Self-formation of layered neural structures in three-dimensional culture of ES cells

In vitro neural differentiation culture of embryonic stem cells (ESCs) provides a promising tool for preparing neural cells for replacement therapies and a versatile system for understanding mechanisms of neurogenesis. Consistent with the neural-default model, neural differentiation spontaneously occurs in ESCs cultured in medium containing minimal extrinsic signals. Both adherent monolayer culture and floating aggregation culture can be used for ESC conversion into neural progenitors. The floating aggregation culture has an advantage for recapitulating the formation of three-dimensional (3D) neural tissue structure such as layer formation. In this article, we review recent progress in neural differentiation culture of ESCs using 3D culture, focusing on self-organization phenomena of stratified cortex and retinal tissues. These self-organizing processes are driven by both cell intrinsic programs and local cell-cell interactions. A simple in vitro system using ESCs is useful for elucidating mechanistic dynamics in the complex orchestration of neural development.

[1]  J. Thomson,et al.  Embryonic stem cell lines derived from human blastocysts. , 1998, Science.

[2]  Yoshiki Sasai,et al.  Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. , 2010, Cell stem cell.

[3]  J. Rubenstein,et al.  Regionalization of the prosencephalic neural plate. , 1998, Annual review of neuroscience.

[4]  T. Sargent,et al.  Development of neural inducing capacity in dissociated Xenopus embryos. , 1989, Developmental biology.

[5]  Hynek Wichterle,et al.  Functional diversity of ESC-derived motor neuron subtypes revealed through intraspinal transplantation. , 2010, Cell stem cell.

[6]  Y. Sasai,et al.  Ectodermal patterning in vertebrate embryos. , 1997, Developmental biology.

[7]  Y. Yanagawa,et al.  Subregional Specification of Embryonic Stem Cell-Derived Ventral Telencephalic Tissues by Timed and Combinatory Treatment with Extrinsic Signals , 2011, The Journal of Neuroscience.

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

[9]  K. Sekiguchi,et al.  Regulation of Mesodermal Differentiation of Mouse Embryonic Stem Cells by Basement Membranes* , 2007, Journal of Biological Chemistry.

[10]  M. Hatten,et al.  Differentiation of ES cells into cerebellar neurons , 2007, Proceedings of the National Academy of Sciences.

[11]  Hiroyuki Miyoshi,et al.  Self-formation of functional adenohypophysis in three-dimensional culture , 2011, Nature.

[12]  Yoshiki Sasai,et al.  A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin , 1995, Nature.

[13]  M. Takeichi,et al.  Identification of the laminar-inducing factor: Wnt-signal from the anterior rim induces correct laminar formation of the neural retina in vitro. , 2003, Developmental biology.

[14]  Yoshiki Sasai,et al.  Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. , 2008, Cell stem cell.

[15]  Hitoshi Niwa,et al.  How is pluripotency determined and maintained? , 2007, Development.

[16]  K. Mizuseki,et al.  Induction of Midbrain Dopaminergic Neurons from ES Cells by Stromal Cell–Derived Inducing Activity , 2000, Neuron.

[17]  Luis Puelles,et al.  Forebrain gene expression domains and the evolving prosomeric model , 2003, Trends in Neurosciences.

[18]  M. Eiraku,et al.  Mouse embryonic stem cell culture for generation of three-dimensional retinal and cortical tissues , 2011, Nature Protocols.

[19]  Andrew Lumsden,et al.  Patterning the Vertebrate Neuraxis , 1996, Science.

[20]  Y. Sasai,et al.  Dorsoventral Patterning in Xenopus: Inhibition of Ventral Signals by Direct Binding of Chordin to BMP-4 , 1996, Cell.

[21]  J. Emery,et al.  Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. , 1994, Genes & development.

[22]  R. McKay,et al.  New cell lines from mouse epiblast share defining features with human embryonic stem cells , 2007, Nature.

[23]  Janet Rossant,et al.  Direct Neural Fate Specification from Embryonic Stem Cells A Primitive Mammalian Neural Stem Cell Stage Acquired through a Default Mechanism , 2001, Neuron.

[24]  H. Wichterle,et al.  Directed Differentiation of Embryonic Stem Cells into Motor Neurons , 2002, Cell.

[25]  R. Harland,et al.  The Spemann Organizer Signal noggin Binds and Inactivates Bone Morphogenetic Protein 4 , 1996, Cell.

[26]  L. Grabel,et al.  Embryonic stem cell neurogenesis and neural specification , 2010, Journal of cellular biochemistry.

[27]  M. Peschanski,et al.  Striatal progenitors derived from human ES cells mature into DARPP32 neurons in vitro and in quinolinic acid-lesioned rats , 2008, Proceedings of the National Academy of Sciences.

[28]  J. Rubenstein,et al.  Deriving Excitatory Neurons of the Neocortex from Pluripotent Stem Cells , 2011, Neuron.

[29]  T. Jessell,et al.  Diversity and Pattern in the Developing Spinal Cord , 1996, Science.

[30]  Yoshiki Sasai,et al.  Lonely death dance of human pluripotent stem cells: ROCKing between metastable cell states. , 2011, Trends in cell biology.

[31]  Y. Sasai,et al.  A common plan for dorsoventral patterning in Bilateria , 1996, Nature.

[32]  M. Götz,et al.  Neurotrophin receptor-mediated death of misspecified neurons generated from embryonic stem cells lacking Pax6. , 2007, Cell stem cell.

[33]  H. Kiyonari,et al.  Intrinsic transition of embryonic stem-cell differentiation into neural progenitors , 2011, Nature.

[34]  T. Jessell,et al.  The specification of dorsal cell fates in the vertebrate central nervous system. , 1999, Annual review of neuroscience.

[35]  C. Englund,et al.  Pax6, Tbr2, and Tbr1 Are Expressed Sequentially by Radial Glia, Intermediate Progenitor Cells, and Postmitotic Neurons in Developing Neocortex , 2005, The Journal of Neuroscience.

[36]  J. Slack,et al.  Clonal analysis of mesoderm induction in Xenopus laevis. , 1989, Developmental biology.

[37]  Y. Sasai,et al.  In vitro differentiation of retinal cells from human pluripotent stem cells by small-molecule induction , 2009, Journal of Cell Science.

[38]  M. Tomishima,et al.  Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling , 2009, Nature Biotechnology.

[39]  Tetsu Akiyama,et al.  The Wnt/β-catenin pathway directs neuronal differentiation of cortical neural precursor cells , 2004, Development.

[40]  H. Wichterle,et al.  Programming embryonic stem cells to neuronal subtypes , 2011, Current Opinion in Neurobiology.

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

[42]  E. Soriano,et al.  The Cells of Cajal-Retzius: Still a Mystery One Century After , 2005, Neuron.

[43]  L. Recht,et al.  Murine Embryonic Stem Cell-Derived Pyramidal Neurons Integrate into the Cerebral Cortex and Appropriately Project Axons to Subcortical Targets , 2010, The Journal of Neuroscience.

[44]  M. Maden Retinoid signalling in the development of the central nervous system , 2002, Nature Reviews Neuroscience.

[45]  S. Fuhrmann Eye morphogenesis and patterning of the optic vesicle. , 2010, Current topics in developmental biology.

[46]  Y. Sasai Regulation of neural determination by evolutionarily conserved signals: anti-BMP factors and what next? , 2001, Current Opinion in Neurobiology.

[47]  P. Vanderhaeghen,et al.  Mechanisms of neural specification from embryonic stem cells , 2010, Current Opinion in Neurobiology.

[48]  J. Fish,et al.  OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling , 2010, Nature Neuroscience.

[49]  I. Cobos,et al.  FGF15 promotes neurogenesis and opposes FGF8 function during neocortical development , 2008, Neural Development.

[50]  J. Rubenstein,et al.  The embryonic vertebrate forebrain: the prosomeric model. , 1994, Science.

[51]  S. Anderson,et al.  Prospective Isolation of Cortical Interneuron Precursors from Mouse Embryonic Stem Cells , 2010, The Journal of Neuroscience.

[52]  Ariel J. Levine,et al.  Proposal of a model of mammalian neural induction. , 2007, Developmental biology.

[53]  J. Rubenstein,et al.  Genes and signaling events that establish regional patterning of the mammalian forebrain. , 2009, Seminars in cell & developmental biology.

[54]  J. Olavarria,et al.  Beyond Laminar Fate: Toward a Molecular Classification of Cortical Projection/Pyramidal Neurons , 2003, Developmental Neuroscience.

[55]  S. Chandran,et al.  Embryonic Stem Cell‐Derived Neural Progenitors Display Temporal Restriction to Neural Patterning , 2006, Stem cells.

[56]  T. Adachi,et al.  Self-organizing optic-cup morphogenesis in three-dimensional culture , 2011, Nature.

[57]  M. Ungless,et al.  Temporally controlled modulation of FGF/ERK signaling directs midbrain dopaminergic neural progenitor fate in mouse and human pluripotent stem cells , 2011, Development.

[58]  Pierre Vanderhaeghen,et al.  An intrinsic mechanism of corticogenesis from embryonic stem cells , 2008, Nature.

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

[60]  K. Mizuseki,et al.  Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[61]  M. Eiraku,et al.  Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation , 2008, Proceedings of the National Academy of Sciences.

[62]  T. Adachi,et al.  Relaxation-expansion model for self-driven retinal morphogenesis , 2012, BioEssays : news and reviews in molecular, cellular and developmental biology.

[63]  Y. Yanagawa,et al.  Ontogeny-recapitulating generation and tissue integration of ES cell–derived Purkinje cells , 2010, Nature Neuroscience.

[64]  R. S. Goldstein,et al.  Derivation of neural precursors from human embryonic stem cells in the presence of noggin , 2005, Molecular and Cellular Neuroscience.

[65]  D. Arendt,et al.  Inversion of dorsoventral axis? , 1994, Nature.

[66]  G. Fishell,et al.  Cortex shatters the glass ceiling. , 2008, Cell stem cell.

[67]  M. Trotter,et al.  Derivation of pluripotent epiblast stem cells from mammalian embryos , 2007, Nature.

[68]  L. Tacke,et al.  Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. , 1989, Cell differentiation and development : the official journal of the International Society of Developmental Biologists.

[69]  H. Clevers,et al.  Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche , 2009, Nature.

[70]  Y. Sasai,et al.  Generation of cerebellar neuron precursors from embryonic stem cells. , 2006, Developmental biology.

[71]  R. Harland,et al.  Neural induction by the secreted polypeptide noggin. , 1993, Science.

[72]  M. Tomishima,et al.  Efficient derivation of functional floor plate tissue from human embryonic stem cells. , 2010, Cell stem cell.

[73]  Y. Sasai,et al.  Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus , 1995, Nature.

[74]  D. van der Kooy,et al.  Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences , 2006, The Journal of cell biology.

[75]  Jeh-Ping Liu The function of growth/differentiation factor 11 (Gdf11) in rostrocaudal patterning of the developing spinal cord , 2006, Development.

[76]  K. Mizuseki,et al.  Directed differentiation of telencephalic precursors from embryonic stem cells , 2005, Nature Neuroscience.

[77]  William A. Harris,et al.  Actomyosin Is the Main Driver of Interkinetic Nuclear Migration in the Retina , 2009, Cell.

[78]  S. Martinez,et al.  Neuroepithelial secondary organizers and cell fate specification in the developing brain , 2003, Brain Research Reviews.

[79]  Y. Gotoh,et al.  Mechanisms that regulate the number of neurons during mouse neocortical development , 2010, Current Opinion in Neurobiology.

[80]  Jun Yamashita,et al.  Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors , 2000, Nature.

[81]  P. Nieuwkoop Activation and organization of the central nervous system in amphibians.† Part I. Induction and activation , 1952 .

[82]  W. Harris,et al.  Lineage in the vertebrate retina , 2006, Trends in Neurosciences.

[83]  Austin G Smith,et al.  Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture , 2003, Nature Biotechnology.

[84]  M. Whitman,et al.  The role and regulation of GDF11 in Smad2 activation during tailbud formation in the Xenopus embryo , 2010, Mechanisms of Development.

[85]  D. Kimelman,et al.  Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development , 2005, Development.

[86]  T. Jessell,et al.  Convergent Inductive Signals Specify Midbrain, Hindbrain, and Spinal Cord Identity in Gastrula Stage Chick Embryos , 1999, Neuron.

[87]  Elmar Willbold,et al.  Of layers and spheres: the reaggregate approach in tissue engineering , 2002, Trends in Neurosciences.

[88]  S. Nishikawa,et al.  A ROCK inhibitor permits survival of dissociated human embryonic stem cells , 2007, Nature Biotechnology.