Ventricle-directed migration in the developing cerebral cortex

Nadarajah, Bagirathy; Alifragis, Pavlos; Wong, Rachel; Parnavelas, John G.

doi:10.1038/nn813

Cited by 199 publications

(127 citation statements)

References 30 publications

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“…In the current study, we showed that most migrating enteric neurons extended a long-leading process that projected along the same pathway that the cell body will later follow, which is very similar to the behavior of migrating neurons in the developing CNS (Nadarajah et al, 2001(Nadarajah et al, , 2002Tanaka et al, 2003;Bellion et al, 2005;Bless et al, 2005). The presence of a long-leading process was not, however, indicative of a migrating neuron, as the majority of stationary enteric neurons also possessed long-leading processes.…”

Section: Mode Of Enteric Neuron Migrationsupporting

confidence: 67%

“…6). Almost all neurons exhibited a saltatory mode of migration, alternating between stationary or slowmoving phases and fast-moving phases, similar to neuronal \locomotion" described in the developing cerebral cortex (Nadarajah et al, 2001(Nadarajah et al, , 2002. In stationary phases, the center of the cell body could sometimes be observed to shift, which was often accompanied by changes in the leading process.…”

Section: Characterization Of Gfp + Neurons In the Gut Of Embryonic Thmentioning

confidence: 62%

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The migratory behavior of immature enteric neurons

Hao

Anderson

Kobayashi

et al. 2008

Developmental Neurobiology

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While they are migrating caudally along the developing gut, around 10%-20% of enteric neural crest-derived cells start to express pan-neuronal markers and tyrosine hydroxylase (TH). We used explants of gut from embryonic TH-green fluorescence protein (GFP) mice and time-lapse microscopy to examine whether these immature enteric neurons migrate and their mode of migration. In the gut of E10.5 and E11.5 TH-GFP mice, around 50% of immature enteric neurons (GFP + cells) migrated, with an average speed of around 15 lm/h. This is slower than the speed at which the population of enteric neural crest-derived cells advances along the developing gut, and hence neuronal differentiation seems to slow, but not necessarily halt, the caudal migration of enteric neural crest cells. Most migrating immature enteric neurons migrated caudally by extending a long-leading process followed by translocation of the cell body. This mode of migration is different from that of non-neuronal enteric neural crestderived cells and neural crest cells in other locations, but resembles that of migrating neurons in many regions of the developing central nervous system (CNS). In migrating immature enteric neurons, a swelling often preceded the movement of the nucleus in the direction of the leading process. However, the centrosomal marker, pericentrin, was not localized to either the leading process or swelling. This seems to be the first detailed report of neuronal migration in the developing mammalian peripheral nervous system. ' 2008 Wiley Periodicals, Inc. Develop Neurobiol 69: 22-35, 2009

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Section: Mode Of Enteric Neuron Migrationsupporting

confidence: 67%

Section: Characterization Of Gfp + Neurons In the Gut Of Embryonic Thmentioning

confidence: 62%

The migratory behavior of immature enteric neurons

Hao

Anderson

Kobayashi

et al. 2008

Developmental Neurobiology

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“…Using time-lapse imaging of cortical slices together with tracer-labeling techniques, Nadarajah et al (46) have shown that interneurons arising in the ventral telencephalon actively migrate towards the cortical VZ upon reaching the dorsal telencephalon, a mode of movement that has been termed ventricle-directed migration. After a pause in this proliferative zone, they migrate radially in the direction of the pial surface to take up positions in the developing CP (Figure 3).…”

Section: Mgementioning

confidence: 99%

“…How is it that two neuronal types generated in two distinct regions of the developing brain, the pallium and subpallium, and shown to follow different migratory paths, can assemble in the cortex in a way that they are linked temporally and spatially? Nadarajah and colleagues (46) have proposed that cortical interneurons follow ventricle-directed migration actively seeking the VZ in order to obtain the type of positional information that the pyramidal cells acquire prior to becoming postmitotic. These cues may be obtained from the local environment or from the pyramidal cells themselves through neural-neural interactions.…”

Section: Mgementioning

confidence: 99%

The origin of cortical neurons

Parnavelas

2002

Braz J Med Biol Res

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Neurons of the mammalian cerebral cortex comprise two broad classes: pyramidal neurons, which project to distant targets, and the inhibitory nonpyramidal cells, the cortical interneurons. Pyramidal neurons are generated in the germinal ventricular zone, which lines the lateral ventricles, and migrate along the processes of radial glial cells to their positions in the developing cortex in an inside-out sequence. The GABA-containing nonpyramidal cells originate for the most part in the ganglionic eminence, the primordium of the basal ganglia in the ventral telencephalon. These cells follow tangential migratory routes to enter the cortex and are in close association with the corticofugal axonal system. Once they enter the cortex, they move towards the ventricular zone, possibly to obtain positional information, before they migrate radially in the direction of the pial surface to take up their positions in the developing cortex. The mechanisms that guide interneurons throughout these long and complex migratory routes are currently under investigation. Correspondence

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“…During migration, future cortical interneurons exhibit saltatory nuclear movements and develop a branched leading process that undergoes complex morphological changes (Nadarajah et al, 2002;Polleux et al, 2002;Ang et al, 2003;Moya and Valdeolmillos, 2004). The present study was aimed at better analyzing these changes and the full migration cycle of cortical interneu-rons.…”

Section: Introductionmentioning

confidence: 99%

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

Bellion

Baudoin²,

Alvarez³

et al. 2005

Journal of Neuroscience

319

415

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During rodent cortex development, cells born in the medial ganglionic eminence (MGE) of the basal telencephalon reach the embryonic cortex by tangential migration and differentiate as interneurons. Migrating MGE cells exhibit a saltatory progression of the nucleus and continuously extend and retract branches in their neuritic arbor. We have analyzed the migration cycle of these neurons using in vitro models.We show that the nucleokinesis in MGE cells comprises two phases. First, cytoplasmic organelles migrate forward, and second, the nucleus translocates toward these organelles. During the first phase, a large swelling that contains the centrosome and the Golgi apparatus separates from the perinuclear compartment and moves rostrally into the leading neurite, up to 30 m from the waiting nucleus. This long-distance migration is associated with a splitting of the centrioles that line up along a linear Golgi apparatus. It is followed by the second, dynamic phase of nuclear translocation toward the displaced centrosome and Golgi apparatus.The forward movement of the nucleus is blocked by blebbistatin, a specific inhibitor of nonmuscle myosin II. Because myosin II accumulates at the rear of migrating MGE cells, actomyosin contraction likely plays a prominent role to drive forward translocations of the nucleus toward the centrosome. During this phase of nuclear translocation, the leading growth cone either stops migrating or divides, showing a tight correlation between leading edge movements and nuclear movements.

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Ventricle-directed migration in the developing cerebral cortex

Cited by 199 publications

References 30 publications

The migratory behavior of immature enteric neurons

The migratory behavior of immature enteric neurons

The origin of cortical neurons

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

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