuni

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Precisely arranged cytoarchitectures such as layers and nuclei depend on neuronal migration, of which many in vitro studies have revealed the mode and underlying mechanisms. However, how neuronal migration is achieved in vivo remains unknown. Here we established an imaging system that allows direct visualization of cortical interneuron migration in living mouse embryos. We found that during nucleokinesis, translocation of the Golgi apparatus either precedes or occurs in parallel to that of the nucleus, suggesting the existence of both a Golgi/centrosome-dependent and -independent mechanism of nucleokinesis. Changes in migratory direction occur when the nucleus enters one of the leading process branches, which is accompanied by the retraction of other branches. The nucleus occasionally swings between two branches before translocating into one of them, the occurrence of which is most often preceded by Golgi apparatus translocation into that branch. These in vivo observations provide important insight into the mechanisms of neuronal migration and demonstrate the usefulness of our system for studying dynamic events in living animals.cortex | GABAergic interneuron | in utero electroporation | in vivo imaging N euronal migration is a critical step in the construction of the nervous system. During development, neurons migrate from the sites of their birth to their final destinations, where they form neuronal architectures, such as laminated structures and nuclei, that are necessary for information processing in the nervous system.Because neuronal migration is a dynamic phenomenon, realtime imaging could provide important insight into its mechanisms. Studies using real-time imaging of neurons in dissociated culture have demonstrated various aspects of neuronal migration, including the fact that radial fibers (1) and neighboring cells (2) act as the substrate for migration and the molecular mechanisms driving nucleokinesis (3, 4). Real-time imaging has also helped reveal the dynamics and roles of cytoplasmic organelles and cytoskeletal components, such as the centrosome (5-9), microtubules (9), and even of some molecules like calcium (10) and actin (7,11,12) during migration. In addition, slice and explant preparations have demonstrated aspects of migratory behaviors, including locomotion and translocation (13), branch-induced changes in migratory direction (14), multidirectional migration (15), random-walk-like behavior (16), pausing behavior, and the transition from tangential to radial migration (17).However, as informative as these neural migration studies are, they are limited because they are all in vitro and do not necessarily show neuronal behaviors in vivo. Here, we observed migrating neurons in the brain of living mouse embryos and analyzed their behavior, including the dynamics of the nucleus and the Golgi apparatus. We took advantage of the fact that cortical interneurons tangentially migrate near the surface of the cortex. These neurons are generated in the ganglionic eminences (GEs) in the basal forebrain a...

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Section: Multidirectional Migration Of Cortical Interneurons In Livinmentioning

confidence: 57%

Section: Branch Rather Than the Turning Of A Lp Tip Is Critical Formentioning

confidence: 99%

mentioning

confidence: 99%

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Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos

Yanagida

Miyoshi

Toyokuni

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Migratory interneurons, derived from the medial and lateral ganglionic eminences, can exhibit multipolar morphology (Nadarajah et al, 2003;Tanaka et al, 2006) and exhibit dynamic branch growth, leading to the formation of new leading processes (Britto et al, 2009;Martini et al, 2009). Time-lapse imaging in vitro has revealed that young cortical interneurons, migrating in the intermediate zone and marginal zone, also move in an undirected, random walk pattern (Tabata and Nakajima, 2003;Tanaka et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Wandering Neuronal Migration in the Postnatal Vertebrate Forebrain

Scott

Gardner

et al. 2012

J. Neurosci.

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Most non-mammalian vertebrate species add new neurons to existing brain circuits throughout life, a process thought to be essential for tissue maintenance, repair, and learning. How these new neurons migrate through the mature brain and which cues trigger their integration within a functioning circuit is not known. To address these questions, we used two-photon microscopy to image the addition of genetically labeled newly generated neurons into the brain of juvenile zebra finches. Time-lapse in vivo imaging revealed that the majority of migratory new neurons exhibited a multipolar morphology and moved in a nonlinear manner for hundreds of micrometers. Young neurons did not use radial glia or blood vessels as a migratory scaffold; instead, cells extended several motile processes in different directions and moved by somal translocation along an existing process. Neurons were observed migrating for ϳ2 weeks after labeling injection. New neurons were observed to integrate in close proximity to the soma of mature neurons, a behavior that may explain the emergence of clusters of neuronal cell bodies in the adult songbird brain. These results provide direct, in vivo evidence for a wandering form of neuronal migration involved in the addition of new neurons in the postnatal brain.

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“…Pour se déplacer, les neurones GABAergiques embryonnaires étendent à l'avant un prolongement explorateur branché [5][6][7] (Figure 1B). Les neurones naissent et se multiplient au centre du cerveau dans le neuroépithélium bordant les ventricules, puis migrent vers les régions périphériques où ils s'organisent en noyaux ou en couches.…”

Section: Transformations Accompagnant La Migration Des Neurones Gabaeunclassified

Cils et migrations neuronales

Métin

2014

Med Sci (Paris)

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> Dans un article fondateur paru en 1977, G. Albrecht-Buehler décrivait un cil primaire à la surface de fibroblastes en migration, et remarquait que le cil est orienté parallèlement à la direction de migration des cellules. La présence d'un cil primaire a été notée sur les progéniteurs neuraux et sur les neurones postmitotiques depuis longtemps. Cependant, ce n'est que récemment qu'un cil primaire a été observé sur les interneurones corticaux en migration. Comme dans les fibroblastes, le cil des interneurones contrôle la direction de la migration. Il joue un rôle particulièrement important dans la réorientation des interneurones vers la plaque corticale. Le morphogène Shh (Sonic hedgehog), qui est exprimé dans les voies de migration des interneurones, est l'un des signaux qui contrôlent cette réorientation. < Les mouvements migratoires dans le cortex cérébral embryonnaireLe cortex cérébral comprend essentiellement deux populations de neurones : les neurones excitateurs et les interneurones inhibiteurs. Les neurones excitateurs sont organisés en couches parallèles à la surface du cortex. Ils sont produits localement et rejoignent la plaque corticale qui préfigure le cortex adulte ( Figure 1A, zone orange) en migrant le long des cellules de glie radiaire, leurs cellules progénitrices. On sait depuis une vingtaine d'années que les interneurones inhibiteurs GABA (acide -aminobutyrique)-ergiques sont générés en dehors du cortex, dans la partie ventrale du cerveau antérieur [3] ( Figure 1A). Ils naissent en majorité dans l'éminence ganglionnaire médiane (EGM), une structure qui s'efface chez l'embryon à la fin de la gestation, et dans deux autres régions identifiées plus récemment [4]. Ces trois régions produisent différentes classes d'interneurones qui migrent d'abord vers la frontière séparant le cerveau ventral et le cortex. Après avoir traversé cette frontière, les neurones se distribuent de part et d'autre de la plaque corticale et s'organisent en deux flux parallèles ( Figure 1A). Un flux dense occupe la zone marginale au-dessus de la plaque corticale. Un second flux, assez large, formé d'une cohorte de cellules migrant individuellement, s'établit le long de la zone proliférative. Régulièrement, des cellules quittent ces flux tangentiels et prennent une direction oblique ou radiale pour rejoindre et coloniser la plaque corticale sous laquelle se forme un flux supplé-mentaire. Les changements de trajectoire affectent à chaque instant un nombre limité de cellules de la cohorte, à tous les niveaux latéro-médians. Ces réorientations sont compatibles avec un processus stochastique, comme avec un mécanisme de sortie des flux tangentiels finement régulé. Transformations accompagnant la migration des neurones GABAergiquesPour se déplacer, les neurones GABAergiques embryonnaires étendent à l'avant un prolongement explorateur branché [5][6][7] (Figure 1B). Les neurones naissent et se multiplient au centre du cerveau dans le neuroépithélium bordant les ventricules, puis migrent vers les régions périphériques où ils s'orga...

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Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration

Cited by 124 publications

References 36 publications

Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos

Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos

Wandering Neuronal Migration in the Postnatal Vertebrate Forebrain

Cils et migrations neuronales

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