SubpallialDlx2-Expressing Cells Give Rise to Astrocytes and Oligodendrocytes in the Cerebral Cortex and White Matter

Abstract

The precise origins of postnatal subventricular zone (SVZ) cells are not known. Furthermore, the gliogenic potential of progenitors expressing Dlx genes that migrate ventrodorsally from the ganglionic eminences has not been explored in vivo. Here, we identify the embryonic origins of two distinct populations of postnatal SVZ cells: SVZ border cells, which express Zebrin II, and migratory cells in the central SVZ, which are generally devoid of Zebrin II expression (Staugaitis et al., 2001). Zebrin II is expressed by all cells of the telencephalic primordium, with its expression becoming restricted to astrocytes in the mature telencephalon. As the neuroepithelium folds during corticostriatal sulcus formation (embryonic day 13-15), a wedge of Zebrin II+ cells is created at the presumptive site of the dorsolateral SVZ. At this time, Dlx2-expressing cells and their progeny begin to migrate ventrodorsally along a medial path from the ganglionic eminences. These migratory subpallial cells invade the wedge of Zebrin II+ cells to form the central region of the SVZ. We used a Dlx2/tauLacZ knock-in to perform a short-term lineage analysis of Dlx2-expressing cells throughout SVZ formation and the postnatal peak of gliogenesis. Dlx2/tauLacZ [beta-galactosidase (beta-gal)]-expressing cells populate the central SVZ, whereas Zebrin II-expressing cells form its borders. Furthermore, beta-gal expression demonstrates a lineage relationship between Dlx2-expressing cells and glia residing in the dorsal telencephalon. We propose a model for the formation of the postnatal SVZ and demonstrate that subpallium-derived Dlx2-expressing cells give rise to astrocytes and oligodendrocytes in the white matter and cerebral cortex.

Down-regulation of the axonal polysialic acid–neural cell adhesion molecule expression coincides with the onset of myelination in the human fetal forebrain

“…Expression of PSA-NCAM by various progenitor cell populations in the central nervous system was reported (Gascon et al, 2007;Vitry et al, 2001;Allan and Greer, 1998;Oumesmar et al, 1995), including in vivo expression by glial restricted progenitors in the perinatal mouse subvetricular zone (Marshall and Goldman, 2002). In vitro isolated PSA-NCAM+ cells considered "oligodendrocyte pre-progenitors" (Ben-Hur et al, 1998, Decker et al, 2000 were used to give rise to both glia and neurons upon transplantation, depending on their insertion site in the developing mouse brain (Vitry et al, 2001).…”

Downregulation of Activating Transcription Factor 5 Is Required for Differentiation of Neural Progenitor Cells into Astrocytes

“…For culture studies, we dissected the SVZ from the P1 rat forebrain, dissociated the cells, and immunopanned with an anti-PSA-NCAM antibody. This antigen is expressed on the migratory SVZ cells that give rise to oligodendrocytes, astrocytes, and olfactory interneurons and distinguishes this population from VZ cells, which do not express PSA-NCAM (Marshall and Goldman, 2002). The freshly isolated cells were continuously exposed for 5 d to retroviruses expressing eGFP (control), eGFP-Flag-Azip-ATF5, or Flag-ATF5 and eGFP via a transmembrane apparatus (see Materials and Methods) to achieve a high rate of infection.…”

Analysis of Stem Cell Lineage Progression in the Neonatal Subventricular Zone Identifies EGFR+/NG2− Cells as Transit-Amplifying Precursors

“…The predominant one consists of small, migratory, highly proliferative, Dlx2 immunopositive cells, which include neuronal and glial progenitors [4,5]. The second type is represented by larger, less mobile, and proliferative cells which are direct descendant of embryonic radial glia precursors [5] and after birth will give rise to astroglial stem cells and other cell types [5,6]. Similar to TAPs in the adult SVZ, some Dlx2 immunopositive cells in the neonatal SVZ are EGF receptor (EGFR) immunopositive and divide rapidly [7].…”