Cajal-Retzius Cells Instruct Neuronal Migration by Coincidence Signaling between Secreted and Contact-Dependent Guidance Cues

Gil-Sanz, Cristina; Franco, Santos J.; Martínez-Garay, Isabel; Espinosa, Ana; Harkins‐Perry, Sarah; Müller, Ulrich

doi:10.1016/j.neuron.2013.06.040

Cited by 123 publications

(134 citation statements)

References 56 publications

(106 reference statements)

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“…Reelin is well known to control some cell adhesion molecules, such as N-cadherin (11,14,26) and integrin α5β1 (12). In regard to the adhesion molecule mediating the Reelin-dependent neuronal aggregation, we thought that N-cadherin might be a good candidate because N-cadherin is present in abundance in the cortical MZ (27).…”

Section: Resultsmentioning

confidence: 99%

“…Reelin signaling to Rap1 promotes N-cadherin functions via nectin3 and afadin toward mediating cell-cell interactions between the migrating neurons and Cajal-Retzius cells (26). However, these studies did not address the time-dependent dynamic changes of cell adhesion mediated by N-cadherin.…”

Section: Discussionmentioning

confidence: 99%

“…The p120 catenin-cadherin binding is strengthened by the interaction of p120 catenin with nectin-associated afadin in a Rap1-dependent manner (40). Reelin recruits p120 catenin and N-cadherin to the nectin and afadin complexes, enhancing the N-cadherin-mediated cell adhesion (26). Thus, p120 catenin is also a candidate molecule connecting the Reelin-Dab1 pathway and N-cadherin.…”

Section: Discussionmentioning

confidence: 99%

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Reelin transiently promotes N-cadherin–dependent neuronal adhesion during mouse cortical development

Matsunaga

Noda

Murakawa

et al. 2017

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

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Reelin is an essential glycoprotein for the establishment of the highly organized six-layered structure of neurons of the mammalian neocortex. Although the role of Reelin in the control of neuronal migration has been extensively studied at the molecular level, the mechanisms underlying Reelin-dependent neuronal layer organization are not yet fully understood. In this study, we directly showed that Reelin promotes adhesion among dissociated neocortical neurons in culture. The Reelin-mediated neuronal aggregation occurs in an N-cadherin-dependent manner, both in vivo and in vitro. Unexpectedly, however, in a rotation culture of dissociated neocortical cells that gradually reaggregated over time, we found that it was the neural progenitor cells [radial glial cells (RGCs)], rather than the neurons, that tended to form clusters in the presence of Reelin. Mathematical modeling suggested that this clustering of RGCs could be recapitulated if the Reelin-dependent promotion of neuronal adhesion were to occur only transiently. Thus, we directly measured the adhesive force between neurons and N-cadherin by atomic force microscopy, and found that Reelin indeed enhanced the adhesiveness of neurons to N-cadherin; this enhanced adhesiveness began to be observed at 30 min after Reelin stimulation, but declined by 3 h. These results suggest that Reelin transiently (and not persistently) promotes N-cadherin-mediated neuronal aggregation. When N-cadherin and stabilized β-catenin were overexpressed in the migrating neurons, the transfected neurons were abnormally distributed in the superficial region of the neocortex, suggesting that appropriate regulation of N-cadherin-mediated adhesion is important for correct positioning of the neurons during neocortical development.T he mammalian neocortex is highly organized into six neuronal layers. This laminar structure is responsible for the complex motor, sensory, and cognitive functions of the mammalian brain (1). Neuronal migration plays an important role in the establishment of this layered structure. Cortical neurons are generated within the ventricular zone (VZ) or subventricular zone (SVZ), and migrate along radial fibers toward the pial surface. Newly born excitatory neurons migrate radially into the cortical plate (CP) past the neurons born earlier, resulting in a birth date-dependent "inside-out" alignment of the neurons in the CP (2-4).Reelin is a glycoprotein that is secreted by the Cajal-Retzius cells in the marginal zone (MZ) of the cortex during neocortical development (5-7). This glycoprotein is essential for establishment of the aforementioned birth date-dependent layered structure of the neocortex, because the CP neurons show an almost inverted alignment in the neocortex of the Reelindeficient, reeler mice. In addition, neurons born at the same time tend to be distributed broadly and not to form clear layers in the reeler cortex (8, 9). Although extensive studies, including at the molecular level, have been conducted to determine the role of Reelin in neuronal migration i...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Reelin transiently promotes N-cadherin–dependent neuronal adhesion during mouse cortical development

Matsunaga

Noda

Murakawa

et al. 2017

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

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“…In addition, there are evidences that confirm that CR cells expressed nectin1 that mediates heterotypic interactions with nectin3 in the leading processes of migrating projection neurons. The interactions between both nectins control radial migration by acting in concert with Reelin and Cdh2 to promote interactions between migrating neurons and CR cells 21 . The activity of CXCL12 and its receptors has been found to play a role in controlling the migration of other cortical neurons (for example, GABAergic interneurons) that are also influenced by the action of Semaphorins and their receptors 22,23 .…”

mentioning

confidence: 99%

Sema3E/PlexinD1 regulates the migration of hem-derived Cajal-Retzius cells in developing cerebral cortex

et al. 2014

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During the development of the cerebral cortex, Cajal-Retzius (CR) cells settle in the preplate and coordinate the precise growth of the neocortex. Indeed, CR cells migrate tangentially from specific proliferative regions of the telencephalon (for example, the cortical hem (CH)) to populate the entire cortical surface. This is a very finely tuned process regulated by an emerging number of factors that has been sequentially revealed in recent years. However, the putative participation of one of the major families of axon guidance molecules in this process, the Semaphorins, was not explored. Here we show that Semaphorin-3E (Sema3E) is a natural negative regulator of the migration of PlexinD1-positive CR cells originating in the CH. Our results also indicate that Sema3E/PlexinD1 signalling controls the motogenic potential of CR cells in vitro and in vivo. Indeed, absence of Sema3E/PlexinD1 signalling increased the migratory properties of CR cells. This modulation implies negative effects on CXCL12/CXCR4 signalling and increased ADF/Cofilin activity.

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“…6.10). N-Cadherin is required for cell-cell adhesion between migrating projection neurons and RGCs during glia-dependent migration and the attachment between projection neurons and CR cells in the marginal zone during glia-independent migration (Gil-Sanz et al 2013;Kawauchi et al 2010). However, how N-cadherin acquires heterotypic cell-cell adhesions between CR cells and projection neurons remained unclear.…”

Section: Heterotypic Adhesion: Neuronal Cell Adhesion and Migrationmentioning

confidence: 99%

Cooperative Roles of Nectins with Cadherins in Physiological and Pathological Processes

Fujiwara

Mizoguchi

Takai

2016

The Cadherin Superfamily

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Mammalian tissues and organs are composed of cells of different types and these cells adhere to one another to form societies of cells including the mesenchyme and the epithelium. Cell-cell adhesion in the mesenchyme is weak whereas cells are organized into closely adherent barrier-forming sheets by cellcell adhesions in the epithelium. Cell-cell adhesion is organized to allow the release or incorporation of individual cells during various physiological or pathological processes, for example, organ development and growth, maintenance and repair of tissues, or tumorigenesis. One prominent cell-cell adhesion apparatus is adherens junctions (AJs). The central structural components of AJs are transmembrane cellcell adhesion molecules, cadherins and nectins. Nectins recruit cadherins to the cell-cell contact sites and mediate cell-cell adhesions that control local membrane dynamics for cell polarization and coordinate shape change at the cellular level. Nectins are engaged in calcium-independent homophilic and heterophilic transinteractions between opposing cells in numerous tissues and cell types to form homotypic and heterotypic cell-cell adhesion, whereas cadherins are primarily involved in calcium-dependent homophilic trans-interactions between opposing cells to form homotypic cell-cell adhesion. Nectins function cooperatively with or independently of cadherins to control physiological processes and cooperative ones include the formation of AJs and apico-basal polarity, apical constriction, contact inhibition of cell movement and proliferation, formation of synapse, formation of checkerboard-like cell arrangement, ciliary epithelium and lens, and

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Cajal-Retzius Cells Instruct Neuronal Migration by Coincidence Signaling between Secreted and Contact-Dependent Guidance Cues

Cited by 123 publications

References 56 publications

Reelin transiently promotes N-cadherin–dependent neuronal adhesion during mouse cortical development

Reelin transiently promotes N-cadherin–dependent neuronal adhesion during mouse cortical development

Sema3E/PlexinD1 regulates the migration of hem-derived Cajal-Retzius cells in developing cerebral cortex

Cooperative Roles of Nectins with Cadherins in Physiological and Pathological Processes

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