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• W2022050898 abstract "Recreating developmental structures in vitro has been a primary challenge for stem cell biologists. Recent studies in Cell Stem Cell (Eiraku et al., 2008Eiraku M. Watanabe K. Matsuo-Takasaki M. Kawada M. Yonemura S. Matsumura M. Wataya T. Nishiyama A. Muguruma K. Sasai Y. Cell Stem Cell. 2008; 3 (this issue): 519-532Abstract Full Text Full Text PDF PubMed Scopus (965) Google Scholar) and Nature (Gaspard et al., 2008Gaspard N. Bouschet T. Hourez R. Dimidschstein J. Naeije G. van den Ameele J. Espuny-Camacho I. Herpoel A. Passante L. Schiffmann S.N. et al.Nature. 2008; 455: 351-357Crossref PubMed Scopus (482) Google Scholar) demonstrate that embryonic stem cells can recapitulate early cortical development, enabling them to generate specific cortical subtypes. Recreating developmental structures in vitro has been a primary challenge for stem cell biologists. Recent studies in Cell Stem Cell (Eiraku et al., 2008Eiraku M. Watanabe K. Matsuo-Takasaki M. Kawada M. Yonemura S. Matsumura M. Wataya T. Nishiyama A. Muguruma K. Sasai Y. Cell Stem Cell. 2008; 3 (this issue): 519-532Abstract Full Text Full Text PDF PubMed Scopus (965) Google Scholar) and Nature (Gaspard et al., 2008Gaspard N. Bouschet T. Hourez R. Dimidschstein J. Naeije G. van den Ameele J. Espuny-Camacho I. Herpoel A. Passante L. Schiffmann S.N. et al.Nature. 2008; 455: 351-357Crossref PubMed Scopus (482) Google Scholar) demonstrate that embryonic stem cells can recapitulate early cortical development, enabling them to generate specific cortical subtypes. Pyramidal cells are the principal excitatory neurons within the cortex, comprising approximately 80% of all neurons within this structure. They are derived from radial glial progenitors within the pallium and are generated in a temporally controlled manner. Within the cortex, progenitors first generate Cajal-Retzius cells, which reside in the most superficial layer, followed by deep layer neurons. Subsequent neurogenesis then generates successively more superficial populations, as cortical neurogenesis proceeds in an inside-out manner. Gaspard et al., 2008Gaspard N. Bouschet T. Hourez R. Dimidschstein J. Naeije G. van den Ameele J. Espuny-Camacho I. Herpoel A. Passante L. Schiffmann S.N. et al.Nature. 2008; 455: 351-357Crossref PubMed Scopus (482) Google Scholar and Eiraku et al., 2008Eiraku M. Watanabe K. Matsuo-Takasaki M. Kawada M. Yonemura S. Matsumura M. Wataya T. Nishiyama A. Muguruma K. Sasai Y. Cell Stem Cell. 2008; 3 (this issue): 519-532Abstract Full Text Full Text PDF PubMed Scopus (965) Google Scholar have both recently demonstrated that mouse embryonic stem cells (ESCs) can be induced to follow a program of neurogenesis similar to that observed in the developing cortex. Birthdating studies by both groups showed that the first neurons generated in their cultures are reelin-positive Cajal-Retzius cells. Next observed were neurons exhibiting deep layer characteristics, followed by the progressive appearance of neurons displaying more superficial layer markers. Both groups demonstrated that the resulting neuronal populations are largely excitatory and glutamatergic—Gaspard et al. through electrophysiology and Eiraku et al. by using calcium imaging. Functionally, both groups observed that ESC-derived pyramidal cells preferentially integrated within cortical rather than striatal tissue in coculture experiments and established either cortico-cortico or cortico-fugal projections when transplanted into neonatal cortex. In a particularly compelling experiment, Gaspard et al. employed a TauEGFP reporter knockin ESC line to demonstrate that the cortical populations they generated tended to project along specific pathways after in vivo transplantation. Notably, these transplant studies suggested that the identity of the cells were primarily visual and limbic deep layer pyramidal neurons, a fate they maintained even when transplanted into the prefrontal region. Similar data from the Sasai group also suggested that the fate of the resulting neurons was determined in vitro prior to transplantation, arguing against a requirement for in vivo cues being required for the establishment of the observed cell identities. Although their findings were similar, there are some key differences between the two studies. Most importantly, the Sasai group differentiated their mouse ESCs through embryoid body (EB) formation (Osakada et al., 2008Osakada F. Ikeda H. Mandai M. Wataya T. Watanabe K. Yoshimura N. Akaike A. Sasai Y. Takahashi M. Nat. Biotechnol. 2008; 26: 215-224Crossref PubMed Scopus (505) Google Scholar, Watanabe et al., 2005Watanabe K. Kamiya D. Nishiyama A. Katayama T. Nozaki S. Kawasaki H. Watanabe Y. Mizuseki K. Sasai Y. Nat. Neurosci. 2005; 8: 288-296Crossref PubMed Scopus (610) Google Scholar), whereas Vanderhaegen's group used an adherent monolayer approach (Ying et al., 2003Ying Q.L. Stavridis M. Griffiths D. Li M. Smith A. Nat. Biotechnol. 2003; 21: 183-186Crossref PubMed Scopus (1154) Google Scholar). EBs form spontaneously when ESCs are cultured in suspension and in the absence of leukemia inhibitory factor. Floating ESCs readily form aggregates that, when neuralized, arrange themselves into structures that have been termed neural rosettes (Lee et al., 2000Lee S.H. Lumelsky N. Studer L. Auerbach J.M. McKay R.D. Nat. Biotechnol. 2000; 18: 675-679Crossref PubMed Scopus (1125) Google Scholar). The simplicity of the methods utilized by Gaspard and colleagues is striking when compared with the Sasai approach. For example, Eiraku et al. took considerable pains to regulate the starting size of their EB aggregate, while Vanderhaegan ostensibly achieved the same end goal by using relatively standard tissue culture methods. Thus, one might conclude that the more convoluted approach used by the Sasai group is overly cumbersome. However, the ability of the Sasai group to prod ESCs to self-organize into a structure that resembles that seen in vivo may provide important insights as to which developmental steps contribute in the determination of precise cortical fates. By using an EB approach, Eiraku et al. were able to analyze not only the end product, but could, in a three-dimensional context, also examine the neural progenitors and immature neurons that gave rise to the more complex structures. In their study, Eiraku et al. employed a FoxG1venus knockin ESC line to serve as a reporter of telencephalic differentiation. By standardizing EB formation through aggregating a defined number of ESCs per well, the authors more than doubled their previous differentiation efficiency to ∼66% (Watanabe et al., 2005Watanabe K. Kamiya D. Nishiyama A. Katayama T. Nozaki S. Kawasaki H. Watanabe Y. Mizuseki K. Sasai Y. Nat. Neurosci. 2005; 8: 288-296Crossref PubMed Scopus (610) Google Scholar). Using these optimized conditions, Eiraku et al. found that most EB aggregates started off as hollow spheres, which resembled developing neuroepithelium. As seen in vivo, the mitotically active cells were confined largely to the lumen of the sphere and expressed CD133 (prominin), characteristic of ventricular zone neural stem cells. Over the course of a week in culture, the spheres collapsed to form smaller spheres termed neural rosettes (Figure 1A). Each rosette maintains the same basic organization of the original sphere, with CD133+ ventricular cells restricted to the luminal surface, nested within sequentially broader domains of Pax6 and Tbr1 expression extending outward. Further mimicking the organization observed in vivo, the earliest born reelin+ Cajal-Retzius cells are found along the outside of these rosettes. Thus, at this stage, after approximately 10 days in culture, the organization of these rosettes is strikingly similar to that observed in the embryonic mouse cortex at E11.5 (Figure 1B). Remarkably, the authors also demonstrate that the same holds true for human ESCs cultured under these conditions, albeit forming at a considerably slower rate than their murine counterparts (Eiraku et al., 2008Eiraku M. Watanabe K. Matsuo-Takasaki M. Kawada M. Yonemura S. Matsumura M. Wataya T. Nishiyama A. Muguruma K. Sasai Y. Cell Stem Cell. 2008; 3 (this issue): 519-532Abstract Full Text Full Text PDF PubMed Scopus (965) Google Scholar). For as yet unknown reasons, EBs, whether mouse or human, fail to recapitulate later aspects of cortical development. Pyramidal neurons, such as layer V Ctip2+/Emx1+ and upper layer Brn2+ neurons that are born later during development were produced in smaller numbers and were randomly distributed in the EBs rather than in an inside/out fashion. Similarly, Gaspard et al. also had better success generating early born neurons (Cajal-Retzius and layer VI and V pyramidal cells) than in generating upper layer pyramidal cells in vitro. Consistent with these findings, in vitro analysis of wild-type cortical stem cells was observed to produce upper layer pyramidal neurons in fewer than deep layer pyramidal neurons (Shen et al., 2006Shen Q. Wang Y. Dimos J.T. Fasano C.A. Phoenix T.N. Lemischka I.R. Ivanova N.B. Stifani S. Morrisey E.E. Temple S. Nat. Neurosci. 2006; 9: 743-751Crossref PubMed Scopus (467) Google Scholar). The failure to date to reproduce later events in cortical neurogenesis in vitro could stem from a number of causes. Eiraku et al. suggested that the problem may be structural, resulting perhaps from the lack of a supportive framework. An alternative possibility may lay in the suggestion that while early pyramidal cell populations are generated by neural stem cells of the ventricular zone (VZ), subsequent populations are derived from the subventricular zone (SVZ) (Leone et al., 2008Leone D.P. Srinivasan K. Chen B. Alcamo E. McConnell S.K. Curr. Opin. Neurobiol. 2008; 18: 28-35Crossref PubMed Scopus (281) Google Scholar, Tarabykin et al., 2001Tarabykin V. Stoykova A. Usman N. Gruss P. Development. 2001; 128: 1983-1993PubMed Google Scholar). Perhaps then the failure of EBs to produce upper layer cortical pyramidal neurons reflects a failure in the in vitro environment to robustly generate an SVZ. In support of this notion, similar problems have been reported in ex vivo brain slices, where proliferation is strongly curtailed (Haydar et al., 2000Haydar T.F. Wang F. Schwartz M.L. Rakic P. J. Neurosci. 2000; 20: 5764-5774Crossref PubMed Google Scholar). Indeed, a recent study has demonstrated that notch signaling is differently utilized in VZ and SVZ progenitors, suggesting fundamental differences between these two progenitor pools (Mizutani et al., 2007Mizutani K. Yoon K. Dang L. Tokunaga A. Gaiano N. Nature. 2007; 449: 351-355Crossref PubMed Scopus (414) Google Scholar). Such a line of reasoning is consistent with the observation that Eiraku et al. did not significantly enrich for Brn2+ upper layer pyramidal cells by sorting for FoxG1Venus+ cells at later time points in the presence of DAPT, an inhibitor of notch signaling. Going forward, it will be necessary to demonstrate that ESC-derived cortical progenitors are capable of generating all pyramidal cell lineages in large numbers and not just the earliest born populations. Moreover, it will be necessary to demonstrate that specific lineages can be preferentially produced and isolated and that the whole process can be accomplished with high efficiency. Clearly, obstacles still exist for the robust generation of upper layer pyramidal cells. There seems little doubt, however, that the ability to recapitulate and monitor events associated with cortical development in vitro provides an invaluable tool for systematically refining culture conditions, ultimately to replicate what Claude Bernard famously termed the “internal milieu.” Self-Organized Formation of Polarized Cortical Tissues from ESCs and Its Active Manipulation by Extrinsic SignalsEiraku et al.Cell Stem CellNovember 06, 2008In BriefHere, we demonstrate self-organized formation of apico-basally polarized cortical tissues from ESCs using an efficient three-dimensional aggregation culture (SFEBq culture). The generated cortical neurons are functional, transplantable, and capable of forming proper long-range connections in vivo and in vitro. The regional identity of the generated pallial tissues can be selectively controlled (into olfactory bulb, rostral and caudal cortices, hem, and choroid plexus) by secreted patterning factors such as Fgf, Wnt, and BMP. 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• W2022050898 title "Cortex Shatters the Glass Ceiling" @default.
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