Generation of Reelin-Positive Marginal Zone Cells from the Caudomedial Wall of Telencephalic Vesicles

Abstract

An early and fundamental step of the laminar organization of developing neocortex is controlled by the developmental programs that critically depend on the activities of reelin-positive cells in the marginal zone. However, the ontogeny of reelin-positive cells remained elusive. To gain insights into the spatial and temporal regulation of reelin-positive marginal zone cell development, we used a transgenic mouse line in which we defined the green fluorescent protein (GFP) transgene as a novel reliable molecular marker of reelin-positive marginal zone cells from the early stages of their development. We further used exo utero electroporation-mediated gene transfer that allows us to mark progenitor cells and monitor the descendants in the telencephalon in vivo. We show here the generation of reelinpositive marginal zone cells from the caudomedial wall of telencephalic vesicles, including the cortical hem, where the prominent expression of GFP is initially detected. These neurons tangentially migrate at the cortical marginal zone and are distributed throughout the entire neocortex in a caudomedial-high to rostrolateral-low gradient during the dynamic developmental period of corticogenesis. Therefore, our findings on reelin-positive marginal zone cells, in addition to the cortical interneurons, add to the emerging view that the neocortex consists of neuronal subtypes that originate from a focal source extrinsic to the neocortex, migrate tangentially into the neocortex, and thereby underlie neural organization of the neocortex.

A Novel Transient Glutamatergic Population Migrating from the Pallial–Subpallial Boundary Contributes to Neocortical Development

“…early stages of PP/CP formation from a focal pallial progenitor domain at the PSB. Although previously thought to be a feature of GABAergic interneurons (Marín and Rubenstein, 2003), tangential migration of glutamatergic neurons has now been reported for several populations during development (Walsh and Cepko, 1992;O'Rourke et al, 1995;Rakic, 1995), including Satb2 ϩ and CajalRetzius neurons (Takiguchi-Hayashi et al, 2004;Bielle et al, 2005;Britanova et al, 2006;Yoshida et al, 2006). At least two of the glutamatergic transient neurons forming the preplate/early CP, CR and Dbx1-derived CP neurons, have now been shown by genetic tracing to be generated at the borders of the developing pallium.…”

“…CR subtypes arise from focal progenitor domains at the edges of the developing pallium and invade the preplate by tangential migration (Takiguchi-Hayashi et al, 2004;Bielle et al, 2005;Yoshida et al, 2006). Notably, both CR and SP cells mostly disappear at the end of development (Meyer et al, 1998;Supèr et al, 1998).…”

Multiple roles of chemokine CXCL12 in the central nervous system: A migration from immunology to neurobiology

“…Recent studies suggest three major CR cell sources in the embryonic telencephalon, including the cortical hem, the septum and the ventral pallium (TakiguchiHayashi K et al, 2004;Bielle F et al, 2005;Yoshida M et al, 2006). CR cells initially radially spread from VZ to MZ and subsequently migrate long distances tangentially along the cortical surface (Takiguchi-Hayashi K et al, 2004;Bielle F et al, 2005;Muzio L and Mallamaci A, 2005;Yoshida M et al, 2006). Expression of CXCR4 is detected in the MZ CR cells from preplate (E13.5) to early postnatal stage (P3) of neocortical development (Stumm RK et al, 2003;Borrell V and Marin O, 2006) while expression of CXCL12 is detected in the meninges (Stumm RK et al, 2003;Borrell V and Marin O, 2006).…”

Foxg1Confines Cajal-Retzius Neuronogenesis and Hippocampal Morphogenesis to the Dorsomedial Pallium

“…On the basis of that finding, they proposed that Foxg1 is a key promoter of neocortical lamination, essential to neocortical neuroblasts in switching from preplate neuronogenesis to cortical plate neuronogenesis. Remarkably, in the wildtype telencephalon, Reln on neurons are clustered tightly in the archicortex and arranged loosely in the neocortex and paleocortex, which reflects early confinement of their generation to the dorsomedial-most pallial primordium (Meyer et al, 2002;Takiguchi-Hayashi et al, 2004). Thus if the Foxg1 gradient is relevant to cortical arealization, overproduction of Reln on neurons occurring in Foxg1 Ϫ / Ϫ mutants may not be attributable to disrupted laminar histogenetic progression of their neocortical neuroblasts but, rather, may stem from large-scale lateral-tomedial repatterning of their cortical primordium.…”