Temporal fate specification and neural progenitor competence during development

The vast diversity of neurons and glia of the CNS is generated from a small, heterogeneous population of progenitors that undergo transcriptional changes during development to sequentially specify distinct cell fates. Guided by cell-intrinsic and -extrinsic cues, invertebrate and mammalian neural progenitors carefully regulate when and how many of each cell type is produced, enabling the formation of functional neural circuits. Emerging evidence indicates that neural progenitors also undergo changes in global chromatin architecture, thereby restricting when a particular cell type can be generated. Studies of temporal-identity specification and progenitor competence can provide insight into how we could use neural progenitors to more effectively generate specific cell types for brain repair.

[1]  Constance L. Cepko,et al.  A common progenitor for neurons and glia persists in rat retina late in development , 1987, Nature.

[2]  C. Holt,et al.  Cellular determination in the xenopus retina is independent of lineage and birth date , 1988, Neuron.

[3]  S. Mcconnell,et al.  Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  R. Wetts,et al.  Multipotent precursors can give rise to all major cell types of the frog retina. , 1988, Science.

[5]  C. Cepko,et al.  Lineage-independent determination of cell type in the embryonic mouse retina , 1990, Neuron.

[6]  M. Raff,et al.  Rod photoreceptor development in vitro: Intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina , 1990, Neuron.

[7]  S. Mcconnell,et al.  Cell cycle dependence of laminar determination in developing neocortex , 1991 .

[8]  D. Altshuler,et al.  A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro. , 1992, Development.

[9]  M. Raff,et al.  Diffusible rod-promoting signals in the developing rat retina. , 1992, Development.

[10]  C. Doe,et al.  Identification and cell lineage of individual neural precursors in the Drosophila CNS , 1993, Trends in Neurosciences.

[11]  C. Cepko,et al.  Clonal analysis in the chicken retina reveals tangential dispersion of clonally related cells. , 1994, Developmental biology.

[12]  A. Joyner,et al.  Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. , 1994, Development.

[13]  C. Doe,et al.  New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system , 1995, Mechanisms of Development.

[14]  C. Doe,et al.  Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca. , 1995, Development.

[15]  C Q Doe,et al.  The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. , 1996, Developmental biology.

[16]  C. Rickert,et al.  The Embryonic Central Nervous System Lineages ofDrosophila melanogaster , 1996 .

[17]  C. Doe,et al.  Numb Antagonizes Notch Signaling to Specify Sibling Neuron Cell Fates , 1996, Neuron.

[18]  S. Mcconnell,et al.  Restriction of Late Cerebral Cortical Progenitors to an Upper-Layer Fate , 1996, Neuron.

[19]  M. Greenberg,et al.  Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. , 1997, Science.

[20]  C. Rickert,et al.  The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. , 1996, Developmental biology.

[21]  C. Doe,et al.  Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. , 1998, Development.

[22]  M. Götz,et al.  Pax6 Controls Radial Glia Differentiation in the Cerebral Cortex , 1998, Neuron.

[23]  C. Ware,et al.  Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Nagle,et al.  Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. , 1998, Genes & development.

[25]  S. Wiese,et al.  Developmental Requirement of gp130 Signaling in Neuronal Survival and Astrocyte Differentiation , 1999, The Journal of Neuroscience.

[26]  Daniel A. Lim,et al.  Subventricular Zone Astrocytes Are Neural Stem Cells in the Adult Mammalian Brain , 1999, Cell.

[27]  C Q Doe,et al.  Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. , 1999, Development.

[28]  C. Cepko,et al.  Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. , 1999, Development.

[29]  T. Brody,et al.  Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. , 2000, Developmental biology.

[30]  S. Mcconnell,et al.  Progressive restriction in fate potential by neural progenitors during cerebral cortical development. , 2000, Development.

[31]  T. Jessell Neuronal specification in the spinal cord: inductive signals and transcriptional codes , 2000, Nature Reviews Genetics.

[32]  C. Cepko,et al.  Late Retinal Progenitor Cells Show Intrinsic Limitations in the Production of Cell Types and the Kinetics of Opsin Synthesis , 2000, The Journal of Neuroscience.

[33]  F. J. Livesey,et al.  Vertebrate neural cell-fate determination: Lessons from the retina , 2001, Nature Reviews Neuroscience.

[34]  V. Tarabykin,et al.  Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. , 2001, Development.

[35]  Bret J. Pearson,et al.  Drosophila Neuroblasts Sequentially Express Transcription Factors which Specify the Temporal Identity of Their Neuronal Progeny , 2001, Cell.

[36]  A. Ghosh,et al.  Sequential specification of neurons and glia by developmentally regulated extracellular factors. , 2001, Development.

[37]  滝沢 琢己 DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain , 2002 .

[38]  T. Takizawa,et al.  Cardiotrophin-like cytokine induces astrocyte differentiation of fetal neuroepithelial cells via activation of STAT3. , 2002, Cytokine.

[39]  M. Lehmann,et al.  The Drosophila Pipsqueak protein defines a new family of helix-turn-helix DNA-binding proteins , 2002, Development Genes and Evolution.

[40]  J. Urban,et al.  Hunchback is required for the specification of the early sublineage of neuroblast 7-3 in the Drosophila central nervous system. , 2002, Development.

[41]  Tetsuo Noda,et al.  Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. , 2002, Genes & development.

[42]  Marie-Christine Chaboissier,et al.  The Sox9 transcription factor determines glial fate choice in the developing spinal cord. , 2003, Genes & development.

[43]  Bret J. Pearson,et al.  Regulation of neuroblast competence in Drosophila , 2003, Nature.

[44]  M. Greenberg,et al.  Basic Helix-Loop-Helix Factors in Cortical Development , 2003, Neuron.

[45]  R. Bodmer,et al.  Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. , 2004, Cerebral cortex.

[46]  C. Walsh,et al.  Expression of Cux‐1 and Cux‐2 in the subventricular zone and upper layers II–IV of the cerebral cortex , 2004, The Journal of comparative neurology.

[47]  David Perret,et al.  Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[48]  A. Kriegstein,et al.  Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases , 2004, Nature Neuroscience.

[49]  Bret J. Pearson,et al.  Specification of temporal identity in the developing nervous system. , 2004, Annual review of cell and developmental biology.

[50]  Sara G. Becker-Catania,et al.  A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis , 2005, Nature Neuroscience.

[51]  D. Kaplan,et al.  Evidence that Embryonic Neurons Regulate the Onset of Cortical Gliogenesis via Cardiotrophin-1 , 2005, Neuron.

[52]  Masataka Okabe,et al.  seven-up Controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. , 2005, Developmental cell.

[53]  Bret J. Pearson,et al.  Regulation of temporal identity transitions in Drosophila neuroblasts. , 2005, Developmental cell.

[54]  Guoping Fan,et al.  DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling , 2005, Development.

[55]  A. Gould,et al.  Drosophila Grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts , 2005, Development.

[56]  S. Mcconnell,et al.  Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[57]  H. Horvitz,et al.  The let-7 MicroRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. , 2005, Developmental cell.

[58]  N. Šestan,et al.  Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Urban,et al.  Connecting Temporal Identity to Mitosis: The Regulation of Hunchback in Drosophila Neuroblast Lineages , 2006, Cell cycle.

[60]  Hiroyuki Nakamura,et al.  Brain-Derived Neurotrophic Factor Participates in Determination of Neuronal Laminar Fate in the Developing Mouse Cerebral Cortex , 2006, The Journal of Neuroscience.

[61]  Chris Q Doe,et al.  Regulation of neuroblast competence: multiple temporal identity factors specify distinct neuronal fates within a single early competence window. , 2006, Genes & development.

[62]  John T. Dimos,et al.  The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells , 2006, Nature Neuroscience.

[63]  Chris Q Doe,et al.  Regulation of spindle orientation and neural stem cell fate in the Drosophila optic lobe , 2007, Neural Development.

[64]  Tzumin Lee,et al.  Gradients of the Drosophila Chinmo BTB-Zinc Finger Protein Govern Neuronal Temporal Identity , 2006, Cell.

[65]  Chris Q Doe,et al.  Pdm and Castor specify late-born motor neuron identity in the NB7-1 lineage. , 2006, Genes & development.

[66]  Georg Vogler,et al.  Timing of identity: spatiotemporal regulation of hunchback in neuroblast lineages of Drosophila by Seven-up and Prospero , 2006, Development.

[67]  C. Cepko,et al.  Temporal order of bipolar cell genesis in the neural retina , 2008, Neural Development.

[68]  P. Arlotta,et al.  Neuronal subtype specification in the cerebral cortex , 2007, Nature Reviews Neuroscience.

[69]  H. Reichert,et al.  Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development , 2008, Neural Development.

[70]  F. Miller,et al.  Timing Is Everything: Making Neurons versus Glia in the Developing Cortex , 2007, Neuron.

[71]  E. Moss,et al.  Heterochronic Genes and the Nature of Developmental Time , 2007, Current Biology.

[72]  F. Guillemot Cell fate specification in the mammalian telencephalon , 2007, Progress in Neurobiology.

[73]  O. Britanova,et al.  Satb2 Is a Postmitotic Determinant for Upper-Layer Neuron Specification in the Neocortex , 2008, Neuron.

[74]  Makoto Sato,et al.  Drosophila optic lobe neuroblasts triggered by a wave of proneural gene expression that is negatively regulated by JAK/STAT , 2008, Development.

[75]  Ying Chen,et al.  Progeny , 2008 .

[76]  A. Kriegstein,et al.  Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis , 2008, The Journal of comparative neurology.

[77]  T. Shimazaki,et al.  Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development , 2008, Nature Neuroscience.

[78]  P. Arlotta,et al.  Ctip2 Controls the Differentiation of Medium Spiny Neurons and the Establishment of the Cellular Architecture of the Striatum , 2008, The Journal of Neuroscience.

[79]  Christiane Haffner,et al.  miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex , 2008, Development.

[80]  Chris Q Doe,et al.  Pdm and Castor close successive temporal identity windows in the NB3-1 lineage , 2008, Development.

[81]  S. Nelson,et al.  The Fezf2–Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex , 2008, Proceedings of the National Academy of Sciences.

[82]  S. Bowman,et al.  The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. , 2008, Developmental cell.

[83]  Chris Q Doe,et al.  Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells , 2008, Developmental neurobiology.

[84]  Michael B. Stadler,et al.  Individual Retinal Progenitor Cells Display Extensive Heterogeneity of Gene Expression , 2008, PloS one.

[85]  Stefan Krauss,et al.  COUP-TFI coordinates cortical patterning, neurogenesis, and laminar fate and modulates MAPK/ERK, AKT, and beta-catenin signaling. , 2008, Cerebral cortex.

[86]  Yuri B Schwartz,et al.  Polycomb complexes and epigenetic states. , 2008, Current opinion in cell biology.

[87]  B. Cubelos,et al.  Cux-2 controls the proliferation of neuronal intermediate precursors of the cortical subventricular zone. , 2008, Cerebral cortex.

[88]  S. Mcconnell,et al.  Satb2 Regulates Callosal Projection Neuron Identity in the Developing Cerebral Cortex , 2008, Neuron.

[89]  A. Gould,et al.  Temporal Transcription Factors and Their Targets Schedule the End of Neural Proliferation in Drosophila , 2008, Cell.

[90]  M. Cayouette,et al.  Ikaros Confers Early Temporal Competence to Mouse Retinal Progenitor Cells , 2008, Neuron.

[91]  B. Harris Cellular determination in the Xenopus retina is independent of lineage and birth date. , 2008, Neuron.

[92]  S. Mcconnell,et al.  The determination of projection neuron identity in the developing cerebral cortex , 2008, Current Opinion in Neurobiology.

[93]  Michael T. McManus,et al.  Conditional Loss of Dicer Disrupts Cellular and Tissue Morphogenesis in the Cortex and Hippocampus , 2008, The Journal of Neuroscience.

[94]  Heinrich Reichert,et al.  Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain , 2009, Neural Development.

[95]  T. Sun,et al.  Different timings of dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[96]  M. Vidal,et al.  Polycomb Limits the Neurogenic Competence of Neural Precursor Cells to Promote Astrogenic Fate Transition , 2009, Neuron.

[97]  D. Spector,et al.  Nuclear neighborhoods and gene expression. , 2009, Current opinion in genetics & development.

[98]  S. Thor,et al.  Neuronal Subtype Specification within a Lineage by Opposing Temporal Feed-Forward Loops , 2009, Cell.

[99]  Xiumei Wang,et al.  MicroRNAs couple cell fate and developmental timing in retina , 2009, Proceedings of the National Academy of Sciences.

[100]  S. Shi,et al.  Specific synapses develop preferentially among sister excitatory neurons in the neocortex , 2009, Nature.

[101]  T. Reh,et al.  Dicer Is Required for the Transition from Early to Late Progenitor State in the Developing Mouse Retina , 2010, The Journal of Neuroscience.

[102]  C. Desplan,et al.  Stochastic mechanisms of cell fate specification that yield random or robust outcomes. , 2010, Annual review of cell and developmental biology.

[103]  A. Kriegstein,et al.  Developmental genetics of vertebrate glial–cell specification , 2010, Nature.

[104]  K. Zheng,et al.  MicroRNAs Are Essential for the Developmental Switch from Neurogenesis to Gliogenesis in the Developing Spinal Cord , 2010, The Journal of Neuroscience.

[105]  Omer Ali Bayraktar,et al.  Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex , 2010, Neural Development.

[106]  A. Kriegstein,et al.  Neurogenic radial glia in the outer subventricular zone of human neocortex , 2010, Nature.

[107]  A. Brand,et al.  Development and Stem Cells Research Article , 2022 .

[108]  B. van Steensel,et al.  Role of the nuclear lamina in genome organization and gene expression. , 2010, Cold Spring Harbor symposia on quantitative biology.

[109]  Felix Carbonell,et al.  Reconstruction of rat retinal progenitor cell lineages in vitro reveals a surprising degree of stochasticity in cell fate decisions , 2011, Development.

[110]  S. Thor,et al.  Seven up acts as a temporal factor during two different stages of neuroblast 5-6 development , 2011, Development.

[111]  Oliver Hobert,et al.  Direct Conversion of C. elegans Germ Cells into Specific Neuron Types , 2011, Science.

[112]  S. Mango,et al.  Locking the genome: nuclear organization and cell fate. , 2011, Current opinion in genetics & development.

[113]  C. Doe,et al.  The pipsqueak-domain proteins Distal antenna and Distal antenna-related restrict Hunchback neuroblast expression and early-born neuronal identity , 2011, Development.

[114]  Sungjin Park,et al.  Gde2 regulates cortical neuronal identity by controlling the timing of cortical progenitor differentiation , 2012, Development.

[115]  Y. Y. Shevelyov,et al.  The nuclear lamina as a gene-silencing hub. , 2012, Current issues in molecular biology.

[116]  Michael D. Cleary,et al.  Drosophila Polycomb complexes restrict neuroblast competence to generate motoneurons , 2012, Development.

[117]  N. Sokol,et al.  Let-7-complex microRNAs regulate the temporal identity of Drosophila mushroom body neurons via chinmo. , 2012, Developmental cell.

[118]  J. Sanes,et al.  Direction-selective retinal ganglion cells arise from molecularly specified multipotential progenitors , 2012, Proceedings of the National Academy of Sciences.

[119]  R. Nishinakamura,et al.  Sall1 regulates cortical neurogenesis and laminar fate specification in mice: implications for neural abnormalities in Townes-Brocks syndrome , 2011, Disease Models & Mechanisms.

[120]  S. Mcconnell,et al.  A network of genetic repression and derepression specifies projection fates in the developing neocortex , 2012, Proceedings of the National Academy of Sciences.

[121]  Tzumin Lee,et al.  Hierarchical Deployment of Factors Regulating Temporal Fate in a Diverse Neuronal Lineage of the Drosophila Central Brain , 2012, Neuron.

[122]  J. Posakony,et al.  Identification of hunchback cis-regulatory DNA conferring temporal expression in neuroblasts and neurons. , 2012, Gene expression patterns : GEP.

[123]  A. Espinosa,et al.  Fate-Restricted Neural Progenitors in the Mammalian Cerebral Cortex , 2012, Science.

[124]  Kevin T. Beier,et al.  Transcription factor Olig2 defines subpopulations of retinal progenitor cells biased toward specific cell fates , 2012, Proceedings of the National Academy of Sciences.

[125]  Tzumin Lee,et al.  Lineage Analysis of Drosophila Lateral Antennal Lobe Neurons Reveals Notch-Dependent Binary Temporal Fate Decisions , 2012, PLoS biology.

[126]  A. Kriegstein,et al.  OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease , 2012, Current Opinion in Neurobiology.

[127]  O. Hobert,et al.  Embryonic Priming of a miRNA Locus Predetermines Postmitotic Neuronal Left/Right Asymmetry in C. elegans , 2012, Cell.

[128]  P. Arlotta,et al.  Direct lineage reprogramming of post-mitotic callosal neurons into corticofugal neurons in vivo , 2013, Nature Cell Biology.

[129]  Rie Takayama,et al.  A temporal mechanism that produces neuronal diversity in the Drosophila visual center. , 2013, Developmental biology.

[130]  Mohammad Wahid Ansari,et al.  The legal status of in vitro embryos , 2014 .

[131]  J. D. Macklis,et al.  Molecular logic of neocortical projection neuron specification, development and diversity , 2013, Nature Reviews Neuroscience.

[132]  C. Doe,et al.  Developmentally Regulated Subnuclear Genome Reorganization Restricts Neural Progenitor Competence in Drosophila , 2013, Cell.

[133]  C. Desplan,et al.  Temporal patterning of Drosophila medulla neuroblasts controls neural fates , 2013, Nature.

[134]  C. Doe,et al.  Combinatorial temporal patterning in progenitors expands neural diversity , 2013, Nature.

[135]  F. Cremisi MicroRNAs and cell fate in cortical and retinal development , 2013, Front. Cell. Neurosci..

[136]  J. Buceta,et al.  Sonic hedgehog signaling switches the mode of division in the developing nervous system. , 2013, Cell reports.

[137]  T. Reh,et al.  Conserved microRNA pathway regulates developmental timing of retinal neurogenesis , 2013, Proceedings of the National Academy of Sciences.

[138]  F. J. Livesey,et al.  Ikaros promotes early-born neuronal fates in the cerebral cortex , 2013, Proceedings of the National Academy of Sciences.

[139]  C. Lüscher,et al.  In vivo reprogramming of circuit connectivity in postmitotic neocortical neurons , 2013, Nature Neuroscience.