Proliferation control in neural stem and progenitor cells (original) (raw)

• Neufeld, T. P., de la Cruz, A. F., Johnston, L. A. & Edgar, B. A. Coordination of growth and cell division in the Drosophila wing. Cell 93, 1183–1193 (1998). This paper shows that cell division and cell size/growth are coordinated and that changes in cell division rates are offset by changes in cell size, ensuring constant overall organ size.
  CAS PubMed Google Scholar
• Lanet, E., Gould, A. P. & Maurange, C. Protection of neuronal diversity at the expense of neuronal numbers during nutrient restriction in the Drosophila visual system. Cell Rep. 3, 587–594 (2013).
  CAS PubMed PubMed Central Google Scholar
• Janssens, D. H. et al. Earmuff restricts progenitor cell potential by attenuating the competence to respond to self-renewal factors. Development 141, 1036–1046 (2014).
  CAS PubMed PubMed Central Google Scholar
• Gao, P. et al. Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell 159, 775–788 (2014). This paper provides the most detailed analysis of neuronal lineages in the developing mouse cortex.
  CAS PubMed PubMed Central Google Scholar
• Wang, Y. C. et al. Drosophila intermediate neural progenitors produce lineage-dependent related series of diverse neurons. Development 141, 253–258 (2014).
  PubMed PubMed Central Google Scholar
• Ming, G. L. & Song, H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687–702 (2011).
  CAS PubMed PubMed Central Google Scholar
• Homem, C. C. & Knoblich, J. A. Drosophila neuroblasts: a model for stem cell biology. Development 139, 4297–4310 (2012).
  CAS PubMed Google Scholar
• Chang, K. C., Wang, C. & Wang, H. Balancing self-renewal and differentiation by asymmetric division: Insights from brain tumor suppressors in Drosophila neural stem cells. Bioessays 34, 301–310 (2012).
  PubMed Google Scholar
• Xie, Y. et al. The Drosophila Sp8 transcription factor Buttonhead prevents premature differentiation of intermediate neural progenitors. eLife 3, e03596 (2014).
  PubMed Central Google Scholar
• Zhu, S., Barshow, S., Wildonger, J., Jan, L. Y. & Jan, Y. N. Ets transcription factor Pointed promotes the generation of intermediate neural progenitors in Drosophila larval brains. Proc. Natl Acad. Sci. USA 108, 20615–20620 (2011).
  CAS PubMed PubMed Central Google Scholar
• Komori, H., Xiao, Q., Janssens, D. H., Dou, Y. & Lee, C. Y. Trithorax maintains the functional heterogeneity of neural stem cells through the transcription factor Buttonhead. eLife 3, e03502 (2014).
  PubMed Central Google Scholar
• Xiao, Q., Komori, H. & Lee, C. Y. klumpfuss distinguishes stem cells from progenitor cells during asymmetric neuroblast division. Development 139, 2670–2680 (2012).
  CAS PubMed PubMed Central Google Scholar
• Bowman, S. K. et al. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev. Cell 14, 535–546 (2008).
  CAS PubMed PubMed Central Google Scholar
• Wang, H. et al. Aurora-A acts as a tumor suppressor and regulates self-renewal of Drosophila neuroblasts. Genes Dev. 20, 3453–3463 (2006).
  CAS PubMed PubMed Central Google Scholar
• Almeida, M. S. & Bray, S. J. Regulation of post-embryonic neuroblasts by Drosophila Grainyhead. Mech. Dev. 122, 1282–1293 (2005).
  CAS PubMed Google Scholar
• Berger, C. et al. FACS purification and transcriptome analysis of Drosophila neural stem cells reveals a role for Klumpfuss in self-renewal. Cell Rep. 2, 407–418 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Zacharioudaki, E. & Magadi, S. S. & Delidakis, C. bHLH-O proteins are crucial for Drosophila neuroblast self-renewal and mediate Notch-induced overproliferation. Development 139, 1258–1269 (2012).
  CAS PubMed Google Scholar
• San-Juán, B. P. & Baonza, A. The bHLH factor deadpan is a direct target of Notch signaling and regulates neuroblast self-renewal in Drosophila. Dev. Biol. 352, 70–82 (2011).
  PubMed Google Scholar
• Song, Y. & Lu, B. Regulation of cell growth by Notch signaling and its differential requirement in normal versus tumor-forming stem cells in Drosophila. Genes Dev. 25, 2644–2658 (2011).
  CAS PubMed PubMed Central Google Scholar
• Schweisguth, F. Notch signaling activity. Curr. Biol. 14, R129–R138 (2004).
  CAS PubMed Google Scholar
• Couturier, L., Vodovar, N. & Schweisguth, F. Endocytosis by Numb breaks Notch symmetry at cytokinesis. Nat. Cell Biol. 14, 131–139 (2012).
  CAS PubMed Google Scholar
• Harris, R. E., Pargett, M., Sutcliffe, C., Umulis, D. & Ashe, H. L. Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling. Dev. Cell 20, 72–83 (2011).
  CAS PubMed PubMed Central Google Scholar
• Marchetti, G., Reichardt, I., Knoblich, J. A. & Besse, F. The TRIM-NHL protein Brat promotes axon maintenance by repressing src64B expression. J. Neurosci. 34, 13855–13864 (2014).
  PubMed PubMed Central Google Scholar
• Weng, M., Golden, K. L. & Lee, C. Y. dFezf/Earmuff maintains the restricted developmental potential of intermediate neural progenitors in Drosophila. Dev. Cell 18, 126–135 (2010).
  CAS PubMed PubMed Central Google Scholar
• Koe, C. T. et al. The Brm–HDAC3–Erm repressor complex suppresses dedifferentiation in Drosophila type II neuroblast lineages. eLife 3, e01906 (2014).
  PubMed PubMed Central Google Scholar
• Eroglu, E. et al. SWI/SNF complex prevents lineage reversion and induces temporal patterning in neural stem cells. Cell 156, 1259–1273 (2014).
  CAS PubMed Google Scholar
• Mori, T., Buffo, A. & Gotz, M. The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesis. Curr. Top. Dev. Biol. 69, 67–99 (2005).
  CAS PubMed Google Scholar
• Gotz, M. & Huttner, W. B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell. Biol. 6, 777–788 (2005).
  PubMed Google Scholar
• Noctor, S. C., Martínez-Cerdeño, V., Ivic, L. & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136–144 (2004).
  CAS PubMed Google Scholar
• Pontious, A., Kowalczyk, T., Englund, C. & Hevner, R. F. Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci. 30, 24–32 (2008).
  CAS PubMed Google Scholar
• Gal, J. S. et al. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J. Neurosci. 26, 1045–1056 (2006).
  CAS PubMed PubMed Central Google Scholar
• Stancik, E. K., Navarro-Quiroga, I., Sellke, R. & Haydar, T. F. Heterogeneity in ventricular zone neural precursors contributes to neuronal fate diversity in the postnatal neocortex. J. Neurosci. 30, 7028–7036 (2010).
  CAS PubMed PubMed Central Google Scholar
• Hansen, D. V., Lui, J. H., Parker, P. R. & Kriegstein, A. R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554–561 (2010). This paper describes a novel type of progenitor in the outer SVZ of the developing human cortex — the oRG cell.
  CAS PubMed Google Scholar
• Reillo, I., de Juan Romero, C., García-Cabezas, M. A. & Borrell, V. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb. Cortex 21, 1674–1694 (2011). This paper provides a detailed characterization of oRG cells in the developing ferret brain.
  PubMed Google Scholar
• Kelava, I. et al. Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb. Cortex 22, 469–481 (2012).
  PubMed Google Scholar
• Betizeau, M. et al. Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 80, 442–457 (2013).
  CAS PubMed Google Scholar
• Chenn, A. & McConnell, S. K. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82, 631–641 (1995).
  CAS PubMed Google Scholar
• Zhong, W., Feder, J. N., Jiang, M. M., Jan, L. Y. & Jan, Y. N. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17, 43–53 (1996).
  CAS PubMed Google Scholar
• Kosodo, Y. et al. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J. 23, 2314–2324 (2004).
  CAS PubMed PubMed Central Google Scholar
• Izumi, Y., Ohta, N., Hisata, K., Raabe, T. & Matsuzaki, F. Drosophila Pins-binding protein Mud regulates spindle-polarity coupling and centrosome organization. Nat. Cell Biol. 8, 586–593 (2006).
  CAS PubMed Google Scholar
• Postiglione, M. P. et al. Mouse inscuteable induces apical-basal spindle orientation to facilitate intermediate progenitor generation in the developing neocortex. Neuron 72, 269–284 (2011).
  CAS PubMed PubMed Central Google Scholar
• Morin, X., Jaouen, F. & Durbec, P. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10, 1440–1448 (2007).
  CAS PubMed Google Scholar
• Konno, D. et al. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10, 93–101 (2008).
  CAS PubMed Google Scholar
• Yu, F. et al. A mouse homologue of Drosophila pins can asymmetrically localize and substitute for pins function in Drosophila neuroblasts. J. Cell Sci. 116, 887–896 (2003).
  CAS PubMed Google Scholar
• Mora-Bermudez, F., Matsuzaki, F. & Huttner, W. B. Specific polar subpopulations of astral microtubules control spindle orientation and symmetric neural stem cell division. eLife 3, e02875 (2014).
  PubMed Central Google Scholar
• Shitamukai, A., Konno, D. & Matsuzaki, F. Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J. Neurosci. 31, 3683–3695 (2011).
  CAS PubMed PubMed Central Google Scholar
• Bultje, R. S. et al. Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63, 189–202 (2009).
  CAS PubMed PubMed Central Google Scholar
• Conduit, P. T. & Raff, J. W. Cnn dynamics drive centrosome size asymmetry to ensure daughter centriole retention in Drosophila neuroblasts. Curr. Biol. 20, 2187–2192 (2010).
  CAS PubMed Google Scholar
• Januschke, J., Llamazares, S., Reina, J. & Gonzalez, C. Drosophila neuroblasts retain the daughter centrosome. Nat. Commun. 2, 243 (2011).
  PubMed Google Scholar
• Wang, X. et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947–955 (2009). This paper shows that centrosomes are asymmetrically segregated in neural progenitors of the developing mouse brain.
  CAS PubMed PubMed Central Google Scholar
• Goetz, S. C. & Anderson, K. V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 11, 331–344 (2010).
  CAS PubMed PubMed Central Google Scholar
• Paridaen, J. T., Wilsch-Brauninger, M. & Huttner, W. B. Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155, 333–344 (2013). This paper demonstrates asymmetric inheritance of the primary cilium membrane during neurogenic RG divisions.
  CAS PubMed Google Scholar
• Insolera, R., Bazzi, H., Shao, W., Anderson, K. V. & Shi, S. H. Cortical neurogenesis in the absence of centrioles. Nat. Neurosci. 17, 1528–1535 (2014).
  CAS PubMed PubMed Central Google Scholar
• Pierfelice, T., Alberi, L. & Gaiano, N. Notch in the vertebrate nervous system: an old dog with new tricks. Neuron 69, 840–855 (2011).
  CAS PubMed Google Scholar
• Kawaguchi, D., Yoshimatsu, T., Hozumi, K. & Gotoh, Y. Selection of differentiating cells by different levels of delta-like 1 among neural precursor cells in the developing mouse telencephalon. Development 135, 3849–3858 (2008).
  CAS PubMed Google Scholar
• Yoon, K. J. et al. Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58, 519–531 (2008).
  CAS PubMed Google Scholar
• Dong, Z., Yang, N., Yeo, S. Y., Chitnis, A. & Guo, S. Intralineage directional Notch signaling regulates self-renewal and differentiation of asymmetrically dividing radial glia. Neuron 74, 65–78 (2012).
  CAS PubMed PubMed Central Google Scholar
• Nelson, B. R., Hodge, R. D., Bedogni, F. & Hevner, R. F. Dynamic interactions between intermediate neurogenic progenitors and radial glia in embryonic mouse neocortex: potential role in Dll1-Notch signaling. J. Neurosci. 33, 9122–9139 (2013).
  CAS PubMed PubMed Central Google Scholar
• Ohtsuka, T., Sakamoto, M., Guillemot, F. & Kageyama, R. Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. J. Biol. Chem. 276, 30467–30474 (2001).
  CAS PubMed Google Scholar
• Mizutani, K., Yoon, K., Dang, L., Tokunaga, A. & Gaiano, N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449, 351–355 (2007).
  CAS PubMed Google Scholar
• Shimojo, H., Ohtsuka, T. & Kageyama, R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58, 52–64 (2008). This paper shows how oscillations in Notch signalling regulate the expression of proneural genes and regulate cell fate decisions.
  CAS PubMed Google Scholar
• Baek, J. H., Hatakeyama, J., Sakamoto, S., Ohtsuka, T. & Kageyama, R. Persistent and high levels of Hes1 expression regulate boundary formation in the developing central nervous system. Development 133, 2467–2476 (2006).
  CAS PubMed Google Scholar
• Calegari, F., Haubensak, W., Haffner, C. & Huttner, W. B. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J. Neurosci. 25, 6533–6538 (2005).
  CAS PubMed PubMed Central Google Scholar
• Arai, Y. et al. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2, 154 (2011).
  PubMed Google Scholar
• Calegari, F. & Huttner, W. B. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J. Cell Sci. 116, 4947–4955 (2003).
  CAS PubMed Google Scholar
• Pilaz, L. J. et al. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc. Natl Acad. Sci. USA 106, 21924–21929 (2009).
  CAS PubMed PubMed Central Google Scholar
• Lange, C., Huttner, W. B. & Calegari, F. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5, 320–331 (2009).
  CAS PubMed Google Scholar
• Takahashi, T., Nowakowski, R. S. & Caviness, V. S. J. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15, 6046–6057 (1995).
  CAS PubMed PubMed Central Google Scholar
• Kohwi, M. & Doe, C. Q. Temporal fate specification and neural progenitor competence during development. Nat. Rev. Neurosci. 14, 823–838 (2013).
  PubMed PubMed Central Google Scholar
• Britton, J. S. & Edgar, B. A. Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125, 2149–2158 (1998).
  CAS PubMed Google Scholar
• Speder, P. & Brand, A. H. Gap junction proteins in the blood–brain barrier control nutrient-dependent reactivation of Drosophila neural stem cells. Dev. Cell. 30, 309–321 (2014).
  CAS PubMed PubMed Central Google Scholar
• Sousa-Nunes, R., Yee, L. L. & Gould, A. P. Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471, 508–512 (2011). This paper shows that D. melanogaster NSPCs in the embryo-to-larva transition exit from quiescence in response to larval feeding. Larval feeding is sensed by the fat body, which then stimulates the production of insulin-like peptides by glial cells that in turn activate the TOR pathway in neuroblasts, inducing neuroblast growth and proliferation.
  CAS PubMed PubMed Central Google Scholar
• Chell, J. M. & Brand, A. H. Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143, 1161–1173 (2010). Along with reference 72, this paper shows that in response to nutrition a population of glial cells produces insulin-like peptides that are received by neuroblasts where they activate the TOR pathway, drive neuroblast growth and exit from quiescence.
  CAS PubMed PubMed Central Google Scholar
• Egger, B., Gold, K. S. & Brand, A. H. Regulating the balance between symmetric and asymmetric stem cell division in the developing brain. Fly 5, 237–241 (2011).
  CAS PubMed Google Scholar
• Liu, J., Speder, P. & Brand, A. H. Control of brain development and homeostasis by local and systemic insulin signalling. Diabetes Obes. Metab. 16, S16–S20 (2014).
  Google Scholar
• Lehtinen, M. K. et al. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69, 893–905 (2011).
  CAS PubMed PubMed Central Google Scholar
• Popken, G. J. et al. In vivo effects of insulin-like growth factor-I (IGF-I) on prenatal and early postnatal development of the central nervous system. Eur. J. Neurosci. 19, 2056–2068 (2004).
  PubMed Google Scholar
• Brody, T. & Odenwald, W. F. Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev. Biol. 226, 34–44 (2000).
  CAS PubMed Google Scholar
• Isshiki, T., Pearson, B., Holbrook, S. & Doe, C. Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511–521 (2001).
  CAS PubMed Google Scholar
• Kambadur, R. et al. Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev. 12, 246–260 (1998).
  CAS PubMed PubMed Central Google Scholar
• Pearson, B. J. & Doe, C. Q. Regulation of neuroblast competence in Drosophila. Nature 425, 624–628 (2003).
  CAS PubMed Google Scholar
• Grosskortenhaus, R., Robinson, K. J. & Doe, C. Q. Pdm and Castor specify late-born motor neuron identity in the NEUROBLAST7-1 lineage. Genes Dev. 20, 2618–2627 (2006).
  CAS PubMed PubMed Central Google Scholar
• Maurange, C., Cheng, L. & Gould, A. P. Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 133, 891–902 (2008).
  CAS PubMed Google Scholar
• Chai, P. C., Liu, Z., Chia, W. & Cai, Y. Hedgehog signaling acts with the temporal cascade to promote neuroblast cell cycle exit. PLoS Biol. 11, e1001494 (2013).
  CAS PubMed PubMed Central Google Scholar
• Homem, C. C. et al. Ecdysone and mediator change energy metabolism to terminate proliferation in Drosophila neural stem cells. Cell 158, 874–888 (2014). This paper shows that cell growth in D. melanogaster NSPCs is coupled with cell lifespan, with larger cells being longer-lived and proliferative. Cell growth and lifespan are dependent on the metabolic profile of these NSPCs, with growing, undifferentiated NSPCs relying on glycolysis and non-growing, differentiating NSPCs being more dependent on oxidative phosphorylation.
  CAS PubMed Google Scholar
• Siegrist, S. E., Haque, N. S., Chen, C. H., Hay, B. A. & Hariharan, I. K. Inactivation of both foxo and reaper promotes long-term adult neurogenesis in Drosophila. Curr. Biol. 20, 643–648 (2010).
  CAS PubMed PubMed Central Google Scholar
• White, K. et al. Genetic control of programmed cell death in Drosophila. Science 264, 667–683 (1994).
  Google Scholar
• Bello, B. C., Hirth, F. & Gould, A. P. A pulse of the Drosophila Hox protein Abdominal-A schedules the end of neural proliferation via neuroblast apoptosis. Neuron 37, 209–219 (2003).
  CAS PubMed Google Scholar
• Arya, R., Sarkissian, T., Tan, Y. & White, K. Neural stem cell progeny regulate stem cell death in a Notch and Hox dependent manner. Cell Death Differ. 22, 1378–1387 (2015).
  CAS PubMed PubMed Central Google Scholar
• Cenci, C. & Gould, A. P. Drosophila Grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts. Development 132, 3835–3845 (2005).
  CAS PubMed Google Scholar
• Bayraktar, O. A. & Doe, C. Q. Combinatorial temporal patterning in progenitors expands neural diversity. Nature 498, 449–455 (2013). This paper shows that D. melanogaster intermediate progenitor cells undergo a specific sequence of transcriptional profiles, which is required for the generation of different neuronal/glial progeny over time.
  CAS PubMed PubMed Central Google Scholar
• Fog, C. K., Galli, G. G. & Lund, A. H. PRDM proteins: important players in differentiation and disease. Bioessays 34, 50–60 (2012).
  CAS PubMed Google Scholar
• Pinheiro, I. et al. Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 150, 948–960 (2012).
  CAS PubMed Google Scholar
• Suzuki, T., Kaido, M., Takayama, R. & Sato, M. A temporal mechanism that produces neuronal diversity in the Drosophila visual center. Dev. Biol. 380, 12–24 (2013).
  CAS PubMed Google Scholar
• Li, X. et al. Temporal patterning of Drosophila medulla neuroblasts controls neural fates. Nature 498, 456–462 (2013). This paper shows that D. melanogaster OL medulla neuroblasts sequentially express a series of transcription factors that, together with Notch, generate a variety of neuronal progeny.
  CAS PubMed PubMed Central Google Scholar
• Frantz, G. D. & McConnell, S. K. Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17, 55–61 (1996).
  CAS PubMed Google Scholar
• Desai, A. R. & McConnell, S. K. Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127, 2863–2872 (2000).
  CAS PubMed Google Scholar
• Gaspard, N. et al. An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351–357 (2008).
  CAS PubMed Google Scholar
• Shen, Q. et al. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat. Neurosci. 9, 743–751 (2006).
  CAS PubMed Google Scholar
• Eiraku, M. et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519–532 (2008).
  CAS PubMed Google Scholar
• Franco, S. J. et al. Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337, 746–749 (2012).
  CAS PubMed PubMed Central Google Scholar
• Guo, C. et al. Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 80, 1167–1174 (2013).
  CAS PubMed Google Scholar
• Götz, M., Stoykova, A. & Gruss, P. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21, 1031–1044 (1998).
  PubMed Google Scholar
• Quaggin, S. E., Heuvel, G. B., Golden, K., Bodmer, R. & Igarashi, P. Primary structure, neural-specific expression, and chromosomal localization of Cux-2, a second murine homeobox gene related to Drosophila cut. J. Biol. Chem. 271, 22624–22634 (1996).
  CAS PubMed Google Scholar
• Naka, H., Nakamura, S., Shimazaki, T. & Okano, H. Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat. Neurosci. 11, 1014–1023 (2008).
  CAS PubMed Google Scholar
• Alsio, J. M., Tarchini, B., Cayouette, M. & Livesey, F. J. Ikaros promotes early-born neuronal fates in the cerebral cortex. Proc. Natl Acad. Sci. USA 110, E716–E725 (2013).
  CAS PubMed PubMed Central Google Scholar
• Mattar, P., Ericson, J., Blackshaw, S. & Cayouette, M. A conserved regulatory logic controls temporal identity in mouse neural progenitors. Neuron 85, 497–504 (2015).
  CAS PubMed PubMed Central Google Scholar
• Culican, S. M., Baumrind, N. L., Yamamoto, M. & Pearlman, A. L. Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J. Neurosci. 10, 684–692 (1990).
  CAS PubMed PubMed Central Google Scholar
• Rowitch, D. H. & Kriegstein, A. R. Developmental genetics of vertebrate glial-cell specification. Nature 468, 214–222 (2010).
  CAS PubMed Google Scholar
• Fan, G. et al. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132, 3345–3356 (2005).
  CAS PubMed Google Scholar
• Chambers, C. B. et al. Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128, 689–702 (2001).
  CAS PubMed Google Scholar
• Namihira, M. et al. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev. Cell 16, 245–255 (2009).
  CAS PubMed Google Scholar
• Hirabayashi, Y. et al. Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63, 600–613 (2009).
  CAS PubMed Google Scholar
• Barnabe-Heider, F. et al. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48, 253–265 (2005).
  CAS PubMed Google Scholar
• Homem, C. C., Reichardt, I., Berger, C., Lendl, T. & Knoblich, J. A. Long-term live cell imaging and automated 4D analysis of neuroblast lineages. PLoS ONE 8, e79588 (2013).
  CAS PubMed PubMed Central Google Scholar
• Truman, J. W. & Bate, M. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 125, 145–157 (1988).
  CAS PubMed Google Scholar
• Layalle, S., Arquier, N. & Leopold, P. The TOR pathway couples nutrition and developmental timing in Drosophila. Dev. Cell 15, 568–577 (2008).
  CAS PubMed Google Scholar
• Colombani, J., Andersen, D. S. & Leopold, P. Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 336, 582–585 (2012).
  CAS PubMed Google Scholar
• Garelli, A., Gontijo, A. M., Miguela, V., Caparros, E. & Dominguez, M. Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science 336, 579–582 (2012).
  CAS PubMed Google Scholar
• Frerman, F. E. & Goodman, S. I. Deficiency of electron transfer flavoprotein or electron transfer flavoprotein:ubiquinone oxidoreductase in glutaric acidemia type II fibroblasts. Proc. Natl Acad. Sci. USA 82, 4517–4520 (1985).
  CAS PubMed PubMed Central Google Scholar
• Knobloch, M. et al. Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis. Nature 493, 226–230 (2013). This paper shows that mouse adult neurogenesis requires de novo lipogenesis, thus demonstrating that there is a functional coupling between the regulation of lipid metabolism and adult NSPC proliferation.
  CAS PubMed Google Scholar
• McIntyre, R. E. et al. Disruption of mouse Cenpj, a regulator of centriole biogenesis, phenocopies Seckel syndrome. PLoS Genet. 8, e1003022 (2012).
  CAS PubMed PubMed Central Google Scholar
• Martin, C. A. et al. Mutations in PLK4, encoding a master regulator of centriole biogenesis, cause microcephaly, growth failure and retinopathy. Nat. Genet. 46, 1283–1292 (2014).
  CAS PubMed PubMed Central Google Scholar
• Buchman, J. J. et al. Cdk5rap2 interacts with pericentrin to maintain the neural progenitor pool in the developing neocortex. Neuron 66, 386–402 (2010).
  CAS PubMed Google Scholar
• Barrera, J. A. et al. CDK5RAP2 regulates centriole engagement and cohesion in mice. Dev. Cell 18, 913–926 (2010).
  CAS PubMed PubMed Central Google Scholar
• Fish, J. L., Kosodo, Y., Enard, W., Paabo, S. & Huttner, W. B. Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl Acad. Sci. USA 103, 10438–10443 (2006).
  CAS PubMed PubMed Central Google Scholar
• Rujano, M. A., Sanchez-Pulido, L., Pennetier, C., le Dez, G. & Basto, R. The microcephaly protein Asp regulates neuroepithelium morphogenesis by controlling the spatial distribution of myosin II. Nat. Cell Biol. 15, 1294–1306 (2013).
  CAS PubMed Google Scholar
• Buchman, J. J., Durak, O. & Tsai, L. H. ASPM regulates Wnt signaling pathway activity in the developing brain. Genes Dev. 25, 1909–1914 (2011).
  CAS PubMed PubMed Central Google Scholar
• Chen, J. F. et al. Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size. Nat. Commun. 5, 3885 (2014).
  CAS PubMed Google Scholar
• Gruber, R. et al. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1–Cdc25 pathway. Nat. Cell Biol. 13, 1325–1334 (2011).
  CAS PubMed Google Scholar
• Varmark, H. et al. Asterless is a centriolar protein required for centrosome function and embryo development in Drosophila. Curr. Biol. 17, 1735–1745 (2007).
  CAS PubMed Google Scholar
• Dzhindzhev, N. S. et al. Asterless is a scaffold for the onset of centriole assembly. Nature 467, 714–718 (2010).
  CAS PubMed Google Scholar
• Giansanti, M. G., Gatti, M. & Bonaccorsi, S. The role of centrosomes and astral microtubules during asymmetric division of Drosophila neuroblasts. Development 128, 1137–1145 (2001).
  CAS PubMed Google Scholar
• Gilmore, E. C. & Walsh, C. A. Genetic causes of microcephaly and lessons for neuronal development. Wiley Interdiscip. Rev. Dev. Biol. 2, 461–478 (2013).
  CAS PubMed Google Scholar
• Malatesta, P., Hartfuss, E. & Gotz, M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–5263 (2000).
  CAS PubMed Google Scholar
• Feng, Y. & Walsh, C. A. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44, 279–293 (2004).
  CAS PubMed Google Scholar
• Lancaster, M. A. et al. Cerebral organoids model human brain development and microcephaly. Nature 501, 373–379 (2013). This paper describes cerebral organoids, an ESC-derived three-dimensional model of human brain development.
  CAS PubMed Google Scholar
• Groszer, M. et al. Negative regulation of neural stem/progenitor cell proliferation by the PTEN tumor suppressor gene in vivo. Science 294, 2186–2189 (2001).
  CAS PubMed Google Scholar
• D'Gama, A. M. et al. Mammalian target of rapamycin pathway mutations cause hemimegalencephaly and focal cortical dysplasia. Ann. Neurol. 77, 720–725 (2015).
  CAS PubMed PubMed Central Google Scholar
• Poduri, A. et al. Somatic activation of AKT3 causes hemispheric developmental brain malformations. Neuron 74, 41–48 (2012).
  CAS PubMed PubMed Central Google Scholar
• Mirzaa, G. M. & Poduri, A. Megalencephaly and hemimegalencephaly: breakthroughs in molecular etiology. Am. J. Med. Genet. C. Semin. Med. Genet. 166, 156–172 (2014).
  CAS Google Scholar
• Marsh, D. J. et al. Germline mutations in PTEN are present in Bannayan–Zonana syndrome. Nat. Genet. 16, 333–334 (1997).
  CAS PubMed Google Scholar
• Mirzaa, G. M. et al. De novo CCND2 mutations leading to stabilization of cyclin D2 cause megalencephaly-polymicrogyria-polydactyly-hydrocephalus syndrome. Nat. Genet. 46, 510–515 (2014).
  CAS PubMed PubMed Central Google Scholar
• Spaeth, J. M., Kim, N. H. & Boyer, T. G. Mediator and human disease. Semin. Cell. Dev. Biol. 22, 776–787 (2011).
  CAS PubMed PubMed Central Google Scholar
• Tsurusaki, Y. et al. Coffin–Siris syndrome is a SWI/SNF complex disorder. Clin. Genet. 85, 548–554 (2014).
  CAS PubMed Google Scholar
• Fietz, S. A. et al. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 13, 690–699 (2010). This paper characterizes oRG cells in the human and ferret cortex, and demonstrates the role of integrin signalling in oRG cell expansion.
  CAS PubMed Google Scholar
• Wilkinson, R. & Wiedenheft, B. A. CRISPR method for genome engineering. F1000Prime Rep. 6, 3 (2014).
  Google Scholar
• Kadoshima, T. et al. Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex. Proc. Natl Acad. Sci. USA 110, 20284–20289 (2013).
  CAS PubMed PubMed Central Google Scholar
• Smart, I. H., Dehay, C., Giroud, P., Berland, M. & Kennedy, H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 12, 37–53 (2002).
  PubMed Google Scholar
• Wang, X., Tsai, J. W., LaMonica, B. & Kriegstein, A. R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 14, 555–561 (2011).
  CAS PubMed PubMed Central Google Scholar
• Lui, J. H., Hansen, D. V. & Kriegstein, A. R. Development and evolution of the human neocortex. Cell 146, 18–36 (2011).
  CAS PubMed PubMed Central Google Scholar
• Lui, J. H. et al. Radial glia require PDGFD–PDGFRβ signalling in human but not mouse neocortex. Nature 515, 264–268 (2014).
  CAS PubMed PubMed Central Google Scholar
• Hietakangas, V. & Cohen, S. M. Regulation of tissue growth through nutrient sensing. Annu. Rev. Genet. 43, 389–410 (2009).
  CAS PubMed Google Scholar
• Gruenwald, P. Chronic fetal distress and placental insufficiency. Biol. Neonat. 5, 215–265 (1963).
  CAS PubMed Google Scholar
• Cheng, L. Y. et al. Anaplastic lymphoma kinase spares organ growth during nutrient restriction in Drosophila. Cell 146, 435–447 (2011).
  CAS PubMed Google Scholar
• Loren, C. E. et al. Identification and characterization of DAlk: a novel Drosophila melanogaster RTK which drives ERK activation in vivo. Genes Cells 6, 531–544 (2001).
  CAS PubMed PubMed Central Google Scholar
• Jackson, A. P. et al. Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 71, 136–142 (2002).
  CAS PubMed PubMed Central Google Scholar
• Lin, S. Y. & Elledge, S. J. Multiple tumor suppressor pathways negatively regulate telomerase. Cell 113, 881–889 (2003).
  CAS PubMed Google Scholar
• Brunk, K. et al. Microcephalin coordinates mitosis in the syncytial Drosophila embryo. J. Cell Sci. 120, 3578–3588 (2007).
  CAS PubMed Google Scholar
• Rickmyre, J. L. et al. The Drosophila homolog of MCPH1, a human microcephaly gene, is required for genomic stability in the early embryo. J. Cell Sci. 120, 3565–3577 (2007).
  CAS PubMed Google Scholar
• Bilguvar, K. et al. Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature 467, 207–210 (2010).
  CAS PubMed PubMed Central Google Scholar
• Nicholas, A. K. et al. WDR62 is associated with the spindle pole and is mutated in human microcephaly. Nat. Genet. 42, 1010–1014 (2010).
  CAS PubMed PubMed Central Google Scholar
• Yu, T. W. et al. Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture. Nat. Genet. 42, 1015–1020 (2010).
  CAS PubMed PubMed Central Google Scholar
• Bond, J. et al. A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat. Genet. 37, 353–355 (2005).
  CAS PubMed Google Scholar
• Guernsey, D. L. et al. Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4. Am. J. Hum. Genet. 87, 40–51 (2010).
  CAS PubMed PubMed Central Google Scholar
• Bond, J. et al. ASPM is a major determinant of cerebral cortical size. Nat. Genet. 32, 316–320 (2002).
  CAS PubMed Google Scholar
• Kumar, A., Girimaji, S. C., Duvvari, M. R. & Blanton, S. H. Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly. Am. J. Hum. Genet. 84, 286–290 (2009).
  CAS PubMed PubMed Central Google Scholar
• Stevens, N. R., Dobbelaere, J., Brunk, K., Franz, A. & Raff, J. W. Drosophila Ana2 is a conserved centriole duplication factor. J. Cell Biol. 188, 313–323 (2010).
  CAS PubMed PubMed Central Google Scholar
• Hussain, M. S. et al. A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function. Am. J. Hum. Genet. 90, 871–878 (2012).
  CAS PubMed PubMed Central Google Scholar
• Lin, Y. C. et al. Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. EMBO J. 32, 1141–1154 (2013).
  CAS PubMed PubMed Central Google Scholar
• Sir, J. H. et al. A primary microcephaly protein complex forms a ring around parental centrioles. Nat. Genet. 43, 1147–1153 (2011).
  CAS PubMed PubMed Central Google Scholar