Ryoichiro Kageyama Tetsuo Yamamori Editors. Cortical Development. Neural Diversity and Neocortical Organization
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2 Ryoichiro Kageyama Tetsuo Yamamori Editors Cortical Development Neural Diversity and Neocortical Organization
3 Cortical Development
4
5 Ryoichiro Kageyama Tetsuo Yamamori Editors Cortical Development Neural Diversity and Neocortical Organization
6 Editors Ryoichiro Kageyama Kyoto University Kyoto, Japan Tetsuo Yamamori National Institute for Basic Biology Okazaki, Japan ISBN ISBN (ebook) DOI / Springer Tokyo Heidelberg New York Dordrecht London Library of Congress Control Number: Springer Japan 2013 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. Exempted from this legal reservation are brief excerpts in connection with reviews or scholarly analysis or material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Duplication of this publication or parts thereof is permitted only under the provisions of the Copyright Law of the Publisher s location, in its current version, and permission for use must always be obtained from Springer. Permissions for use may be obtained through RightsLink at the Copyright Clearance Center. Violations are liable to prosecution under the respective Copyright Law. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. While the advice and information in this book are believed to be true and accurate at the date of publication, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein. Printed on acid-free paper Springer is part of Springer Science+Business Media (
7 Preface Development of the cerebral cortex, the center for higher brain functions such as cognition, memory, and decision making, is one of the major targets of current research. This book reviews recent progress in cortical development research, focusing on the mechanisms of neural stem cell regulation, neuronal diversity and connectivity formation, and neocortical organization. The cerebral cortex is divided into many areas, including motor, sensory, and visual cortices, each of which consists of six layers containing a variety of neurons with different activities and connections. Such diversity of neuronal types and connections is generated at various levels. First, the competency of neural stem cells changes over time, giving sequential rise to distinct types of neurons and glial cells: initially deep layer neurons, then superficial layer neurons, and lastly astrocytes. The activities and connections of neurons are further modulated via interactions with other brain regions, such as the thalamocortical circuit, and via input from the environment. Extensive studies are gradually elucidating the mechanisms by which the diversity in such neuronal types and connections is formed. To accelerate exchanges of the most recent findings and interactions among leading researchers, we organized a symposium titled Cortical Development in Okazaki, Japan, held March 10 13, 2012, which was supported by a Grant-in-Aid for Scientific Research on the Innovative Area Neural Diversity and Neocortical Organization from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. The symposium was very timely and attracted many young researchers, who were eager to interact with leading researchers and learn about the most recent hot topics. Because the symposium was so successful, we decided to publish a book on cortical development and asked the researchers in this field to contribute chapters. We were happy that many of them responded positively and, although they were very busy, contributed chapters that review hot topics in this field. Many of the topics discussed in the symposium are included in this book. v
8 vi Preface We are pleased to be able to publish this book, and we would like to thank all the authors who contributed state-of-the-art reviews to it. We also thank our editorial partners, Mr. Kaoru Hashimoto and Ms. Mari Hata at Springer Japan, for their initial suggestion and continued promotion of the project. Ryoichiro Kageyama Tetsuo Yamamori
9 Contents 1 Dynamic Notch Signaling in Neural Progenitor Cells... 1 Hiromi Shimojo, Yuki Maeda, Toshiyuki Ohtsuka, and Ryoichiro Kageyama 2 Proneural Proteins and the Development of the Cerebral Cortex Julian Heng and François Guillemot 3 The Role of the Transcription Factor Pax6 in Brain Development and Evolution: Evidence and Hypothesis Noriko Osumi and Takako Kikkawa 4 Regulatory Mechanisms Underlying the Neurogenesis-to-Gliogenesis Switch by Neural Stem Cells Takuya Shimazaki 5 Specification of GABAergic Neocortical Interneurons Goichi Miyoshi, Robert P. Machold, and Gord Fishell 6 Regulation of Cortical Circuit Formation Fernanda M. Rodríguez-Tornos, Beatriz Cubelos, and Marta Nieto 7 Neocortical Neurogenesis and Circuit Assembly Peng Gao, Khadeejah T. Sultan, Xin-Jun Zhang, and Song-Hai Shi 8 Hierarchical Organization of Neocortical Neuron Types Yasuo Kawaguchi 9 Emerging Roles of Heparan Sulfate in Axon Guidance Signaling Masayuki Masu vii
10 viii Contents 10 The Roles of RECK, a Membrane-Anchored Regulator of Pericellular Proteolysis, in Neural Development Makoto Noda 11 Synapse Formation in the Brain Masayoshi Mishina, Tomoyuki Yoshida, Misato Yasumura, and Takeshi Uemura 12 Genomic Imprinting in the Mammalian Brain Wei-Chao Huang and Christopher Gregg 13 Genes Selectively Expressed in the Visual Cortex of the Old World Monkey Yusuke Komatsu, Shigeko Toita, Masanari Ohtsuka, Toru Takahata, Shiro Tochitani, and Tetsuo Yamamori Index
11 Chapter 1 Dynamic Notch Signaling in Neural Progenitor Cells Hiromi Shimojo, Yuki Maeda, Toshiyuki Ohtsuka, and Ryoichiro Kageyama Abstract Notch signaling plays an essential role in maintenance of neural progenitor cells. Differentiating neurons express Notch ligands such as Delta-like1 (Dll1), which activate Notch signaling in neighboring cells. Activation of Notch signaling induces the expression of Hes1 and Hes5, which repress proneural gene expression, thereby maintaining neural progenitor cells. Thus, differentiating neurons keep their neighbors undifferentiated. Interestingly, Hes1 expression oscillates with a period of 2 3 h by negative feedback, and Hes1 oscillations drive the oscillatory expression of Dll1 and the proneural gene Neurogenin2 (Neurog2 ). Neurog2 oscillation cannot induce neuronal differentiation, and Dll1 oscillation leads to the mutual activation of Notch signaling between neighboring cells. Thus, neural progenitor cells also keep each other undifferentiated via oscillation in Notch signaling. Not all cells express Hes1 in an oscillatory manner: cells in boundary regions such H. Shimojo R. Kageyama (*) Institute for Virus Research, Kyoto University, Shogoin-Kawahara, Sakyo-ku, Kyoto , Japan Japan Science and Technology Agency, CREST, Shogoin-Kawahara, Sakyo-ku, Kyoto , Japan World Premier International Research Initiative Institute for Integrated Cell-Material Sciences (WPI-iCeMS), Kyoto University, Kyoto , Japan rkageyam@virus.kyoto-u.ac.jp Y. Maeda Institute for Virus Research, Kyoto University, Shogoin-Kawahara, Sakyo-ku, Kyoto , Japan Graduate School of Biostudies, Kyoto University, Kyoto , Japan T. Ohtsuka Institute for Virus Research, Kyoto University, Shogoin-Kawahara, Sakyo-ku, Kyoto , Japan Japan Science and Technology Agency, CREST, Shogoin-Kawahara, Sakyo-ku, Kyoto , Japan R. Kageyama and T. Yamamori (eds.), Cortical Development: Neural Diversity and Neocortical Organization, DOI / _1, Springer Japan
12 2 H. Shimojo et al. as the isthmus express Hes1 in a sustained manner, and this sustained Hes1 expression seems to be important for the maintenance of boundary regions. Thus, Notch signaling molecules regulate various aspects of neural development by changing the expression dynamics. Keywords Basal progenitor Neuroepithelial cell Oscillatory expression OSVZ progenitor Proneural gene Radial glia 1.1 Introduction Neuroepithelial cells, which extend from the ventricular surface to the pial surface of the neural tube, repeat symmetric cell division, where each neuroepithelial cell divides into two neuroepithelial cells (Fig. 1.1 ) (Alvarez-Buylla et al ; Fishell and Kriegstein 2003 ; Fujita 2003 ; Götz and Huttner 2005 ; Miller and Gauthier 2007 ). As the wall of the neural tube becomes thicker, neuroepithelial cells gradually elongate and become radial glial cells, which have cell bodies in the ventricular zone and radial fibers reaching the pial surface (Fig. 1.1 ). Radial glial cells undergo asymmetric cell division, where each radial glial cell divides into two distinct cell types, a radial glial cell and an immature neuron or a progenitor (Fig. 1.1 ) (Malatesta et al ; Miyata et al ; Noctor et al ). Immature neurons migrate Fig. 1.1 Neural progenitor cells and their differentiation in the embryonic brain. Initially, neuroepithelial cells undergo self-renewal by symmetric division and expand. As development proceeds, neuroepithelial cells elongate to become radial glial cells, which have cell bodies in the inner region (the ventricular zone) of the neural tube and radial fibers that reach the pial surface. Radial glial cells give rise to neurons or basal progenitors. After the production of neurons, some radial glial cells give rise to oligodendrocytes and ependymal cells. Radial glial cells finally differentiate into astrocytes. Both neuroepithelial cells and radial glial cells are considered embryonic neural progenitor cells
13 1 Dynamic Notch Signaling 3 outside of the ventricular zone along radial fibers into the cortical plate, where these cells become mature neurons. Progenitors migrate out of the ventricular zone into the subventricular zone (SVZ), proliferate further, and give rise to more neurons, which then migrate into the cortical plate (see Fig. 1.6 ). Radial glial cells give rise to different types of neurons, initially deep layer neurons and then superficial layer neurons, by repeating asymmetric cell division (Fig. 1.1 ). Radial glial cells also give rise to oligodendrocytes and ependymal cells and finally differentiate into astrocytes (Fig. 1.1 ). Both neuroepithelial and radial glial cells are considered neural progenitor cells. As described above, neural progenitor cells produce a variety of cell types sequentially during development by gradually changing their competency over time. Thus, it is very important to maintain neural progenitor cells until the final point of development in order to generate the proper number of cells and the full diversity of cell types. It has been shown that Notch signaling plays an essential role in the maintenance of neural progenitor cells (Kopan and Ilagan 2009 ; Fortini 2009 ; Pierfelice et al ). Here, we review the recent progress on the mechanism and role of Notch signaling in neural development. 1.2 The Core Pathway of Notch Signaling Notch signaling plays an important role in cell proliferation and differentiation by communication between neighboring cells. Notch ligands such as the transmembrane proteins Delta-like1 (Dll1) and Jagged1 activate Notch receptors such as the transmembrane protein Notch1 in neighboring cells. Notch is cleaved at the S1 site by Furin into two fragments that remain associated to form the functional heterodimer receptor consisting of the Notch extracellular domain and the transmembrane part (Fig. 1.2 ). Upon Notch ligand binding, Notch receptors undergo successive cleavages: the transmembrane part of Notch proteins is cleaved at the S2 site by TACE and then at the S3 site by γ-secretase, releasing the Notch intracellular domain (NICD) from the transmembrane domain (Fig. 1.2 ). NICD next moves to the nucleus and forms a complex with the DNA-binding protein Rbpj and the transcriptional co-activator Maml (Fig. 1.2 ). This ternary complex (NICD-Rbpj-Maml) activates target genes such as the basic helix-loop-helix (bhlh) repressor genes Hes1 and Hes5, mammalian homologues of Drosophila hairy and Enhancer of split (Jarriault et al ; Fortini 2009 ; Honjo 1996 ; Kageyama et al ; Kopan and Ilagan 2009 ; Pierfelice et al ). Hes factors act as repressors by interacting with the corepressor TLE/Grg, a homologue of Drosophila Groucho, through the C-terminal Trp-Arg-Pro-Trp sequence called the WRPW domain (Akazawa et al ; Sasai et al ; Grbavec and Stifani 1996 ). Groucho is known to modify the chromatin structure by recruiting the histone deacetylase Rpd3 (Chen et al ). Hes1 and Hes5 repress the proneural genes such as the bhlh transcriptional activators Ascl1 and Neurogenin2 (Neurog2 ), which induce neuronal differentiation (Bertrand et al ; Ross et al ). As a result, Hes1 and Hes5 inhibit neuronal differentiation and maintain neural progenitor cells (Ishibashi et al ; Ohtsuka et al ; Hatakeyama et al ; Kageyama
14 4 H. Shimojo et al. Fig. 1.2 The core pathway of Notch signaling. Proneural genes such as Ascl1 (also called Mash1) and Neurog2 (Ngn2) promote neuronal differentiation and induce the expression of Dll1, which in turn activates Notch signaling in neighboring cells. Notch is cleaved at the S1 site by Furin into two fragments that remain associated to form the functional heterodimer receptor consisting of the Notch extracellular domain and the transmembrane part. Upon activation of Notch, the Notch intracellular domain (NICD) is released from the transmembrane domain and transferred to the nucleus, where it forms a complex with the DNA-binding protein Rbpj and the transcriptional co-activator Maml. The NICD-Rbpj-Maml ternary complex induces the expression of transcriptional repressor genes such as Hes1 and Hes5. Hes1 and Hes5 repress the expression of proneural genes and Dll1, thereby leading to the maintenance of neural progenitor cells et al ). Hes genes also repress the expression of Notch ligand genes. Notch ligand expression is induced by proneural genes, and therefore neurons express Notch ligands and inhibit neighboring cells to differentiate into neurons by activating Notch signaling. This process, called lateral inhibition, is essential to maintain neural progenitor cells in the developing nervous system. In the absence of Notch signaling, all cells express proneural genes and initiate neuronal differentiation, resulting in premature depletion of neural progenitor cells without generating later-born cell types (Ishibashi et al ; Hatakeyama et al ; Imayoshi et al ). While the Notch signaling pathway is important for maintenance of neural progenitor cells, this regulation also suggests that neurons expressing Notch ligands are required to activate the Notch pathway, raising the question as to how neural progenitor cells are maintained during early stages of development before neurons are born. 1.3 Oscillatory Expression of Notch Signaling Genes In the developing mouse dorsal telencephalon, neural progenitor cells express the proneural gene Neurog2, the Notch ligand gene Dll1, and Hes1 in a salt-and-pepper pattern at early stages before neurons are born. It is likely that Neurog2 induces the
15 1 Dynamic Notch Signaling 5 Fig. 1.3 Oscillatory expression of Hes1 by negative feedback. Hes1 expression oscillates with a period of ~2 3 h in many cell types such as neural progenitor cells and fibroblasts. Hes1 represses its own expression by directly binding to its promoter. This negative feedback leads to the disappearance of Hes1 mrna and protein, because they are extremely unstable, allowing the next round of its expression. In this way, Hes1 autonomously starts oscillatory expression expression of Dll1, which upregulates Hes1 expression in neighboring cells, suggesting that Notch signaling is active before neurons are born. This observation raises another question: why neurons are not formed during early stages, although the proneural gene Neurog2 is expressed. It was previously shown that Hes1 expression oscillates with a period of about 2 3 h in many cell types (Hirata et al ). This oscillatory expression is regulated by negative feedback with a delayed timing (Fig. 1.3 ) (Hirata et al ).
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