Cajal–Retzius cells and subplate neurons differentially express vesicular glutamate transporters 1 and 2 during development of mouse cortex

Abstract

In the light of the various neurobiological effects of glutamate in brain development, although some embryonic cells are a probable source of glutamate involved in the development of precursor cells and/or immature neurons, little is known about when and where glutamate plays its crucial roles during corticogenesis. To investigate these roles, we focused on the developmental expression of vesicular glutamate transporter (VGLUT)1 and VGLUT2, which are regarded as the best markers for verifying glutamatergic neuron identity, especially the spatiotemporal distributions of their transcripts and proteins in the developing mouse cortex and hippocampus. In situ hybridization studies revealed that VGLUT1 mRNA is expressed in preplate and marginal zone cells at embryonic day (E)10 and in subplate cells by E13, whereas VGLUT2 mRNA is expressed in preplate and marginal zone cells at E10 and in cells of the subventricular zone by E13. Reverse transcriptase–polymerase chain reaction analysis detected full‐length VGLUT1 and VGLUT2 gene transcripts in the embryonic brain. By dual labeling combined with immunostaining for microtubule‐associated protein 2 (MAP2) or reelin, we showed that MAP2‐positive preplate and marginal zone neurons and subplate neurons express VGLUT1, while reelin‐positive preplate and marginal zone cells and MAP2‐negative subventricular zone cells express VGLUT2. The present study is the first to provide morphologically reliable evidence showing that Cajal–Retzius cells and subplate neurons are glutamatergic, and that the two cells differentially express VGLUT1 and VGLUT2, respectively, as the specific transport system of glutamate in some events orchestrated by these cells during the cortical development of mice.

Cajal–Retzius cells: Update on structural and functional properties of these mystic neurons that bridged the 20th century

“…On the other hand, studies using morphological and immunohistochemical markers strongly suggest that CRc are glutamatergic (Del Rio et al, 1995;Hevner et al, 2003), and provide no evidence for GABA expression (Alcantara et al, 1998;Bystron et al, 2006). In accordance with these observations, CRc express vesicular glutamate transporters (Ina et al, 2007), while no clear evidence for vGAT expression in putative CRc has been published yet (see e.g. Takayama and Inoue, 2010).…”

Pallio-Pallial Tangential Migrations and Growth Signaling: New Scenario for Cortical Evolution?

“…The standard CR cells located in layer I are glutamatergic and calretinin immunoreactive [Ina et al, 2007], and all of the described pallial sources, including the pallial septum and the nontelencephalic prethalamic eminence, share expression of general pallial markers such as Pax6 in the ventricular zone and Tbr1 in the mantle [Puelles et al, 2000]. However, the developing layer I also contains various sorts of GABAergic neurons originated in the subpallium via the so-called subpial migratory stream [Anderson et al, 1997;Stühmer et al, 2002;Marin and Rubenstein, 2003].…”

Characterization of hippocampal Cajal-Retzius cells during development in a mouse model of Alzheimer′s disease (Tg2576)

“…In the present study, most reelin-positive mossy cells in the hilus were glutamatergic before postnatal day 180. However, few glutamatergic Cajal-Retzius cells are located in the molecular layer of the dentate gyrus[434445]. After postnatal day 360, all Cajal-Retzius cells in the molecular layer of dentate gyrus were also glutamate-positive, a characteristic of projection neurons or excitatory neurons.…”