The evolution of basal progenitors in the developing non-mammalian brain.

Tadashi Nomura,Chiaki Ohtaka-Maruyama,Yoshio Wakamatsu,Katsuhiko Ono,Yasunori Murakami,Federico Calegari,Hitoshi Gotoh,Wataru Yamashita,Kunihiro Suzuki

doi:10.1242/dev.127100

Abstract

The amplification of distinct neural stem/progenitor cell subtypes during embryogenesis is essential for the intricate brain structures present in various vertebrate species. For example, in both mammals and birds, proliferative neuronal progenitors transiently appear on the basal side of the ventricular zone of the telencephalon (basal progenitors), where they contribute to the enlargement of the neocortex and its homologous structures. In placental mammals, this proliferative cell population can be subdivided into several groups that include Tbr2+ intermediate progenitors and basal radial glial cells (bRGs). Here, we report that basal progenitors in the developing avian pallium show unique morphological and molecular characteristics that resemble the characteristics of bRGs, a progenitor population that is abundant in gyrencephalic mammalian neocortex. Manipulation of LGN (Leu-Gly-Asn repeat-enriched protein) and Cdk4/cyclin D1, both essential regulators of neural progenitor dynamics, revealed that basal progenitors and Tbr2+ cells are distinct cell lineages in the developing avian telencephalon. Furthermore, we identified a small population of subapical mitotic cells in the developing brains of a wide variety of amniotes and amphibians. Our results suggest that unique progenitor subtypes are amplified in mammalian and avian lineages by modifying common mechanisms of neural stem/progenitor regulation during amniote brain evolution.

Highlights

IntroductionRecent studies have described basal radial glial cells (bRGs), a unique basal progenitors (BPs) subtype that maintains radial glial features within the developing mammalian neocortex (Fietz et al, 2010; Hansen et al, 2010; Reillo et al, 2011; Betizeau et al, 2013; Borrell and Götz, 2014)
basal progenitors (BPs) and Tbr2+ cells are distinct populations in the developing chicken pallium Previous studies have shown that basal mitotic cells are present in the developing avian pallium (Cheung et al, 2007; AbdelMannan et al, 2008; Charvet et al, 2009; Striedter and Charvet, 2009), which contains a region that is thought to be homologous to the mammalian neocortex (Puelles, 2001; Striedter, 2005) (Fig. 1A,B)
62.49% of EdU+ cells were Sox2+ and 37.51% were Sox2− [the mean of dorsal pallium (DP) and dorsal ventricular ridge (DVR)], suggesting that the former comprised ‘neural’ progenitors, whereas the latter were non-neuronal in lineage (Fig. 1D)

Summary

Introduction

Recent studies have described basal radial glial cells (bRGs), a unique BP subtype that maintains radial glial features within the developing mammalian neocortex (Fietz et al, 2010; Hansen et al, 2010; Reillo et al, 2011; Betizeau et al, 2013; Borrell and Götz, 2014). A small population of basal/subapical mitotic cells was detected in the developing brains of a wide variety of tetrapods. These results suggest that BPs are amplified in mammalian and avian lineages by modifying common mechanisms of neural stem/ progenitor regulation during amniote brain evolution

Methods

Results

Conclusion