Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex

Ang, Eugenius S. B. C.; Haydar, Tarik F.; Glunčić, Vicko; Rakić, Paško

doi:10.1523/jneurosci.23-13-05805.2003

Cited by 258 publications

(229 citation statements)

References 72 publications

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“…The USW may also disturb exocytosis, essential for the extension of the leading tip of migrating neurons or disrupt cytoskeletal rearrangement essential for the translocation of the nucleus within its leading process (18,20,21,37). Based on the present results, the effect on other forms of cell motility, such as tangential neuronal migration (13,15,17) or spinning of the mitotic spindle (40), cannot be excluded. Finally, although we cannot fully estimate the contribution of the indirect, humorally mediated effect of stress caused by the exposure of pregnant mothers to the experimental procedure, it appears to play a role only in extended exposures (420 min) based on comparisons between normal control durations and all sham control durations.…”

Section: Discussionmentioning

confidence: 76%

“…When the rate of neuronal migration and the sequence of arrival are altered because of genetic and͞or environmental factors, various consequences, including abnormal behavior, have been observed (7-13). In terms of orientation and directionality of movement, neuronal migration to the cerebral cortex can be classified into radial (proceeding radially from the ventricular to the pial surface) (5, 14) and tangential (running parallel to the brain surface) (15)(16)(17). Contact interaction between migrating neurons and the surfaces of neighboring cells plays a decisive role in selecting the migratory pathway and determining their final position (18,19).…”

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confidence: 99%

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Prenatal exposure to ultrasound waves impacts neuronal migration in mice

Ang

Glunčić

Duque

et al. 2006

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

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243

172

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Neurons of the cerebral neocortex in mammals, including humans, are generated during fetal life in the proliferative zones and then migrate to their final destinations by following an inside-tooutside sequence. The present study examined the effect of ultrasound waves (USW) on neuronal position within the embryonic cerebral cortex in mice. We used a single BrdU injection to label neurons generated at embryonic day 16 and destined for the superficial cortical layers. Our analysis of over 335 animals reveals that, when exposed to USW for a total of 30 min or longer during the period of their migration, a small but statistically significant number of neurons fail to acquire their proper position and remain scattered within inappropriate cortical layers and͞or in the subjacent white matter. The magnitude of dispersion of labeled neurons was variable but systematically increased with duration of exposure to USW. These results call for a further investigation in larger and slower-developing brains of non-human primates and continued scrutiny of unnecessarily long prenatal ultrasound exposure.brain malformations ͉ cerebral cortex ͉ embryonic development A fundamental feature of cerebral cortical organization is that positions of its neuronal constituents into horizontal (laminar) and vertical (radial) arrays ultimately define their connectivity and function (1). Cortical neurons acquire appropriate positions by migration from the site of their origin in the proliferative zones lining the cerebral ventricle, according to a precise schedule (2, 3) and along well defined pathways (4-6). When the rate of neuronal migration and the sequence of arrival are altered because of genetic and͞or environmental factors, various consequences, including abnormal behavior, have been observed (7-13). In terms of orientation and directionality of movement, neuronal migration to the cerebral cortex can be classified into radial (proceeding radially from the ventricular to the pial surface) (5, 14) and tangential (running parallel to the brain surface) (15)(16)(17). Contact interaction between migrating neurons and the surfaces of neighboring cells plays a decisive role in selecting the migratory pathway and determining their final position (18,19). Neuronal migration involves translocation of the nucleus and the surrounding cytoplasm with the leading process, which requires rearrangement of the cytoskeleton (20, 21). As a consequence of these complex cellular and molecular interactions, the process of neuronal migration is highly sensitive to a variety of biological, physical, and chemical agents, as well as to specific genetic mutations (7-13). For example, repeated exposure of the rodent and primate fetal brain to environmental agents, such as alcohol (9), drugs (22), neurotrophic viruses (23), and ionizing irradiation (24, 25), causes misplacement of neurons and behavioral deficits.To our knowledge, the effect of ultrasound waves (USW) on the rate of migration in the cerebral cortex has never been tested, although it has been reported ...

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Section: Discussionmentioning

confidence: 76%

mentioning

confidence: 99%

Prenatal exposure to ultrasound waves impacts neuronal migration in mice

Ang

Glunčić

Duque

et al. 2006

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

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243

172

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“…Brain slices retain the in vivo pattern of migration and represent a cell environment close to the physiological situation (Ang et al, 2003). Imaging of moving interneurons was achieved with confocal video-microscopy for spatial resolution complemented by wide field fluorescence images.…”

Section: Resultsmentioning

confidence: 99%

Actomyosin Contraction at the Cell Rear Drives Nuclear Translocation in Migrating Cortical Interneurons

Martini

Valdeolmillos²

2010

Journal of Neuroscience

112

134

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Neuronal migration is a complex process requiring the coordinated interaction of cytoskeletal components and regulated by calcium signaling among other factors. Migratory neurons are polarized cells in which the largest intracellular organelle, the nucleus, has to move repeatedly. Current views support a central role for pulling forces that drive nuclear movement. The participation of actomyosin driven forces acting at the nucleus rear has been suggested, however its precise contribution has not been directly addressed. By analyzing interneurons migrating in cortical slices of mouse brains, we have found that nucleokinesis is associated with a precise pattern of actin dynamics characterized by the initial formation of a cup-like actin structure at the rear nuclear pole. Time-lapse experiments show that progressive actomyosin contraction drives the nucleus forward. Nucleokinesis concludes with the complete contraction of the cup-like structure, resulting in an actin spot at the base of the retracting trailing process. Our results demonstrate that this actin remodeling requires a threshold calcium level provided by low-frequency spontaneous fast intracellular calcium transients. Microtubule stabilization with taxol treatment prevents actin remodeling and nucleokinesis, whereas cells with a collapsed microtubule cytoskeleton induced by nocodazole treatment, display nearly normal actin dynamics and nucleokinesis. In summary, the results presented here demonstrate that actomyosin forces acting at the rear side of the nucleus drives nucleokinesis in tangentially migrating interneurons in a process that requires calcium and a dynamic cytoskeleton of microtubules.

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“…Time-lapse live imaging was performed as previously reported (43). Calcium imaging was performed as previously described (28,31).…”

Section: Methodsmentioning

confidence: 99%

The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone

Liu

Hashimoto-Torii

Torii

et al. 2008

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

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P2Y1 ͉ calcium transient ͉ embryonic neocortex ͉ SVZ F or almost four decades we have known that neurons destined for the cerebral cortex in all mammalian species, including the human, are generated in the primary and secondary proliferative layers situated near the embryonic cerebral ventricle, respectively called the ventricular (VZ) and subventricular zones (SVZ) (1, 2). It is also generally recognized that the SVZ is formed by a subclass of neuronal progenitors that lose their attachment to the ventricular surface and translocate their nucleus and surrounding somatic cytoplasm to the SVZ, where they continue to divide and produce neurons destined predominantly for the upper cortical layers (3-5). The use of in vitro imaging has revealed that the SVZ progenitors (recently renamed the intermediate neuronal progenitors or INPs, to emphasize their continuous proliferation), originate in the VZ by asymmetric mitotic division of the neuroepithelial cells (6). After translocation of their soma to the SVZ, INPs amplify production of cortical neurons via asymmetrical and symmetric modes of mitotic divisions (6-9). The relative large size of the SVZ in primates, particularly in humans, has inspired suggestions that cells in this zone contribute to the expansion and elaboration of the neocortex during evolution (2, 10, 11). Furthermore, genetic and environmental disturbances of neuronal production in the SVZ affect the development and function of the cerebral cortex (5,(12)(13)(14).Considering the developmental and clinical significance of the SVZ, surprisingly little is known about its origin and how INPs are distinguished from other proliferative neural precursors and postmitotic migrating neurons. Similar to the postmitotic neurons, INPs leave the VZ by extending their basal processes toward the cortical plate (CP) along radial glia (RG) shafts and translocating their nuclei within the growing leading processes (1, 6). However, they stop migration after reaching the level of the SVZ, where they re-enter the cell cycle. It has been found that genes, such as p27, Ngn2, FLNa, and MEKK4 are involved in the final mitotic division and onset of migration from the VZ via modulation of the actin cytoskeleton (15-17). Reelin (18) and the neurotransmitters GABA and glutamate and their receptors might also contribute to this process (19,20). However, the nature of the complex intercellular signaling involved in the migration and settlement of INPs in the SVZ remains unexplored.We started with the assumption that Ca 2ϩ , a ubiquitous secondary messenger, and ATP released via gap junctions and hemichannels in the VZ might be involved in the cell-cell communication and the initiation of INP migration. Our hypothesis was based on the previous findings that Ca 2ϩ signaling influences the mitosis of neuronal progenitors and their nuclear interkinetic translocation in the embryonic retina (21), and that [Ca 2ϩ ] fluctuations also affect cellular migration in cerebellar granular cells (22-24), cultured neuronal progenitors (25), and p...

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Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex

Cited by 258 publications

References 72 publications

Prenatal exposure to ultrasound waves impacts neuronal migration in mice

Prenatal exposure to ultrasound waves impacts neuronal migration in mice

Actomyosin Contraction at the Cell Rear Drives Nuclear Translocation in Migrating Cortical Interneurons

The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone

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