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Methods in Molecular Biology 1597 Takashi Tsuji Editor Organ Regeneration 3D Stem Cell Culture & Manipulation M M B ethods in olecular iology Series Editor John M. Walker School of Life and Medical Sciences University of Hertfordshire Hatfield, Hertfordshire, AL10 9AB, UK For further volumes: http://www.springer.com/series/7651 Organ Regeneration 3D Stem Cell Culture & Manipulation Edited by Takashi Tsuji Laboratory for Organ Regeneration, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan Organ Technologies Inc., Tokyo, Japan Editor Takashi Tsuji Laboratory for Organ Regeneration RIKEN Center for Developmental Biology Kobe, Hyogo, Japan Organ Technologies Inc. Tokyo, Japan ISSN 1064-3745 ISSN 1940-6029 (electronic) Methods in Molecular Biology ISBN 978-1-4939-6947-0 ISBN 978-1-4939-6949-4 (eBook) DOI 10.1007/978-1-4939-6949-4 Library of Congress Control Number: 2017933953 © Springer Science+Business Media LLC 2017 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. 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. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Printed on acid-free paper This Humana Press imprint is published by Springer Nature The registered company is Springer Science+Business Media LLC The registered company address is: 233 Spring Street, New York, NY 10013, U.S.A. Dedication This book is dedicated to the memory of Yoshiki Sasai, a scientist who made a great contri- bution to the advancement of developmental biology. v Preface Organogenesis is a complex process that involves tissue self-organization, cell-cell interac- tions, regulations of cell signaling molecules, and cell movements. During embryonic development, organ-forming fields are organized in a process depending on the body plan. Various lineages of stem cells are produced and play central roles in organ development. In recent years, stem cell researchers have made advances in various aspects of three- dimensional organogenesis including cell growth, differentiation, and morphogenesis. Studies using multipotent stem cells have provided knowledge of the complex pattern formation and tis- sue self-organization during embryogenesis. Stem cell research not only promotes basic biology but also can aid the development of regenerative medicine as a potential future clinical application. The current approaches to developing future regenerative therapies are influenced by our understanding of embryonic development, stem cell biology, and tissue engineering technology. To restore the partial loss of organ function, stem cell transplantation therapies were developed for several dis- eases such as hematopoietic malignancies, Parkinson’s disease, myocardial infarction, and hepatic insufficiency. The next generation of regenerative therapy will be the development of fully functioning bioengineered organs that can replace lost or damaged organs follow- ing disease, injury, or aging. It is expected that bioengineering technology will be devel- oped to reconstruct fully functional organs in vitro through the precise arrangement of several different cell types. In recent years, significant advances in techniques for organ regeneration have been made using three-dimensional stem cell culture in vitro. Several groups recently reported the generation of neuroectodermal and endodermal organs via the regulation of complex patterning signals during embryogenesis and self-formation of pluripotent stem cells in three-dimensional (3D) stem cell culture. Other groups attempted to generate functional organs that develop by reciprocal epithelial and mesenchymal interactions using embryonic organ inductive stem cells. Several groups reported the generation of three-dimensional mini-organs/tissues by the reproduction of stem cells and their niches. These studies pro- vide a better understanding of organogenesis in developmental biology and open possibili- ties for methodologies to be used in next-generation organ regenerative therapy. Here, we focus on recent studies of organ regeneration from stem cells using in vitro three-dimensional cell culture and manipulation. These protocols have led both basic and clinical researchers to face new challenges in the investigation of organogenesis in develop- mental biology in order to develop applications for next-generation regenerative therapies. I sincerely thank all of the authors for their contributions. I am also grateful to Dr. John Walker, the Editor in Chief of the MIMB series, for his continued support. I also thank Patrick Martin and Yasutaka Okazaki, Editors of the Springer Protocol series. Kobe, Hyogo, Japan Takashi Tsuji vii Contents Dedication....................................................... v Preface.......................................................... vii Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xi 1 Generation of Various Telencephalic Regions from Human Embryonic Stem Cells in Three-Dimensional Culture............................ 1 Taisuke Kadoshima, Hideya Sakaguchi, and Mototsugu Eiraku 2 Generation of a Three-Dimensional Retinal Tissue from Self-Organizing Human ESC Culture ........................................... 17 Atsushi Kuwahara, Tokushige Nakano, and Mototsugu Eiraku 3 3D Culture for Self-Formation of the Cerebellum from Human Pluripotent Stem Cells Through Induction of the Isthmic Organizer........ 31 Keiko Muguruma 4 Reconstitution of a Patterned Neural Tube from Single Mouse Embryonic Stem Cells........................................... 43 Keisuke Ishihara, Adrian Ranga, Matthias P. Lutolf, Elly M. Tanaka, and Andrea Meinhardt 5 Functional Pituitary Tissue Formation............................... 57 Chikafumi Ozone and Hidetaka Suga 6 Directed Differentiation of Mouse Embryonic Stem Cells Into Inner Ear Sensory Epithelia in 3D Culture........................ 67 Jing Nie, Karl R. Koehler, and Eri Hashino 7 Generation of Functional Thyroid Tissue Using 3D-Based Culture of Embryonic Stem Cells......................................... 85 Francesco Antonica, Dominika Figini Kasprzyk, Andrea Alex Schiavo, Mírian Romitti, and Sabine Costagliola 8 Functional Tooth Regeneration.................................... 97 Masamitsu Oshima, Miho Ogawa, and Takashi Tsuji 9 Functional Hair Follicle Regeneration by the Rearrangement of Stem Cells.................................................. 117 Kyosuke Asakawa, Koh-ei Toyoshima, and Takashi Tsuji 10 Functional Salivary Gland Regeneration ............................. 135 Miho Ogawa and Takashi Tsuji 11 Generation of a Bioengineered Lacrimal Gland by Using the Organ Germ Method................................................. 153 Masatoshi Hirayama, Kazuo Tsubota, and Takashi Tsuji 12 Generation of Gastrointestinal Organoids from Human Pluripotent Stem Cells.................................................... 167 Jorge O. Múnera and James M. Wells ix x Contents 13 Generation of a Three-Dimensional Kidney Structure from Pluripotent Stem Cells.................................................... 179 Yasuhiro Yoshimura, Atsuhiro Taguchi, and Ryuichi Nishinakamura 14 Making a Kidney Organoid Using the Directed Differentiation of Human Pluripotent Stem Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195 Minoru Takasato and Melissa H. Little 15 Liver Regeneration Using Cultured Liver Bud......................... 207 Keisuke Sekine, Takanori Takebe, and Hideki Taniguchi 16 Formation of Stomach Tissue by Organoid Culture Using Mouse Embryonic Stem Cells........................................... 217 Taka-aki K. Noguchi and Akira Kurisaki 17 In Vivo Model of Small Intestine .................................. 229 Mahe M. Maxime, Nicole E. Brown, Holly M. Poling, and Helmrath A. Michael Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247 Contributors Francesco antonica • Institute of Interdisciplinary Research in Molecular Human Biology (IRIBHM), Université Libre de Bruxelles, Brussels, Belgium; Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK KyosuKe asaKawa • Laboratory for Organ Regeneration, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan nicole e. Brown • Department of Pediatric General and Thoracic Surgery, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA saBine costagliola • Institute of Interdisciplinary Research in Molecular Human Biology (IRIBHM), Université Libre de Bruxelles, Brussels, Belgium Mototsugu eiraKu • In Vitro Histogenesis team, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan eri HasHino • Department of Otolaryngology—Head and Neck Surgery, and Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, USA MasatosHi HirayaMa • Department of Ophthalmology, Keio University School of Medicine, Tokyo, Japan KeisuKe isHiHara • DFG Research Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany taisuKe KadosHiMa • Cell Asymmetry team, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan; Asubio Pharma Co ., Ltd ., Kobe, Hyogo, Japan doMiniKa Figini KasprzyK • Institute of Interdisciplinary Research in Molecular Human Biology (IRIBHM), Université Libre de Bruxelles, Brussels, Belgium Karl r. KoeHler • Department of Otolaryngology—Head and Neck Surgery, and Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, USA aKira KurisaKi • Graduate School of Life and Environmental Sciences, The University of Tsukuba, Tsukuba, Ibaraki, Japan; Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan atsusHi KuwaHara • Laboratory for In Vitro Histogenesis, RIKEN Center for Developmental Biology, Chuo, Kobe, Japan; Regenerative and Cellular Medicine Office, Sumitomo Dainippon Pharma Co ., Ltd ., Chuo, Kobe, Japan; Environmental Health Science Laboratory, Sumitomo Chemical Co ., Ltd ., Osaka, Japan Melissa H. little • Murdoch Children’s Research Institute, Parkville, VIC, Australia; Department of Pediatrics, University of Melbourne, Parkville, VIC, Australia MattHias p. lutolF • Laboratory of Stem Cell Bioengineering, Institute of Bioengineering, School of Life Sciences and School of Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland; Institute of Chemical Sciences and Engineering, School of Basic Science, EPFL, Lausanne, Switzerland MaHe M. MaxiMe • Department of Pediatric General and Thoracic Surgery, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA; Department of Pediatrics, University of Cincinnati, Cincinnati, OH, USA xi xii Contributors andrea MeinHardt • DFG Research Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden, Germany HelMratH a. MicHael • Department of Pediatric General and Thoracic Surgery, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA; Department of Pediatrics, University of Cincinnati, Cincinnati, OH, USA KeiKo MuguruMa • Laboratory for Cell Asymmetry, RIKEN Center for Developmental Biology, Chuo, Kobe, Japan Jorge o. Múnera • Division of Developmental Biology, Cincinnati Children’s Hospital, Cincinnati, OH, USA toKusHige naKano • Environmental Health Science Laboratory, Sumitomo Chemical Co ., Ltd ., Osaka, Japan Jing nie • Department of Otolaryngology—Head and Neck Surgery, and Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, USA ryuicHi nisHinaKaMura • Department of Kidney Development, Institute of Molecular Embryology and Genetics, Kumamoto University, Kumamoto, Japan taKa-aKi K. nogucHi • Graduate School of Life and Environmental Sciences, The University of Tsukuba, Tsukuba, Ibaraki, Japan MiHo ogawa • Laboratory for Organ Regeneration, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan; Organ Technologies Inc ., Tokyo, Japan MasaMitsu osHiMa • Department of Oral Rehabilitation and Regenerative Medicine, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama, Japan; Laboratory for Organ Regeneration, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan cHiKaFuMi ozone • Department of Endocrinology and Diabetes, Graduate School of Medicine, Nagoya University, Nagoya, Aichi, Japan; Laboratory for Organ Regeneration, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan Holly M. poling • Department of Pediatric General and Thoracic Surgery, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA adrian ranga • Laboratory of Stem Cell Bioengineering, Institute of Bioengineering, School of Life Sciences and School of Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland; Department of Mechanical Engineering, KU Leuven, Belgium Mírian roMitti • Institute of Interdisciplinary Research in Molecular Human Biology (IRIBHM), Université Libre de Bruxelles, Brussels, Belgium Hideya saKagucHi • In Vitro Histogenesis team, RIKEN Center for Developmental Biology, Kobe, Hyogo, Japan; Department of Clinical Application, Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan andrea alex scHiavo • Institute of Interdisciplinary Research in Molecular Human Biology (IRIBHM), Université Libre de Bruxelles, Brussels, Belgium KeisuKe seKine • Department of Regenerative Medicine, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa, Japan HidetaKa suga • Department of Endocrinology and Diabetes, Nagoya University Hospital, Nagoya, Aichi, Japan atsuHiro tagucHi • Department of Kidney Development, Institute of Molecular Embryology and Genetics, Kumamoto University, Kumamoto, Japan

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This volume provides readers with a better understanding of organogenesis in developmental biology and next-generation organ regenerative therapy. This book focuses on recent studies of organ regeneration from stem cells using in vitro 3D cell culture and manipulation. The chapters cover topics such
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