CURRENT TOPICS IN DEVELOPMENTAL BIOLOGY “A meeting-ground for critical review and discussion of developmental processes” A.A Moscona and Alberto Monroy (Volume 1, 1966) SERIES EDITOR Paul M Wassarman Department of Developmental and Regenerative Biology Icahn School of Medicine at Mount Sinai New York, NY, USA CURRENT ADVISORY BOARD Blanche Capel Wolfgang Driever Denis Duboule Anne Ephrussi Susan Mango Philippe Soriano Cliff Tabin Magdalene Zernicka-Goetz FOUNDING EDITORS A.A Moscona and Alberto Monroy FOUNDING ADVISORY BOARD Vincent G Allfrey Jean Brachet Seymour S Cohen Bernard D Davis James D Ebert Mac V Edds, Jr Dame Honor B Fell John C Kendrew S Spiegelman Hewson W Swift E.N Willmer Etienne Wolff Academic Press is an imprint of Elsevier 225 Wyman Street, Waltham, MA 02451, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 125 London Wall, London, EC2Y 5AS, UK The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK First edition 2015 Copyright © 2015 Elsevier Inc All rights reserved No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein) Notices Knowledge and best practice in this field are constantly changing As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein ISBN: 978-0-12-407759-1 ISSN: 0070-2153 For information on all Academic Press publications visit our website at store.elsevier.com CONTRIBUTORS Youngwook Ahn Stowers Institute for Medical Research, Kansas City, Missouri, USA Aria C Attia Division of Human Genetics, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA Tiziano Barberi Pluripotent Stem Cell Differentiation Laboratory, Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, Texas, USA, and Department of Anatomy Neuroscience, The University of Melbourne, Parkville, Victoria, Australia Linda A Barlow Department of Cell and Developmental Biology; Graduate Program in Cell Biology, Stem Cells and Development, and Rocky Mountain Taste and Smell Center, University of Colorado School of Medicine, Anschutz Medical Campus, Aurora, Colorado, USA Onur Birol Program in Developmental Biology, Baylor College of Medicine, Houston, Texas, USA Bianca E Borchin Pluripotent Stem Cell Differentiation Laboratory, Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, Texas, USA, and Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia Samantha A Brugmann Division of Plastic Surgery, Department of Surgery, and Division of Developmental Biology, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA Ching-Fang Chang Division of Plastic Surgery, Department of Surgery, and Division of Developmental Biology, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA Bharesh Chauhan Division of Pediatric Ophthalmology and Strabismus, Department of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA Alwyn Dady* Laboratoire de Biologie du De´veloppement, Universite´ Pierre et Marie Curie-Paris 6, and CNRS, Laboratoire de Biologie du De´veloppement, Paris, France *Present address: Children’s Hospital of Pittsburgh, Rangos Research Building, Pittsburgh, Pennsylvania, USA xi xii Contributors Jean-Loup Duband Laboratoire de Biologie du De´veloppement, Universite´ Pierre et Marie Curie-Paris 6, and CNRS, Laboratoire de Biologie du De´veloppement, Paris, France Rene´e K Edlund Program in Developmental Biology, Baylor College of Medicine, Houston, Texas, USA Katherine A Fantauzzo Department of Developmental and Regenerative Biology, Icahn School of Medicine at Mount Sinai, New York, USA Alessandro Fantin UCL Institute of Ophthalmology, University College London, London, United Kingdom Vincent Fleury Laboratoire Matie`re et Syste`mes Complexes, CNRS et Universite´ Denis-Diderot-Paris 7, Paris, France Andrew K Groves Program in Developmental Biology; Department of Molecular and Human Genetics, and Department of Neuroscience, Baylor College of Medicine, Houston, Texas, USA Ophir D Klein Departments of Orofacial Sciences and Pediatrics; Program in Craniofacial and Mesenchymal Biology, and Institute for Human Genetics, University of California San Francisco, San Francisco, California, USA Takahiro Kunisada Department of Tissue and Organ Development, Regeneration and Advanced Medical Science, Gifu University Graduate School of Medicine, Gifu, and Japan Science and Technology Agency ( JST), Core Research for Evolutional Science and Technology (CREST), Tokyo, Japan Anthony-Samuel LaMantia George Washington University Institute for Neuroscience, and Department of Pharmacology and Physiology, The George Washington University, School of Medicine and Health Sciences, Washington, DC, USA Richard Lang The Visual Systems Group, Abrahamson Pediatric Eye Institute, Division of Pediatric Ophthalmology, Department of Ophthalmology, University of Cincinnati and Children’s Hospital Research Foundation, Cincinnati, Ohio, USA Ming Lou Department of Chemistry and Physics, Lamar University, Beaumont, Texas, USA Sally A Moody Department of Anatomy and Regenerative Biology, The George Washington University, School of Medicine and Health Sciences, and George Washington University Institute for Neuroscience, Washington, DC, USA Contributors xiii Tsutomu Motohashi Department of Tissue and Organ Development, Regeneration and Advanced Medical Science, Gifu University Graduate School of Medicine, Gifu, and Japan Science and Technology Agency ( JST), Core Research for Evolutional Science and Technology (CREST), Tokyo, Japan William A Mun˜oz Stowers Institute for Medical Research, Kansas City, Missouri, USA Jason M Newbern School of Life Sciences, Arizona State University, Tempe, Arizona, USA Noriko Osumi Department of Developmental Neuroscience, Centers for Neuroscience, Tohoku University Graduate School of Medicine, Sendai, Japan Timothy Plageman College of Optometry, The Ohio State University, Columbus, Ohio, USA Alice Plein UCL Institute of Ophthalmology, University College London, London, United Kingdom Christiana Ruhrberg UCL Institute of Ophthalmology, University College London, London, United Kingdom Gerhard Schlosser School of Natural Sciences & Regenerative Medicine Institute (REMEDI), National University of Ireland, Galway, Ireland Elizabeth N Schock Division of Plastic Surgery, Department of Surgery, and Division of Developmental Biology, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA Philippe Soriano Department of Developmental and Regenerative Biology, Icahn School of Medicine at Mount Sinai, New York, USA Rolf W Stottmann Division of Developmental Biology, and Division of Human Genetics, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA Jun Suzuki Department of Developmental Neuroscience, Centers for Neuroscience, and Department of Otorhinolaryngology-Head and Neck Surgery, Tohoku University Graduate School of Medicine, Sendai, Japan Paul A Trainor Stowers Institute for Medical Research, Missouri, and Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, Kansas, USA PREFACE Neural crest cells and placodes give rise to an extraordinary array of cell types and tissues Neural crest cells form bone; cartilage; odontoblasts of teeth; connective tissue; cranial and trunk sensory neurons; peripheral autonomic neurons; and glia, smooth muscle, pigment, and endocrine cells Ectodermal placodes contribute to the major sensory organs including the olfactory epithelium, lens of the eye, inner ear, and teeth and generate most of the cranial sensory neurons, together with hair and mammary glands Neural crest cells and placodes are essential for embryonic development and adult homeostasis and are increasingly clinically significant Collectively, they generate many of the defining characteristics of the craniates and have played major roles in vertebrate evolution Neural crest cells and placodes were discovered independently in the nineteenth century and in different species Neural crest cells were first described by His (1868) in chick embryos, while placodes were described a little latter by van Wijhe (1883) in sharks The study of neural crest cells and placodes exhibits a rich history, serving as important paradigms for vertebrate evolution, cell and tissue induction, epithelial to mesenchymal transformation, migration, and differentiation, while also providing a profound understanding of the underlying pathogenesis of congenital disorders The persistence of neural crest cells and placodes into adulthood serves as important models of stem cell biology and tissue homeostasis and provides insights into cancer and metastasis Recent studies in tunicates and amphioxus point to neural crest cells and placodes having independent evolutionary origins However, neural crest cells and placodes develop similarly in many respects and are mutually interdependent This is particularly true with respect to evolution and development of the vertebrate head and more specifically the peripheral nervous system For example, cranial neural crest cell-derived glia support placodederived neurons during the formation and function of the cranial sensory ganglia Furthermore, cranial neural crest cells establish corridors for the proper migration of epibranchial placode-derived neurons These properties are a reflection of their extensive coevolution This issue of Current Topics and Developmental Biology highlights the current state of our knowledge concerning the evolution and development of neural crest cells and placodes throughout the entire body Where and when xv xvi Preface did these specialized cells occur and how are they governed by signaling pathways and increasingly complex gene regulatory networks? What contributions these cells make to specific tissues and organs and how are they integrated? The answers to these questions together with the derivation and application of stem cell-derived neural crest and placode cells in regenerative medicine have major implications for understanding and potentially treating congenital disorders PAUL A TRAINOR If I have seen further it is by standing on the shoulders of Giants Isaac Newton CHAPTER ONE Neural Crest Cell Evolution: How and When Did a Neural Crest Cell Become a Neural Crest Cell William A Muñoz*, Paul A Trainor*,†,1 *Stowers Institute for Medical Research, Kansas City, Missouri, USA † Department of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, Kansas, USA Corresponding author: e-mail address: pat@stowers.org Contents Introduction Defining Neural Crest Cells Chordate Evolution and Vertebrate Origins Neural Crest Cell Origin Neural Crest Cell Evolution in Vertebrates Cranial Neural Crest Cell Gene Regulatory Network Evolution of Neural Crest Cell Gene Regulatory Networks Conclusions and Perspectives Acknowledgments References 11 13 15 18 20 20 Abstract As vertebrates evolved from protochordates, they shifted to a more predatory lifestyle, and radiated and adapted to most niches of the planet This process was largely facilitated by the generation of novel vertebrate head structures, which were derived from neural crest cells (NCC) The neural crest is a unique vertebrate cell population that is frequently termed the “fourth germ layer” because it forms in conjunction with the other germ layers and contributes to a diverse array of cell types and tissues including the craniofacial skeleton, the peripheral nervous system, and pigment cells among many other tissues and cell types NCC are defined by their origin at the neural plate border, via an epithelial-to-mesenchymal transition (EMT), together with multipotency and polarized patterns of migration These defining characteristics, which evolved independently in the germ layers of invertebrates, were subsequently co-opted through their gene regulatory networks to form NCC in vertebrates Moreover, recent data suggest that the ability to undergo an EMT was one of the latter features co-opted by NCC In this review, we discuss the potential origins of NCC and how they evolved to contribute to nearly all tissues and organs throughout the body, based on paleontological evidence together with an evaluation of the evolution of molecules involved in NCC development and their migratory cell paths Current Topics in Developmental Biology, Volume 111 ISSN 0070-2153 http://dx.doi.org/10.1016/bs.ctdb.2014.11.001 # 2015 Elsevier Inc All rights reserved William A Muñoz and Paul A Trainor INTRODUCTION Neural crest cells (NCC) are considered to be a vertebrate innovation that significantly contributed to the ability of chordates to diversify and radiate to most niches on the planet Originally identified by Wilhelm His in 1868 (Hall, 2000), NCC have been shown to contribute to almost all tissues throughout the body NCC give rise to neurons, glia, Schwann cells, cartilage, bone, smooth muscles, adipocytes, and melanocytes, among many others (Table 1) (Bronner & LeDouarin, 2012; Dupin, Creuzet, & Le Douarin, 2006; Le Douarin & Dupin, 2012) Interestingly, many of these cell types originally arose from the other germ layers, particularly the mesoderm, in vertebrates and nonvertebrate chordates (Bronner & LeDouarin, 2012; Dupin et al., 2006; Etchevers, Vincent, Le Douarin, & Couly, 2001) The function of the NCC and their diversity of cell and tissue derivatives lent to the idea that NCC constituted a “fourth germ layer” (Hall, 2000) One of the most significant accomplishments of the NCC was in contributing to evolution of a “new head” with a hinged jaw, special sense Table Contributions of NCC to tissues throughout the animal Peripheral nervous system Cranial sensory ganglia Sympathetic ganglia Parasympathetic ganglia Sensory dorsal root ganglia Schwann cells Ensheathing olfactory cells Satellite cells of PNS ganglia Central nervous system Meninges Enteric nervous system Ganglia Glial cells Enteric neurons Endocrine system Carotid body cells C cells (thyroid gland) Adrenal-medullary cells Fat tissue Adipocytes Skin and inner ear Melanocytes Dermal cells Blood vessels and heart Smooth muscle cells Pericytes Heart conotruncus Striated muscles Connective cells Tendons Extraocular muscles Craniofacial skeleton Odontoblasts Osteocytes Chondrocytes The tissues with NCC contributions and the terminally differentiated NCC-derived cell types that populate the respective tissues are summarized here Neural Crest Cell Evolution organs, and neural circuitry These novel, predominately NCC-derived tissues facilitated vertebrates becoming predatory, shifting away from the filtration feeding lifestyle of their Amphioxus-like ancestors (Gans & Northcutt, 1983; Northcutt & Gans, 1983) Additionally, NCC have become integral in the organization of the vertebrate brain, possibly facilitating its enhanced growth in vertebrates (Creuzet, Martinez, & Le Douarin, 2006; Le Douarin, Couly, & Creuzet, 2012) Deficiencies in NCC development are known to result in various birth defects including craniofacial and heart anomalies, disorders affecting the bowel and other organs, and loss of pigmentation in the skin and hair In contrast overproliferation of NCC can result in several aggressive tumor types (Butler Tjaden & Trainor, 2013; Noack Watt & Trainor, 2014) Therefore, the innovation of NCC is one of the most significant factors contributing to vertebrate evolution and diversity Understanding the mechanisms controlling the specification, migration, and terminal specification of NCC will provide insights into the evolutionary history of vertebrates and may lead to the development of therapies for treating disorders of NCC development, which are known collectively as neurocristopathies DEFINING NEURAL CREST CELLS NCC have been the focus of extensive research since their initial discovery, particularly with respect to the mechanisms underlying their formation, the signals that determine how and where they migrate, and to what cell types and tissues they contribute NCC are induced to form at the neural plate border, which is the junction between the neural ectoderm and surface ectoderm (Simoes-Costa & Bronner, 2013) During neurulation, the neural ectoderm elevates to form neural folds, which then join to form the neural tube During this process dorsal neuroepithelial cells lose their intercellular connections, acquire apicobasal polarity, and undergo and epithelial-to-mesenchymal transition (EMT) These processes facilitate the delamination and migration of NCC in streams or in chains (Fig 1A and B), which then proceed to their terminal sites of differentiation (Fig 1C) (Baker & Bronner-Fraser, 1997; Groves & LaBonne, 2014; Mayor & Theveneau, 2013) During their emigration from the neural plate or neural tube, NCC maintain a stem cell-like, multipotent state with the capacity for self-renewal (Bronner-Fraser & Fraser, 1988, 1989; Coelho-Aguiar, Le Douarin, & Dupin, 2013; Crane & Trainor, 2006; Dupin & Sommer, 2012; Le 512 Bianca E Borchin and Tiziano Barberi Grskovic, M., Javaherian, A., Strulovici, B., & Daley, G Q (2011) Induced pluripotent stem cells—Opportunities for disease modelling and drug discovery Nature Reviews Drug Discovery, 10(12), 915–929 http://dx.doi.org/10.1038/nrd3577 Inman, G J., Nicolas, F J., Callahan, J F., Harling, J D., Gaster, L M., Reith, A D., et al (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7 Molecular Pharmacology, 62(1), 65–74 Ito, M., Kawa, Y., Ono, H., Okura, M., Baba, T., Kubota, Y., et al (1999) Removal of stem cell factor or addition of monoclonal anti-c-KIT antibody induces apoptosis in murine melanocyte precursors The Journal of Investigative Dermatology, 112(5), 796–801 http:// dx.doi.org/10.1046/j.1523-1747.1999.00552.x Jessell, T M (2000) Neuronal specification in the spinal cord: Inductive signals and transcriptional codes Nature Reviews Genetics, 1(1), 20–29 http://dx.doi.org/ 10.1038/35049541 Jiang, X., Gwye, Y., McKeown, S J., Bronner-Fraser, M., Lutzko, C., & Lawlor, E R (2009) Isolation and characterization of neural crest stem cells derived from in vitrodifferentiated human embryonic stem cells Stem Cells and Development, 18(7), 1059–1070 http://dx.doi.org/10.1089/scd.2008.0362 Katsu, T., Ujike, H., Nakano, T., Tanaka, Y., Nomura, A., Nakata, K., et al (2003) The human frizzled-3 (FZD3) gene on chromosome 8p21, a receptor gene for Wnt ligands, is associated with the susceptibility to schizophrenia Neuroscience Letters, 353(1), 53–56 Kawasaki, H., Mizuseki, K., Nishikawa, S., Kaneko, S., Kuwana, Y., Nakanishi, S., et al (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cellderived inducing activity Neuron, 28(1), 31–40 Koehler, K R., Mikosz, A M., Molosh, A I., Patel, D., & Hashino, E (2013) Generation of inner ear sensory epithelia from pluripotent stem cells in 3D culture Nature, 500(7461), 217–221 http://dx.doi.org/10.1038/nature12298 Lazzari, G., Colleoni, S., Giannelli, S G., Brunetti, D., Colombo, E., Lagutina, I., et al (2006) Direct derivation of neural rosettes from cloned bovine blastocysts: A model of early neurulation events and neural crest specification in vitro Stem Cells, 24(11), 2514–2521 http://dx.doi.org/10.1634/stemcells 2006-0149 Lecanda, F., Cheng, S L., Shin, C S., Davidson, M K., Warlow, P., Avioli, L V., et al (2000) Differential regulation of cadherins by dexamethasone in human osteoblastic cells Journal of Cellular Biochemistry, 77(3), 499–506 Lee, G., Kim, H., Elkabetz, Y., Al Shamy, G., Panagiotakos, G., Barberi, T., et al (2007) Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells Nature Biotechnology, 25(12), 1468–1475 http://dx.doi.org/ 10.1038/nbt1365 Lee, G., Papapetrou, E P., Kim, H., Chambers, S M., Tomishima, M J., Fasano, C A., et al (2009) Modelling pathogenesis and treatment of familial dysautonomia using patientspecific iPSCs Nature, 461(7262), 402–406 http://dx.doi.org/10.1038/nature08320 Lee, G., Ramirez, C N., Kim, H., Zeltner, N., Liu, B., Radu, C., et al (2012) Large-scale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression Nature Biotechnology, 30(12), 1244–1248 http://dx.doi.org/10.1038/nbt.2435 Leung, A W., Kent Morest, D., & Li, J Y (2013) Differential BMP signaling controls formation and differentiation of multipotent preplacodal ectoderm progenitors from human embryonic stem cells Developmental Biology, 379(2), 208–220 http://dx.doi.org/ 10.1016/j.ydbio.2013.04.023 Li, W., & Cornell, R A (2007) Redundant activities of Tfap2a and Tfap2c are required for neural crest induction and development of other non-neural ectoderm derivatives in hPSCs into CP and NC 513 zebrafish embryos Developmental Biology, 304(1), 338–354 http://dx.doi.org/10.1016/j ydbio.2006.12.042 Menendez, L., Yatskievych, T A., Antin, P B., & Dalton, S (2011) Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells Proceedings of the National Academy of Sciences of the United States of America, 108(48), 19240–19245 http://dx.doi.org/10.1073/pnas.1113746108 Mengarelli, I., & Barberi, T (2013) Derivation of multiple cranial tissues and isolation of lens epithelium-like cells from human embryonic stem cells Stem Cells Translational Medicine, 2(2), 94–106 http://dx.doi.org/10.5966/sctm 2012-0100 Mica, Y., Lee, G., Chambers, S M., Tomishima, M J., & Studer, L (2013) Modeling neural crest induction, melanocyte specification, and disease-related pigmentation defects in hESCs and patient-specific iPSCs Cell Reports, 3(4), 1140–1152 http://dx.doi.org/ 10.1016/j.celrep.2013.03.025 Mizuseki, K., Sakamoto, T., Watanabe, K., Muguruma, K., Ikeya, M., Nishiyama, A., et al (2003) Generation of neural crest-derived peripheral neurons and floor plate cells from mouse and primate embryonic stem cells Proceedings of the National Academy of Sciences of the United States of America, 100(10), 5828–5833 http://dx.doi.org/10.1073/ pnas.1037282100 Morrison, S J., White, P M., Zock, C., & Anderson, D J (1999) Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells Cell, 96(5), 737–749 Motohashi, T., Aoki, H., Chiba, K., Yoshimura, N., & Kunisada, T (2007) Multipotent cell fate of neural crest-like cells derived from embryonic stem cells Stem Cells, 25(2), 402–410 http://dx.doi.org/10.1634/stemcells 2006-0323 Noisa, P., Lund, C., Kanduri, K., Lund, R., Lahdesmaki, H., Lahesmaa, R., et al (2014) Notch signaling regulates the differentiation of neural crest from human pluripotent stem cells Journal of Cell Science, 127(Pt 9), 2083–2094 http://dx.doi.org/10.1242/ jcs.145755 Ozair, M Z., Noggle, S., Warmflash, A., Krzyspiak, J E., & Brivanlou, A H (2013) SMAD7 directly converts human embryonic stem cells to telencephalic fate by a default mechanism Stem Cells, 31(1), 35–47 http://dx.doi.org/10.1002/stem.1246 Patthey, C., & Gunhaga, L (2011) Specification and regionalisation of the neural plate border The European Journal of Neuroscience, 34(10), 1516–1528 http://dx.doi.org/10.1111/ j.1460-9568.2011.07871.x Pla, P., & Larue, L (2003) Involvement of endothelin receptors in normal and pathological development of neural crest cells The International Journal of Developmental Biology, 47(5), 315–325 Pomp, O., Brokhman, I., Ben-Dor, I., Reubinoff, B., & Goldstein, R S (2005) Generation of peripheral sensory and sympathetic neurons and neural crest cells from human embryonic stem cells Stem Cells, 23(7), 923–930 http://dx.doi.org/10.1634/stemcells 2005-0038 Qiu, X., Yang, J., Liu, T., Jiang, Y., Le, Q., & Lu, Y (2012) Efficient generation of lens progenitor cells from cataract patient-specific induced pluripotent stem cells PLoS One, 7(3), e32612 http://dx.doi.org/10.1371/journal.pone.0032612 Rada-Iglesias, A., Bajpai, R., Prescott, S., Brugmann, S A., Swigut, T., & Wysocka, J (2012) Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest Cell Stem Cell, 11(5), 633–648 http://dx.doi.org/10.1016/j.stem.2012.07 006 Reichert, S., Randall, R A., & Hill, C S (2013) A BMP regulatory network controls ectodermal cell fate decisions at the neural plate border Development, 140(21), 4435–4444 http://dx.doi.org/10.1242/dev.098707 514 Bianca E Borchin and Tiziano Barberi Saika, S., Kawashima, Y., Miyamoto, T., Okada, Y., Tanaka, S., Yamanaka, O., et al (1998) Immunolocalization of hyaluronan and CD44 in quiescent and proliferating human lens epithelial cells Journal of Cataract and Refractive Surgery, 24(9), 1266–1270 Sauka-Spengler, T., & Bronner-Fraser, M (2008) A gene regulatory network orchestrates neural crest formation Nature Reviews Molecular Cell Biology, 9(7), 557–568 http://dx doi.org/10.1038/nrm2428 Stemple, D L., & Anderson, D J (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest Cell, 71(6), 973–985 Streit, A (2007) The preplacodal region: An ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia The International Journal of Developmental Biology, 51(6–7), 447–461 http://dx.doi.org/10.1387/ ijdb.072327as Stripecke, R., Carmen Villacres, M., Skelton, D., Satake, N., Halene, S., & Kohn, D (1999) Immune response to green fluorescent protein: Implications for gene therapy Gene Therapy, 6(7), 1305–1312 Suga, H., Kadoshima, T., Minaguchi, M., Ohgushi, M., Soen, M., Nakano, T., et al (2011) Self-formation of functional adenohypophysis in three-dimensional culture Nature, 480(7375), 57–62 http://dx.doi.org/10.1038/nature10637 Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell, 131(5), 861–872 http://dx.doi.org/10.1016/j.cell.2007.11.019 Thomson, J A., Itskovitz-Eldor, J., Shapiro, S S., Waknitz, M A., Swiergiel, J J., Marshall, V S., et al (1998) Embryonic stem cell lines derived from human blastocysts Science, 282(5391), 1145–1147 Wilson, Y M., Richards, K L., Ford-Perriss, M L., Panthier, J J., & Murphy, M (2004) Neural crest cell lineage segregation in the mouse neural tube Development, 131(24), 6153–6162 http://dx.doi.org/10.1242/dev.01533 Wormstone, I M., Tamiya, S., Marcantonio, J M., & Reddan, J R (2000) Hepatocyte growth factor function and c-Met expression in human lens epithelial cells Investigative Ophthalmology & Visual Science, 41(13), 4216–4222 Yan, Q., Gong, L., Deng, M., Zhang, L., Sun, S., Liu, J., et al (2010) Sumoylation activates the transcriptional activity of Pax-6, an important transcription factor for eye and brain development Proceedings of the National Academy of Sciences of the United States of America, 107(49), 21034–21039 http://dx.doi.org/10.1073/pnas.1007866107 Yang, C., Yang, Y., Brennan, L., Bouhassira, E E., Kantorow, M., & Cvekl, A (2010) Efficient generation of lens progenitor cells and lentoid bodies from human embryonic stem cells in chemically defined conditions The FASEB Journal, 24(9), 3274–3283 http://dx doi.org/10.1096/fj.10-157255 Zeng, H., Guo, M., Martins-Taylor, K., Wang, X., Zhang, Z., Park, J W., et al (2010) Specification of region-specific neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells PLoS One, 5(7), e11853 http://dx.doi.org/ 10.1371/journal.pone.0011853 Zhou, Y., & Snead, M L (2008) Derivation of cranial neural crest-like cells from human embryonic stem cells Biochemical and Biophysical Research Communications, 376(3), 542–547 http://dx.doi.org/10.1016/j.bbrc.2008.09.032 INDEX Note: Page numbers followed by “f ” indicate figures and “t ” indicate tables A B a7.6 blastomeres, C intestinalis, 10–11 a9.49 blastomeres, C intestinalis, 11 AC See Apical constriction (AC) Actin cytoskeleton extrinsic force transmission, filopodia, 382–384 guanine nucleotide dissociation inhibitors, 378–379 intrinsic force generation, 384–389 placode formation, in epithelial morphogenesis, 379–382 Rho GTPase-activating proteins, 378–379 Rho guanine-nucleotide exchange factors, 378–379 Activin βA, 426–427 Adenohypophyseal cell types, differentiation of, 248 Adenohypophyseal placodes, 240–242 ADP ribosylation factor-like interacting protein (Arl6ip1), 115–116 Adult taste cell renewal and embryonic development, 409–410 Ajuba LIM proteins, 56 ALK inhibitor, 503 Anteroposterior patterning, 244f, 246, 250–251 Anti-Akt-phosphosubstrate antibody, 163 Antiphosphatases, 52–54 Ap2-Cre alleles, 160–161 Apical constriction (AC), 384–385 bicellular deformations, 387 DRhoGEF2, 385–386 Drosophila gastrulation, 385–386 myosin filaments, 385–386 p120-catenin, 387 Shroom3, 386–387 Apical progenitor cells, 357 Ascl1, 408 Axin2 expression levels, 122 Axonally derived Nrg-1, 214–215 Bardet–Biedl syndrome (BBS), 104–105, 113–115 BAs See Branchial arches (BAs) Basal body–ciliary vesicle complex, 103 Basal progenitor cells, 357 Basic helix loop helix (bHLH) transcription factors, 249–250 Bax, 213 Bbs1 and Bbs4 morphant zebrafish, 124 bbs zebrafish morphants, NCC migration, 105 β-catenin, 467–468 Bilateria, 272 ectodermal patterning, 268–270 neurosecretory and sensory cell types, 270–272 Bimetallic strip mechanism, of optic cup morphogenesis, 390–391 Bioluminescence resonance energy transfer (BRET), RTK signaling, 165–166 Biosensors, RTK signaling, 165–166 Bmi-1, 57 BmprIa inactivation, 426 BMP signaling in CP development, 509 PPE gene induction, 310–311 skin appendage placode formation, 446 Bone morphogenetic protein (BMP)-4, 473, 500 Border specifiers, 30–31, 45 Boundary cap progenitors, 209–210 Branchial arches (BAs) development of, 469–471 ectoderm, mesoderm, and endoderm, 469–471 germ layers and neural crest cells in, 470f signals and transcriptional regulators, 472–474 Branchio-oculo-facial syndrome, 333 515 516 Branchio-otic-renal syndrome (BOR), 333–334 Branchio-otic syndrome (BOS3), 333–334 Brn3a, 211–212 C Cadherin-11 (CAD11), 502 Cadherin-6B, 33–34 Canonical Wnt signaling, disruption of, 467–468 Cardiac NCC-mediated vascular remodeling, signaling pathways in, 188–191 Cardiac neural crest cells (NCCs), 5–7, 138–141 ablation of, 188 cardiac conduction system, 193 cardiac valves, 191–192 congenital abnormalities, 193–195 description of, 183–184 fibroblast growth factor 8, 189 history of, 183–184 migration, 183–184, 185f murine OFT and PAA development, 183–184, 185f in myocardial development, 192–193 outflow tract septation, 187–188 PAA remodeling, 184–187 SEMA3C, 191 transforming growth factor β family, 189 VEGF-A, 190, 191 Catweasel (Cwe) mouse mutant, 333–334 CD44 surface markers, 509 Cellular differentiation, regulation of, 321 cranial ganglion sensory neurons, 327–330 olfactory receptor neurons, 322–326 Cellular reprogramming, iPSC discovery, 499 Cephalic NCCs See Cranial neural crest cells (NCCs) CHARGE syndrome, 194–195 CHD-7, 49 CHD7 gene, 194–195 Chemotaxis, 105 Index Chordates, 264–265 ectodermal patterning, 260–262 neurosecretory and sensory cell types, 262–264 Chromatin remodellers, 49 Ciliary mutants, craniofacial phenotypes of, 107f Ciliogenesis, 101–103 Cilium, 98 functional domains, 101–102 primary (see Primary cilium) structure of, 98–99 types of, 98–99 Ciona intestinalis a9.49 blastomere, 11 a7.6 blastomere pair, 10–11 Circumvallate papilla (CVP), 405–406 Class semaphorin (SEMA3), cardiac NCC, 191 c-MET surface markers, 509 Coculture method NCC derivation, 500–501 schematic illustration, 504, 506f Common placodal field See Preplacodal ectoderm (PPE) Complex sequential signaling, 463–467 Congenital malformations, 141–142 Core epithelium-to-mesenchyme transition (EMT) regulatory factors activity of, 54–59 control mechanism of, 43, 44f epigenetic control of, 47–49 Snail-1/2, 41–43 stability and intracellular location, control of, 49–54 transcriptional and translational controls of, 45–47 Twist-1, 41–43 Corneal keratocytes, 75 Cranial neural crest cells (NCCs), 138–141, 471 description, 5–7 gene regulatory network, 13–15 Cranial placodes (CPs) derivation from hESC/hIPSC, 508–510 description of, 498 517 Index Cranial sensory placodes cranial sensory neurons, genesis of, 303–304 description of, 302 ectodermal domains, 302–303, 303f preplacodal ectoderm (see Preplacodal ectoderm (PPE)) Craniofacial ciliopathies animal models for, 108–112, 109t human, 113–115, 114t Craniofacial-deafness-hand syndrome, PAX3 mutation, 333 CVP See Circumvallate papilla (CVP) D Dachshund (Dac), 316–317 Dental papilla, 424–425 Dependence receptors, 216–217 Dermal condensation, 434–435, 436, 438 Deuterostomes, 265, 267–268 ectodermal patterning, 266–267 neurosecretory and sensory cell types, 267 Developmental systems drift, 237 DGS See DiGeorge syndrome (DGS) Diabetic patients, taste preferences in, 402 Diastema, 422–424 Differentiated NCC-derived cells, 78–82 DiGeorge syndrome (DGS), 194 Dimeric glycoprotein hormones, 247 Distal-less-related homeobox transcription factors, 306 Dkk1, 428 DLX3 mutations, 333 DLX5 mutations, 333 DNA methylation, 47–48 DNA-methyltransferases (DNMTs), 47–48 Dorsal root entry zone (DREZ)-associated boundary cap cells, 209 Dorsal root ganglia (DRG) satellite glia in, 213–214 sensory neurogenesis in, 210–212 Wnt/β-catenin signaling, 203 Dorsoventral patterning, 243–245, 244f, 250–251 DRG See Dorsal root ganglia (DRG) Drosophila Eyes absent (Eya), 314–316 Drosophila melanogaster, 474 Drosophila Sine oculis (SO), 313–314 Ductus arteriosus, 186 Dyneins, 100 Dysgenetic neurocristopathies, 141–142 E Ear development of, 484 inner (see Inner ear) mammalian (see Mammalian ear) outer (see Outer ear) Ectoderm, 469–471 Ectodermal patterning bilateria, 268–270 chordates, 260–262 deuterostomes, 266–267 and placode induction, 243, 244f tunicate–vertebrate clade, 251–256 Ectodysplasin (Eda) signaling pathway, tooth development, 429 Egr2/Krox-20, 209–210 Emberger syndrome, 333 Embryoid bodies (EB) method NCC derivation, 501–503 schematic illustration, 504, 506f validity and utility, 505 Embryonic development and adult taste cell renewal, 409–410 Embryonic olfactory epithelium, 357 Embryonic taste bud development, 404t Endoderm, 469–471 Endothelin (EDN1), 473 Enlarged vestibular aqueduct syndrome, 333 Epibranchial placodes, 242 Epidermal NCSC (EPI-NCSC), 77 Epigenetic profiling, NCC, 19 EPI-NCSC See Epidermal NCSC (EPI-NCSC) Epithelial cell elongation, 387–388 Epithelial morphogenesis, placode formation in, 379–382 Eps8, 382–383 ErbB receptors, 142–143 Erythropoietin-producing hepatocellular carcinoma (Eph) receptors, 144–146 Eumetazoa ectodermal patterning, 273 neurosecretory and sensory cell types, 273–275 518 Eustachian tube, 462–463 Evagination, 376–378 Evolution, 236–237 Extracellular ciliogenesis, 102–103, 102f Eya domain (ED), 314–316 EYA1 mutations, 334 Eye morphogenesis, in mouse actin cytoskeleton, 378–389 evagination, 376–378 features of, 376–378, 377f force sensors, 392 invagination, 376–378 optic cup (see Optic cup (embryology), shaping of ) pathways, schematic illustration, 379–380, 381f F Familiar dysautonomia (FD), hiPSC derivation from, 501 F-box protein partner of paired (PPA), 50 FBXL-14, 50 Fibroblast growth factor (FGF8) cardiac NCC, 189 Fibroblast growth factor (FGF) receptors, 146–149 Fibroblast growth factor (FGF) signaling pathway hair follicle development, 438 PPE gene induction, 310 skin appendage placode formation, 446 tooth development, 427 Filopodia contractile function of, 383–384 definition of, 382 laser ablation studies of, 383–384 Rho family GTPase Cdc42, 382–383 role in morphogenesis, 383–384 Filopodiogenesis pathway, 382–383 Fluorescence-activated cell sorting (FACS) purification, of putative NCSC, 500–501 Fluorescence resonance energy transfer (FRET) biosensors, RTK signaling, 166 Forkhead (FKH) proteins archetypal pioneer factors, 474–476 pioneer factors, 474–476 as transcription factors, 474–476 Index F€ orster resonance energy transfer (FRET) biosensors, RTK signaling, 166 Four-helix cytokine-like proteins, 247 Fourth germ layer See Neural crest (NC) FOXA proteins, 475–476 FoxD3, 17 FoxD genes, 17 Foxg1-Cre transgene, 160–161 Foxi1, 309 Foxi1/3 factors expression, regulation and function of, 477–479 functional role of, 479–480 role in jaw, middle ear, and outer ear development, 481–483 Foxi2 factors, 479 FOXI1 mutations, 333 FOX proteins, 475 Frizzled-3 (FZD3), 502 Fto zebrafish morphants , NCC migration, 105 Fuzzy mouse, NCC development, 112 G GATA2 and GATA3 mutations, 333 Gene regulatory network (GRN), NCC, cranial NCC, 13–15 evolution of, 15–18 Genetic co-option, in NCCs, 15–16, 16f Genetic knockin approaches, RTKs, 161–162 Genetic lineage-tracing system, 367 Genetic piracy, 237 Genomewide chromatin immunoprecipitation analyses, 447–448 Gleevec, 163 Gli1, 412 Gli2, 412 Glial cell plasticity embryogenesis, 80–81 Schwann cells, 79–80 Gliogenesis, in PNS axonally derived Nrg-1, 214–215 Delta signaling, 214 Notch signaling, 214 Schwann cell progenitors, 213–215 Globose basal cells (GBCs), 357–358, 365 519 Index Glycogen synthase kinase-3β (GSK-3β)dependent process, 49–50 Glycogen synthase kinase-3β (GSK-3β)independent ubiquitin ligases, 50 GnRH neurons, 366–367 Gonadotropin-releasing hormone (GnRH) forms, 248 G-protein-coupled receptor 161 (Gpr161), 121 Groucho, 316 Growth arrest specific-1 (Gas1), 432–433 GSK-3 inhibitor, 503–504 H Hair cells, 249, 462 Hair follicle development Eda signaling pathway, 437 Fgf signaling pathway, 438 and hair placode induction, 439 heterotopic transplant assays, 434–435 initiation of, 434–435 molecular and cellular mechanisms, 440–441 Shh signaling pathway, 438 Tgf-β/Bmp signaling pathway, 437 waves of, 434 Wnt/β-catenin signaling pathway, 436–437 HBCs See Horizontal basal cells (HBCs) Hedgehog pathway, 473–474 Hepatocyte growth factor (HGF)/scatter factor (SF), 151 hESC/hIPSC, CP cell derivation from, 510t monolayer culture method, 508–509 hESC/hIPSC, NCC derivation from, 505t coculture method, 500–501 embryoid bodies method (see Embryoid bodies (EB) method) monolayer culture method, 503–504, 507 Pax6 expression, 499–500 Hirschsprung disease, 115–116 Histone deacetylases (HDAC), 55 Histone methylation, 48–49 H3K9me3, 48–49 H3K27me3, 48–49 H3K36me3, 48–49 Horizontal basal cells (HBCs), 358 Cre-loxP lineage-tracing studies, 357–358 regulation of cellular dynamics, 361 Human congenital syndromes craniofacial defects, 330–332, 331t hearing loss, 330–332, 331t NB-specifying gene mutations, 333 PPE gene mutations, 333–334 Human craniofacial ciliopathies, 113–115, 114t Human pluripotent stem cells (hPSCs), neural plate border specification of, 498 Hypobranchial placodes, of frogs, 242–243 I Induced pluripotent stem cells (iPSCs), 499 Inductive morphogenesis, 384 Inner ear, 462 development, FOXI family members role in, 476–480 primordium, development of, 463–469 Interrupted aortic arch (IAA), 186–187 Intracellular ciliogenesis, 102–103, 102f Intraflagellar transport (IFT), 103 Invagination, 376–378 IRSp53, 382–383 Islet1, 211–212 Isobaric tag for relative and absolute quantitation (iTRAQ), RTK signaling, 164–165 Isotope labeling approach, RTK signaling, 164–165 iTRAQ See Isobaric tag for relative and absolute quantitation (iTRAQ), RTK signaling J Jaw development, FOXI family members role in, 481–483 Joubert syndrome, 119 Jumonji proteins (Jmj), 48–49 K Kallmann syndrome, 366–367 K14+ cells, 410–411 Kif3a proteins, 104–105 Kit receptors, 149–150 520 L Lamina propria (LP), multipotent stem cells in, 359 Lateral line placodes, 242 LATS-2, 51–52 Lens epithelial cells (LEC), 508, 509 Lens fiber cells, 250 Lens placode, 240–242 Leucine-rich repeat-containing G-protein coupled receptor (LGR5), 410–411 Leukemias, 333 Ligamentum arteriosus, 186 LIM domain only protein (LMO-4), 56–57 Lineage-restricted melanocytes, plasticity of, 81–82 Lingual taste papillae, 412–413 LIV-1, 51–52 LMX1a, 507 LY294002, 163 M Mammalian ear components of, 462–463 development, Foxi1 role in, 476 Mammalian muscle-specific kinase (MuSK) receptors, 151–152 Mammalian NCC development, RTK signaling in Eph receptors, 144–146 ErbB receptors, 142–143 FGF receptors, 146–149 Kit receptors, 149–150 MET receptors, 151 MuSK receptors, 151–152 PDGF receptors, 152–154 PTK7 receptors, 154–155 RET receptors, 155–156 ROR receptors, 156–157 Trk receptors, 157–159 VEGF receptors, 159–160 Mammalian pharyngeal development, Foxi3 role in, 483 Mammary placodes, in mice Eda signaling pathway, 444 Fgf10 expression, 442 formation along mammary line, 441–442, 441f hedgehog signaling, 443–444 Index molecular and cellular mechanisms, 444–445 Tbx3 expression, 442–443 Wnt10b analysis, 441–442 Wnt/β–catenin signaling pathway, 443 Mash1, 408 Mass spectrometry-based proteomic approach, 164 MDM-2, 50–51 Mechanosensation, 108 Meckel–Gruber syndrome (MKS), 113–115 Meckel’s cartilage, 471, 482 Melanomas, origin of, 86–88 Mesoderm, 469–471 Mesp1-Cre alleles, 160–161 Metazoan ectodermal patterning, 273 neurosecretory and sensory cell types, 273–275 Metazoan phylogeny, 238–239 cephalochordates, 239–240 deuterostomes, 240 ecdysozoans, 240 echinoderms, 240 hemichordates, 240 lophotrochozoans, 240 protostomes, 240 tunicates, 239–240 Methimazole, 365–366 Methylation of histone H3, 48–49 MET receptors, 151 MicroRNAs (miRNAs), 46–47 Middle ear, 462–463 branchial arches development, 469–471 FOXI family members role in, 481–483 structures, cranial neural crest cells, 471 Migratory patterns, of trunk NCCs extracellular matrix components, 204 somites, 206–207 timing and choice of, 204–206 Molecular regulators, of NCC migration F-spondin expression, 207–208 long-range, local and contact-dependent molecules, 208 secreted trophic factors, 207 somite-derived factors, 207–208 transcription factors, 207 in vivo clonal analyses, 208–209 Index Molecular signal transduction, primary cilium in, 119–124 Monolayer culture method, 503–504, 507 Morphological diversity, pioneer factors role in, 484–485 Motor exit point (MEP)-associated boundary cap cells, 209 Msk gene, 107–108 MSX1 defects, 333 Msx1 expression, tooth development, 429–430 Multipotency NCC-derived cells after delamination, from neural tube, 84–85 NC-derived lineage-restricted melanoblasts, 82–83 Multipotent stem cells, in lamina propria, 359 Myelinating Schwann cells, 213–214 N NB-specifying genes, 305–306 NCCs See Neural crest cells (NCCs) NC-derived HBCs, 361–364 NCSC See Neural crest stem cells (NCSC) Neoplasms, 141–142 Neural border (NB) zone formation, 302–303, 305–309 Neural crest (NC), 353–354 Neural crest cells (NCCs), 471 amphioxus, BMPs, 14 cadherin expression sequence, 40–41, 42f in cardiovascular development (see Cardiac neural crest cells (NCCs)) categorization of, 5–7 cell sorting mechanisms, 31–32 cephalochordates, 8f, chordates, 8–9 C intestinalis, 10–11 clonal analysis of, 71 contributions of, 4, 4t co-option of genes, 15–16, 16f deficiencies in, 4–5 delamination cadherin-6B, 35–39, 38f EMT regulatory factors, 34–35 521 N- and E-cadherin, 39–40 phase, 28–29 tetraspanin-18, 35–36 delamination of, 14–15 derivation from hESC/hIPSC, 499–510 description of, 70, 138–141, 353–354, 498 E11.5 mouse embryo, 141f, 142 epithelial to mesenchymal transition, 203 extracellular cues, 202–203 features of, gene regulatory network (see Gene regulatory network (GRN), NCC) genomic high-throughput methodology, 15 glial cells (see Glial cell plasticity) induction during gastrulation, 30 Kit expression, 71 mammalian embryogenesis, 138–141 migration and differentiation, in mice, 5, 6f migration phase, 28–29 molecular manipulation, 13–14 molecular regulators of, 207–209 multipotency and regionalization of, 7–8 multipotent, 75 N- and E-cadherin, 31–32, 33 neural plate border transcription factors, 14–15 neurulation, origin of, 9–11 PNS development (see Peripheral nervous system (PNS) development) polonaise movements, 33–34 premigration phase, 28–29 progenitors assembly of, 31 generation of, 29–30 position of, 30–31 regulatory module, 14 Snail proteins, 49–50, 53f, 58f specification, 30, 35f specification of, 202–204 specifiers, 14–15, 16f, 18 ultimate phase, 28–29 ventrally and dorsolaterally migrating NCC, 70 vertebrates, 8–9, 8f, 11–13 522 Neural crest-derived cells (NCDCs) in adult olfactory epithelium, 361–364, 362f description of, 353–354 Neural crest stem cells (NCSC), 71–72 carotid body, 74 in DRG, 72–74 FACS purification, 500–501 hair follicle and dermis, 76–78 P75, 72–74 in palatal tissues, 80 purified, 74 research, 72–74 skin-derived precursors, 76–77, 78 sphere-forming cells, 75–76 Neural ectoderm, 245 Neural plate border transcription factors, 14–15 Neuregulin (Nrg3), 444 Neurocristopathies, 4–5, 141–142 NeuroG and NeuroD expression, 327–328 Neurogenins, 211–212 Neurosecretory cells, 247–249 Neurulation, Nodal cilia, 100 Noggin, 437 Non-myelinating Schwann cells, 213–214 Nonneural ectoderm, 245 preplacodal region formation, 463–467 Notch function, 408 Notch inner cellular domain (NICD), 87 Notch signaling gliogenesis, in PNS, 214 for NC derivation, 504 otic placode induction, 467–469 primary cilium, 123–124 Novelty, 236–237 Ntrk1, 158–159 Nuclear Snail proteins, 51–52 O Odontogenesis, 117 Odorant and pheromone receptor cell, 248–249 OECs See Olfactory ensheathing cells (OECs) Olfactory ectomesenchymal stem cells (OE-MSCs), 359 Index Olfactory ensheathing cells (OECs), 354 description of, 359 origin of, 360–361 Pax7, 360–361 in regenerative medicine, 359 Wnt1-Cre reporter system, 360–361 Olfactory epithelium (OE) adult OE maintenance, 357–358 characteristics, 352 embryonic and adult OE, structure of, 352, 353f primary and secondary neurogenesis, 356–357 Olfactory mucosa (OM), 357 Olfactory placode (OP) BMP and FGF signals, 356 definition of, 354 development, 355–356 fate-mapping studies, 354 formation, 355–356 Pax6 and Dlx5 expression, 355–356 retinoic acid signaling, 356 Olfactory placodes, 240–242 Olfactory receptor cell, 248–249 Olfactory receptor neurons (ORNs) description of, 303–304, 365–366 genesis of, 322–325, 323f identity, 326 placodal ectoderm, 322–325 Optic cup (embryology), shaping of bimetallic strip mechanism, 390–391 Cdc42 conditional mutant mice, 390 lens pit invagination depth, 389–390 Organ culture experiments, 442–443 Oro-facial-digital (OFD) syndrome, 113–115, 119 Otic-epibranchial progenitor domain (OEPD), 467 Otic placode induction by FGFs, 467–469 Foxi1/3 functional role in, 479–480 requirements for, 466f Otic placodes, 242 Otic progenitors, 509 Oto-facio-cervical syndrome, 334 OTX2 mutation, 334 Index Outer ear, 463 branchial arches development, 469–471 FOXI family members role in, 481–483 Outgroup comparison method, 237–238, 238f P PAA remodeling See Pharyngeal arch artery (PAA) remodeling PAK-1, 51–52 Paladin, 52–54 p75 and HNK, hPSC differentiation, 507 Panplacodal progenitors, from hPSCs, 509 Pan-placodal region See Preplacodal ectoderm (PPE) Paratympanic placodes, of birds, 242–243 Pax2-expressing cells, 467–468 Pax9 expression, tooth development, 429–430 Pax6, in lens development, 379–380 PAX2 mutation, 334 PAX3 mutation, 333 PAX6 mutation, 334 PAX8 mutation, 334 PDGF receptors, 152–154 Peptide hormones, 247 Peripheral nervous system (PNS) development gliogenesis in, 213–215 schematic illustration, 204, 205f Schwann cell progenitors, 213–215 trophic signaling mechanisms, 215–217 Persistent truncus arteriosus, 183–184 Pharyngeal arch artery (PAA) remodeling, 184–187 Pharyngeal arches See Branchial arches (BAs) Phospho-specific reagents, for RTK activation antibodies, 162–163 downstream signaling networks, 164 pharmacological inhibitors, 163 in vitro studies, 163 Western blotting techniques, 163 Phosphosubstrate-specific antibodies, 163 Pioneer factors FKH proteins, 474–476 role in morphological diversity, 484–485 523 Placode-derived HBCs, 361–364 Placode formation, in epithelial morphogenesis, 379–382 Placode formation, skin appendages Bmp signaling, 446 cellular mechanisms, 447 Eda pathway, 446 Fgf signaling, 446 Shh signaling, 447 Wnt/β–catenin signaling, 445–446 Planar cell polarity (PCP) pathway, 104–106 Plasticity glial cell, 79–81 lineage-restricted melanocytes, 81–82 Platelet-derived growth factor (PDGF)dependent chemotaxis, 105–106 p75 low-affinity neurotrophin receptor (p75NTR), 212–213 Pluripotent stem cell differentiation, 499 PNS development See Peripheral nervous system (PNS) development Polaris mutants, tooth development, 432–433 Postmigratory NCSC, 72–76, 73t Preneural ectoderm, exposure of, 464–465 Preplacodal ectoderm (PPE) description of, 304–305 development of, 243–245 formation of, 305–306, 307f gene induction by signaling factors, 310–313 NB zone formation, 305–309 patterning and placode induction, 243, 244f regionalization of, 319–321 Ripply3 and Tbx1 expression domains, 312–313 Six and Eya genes, 304–305 subdivisions of, 246–247 transcriptional regulators, 313–318 Presumptive lens–retina interface, 380–382 Primary cilium animal models, 108–113 causes of, 100 9+0 conformation of, 99 definition of, 98–99 differentiation of NCC, 107–108 524 Primary cilium (Continued ) extension and retraction, 101 fibroblast growth factor signaling pathway, 122–123 human craniofacial ciliopathies, 113–115 length, 101 loss of, 115–116, 116f migration of NCC, 105–106 molecular signal transduction, 119–124 NCC specification, 104–105 nonmotile status, 100 Notch signaling, 123–124 platelet-derived growth factor signaling, 123 proliferation of NCC, 106–107 solitary cellular extensions, 100 Sonic hedgehog, 120–121 structure of, 99f tissue–tissue interactions, 116–119 Primary enamel knot, 424–425 Primary hair follicle formation, 434–435, 435f Primary neurogenesis, OE, 356–357 Profundal and trigeminal placodes, 242 Protein tyrosine kinase (PTK7) receptors, 154–155 Proteomics, NCC, 19 Ptch1, 412 p53 tumor suppressor, 50–51 R Rac1 actin modulation pathways, 388–389 Raldh2, 312–313 Rapamycin, 163 Rearranged during transfection (RET) receptors, 155–156 Receptor tyrosine kinase (RTK) signaling biosensors, 165–166 in mammalian NCC development, 142–160 murine NCC development, 138–141, 139t phospho-specific reagents, 162–164 proteomics, 164–165 receptor activation, 138 receptor allelic series, 160–162 schematic representation of, 136, 137f Reichert’s cartilage, 471, 482 Index Retinal pigmented epithelium (RPE), 376–378 Retinoic acid (RA), 391 PPE gene induction, 312–313 RhoA actin modulation pathways, 388–389 RTK-like orphan receptor (ROR) receptors, 156–157 RTK signaling See Receptor tyrosine kinase (RTK) signaling Runx family, of transcription factors, 211–212 S Sacral NCCs, 138–141 Sacral neural crest cells, 5–7 Schwann cell precursors (SCP), 79, 80–81 Secondary enamel knot, 424–425 Secondary neurogenesis, OE, 356–357 Sema6A expression, 209 Sensory neurogenesis, in DRG Brn3a and Islet1, 211–212 Neurogenins, 211–212 proneural transcription factors, 211–212 TrkA+ nociceptive neurons, 210–211 trophic factor signaling, 210 Sensory neuron development Bax, 213 genetic deletion mutants, 212 neurotrophic factor responsiveness, 212 p75 low-affinity neurotrophin receptor, 212–213 Shotgun proteomics strategy, RTK signaling, 164 Shroom3, 386–387 Side population (SP) cells, 75 Signaling pathways, function of, 404t SILAC See Stable isotope labeling with amino acids in cell culture (SILAC), RTK signaling Sine oculis binding protein (Sobp), 316–317 Six genes, 304–305, 329 SIX1 mutations, 333–334 Skin appendages development site of, 422 patterning and morphogenesis of hair follicles, 434–441 mammary glands, 441–445 teeth, 422–434 Index placode formation Bmp signaling, 446 cellular mechanisms, 447 Eda pathway, 446 Fgf signaling, 446 Shh signaling, 447 Wnt/β–catenin signaling, 445–446 position, number and size of, 422 Skin-derived precursors (SKP), 76–77, 78 Snail proteins, 49–50, 53f Somatosensory neurons, 249 Sonic hedgehog (Shh), 473–474 Sonic hedgehog (Shh) signaling pathway, 412–413 hair follicle development, 438 primary cilium, 120–121 skin appendage placode formation, 447 specification of ventral neural tube cells, 33–34 tooth development, 427 SOX10 reporter, for NC cell isolation, 507–508 Spectral counting process, 164 Split-hand/foot malformation syndrome, 333 Sponges, 275 Stable isotope labeling with amino acids in cell culture (SILAC), RTK signaling, 164–165 Stereocilia, 249 Stromal-derived inducing activity (SDIA) method, 500 Supernumerary teeth Bmp signaling, 426 ectopic activation, 431 growth arrest specific-1, 432–433 Osr2-null mice, 431 Sostdc1, 432 Sprouty genes, 427 T Taste description, 402 preferences of, 402 sense of, 402–403 Taste buds classification of, 406–408 development of, 411–413 525 distribution of, 403 pattern of, 402–406 stem cell population, 410–411 Taste cell fate, regulation of, 406–409 Taste cell renewal, molecular regulation of, 411–413 Taste periphery, structure of, 413 Tbx2, 429–430 TBX1 mutation, 334 Tetraspanin-18, 35–36 TFAP2α, 309 TFAP2α mutations, 333 Tooth development Bmp–Wnt feedback loop, 430–431 ectopic activation, 431 Eda signaling pathway, 429 Fgf–Bmp interactions, 425–426 Fgf signaling pathway, 427 growth arrest specific-1, 432–433 molecular and cellular mechanisms of, 424–425 mouse embryogenesis, 424–425 Msx1 expression, 429–430 Pax9 expression, 429–430 Polaris mutants, 432–433 Shh signaling pathway, 427 site positioning of, 422–424, 423f Sostdc1, 432 Tgf-β/Bmp signaling pathway, 426–427 tooth number, position and size, 431–434 Wnt/β–catenin signaling pathway, 428–429 Tooth formation See Odontogenesis Transcriptional regulators, PPE Eya genes, 313 Groucho, 316 roles of, 318 Six2 and Six4, 314 Six genes, 313–314 Six1 role, 314 Transforming growth factor β (TGF β) family, cardiac NCC, 189 Trimethylated lysine of histone H3(H3K4me3), 48–49 Trophic signaling mechanisms, PNS development, 215–217 Tropomyosin-related kinase (Trk) receptors, 157–159 526 Trunk neural crest cells (NCCs), 5–7, 138–141 See also Peripheral nervous system (PNS) development vs cranial NCCs, 203–204 migratory patterns of, 204–207 Tunicate–vertebrate clade, 259–260 ectodermal patterning, 251–256 neurosecretory and sensory cell types, 256–259 Twist-1, 52, 57 Type b interruption See Interrupted aortic arch (IAA) Tyr-Cre allele, 160–161 Tyrosine autophosphorylation sites, 136–137 V Vagal neural crest cells (NCCs), 5–7, 138–141 Vascular endothelial growth factor (VEGF)-A, cardiac NCC, 190 Vascular endothelial growth factor (VEGF) receptors, 159–160 Vertebrate cranial placodes adenohypophyseal placode, 240–242 description of, 237–238 epibranchial placodes, 242 evolutionary history of, 276, 277f hypobranchial placodes, 242–243 lateral line placodes, 242 lens placode, 240–242 neurosecretory and sensory placodal cell types, 247–250 olfactory placode, 240–242 origin and patterning of, 243–247 otic placode, 242 paratympanic placodes, 242–243 Index profundal and trigeminal placodes, 242 schematic illustration, 240, 241f Viscerosensory neurons, 249 Vomeronasal receptor cell, 248–249 W Waardenburg syndrome, PAX3 mutation, 333 Western blotting techniques, 163 Whisker formation, 118 Whole-genome duplication (WGD) events, 15 Wild-type vs Sostdc1-null mice, tooth patterns of, 422–424, 424f Wilms’ tumor protein (WT1), 405–406 Wls gene, 404–405 Wnt agonists, NC cells, 503–504, 507 Wnt/β–catenin signaling pathway dorsal root ganglia, 203 hair follicle development, 436–437 mammary placodes, in mice, 443 skin appendage placode formation, 445–446 tooth development, 428–429 Wnt1-Cre driver, 160–161 Wnt signaling, 464 otic placode induction, 467–469 PPE gene induction, 311–312 WT1 See Wilms’ tumor protein (WT1) X Xenopus embryonic development, ectodermal domains, 302–303, 303f Xenopus, Twist-1 function in, 52 Z Zeb-2 transcription factor, spatial control of, 59–60 Zic3 transcription factor, 10–11 ... consisting of both intrinsic and extrinsic input How these transcriptional regulators and signals were first incorporated into a GRN during evolution is beginning to elucidate the origin of NCC In. .. molecules involved in NCC development and their migratory cell paths Current Topics in Developmental Biology, Volume 111 ISSN 0070-2153 http://dx.doi.org/10.1016/bs.ctdb.2014.11.001 # 2015 Elsevier Inc... experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein In using such information or methods they should be mindful of their own safety