Advances in Experimental Medicine and Biology 1046 Jun Aruga Editor Zic family Evolution, Development and Disease Advances in Experimental Medicine and Biology Volume 1046 Editorial Board IRUN R. COHEN, The Weizmann Institute of Science, Rehovot, Israel ABEL LAJTHA, N.S.Kline Institute for Psychiatric Research, Orangeburg, NY, USA JOHN D. LAMBRIS, University of Pennsylvania, Philadelphia, PA, USA RODOLFO PAOLETTI, University of Milan, Milan, Italy NIMA REZAEI, Tehran University of Medical Sciences Children’s Medical Center, Children’s Medical Center Hospital, Tehran, Iran More information about this series at http://www.springer.com/series/5584 Jun Aruga Editor Zic family Evolution, Development and Disease Editor Jun Aruga Graduate School of Biomedical Sciences Nagasaki University Nagasaki, Nagasaki, Japan ISSN 0065-2598 ISSN 2214-8019 (electronic) Advances in Experimental Medicine and Biology ISBN 978-981-10-7310-6 ISBN 978-981-10-7311-3 (eBook) https://doi.org/10.1007/978-981-10-7311-3 Library of Congress Control Number: 2017963871 © Springer Nature Singapore Pte Ltd. 2018 Chapter 3 was created within the capacity of an US governmental employment. US copyright protection does not apply. 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 Springer imprint is published by Springer Nature The registered company is Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore Preface Studies conducted in the last two decades indicate that Zic family genes are essen- tial components of the animal genome. They code for zinc finger proteins that con- trol cell differentiation in many developmental processes. These processes include maintenance of pluripotency; generation of the mesoderm, neuroectoderm, and neural crest; formation of the body pattern, the neural tube, and the skeletal patterns; and establishment of a platform for higher brain functions. Since the involvement of Zic family genes in early developmental processes has been established across major animal models, they have now become attractive research targets not only in the field of developmental biology but also in the field of evolutionary biology. Most multicellular animals, except sponges and comb jellies, possess Zic genes, and these genes may be involved in the developmental programs of these animals. A compila- tion of such information would allow us to infer the role of Zic genes in the evolu- tion of animal body plans, such as in the emergence and diversification of the central nervous system. Thus, publications dealing with the role of Zic family genes in development and evolution have steadily contributed to the field of basic biology. Zic family genes have often been the subject of medical research. They have been recognized as the causal genes for various genetic disorders such as holoprosen- cephaly, heterotaxy, Dandy-Walker malformation, and craniosynostosis. The impor- tance of these genes in medicine is being increasingly appreciated after the recent discovery of their critical roles in stem cell regulation, both in normal and onco- genic processes. Therefore, Zic family-related medical research has been published in journals of human genetics, stem cell biology, cancer biology, and diseases of the nervous system and is expected to contribute further to the rapidly growing field of translational medicine, which includes stem cell applications, drug development, and cancer diagnosis and treatment. Despite the enrichment of research on the Zic family genes, it is becoming diffi- cult to visualize the overall picture of Zic family-related studies. This is probably because research has been conducted on diverse topics, and only a few researchers may be motivated to study the genes themselves. This book aims to provide essen- tial and comprehensive information on existing research on Zic family genes for future researchers and graduate students in the fields of biology and medicine. The v vi Preface contributing authors were selected based on their critical publications in the field of Zic biology. Their articles have been written such that they are easily comprehen- sible by researchers working in other fields as well. In Part I (Chaps. 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, and 11) of the book, research topics have been ordered according to experimental animal models; a wide range of animals, including cnidarians, ecdy- sozoans, lophotrochozoans, and chordates, have been covered. In Part II (Chaps. 12, 13, 14, 15, 16, 17, and 18), topics closely related to clinical research have been included. To provide warp threads to the story, summaries from the viewpoints of comparative genomics and biochemical properties have been included at the begin- ning and at the end, respectively. This book has been prepared with an interdisciplinary approach, to be useful to both developmental biologists and medical researchers. For instance, the updated results of human genetics research would be of interest not only to medical research- ers but also to those working in the fields of developmental biology and evolution- ary biology. Similarly, the information on the roles Zic family genes play in certain animal models is expected to inspire researchers in the fields of evolutionary biol- ogy and medicine. While editing this book, I came across many important unre- solved questions and hints for future studies. For instance, important findings regarding the molecular function of the Zic genes have been reported in the last couple of years. The notion of Zic proteins as major enhancer function mediators, in conjunction with chromatin remodeling factors, is becoming popular, and it sheds new light on Zic biology and being resolved questions concerning the position of Zic genes regulatory network controlling problems ensures the importance of the Zic gene family in the regenerative medicine. I thank all the contributing authors for sharing their significant findings and insights. Some authors graciously complied with my repeated editorial requests, which I sincerely appreciate. Lastly, I thank Mr. Yasushi Okazaki, Member, Springer Nature, for encouraging me to publish this book on the Zic family. Nagasaki, Japan Jun Aruga August 2017 Contents Part I Zic Family in Animal Evolution and Development 1 Comparative Genomics of the Zic Family Genes ................................. 3 Jun Aruga and Minoru Hatayama 2 Cnidarian Zic Genes ............................................................................... 27 Michael J. Layden 3 Odd-Paired: The Drosophila Zic Gene ................................................... 41 Deborah A. Hursh and Brian G. Stultz 4 Zic Genes in Nematodes: A Role in Nervous System Development and Wnt Signaling ........................................................... 59 Guillaume Bordet and Vincent Bertrand 5 Lophotrochozoan Zic Genes ................................................................... 69 Jun Aruga 6 Ascidian Zic Genes .................................................................................. 87 Yutaka Satou and Kaoru S. Imai 7 Amphibian Zic Genes ............................................................................. 107 Christa Merzdorf and Jennifer Forecki 8 Zic Genes in Teleosts: Their Roles in Dorsoventral Patterning in the Somite ......................................................................... 141 Kota Abe, Toru Kawanishi, and Hiroyuki Takeda 9 Zebrafish Zic Genes Mediate Developmental Signaling...................... 157 Cecilia Lanny Winata and Vladimir Korzh 10 Overview of Rodent Zic Genes ............................................................... 179 Koula E. M. Diamand, Kristen S. Barratt, and Ruth M. Arkell 11 Rodent Zic Genes in Neural Network Wiring ...................................... 209 Eloísa Herrera vii viii Contents Part II Zic Family in Medicine 12 Zic Family Proteins in Emerging Biomedical Studies ......................... 233 Jun Aruga 13 ZIC1 Function in Normal Cerebellar Development and Human Developmental Pathology ....................................................................... 249 Jun Aruga and Kathleen J. Millen 14 ZIC2 in Holoprosencephaly .................................................................... 269 Kristen S. Barratt and Ruth M. Arkell 15 ZIC3 in Heterotaxy.................................................................................. 301 Helen M. Bellchambers and Stephanie M. Ware 16 Deregulation of ZIC Family Members in Oncogenesis ....................... 329 Rob Houtmeyers, Jabob Souopgui, and Sabine Tejpar 17 Roles of ZIC2 in Regulation of Pluripotent Stem Cells ....................... 339 Hisato Kondoh 18 Role of Zic Family Proteins in Transcriptional Regulation and Chromatin Remodeling ................................................................... 353 Minoru Hatayama and Jun Aruga Contributors Kota  Abe Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo, Japan Ruth M. Arkell Early Mammalian Development Laboratory, John Curtin School of Medical Research, The Australian National University, Canberra, ACT, Australia Jun Aruga Department of Medical Pharmacology, Nagasaki University, Graduate School of Biomedical Sciences, Nagasaki, Japan Kristen  S.  Barratt Early Mammalian Development Laboratory, John Curtin School of Medical Research, The Australian National University, Canberra, ACT, Australia Helen M. Bellchambers Department of Pediatrics, Indiana University School of Medicine, Indianapolis, IN, USA Vincent  Bertrand Aix-Marseille Université, CNRS, Institut de Biologie du Développement de Marseille, Marseille, France Guillaume  Bordet Aix-Marseille Université, CNRS, Institut de Biologie du Développement de Marseille, Marseille, France Koula E.M. Diamand Early Mammalian Development Laboratory, John Curtin School of Medical Research, The Australian National University, Canberra, ACT, Australia Jennifer Forecki Department of Cell Biology and Neuroscience, Montana State University, Bozeman, MT, USA Minoru Hatayama Department of Medical Pharmacology, Nagasaki University, Graduate School of Biomedical Sciences, Nagasaki, Japan Eloísa Herrera Instituto de Neurociencias de Alicante, Consejo Superior de Investigaciones Científicas-Universidad Miguel Hernández, CSIC-UMH, Alicante, Spain ix