The Neural Crest Migrating Into the Twenty-First Century
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And Late-Migrating Cranial Neural Crest Cell Populations Have Equivalent Developmental Potential in Vivo
Development 124, 3077-3087 (1997) 3077 Printed in Great Britain © The Company of Biologists Limited 1997 DEV3724 Early- and late-migrating cranial neural crest cell populations have equivalent developmental potential in vivo Clare V. H. Baker1,2,*, Marianne Bronner-Fraser1, Nicole M. Le Douarin2 and Marie-Aimée Teillet2 1Division of Biology, Beckman Institute 139-74, California Institute of Technology, Pasadena, California 91125, USA 2Institut d’Embryologie cellulaire et moléculaire du CNRS et du Collège de France, 49bis avenue de la Belle Gabrielle, 94736 Nogent-sur-Marne Cedex, France *Author for correspondence currently at address1 SUMMARY We present the first in vivo study of the long-term fate and heterochronically for the late-migrating population, it no potential of early-migrating and late-migrating mesen- longer contributes to the jaw skeleton and only forms cephalic neural crest cell populations, by performing dorsal derivatives. When the late-migrating population is isochronic and heterochronic quail-to-chick grafts. Both grafted into a late-stage host whose neural crest had previ- early- and late-migrating populations form melanocytes, ously been ablated, it migrates ventrally into the jaws. neurons, glia, cartilage and bone in isochronic, isotopic Thus, the dorsal fate restriction of the late-migrating mes- chimeras, showing that neither population is lineage- encephalic neural crest cell population in normal develop- restricted. The early-migrating population distributes both ment is due to the presence of earlier-migrating neural dorsally and ventrally during normal development, while crest cells, rather than to any change in the environment or the late-migrating population is confined dorsally and to any intrinsic difference in migratory ability or potential forms much less cartilage and bone. -
Notch Signaling Regulates the Differentiation of Neural Crest From
ß 2014. Published by The Company of Biologists Ltd | Journal of Cell Science (2014) 127, 2083–2094 doi:10.1242/jcs.145755 RESEARCH ARTICLE Notch signaling regulates the differentiation of neural crest from human pluripotent stem cells Parinya Noisa1,2, Carina Lund2, Kartiek Kanduri3, Riikka Lund3, Harri La¨hdesma¨ki3, Riitta Lahesmaa3, Karolina Lundin2, Hataiwan Chokechuwattanalert2, Timo Otonkoski4,5, Timo Tuuri5,6,* and Taneli Raivio2,4,*,` ABSTRACT Kokta et al., 2013). Neural crest cells originate from neuroectoderm at the border between the neural plate and the Neural crest cells are specified at the border between the neural epiderm (Meulemans and Bronner-Fraser, 2004), and they are plate and the epiderm. They are capable of differentiating into marked by the expression of genes that are specific for the neural- various somatic cell types, including craniofacial and peripheral plate border, such as DLX5, MSX1, MSX2 and ZIC1. Later, during nerve tissues. Notch signaling plays important roles during the neural-tube folding process, neural crest cells remain within neurogenesis; however, its function during human neural crest the neural folds and subsequently localize inside the dorsal development is poorly understood. Here, we generated self- portion of the neural tube. These premigratory neural crest cells renewing premigratory neural-crest-like cells (pNCCs) from human express specifier genes, such as SNAIL (also known as SNAI1), pluripotent stem cells (hPSCs) and investigated the roles of Notch SLUG (also known as SNAI2), SOX10 and TWIST1 (LaBonne and signaling during neural crest differentiation. pNCCs expressed Bronner-Fraser, 2000; Mancilla and Mayor, 1996). Following the various neural-crest-specifier genes, including SLUG (also known formation of the neural tube, premigratory neural crest cells as SNAI2), SOX10 and TWIST1, and were able to differentiate into undergo an epithelial-to-mesenchymal transition (EMT) and most neural crest derivatives. -
The Migration of Neural Crest Cells and the Growth of Motor Axons Through the Rostral Half of the Chick Somite
/. Embryol. exp. Morph. 90, 437-455 (1985) 437 Printed in Great Britain © The Company of Biologists Limited 1985 The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite M. RICKMANN, J. W. FAWCETT The Salk Institute and The Clayton Foundation for Research, California division, P.O. Box 85800, San Diego, CA 92138, U.S.A. AND R. J. KEYNES Department of Anatomy, University of Cambridge, Downing St, Cambridge, CB2 3DY, U.K. SUMMARY We have studied the pathway of migration of neural crest cells through the somites of the developing chick embryo, using the monoclonal antibodies NC-1 and HNK-1 to stain them. Crest cells, as they migrate ventrally from the dorsal aspect of the neural tube, pass through the lateral part of the sclerotome, but only through that part of the sclerotome which lies in the rostral half of each somite. This migration pathway is almost identical to the path which pre- sumptive motor axons take when they grow out from the neural tube shortly after the onset of neural crest migration. In order to see whether the ventral root axons are guided along this pathway by neural crest cells, we surgically excised the neural crest from a series of embryos, and examined the pattern of axon outgrowth approximately 24 h later. In somites which contained no neural crest cells, ventral root axons were still found only in the rostral half of the somite, although axonal growth was slightly delayed. These axons were surrounded by sheath cells, which had presumably migrated out of the neural tube, to a point about 50 jan proximal to the growth cones. -
The Genetic Basis of Mammalian Neurulation
REVIEWS THE GENETIC BASIS OF MAMMALIAN NEURULATION Andrew J. Copp*, Nicholas D. E. Greene* and Jennifer N. Murdoch‡ More than 80 mutant mouse genes disrupt neurulation and allow an in-depth analysis of the underlying developmental mechanisms. Although many of the genetic mutants have been studied in only rudimentary detail, several molecular pathways can already be identified as crucial for normal neurulation. These include the planar cell-polarity pathway, which is required for the initiation of neural tube closure, and the sonic hedgehog signalling pathway that regulates neural plate bending. Mutant mice also offer an opportunity to unravel the mechanisms by which folic acid prevents neural tube defects, and to develop new therapies for folate-resistant defects. 6 ECTODERM Neurulation is a fundamental event of embryogenesis distinct locations in the brain and spinal cord .By The outer of the three that culminates in the formation of the neural tube, contrast, the mechanisms that underlie the forma- embryonic (germ) layers that which is the precursor of the brain and spinal cord. A tion, elevation and fusion of the neural folds have gives rise to the entire central region of specialized dorsal ECTODERM, the neural plate, remained elusive. nervous system, plus other organs and embryonic develops bilateral neural folds at its junction with sur- An opportunity has now arisen for an incisive analy- structures. face (non-neural) ectoderm. These folds elevate, come sis of neurulation mechanisms using the growing battery into contact (appose) in the midline and fuse to create of genetically targeted and other mutant mouse strains NEURAL CREST the neural tube, which, thereafter, becomes covered by in which NTDs form part of the mutant phenotype7.At A migratory cell population that future epidermal ectoderm. -
Migratory Patterns and Developmental Potential of Trunk Neural Crest Cells in the Axolotl Embryo
DEVELOPMENTAL DYNAMICS 236:389–403, 2007 RESEARCH ARTICLE Migratory Patterns and Developmental Potential of Trunk Neural Crest Cells in the Axolotl Embryo Hans-Henning Epperlein,1* Mark A.J. Selleck,2 Daniel Meulemans,3 Levan Mchedlishvili,4 Robert Cerny,5 Lidia Sobkow,4 and Marianne Bronner-Fraser3 Using cell markers and grafting, we examined the timing of migration and developmental potential of trunk neural crest cells in axolotl. No obvious differences in pathway choice were noted for DiI-labeling at different lateral or medial positions of the trunk neural folds in neurulae, which contributed not only to neural crest but also to Rohon-Beard neurons. Labeling wild-type dorsal trunks at pre- and early-migratory stages revealed that individual neural crest cells migrate away from the neural tube along two main routes: first, dorsolaterally between the epidermis and somites and, later, ventromedially between the somites and neural tube/notochord. Dorsolaterally migrating crest primarily forms pigment cells, with those from anterior (but not mid or posterior) trunk neural folds also contributing glia and neurons to the lateral line. White mutants have impaired dorsolateral but normal ventromedial migration. At late migratory stages, most labeled cells move along the ventromedial pathway or into the dorsal fin. Contrasting with other anamniotes, axolotl has a minor neural crest contribution to the dorsal fin, most of which arises from the dermomyotome. Taken together, the results reveal stereotypic migration and differentiation of neural crest cells in axolotl that differ from other vertebrates in timing of entry onto the dorsolateral pathway and extent of contribution to some derivatives. -
Fate of the Mammalian Cardiac Neural Crest
Development 127, 1607-1616 (2000) 1607 Printed in Great Britain © The Company of Biologists Limited 2000 DEV4300 Fate of the mammalian cardiac neural crest Xiaobing Jiang1,3, David H. Rowitch4,*, Philippe Soriano5, Andrew P. McMahon4 and Henry M. Sucov2,3,‡ Departments of 1Biological Sciences and 2Cell & Neurobiology, 3Institute for Genetic Medicine, Keck School of Medicine, University of Southern California, 2250 Alcazar St., IGM 240, Los Angeles, CA 90033, USA 4Department of Molecular and Cell Biology, Harvard University, 16 Divinity Ave., Cambridge, MA 02138, USA 5Program in Developmental Biology, Division of Basic Sciences, A2-025, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, PO Box 19024, Seattle, WA 98109, USA *Present address: Department of Pediatric Oncology, Dana Farber Cancer Institute, 44 Binney St., Boston, MA 02115, USA ‡Author for correspondence (e-mail: [email protected]) Accepted 26 January; published on WWW 21 March 2000 SUMMARY A subpopulation of neural crest termed the cardiac neural of these vessels. Labeled cells populate the crest is required in avian embryos to initiate reorganization aorticopulmonary septum and conotruncal cushions prior of the outflow tract of the developing cardiovascular to and during overt septation of the outflow tract, and system. In mammalian embryos, it has not been previously surround the thymus and thyroid as these organs form. experimentally possible to study the long-term fate of this Neural-crest-derived mesenchymal cells are abundantly population, although there is strong inference that a similar distributed in midgestation (E9.5-12.5), and adult population exists and is perturbed in a number of genetic derivatives of the third, fourth and sixth pharyngeal arch and teratogenic contexts. -
Understanding Paraxial Mesoderm Development and Sclerotome Specification for Skeletal Repair Shoichiro Tani 1,2, Ung-Il Chung2,3, Shinsuke Ohba4 and Hironori Hojo2,3
Tani et al. Experimental & Molecular Medicine (2020) 52:1166–1177 https://doi.org/10.1038/s12276-020-0482-1 Experimental & Molecular Medicine REVIEW ARTICLE Open Access Understanding paraxial mesoderm development and sclerotome specification for skeletal repair Shoichiro Tani 1,2, Ung-il Chung2,3, Shinsuke Ohba4 and Hironori Hojo2,3 Abstract Pluripotent stem cells (PSCs) are attractive regenerative therapy tools for skeletal tissues. However, a deep understanding of skeletal development is required in order to model this development with PSCs, and for the application of PSCs in clinical settings. Skeletal tissues originate from three types of cell populations: the paraxial mesoderm, lateral plate mesoderm, and neural crest. The paraxial mesoderm gives rise to the sclerotome mainly through somitogenesis. In this process, key developmental processes, including initiation of the segmentation clock, formation of the determination front, and the mesenchymal–epithelial transition, are sequentially coordinated. The sclerotome further forms vertebral columns and contributes to various other tissues, such as tendons, vessels (including the dorsal aorta), and even meninges. To understand the molecular mechanisms underlying these developmental processes, extensive studies have been conducted. These studies have demonstrated that a gradient of activities involving multiple signaling pathways specify the embryonic axis and induce cell-type-specific master transcription factors in a spatiotemporal manner. Moreover, applying the knowledge of mesoderm development, researchers have attempted to recapitulate the in vivo development processes in in vitro settings, using mouse and human PSCs. In this review, we summarize the state-of-the-art understanding of mesoderm development and in vitro modeling of mesoderm development using PSCs. We also discuss future perspectives on the use of PSCs to generate skeletal tissues for basic research and clinical applications. -
Migration and Proliferation of Cultured Neural Crest Cells in W Mutant Neural Crest Chimeras
Development 112, 131-141 (1991) 131 Printed in Great Britain © The Company of Biologists Limited 1991 Migration and proliferation of cultured neural crest cells in W mutant neural crest chimeras D. HUSZAR*, A. SHARPE and R. JAENISCH Whitehead Institute for Biomedical Research, Nine Cambridge Center, Cambridge, MA 02142, USA and Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA •Present address GenPharm International, 2375 Garcia Avenue, Mountain View, CA 94043, USA Summary Chimeric mice, generated by aggregating preimplan- functional endogenous melanoblast population in W tation embryos, have been instrumental in the study of mutants, in contrast to Balb/c mice, which contain a full the development of coat color patterns in mammals. This complement of melanocytes. Our results suggest that the approach, however, does not allow for direct experimen- W mutation disturbs migration and/or proliferation of tal manipulation of the neural crest cells, which are the endogenous melanoblasts. In order to obtain infor- precursors of melanoblasts. We have devised a system mation on clonal size and extent of intermingling of that allows assessment of the developmental potential donor cells, two genetically marked neural crest cell and migration of neural crest cells in vivo following their populations were mixed and coinjected into W embryos. experimental manipulation in vitro. Cultured C57B1/6 In hau* of the tricolored chimeras, no co-localization of neural crest cells were microinjected in utero into donor crest cells was observed, while, in the other half, a neurulating Balb/c or W embryos and shown to fine intermingling of donor-derived colors had occurred. contribute efficiently to pigmentation in the host animal. -
Sonic Hedgehog a Neural Tube Anti-Apoptotic Factor 4013 Other Side of the Neural Plate, Remaining in Contact with Midline Cells, RESULTS Was Used As a Control
Development 128, 4011-4020 (2001) 4011 Printed in Great Britain © The Company of Biologists Limited 2001 DEV2740 Anti-apoptotic role of Sonic hedgehog protein at the early stages of nervous system organogenesis Jean-Baptiste Charrier, Françoise Lapointe, Nicole M. Le Douarin and Marie-Aimée Teillet* Institut d’Embryologie Cellulaire et Moléculaire, CNRS FRE2160, 49bis Avenue de la Belle Gabrielle, 94736 Nogent-sur-Marne Cedex, France *Author for correspondence (e-mail: [email protected]) Accepted 19 July 2001 SUMMARY In vertebrates the neural tube, like most of the embryonic notochord or a floor plate fragment in its vicinity. The organs, shows discreet areas of programmed cell death at neural tube can also be recovered by transplanting it into several stages during development. In the chick embryo, a stage-matched chick embryo having one of these cell death is dramatically increased in the developing structures. In addition, cells engineered to produce Sonic nervous system and other tissues when the midline cells, hedgehog protein (SHH) can mimic the effect of the notochord and floor plate, are prevented from forming by notochord and floor plate cells in in situ grafts and excision of the axial-paraxial hinge (APH), i.e. caudal transplantation experiments. SHH can thus counteract a Hensen’s node and rostral primitive streak, at the 6-somite built-in cell death program and thereby contribute to organ stage (Charrier, J. B., Teillet, M.-A., Lapointe, F. and Le morphogenesis, in particular in the central nervous system. Douarin, N. M. (1999). Development 126, 4771-4783). In this paper we demonstrate that one day after APH excision, Key words: Apoptosis, Avian embryo, Cell death, Cell survival, when dramatic apoptosis is already present in the neural Floor plate, Notochord, Quail/chick, Shh, Somite, Neural tube, tube, the latter can be rescued from death by grafting a Spinal cord INTRODUCTION generally induces an inflammatory response. -
Specification and Formation of the Neural Crest: Perspectives on Lineage Segregation
Received: 3 November 2018 Revised: 17 December 2018 Accepted: 18 December 2018 DOI: 10.1002/dvg.23276 REVIEW Specification and formation of the neural crest: Perspectives on lineage segregation Maneeshi S. Prasad1 | Rebekah M. Charney1 | Martín I. García-Castro Division of Biomedical Sciences, School of Medicine, University of California, Riverside, Summary California The neural crest is a fascinating embryonic population unique to vertebrates that is endowed Correspondence with remarkable differentiation capacity. Thought to originate from ectodermal tissue, neural Martín I. García-Castro, Division of Biomedical crest cells generate neurons and glia of the peripheral nervous system, and melanocytes Sciences, School of Medicine, University of California, Riverside, CA. throughout the body. However, the neural crest also generates many ectomesenchymal deriva- Email: [email protected] tives in the cranial region, including cell types considered to be of mesodermal origin such as Funding information cartilage, bone, and adipose tissue. These ectomesenchymal derivatives play a critical role in the National Institute of Dental and Craniofacial formation of the vertebrate head, and are thought to be a key attribute at the center of verte- Research, Grant/Award Numbers: brate evolution and diversity. Further, aberrant neural crest cell development and differentiation R01DE017914, F32DE027862 is the root cause of many human pathologies, including cancers, rare syndromes, and birth mal- formations. In this review, we discuss the current -
Migration and Differentiation of Neural Crest and Ventral Neural Tube Cells in Vitro: Implications for in Vitro and in Vivo Studies of the Neural Crest
The Journal of Neuroscience, March 1988, 8(3): 1001-l 01.5 Migration and Differentiation of Neural Crest and Ventral Neural Tube Cells in vitro: Implications for in vitro and in vivo Studies of the Neural Crest J. F. Loring,’ D. L. Barker;,= and C. A. Erickson’ ‘Department of Zoology, University of California, Davis, California 95616, and *Hatfield Marine Sciences Center, Newport, Oregon 97365 During vertebrate development, neural crest cells migrate trunk neural crest cell cultures, a number of classicalneuro- from the dorsal neural tube and give rise to pigment cells transmitters have been reported, including catecholamines(Co- and most peripheral ganglia. To study these complex pro- hen, 1977; Loring et al., 1982;Maxwell et al., 1982) ACh (Kahn cesses it is helpful to make use of in vitro techniques, but et al., 1980; Maxwell et al., 1982) GABA (Maxwell et al., 1982), the transient and morphologically ill-defined nature of neural and 5-HT (Sieber-Blum et al., 1983). In addition, neuroactive crest cells makes it difficult to isolate a pure population of peptides, suchas somatostatin (Maxwell et al., 1984) have been undifferentiated cells. We have used several established reported in neural crest cell culture. techniques to obtain neural crest-containing cultures from In spite of the advantagesof an in vitro approachto analysis quail embryos and have compared their subsequent differ- of neural crest differentiation, it is clear that a fundamental entiation. We confirm earlier reports of neural crest cell dif- problem ariseswhen attempts are made to isolate these cellsin ferentiation in vitro into pigment cells and catecholamine- culture. -
Significance of Neural Crest in Tooth Development
OMPJ VP Jayasekharan et al 10.5005/jp-journals-10037-1018 REVIEW ARTICLE Signifi cance of Neural Crest in Tooth Development: The Molecular Signature 1VP Jayasekharan, 2Jacob Kurien, 3Eapen Cherian, 4Renji K Paul, 5Aravind S Raju ABSTRACT cells to those of mesenchymal cells. In the head region, The neural crest originates from cells located along the lateral incipient neural crest cells send out processes that penetrate margins of the neural plate. Neural crest cells arise as the result the basal lamina underlying the neuroepithelium just before of an inductive action by the non-neural ectoderm adjacent to neural tube closure. the neural plate and possibly by nearby mesoderm as well. As the neural tube forms, a group of cells separate from the neuro- The neural crest provides cells for the development ectoderm. These cells have the capacity to migrate and differen- of future organs and tissues. After the induction of neural tiate extensively within the developing embryo and they are the crest, the neural crest cells are formed within neural plate basis of structures such as spinal sensory ganglia, sympathetic border regions, which rise as neural folds, and ultimately neurons, Schwann cells, pigment cells and meninges. Specifi c interactions occur during the development of tooth and recent converge to form the dorsal midline of the neural tube, and research has concentrated more on the molecular aspects of it is from here that the neural crest cells will emerge in an these interactions. Thus, it is highly imperative to understand and anterior to posterior sequence. During and after migration, digress the complex mechanisms involved in these processes.