Neural Crest Development

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Introduction

Human embryo week 4 neural crest cells
Human embryo neural crest cells (Week 4, Carnegie stage 11)

The neural crest are bilaterally paired strips of cells arising in the ectoderm at the margins of the neural tube. These cells migrate to many different locations and differentiate into many cell types within the embryo. This means that many different systems (neural, skin, teeth, head, face, heart, adrenal glands, gastrointestinal tract) will also have a contribution fron the neural crest cells. An in vitro study[1] has shown neural crest cell migration occurs at different rates along the embryo axis between Carnegie stage 11 to 13 in week 4.


In the body region, neural crest cells also contribute the peripheral nervous system (both neurons and glia) consisting of sensory ganglia (dorsal root ganglia), sympathetic and parasympathetic ganglia and neural plexuses within specific tissues/organs.


In the head region, neural crest cells migrate into the pharyngeal arches (as shown in movie below) forming ectomesenchyme contributing tissues which in the body region are typically derived from mesoderm (cartilage, bone, and connective tissue). General neural development is also covered in Neural Notes.


Historically identified as "neural crest" by Arthur Marshall in 1879.[2] (see history below and original article).


Use the links listed below to study development of specific neural crest populations.

Neural Crest Links: neural crest | Lecture - Early Neural | Lecture - Neural Crest Development | Lecture Movie | Schwann cell | adrenal | melanocyte | peripheral nervous system | enteric nervous system | cornea | cranial nerve neural crest | head | skull | cardiac neural crest | Nicole Le Douarin | Neural Crest Movies | neural crest abnormalities | Category:Neural Crest
Historic Embryology - Neural Crest  
1879 Olfactory Organ | 1905 Cranial and Spinal Nerves | 1908 10 mm Peripheral | 1910 Mammal Sympathetic | 1920 Human Sympathetic | 1939 10 Somite Embryo | 1942 Origin | 1957 Adrenal

Some Recent Findings

Zebrafish neura crest model
Zebrafish neura crest model[3]
  • Krox20 defines a subpopulation of cardiac neural crest cells contributing to arterial valves and bicuspid aortic valve Development[4] "Although cardiac neural crest cells are required at early stages of arterial valve development, their contribution during valvular leaflet maturation remains poorly understood. Here, we show in mouse that neural crest cells from pre-otic and post-otic regions make distinct contributions to the arterial valve leaflets.... Our findings demonstrate a crucial role for Krox20 in arterial valve development and reveal that an excess of neural crest cells may be associated with bicuspid aortic valve." heart
  • The neural border: Induction, specification and maturation of the territory that generates neural crest cells[5] "The neural crest is induced at the edge between the neural plate and the nonneural ectoderm, in an area called the neural (plate) border, during gastrulation and neurulation. In recent years, many studies have explored how this domain is patterned, and how the neural crest is induced within this territory, that also participates to the prospective dorsal neural tube, the dorsalmost nonneural ectoderm, as well as placode derivatives in the anterior area. This review highlights the tissue interactions, the cell-cell signaling and the molecular mechanisms involved in this dynamic spatiotemporal patterning, resulting in the induction of the premigratory neural crest. Collectively, these studies allow building a complex neural border and early neural crest gene regulatory network, mostly composed by transcriptional regulations but also, more recently, including novel signaling interactions."
  • Review - Development of interstitial cells of Cajal in the human digestive tract as the result of reciprocal induction of mesenchymal and neural crest cells[6] "Neural crest cells (NCC) can migrate into different parts of the body and express their strong inductive potential. In addition, they are multipotent and are able to differentiate into various cell types with diverse functions. In the primitive gut, NCC induce differentiation of muscular structures and interstitial cells of Cajal (ICC), and they themselves differentiate into the elements of the enteric nervous system (ENS), neurons and glial cells. ICC develop by way of mesenchymal cell differentiation in the outer parts of the primitive gut wall around the myenteric plexus (MP) ganglia, with the exception of colon, where they appear simultaneously also at the submucosal border of the circular muscular layer around the submucosal plexus (SMP) ganglia. ...Under the impact of stem cell factor (SCF), a portion of c-kit positive precursors lying immediately around the ganglia differentiate into ICC, while the rest differentiate into SMC." Enteric Nervous System
  • Retinoic acid temporally orchestrates colonization of the gut by vagal neural crest cells[7] "The enteric nervous system arises from neural crest cells that migrate as chains into and along the primitive gut, subsequently differentiating into enteric neurons and glia. Little is known about the mechanisms governing neural crest migration en route to and along the gut in vivo. Here, we report that Retinoic Acid (RA) temporally controls zebrafish enteric neural crest cell chain migration. In vivo imaging reveals that RA loss severely compromises the integrity and migration of the chain of neural crest cells during the window of time window when they are moving along the foregut. After loss of RA, enteric progenitors accumulate in the foregut and differentiate into enteric neurons, but subsequently undergo apoptosis resulting in a striking neuronal deficit. Moreover, ectopic expression of the transcription factor meis3 and/or the receptor ret, partially rescues enteric neuron colonization after RA attenuation. Collectively, our findings suggest that retinoic acid plays a critical temporal role in promoting enteric neural crest chain migration and neuronal survival upstream of Meis3 and RET in vivo." Retinoic acid | Zebrafish Development
More recent papers  
Mark Hill.jpg
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This table shows an automated computer PubMed search using the listed sub-heading term.

  • Therefore the list of references do not reflect any editorial selection of material based on content or relevance.
  • References appear in this list based upon the date of the actual page viewing.

References listed on the rest of the content page and the associated discussion page (listed under the publication year sub-headings) do include some editorial selection based upon both relevance and availability.

Links: References | Discussion Page | Pubmed Most Recent | Journal Searches


Search term: Neural Crest Embryology

Joshua C Peterson, Mary Chughtai, Lambertus J Wisse, Adriana C Gittenberger-de Groot, Qingping Feng, Marie-José T H Goumans, J Conny VanMunsteren, Monique R M Jongbloed, Marco C DeRuiter ##Title## Dis Model Mech: 2018; PubMed 30242109

Nadege Bondurand, Sylvie Dufour, Veronique Pingault News from the Endothelin-3/EDNRB signaling pathway: role during enteric nervous system development and involvement in neural crest-associated disorders. Dev. Biol.: 2018; PubMed 30171849

Warren J Scherer Corneal endothelial cell density and cardiovascular mortality: A Global Survey and Correlative Meta-Analysis. Clin Anat: 2018; PubMed 30168608

Daniel Terheyden-Keighley, Xiaoqing Zhang, Beate Brand-Saberi, Carsten Theiss ##Title## Biol Open: 2018; PubMed 30135081

Hatem A Tawfik, Jonathan J Dutton Embryologic and Fetal Development of the Human Orbit. Ophthalmic Plast Reconstr Surg: 2018; PubMed 30134385

Older papers  
  • Bone morphogenetic protein 4 promotes craniofacial neural crest induction from human pluripotent stem cells[8] "Neural crest (NC) cells are a group of cells located in the neural folds at the boundary between the neural and epidermal ectoderm. Cranial NC cells migrate to the branchial arches and give rise to the majority of the craniofacial region, whereas trunk and tail NC cells contribute to the heart, enteric ganglia of the gut, melanocytes, sympathetic ganglia, and adrenal chromaffin cells. ...These BMP4-treated NC cells were capable of differentiation into osteocytes and chondrocytes. The results of the present study indicate that BMP4 regulates cranial positioning during NC development." Bone Morphogenetic Protein
  • An essential role of variant histone h3.3 for ectomesenchyme potential of the cranial neural crest[3] "The neural crest (NC) is a vertebrate-specific cell population that exhibits remarkable multipotency. Although derived from the neural plate border (NPB) ectoderm, cranial NC (CNC) cells contribute not only to the peripheral nervous system but also to the ectomesenchymal precursors of the head skeleton. ...Surprisingly, embryo-wide expression of dominant mutant H3.3 had little effect on embryonic development outside CNC, indicating an unexpectedly specific sensitivity of CNC to defects in H3.3 incorporation. Whereas previous studies had implicated H3.3 in large-scale histone replacement events that generate totipotency during germ line development, our work has revealed an additional role of H3.3 in the broad potential of the ectoderm-derived CNC, including the ability to make the mesoderm-like ectomesenchymal precursors of the head skeleton."
  • Dbx1-expressing cells are necessary for the survival of the mammalian anterior neural and craniofacial structures[9] "Development of the vertebrate forebrain and craniofacial structures are intimately linked processes, the coordinated growth of these tissues being required to ensure normal head formation. In this study, we identify five small subsets of progenitors expressing the transcription factor dbx1 in the cephalic region of developing mouse embryos at E8.5. ... Our results demonstrate that dbx1-expressing cells have a unique function during head development, notably by controlling cell survival in a non cell-autonomous manner."
  • Analysis of early human neural crest development[10] "The outstanding migration and differentiation capacities of neural crest cells (NCCs) have fascinated scientists since Wilhelm His described this cell population in 1868. Today, after intense research using vertebrate model organisms, we have gained considerable knowledge regarding the origin, migration and differentiation of NCCs. However, our understanding of NCC development in human embryos remains largely uncharacterized, despite the role the neural crest plays in several human pathologies. Here, we report for the first time the expression of a battery of molecular markers before, during, or following NCC migration in human embryos from Carnegie Stages (CS) 12 to 18. Our work demonstrates the expression of Sox9, Sox10 and Pax3 transcription factors in premigratory NCCs, while actively migrating NCCs display the additional transcription factors Pax7 and AP-2alpha. Importantly, while HNK-1 labels few migrating NCCs, p75(NTR) labels a large proportion of this population. However, the broad expression of p75(NTR) - and other markers - beyond the neural crest stresses the need for the identification of additional markers to improve our capacity to investigate human NCC development, and to enable the generation of better diagnostic and therapeutic tools."
  • Cranial neural crest migration: new rules for an old road.[11] "In this review, we discuss recent cellular and molecular discoveries of the CNCC migratory pattern. We focus on events from the time when CNCCs encounter the tissue adjacent to the neural tube and their travel through different microenvironments and into the branchial arches. We describe the patterning of discrete cell migratory streams that emerge from the hindbrain, rhombomere (r) segments r1-r7, and the signals that coordinate directed migration."
  • Derivation of neural crest cells from human pluripotent stem cells.[12] "Here we provide protocols for the step-wise differentiation of human embryonic stem cells (hESCs) or human induced pluripotent stem cells (hiPSCs) into neuroectodermal and NC cells using either the MS5 coculture system or a novel defined culture method based on pharmacological inhibition of bone morphogenetic protein and transforming growth factor-beta signaling pathways." (More? Stem Cells)

Neural crest formation stages 01.jpg

Neural crest formation stages and gene regulatory networks.[13]

Neural Crest Origin
System Cell Type
Peripheral Nervous System
(PNS)
Neurons - sensory ganglia, sympathetic and parasympathetic ganglia, enteric nervous system, and plexuses

Neuroglial cells, olfactory ensheathing cells[14]

Schwann cells[15]

Endocrine Adrenal medulla
Calcitonin-secreting cells
Carotid body type I cells
Integumentary Epidermal pigment cells melanocyte
Facial cartilage and bone Facial and anterior ventral skull cartilage and bones
Sensory inner ear, cornea endothelium and stroma
Connective tissue Tooth odontoblast

smooth muscle, and adipose tissue of skin of head and neck

Connective tissue of meninges, salivary, lachrymal, thymus, thyroid, and pituitary glands

Connective tissue and smooth muscle in arteries of aortic arch origin

Links: Neural Crest Development | Category:Neural Crest | Neural Crest collapsible table

Neural Crest Migration

Human

Human neural crest cell migration-in vitro Human neural crest cell migration (in vitro)[1]
  • A Human neural tube (NT) from an embryo at Carnegie stage 13.
  • B After 16 h, most hNCC have migrated away from the dorsal NT.
  • C The intact NT is detached from the culture dish.
  • D An enriched hNCC population remains, phenotypically similar to murine or avian NCC.
  • E Empirical evaluation of hNCC migration (none to few, some and many) from 31 explanted neural tubes. Third-order polynomial regressions reflect the rostral-to-caudal temporal maturation gradient of the human NT and maturation of NCC. Peaks occur during Carnegie stage 11 at cephalic levels, and during late Carnegie stage 12 at rostral trunk levels (segments extending from somites 5 through the last-formed somite pair).

Chicken

Click Here to play on mobile device

Chicken-neural-crest-migration-01.jpg

Chicken embryo sequence shows the migration of DiI-labeled neural crest cells towards the branchial arches as the embryo. White rings indicate migration of individual cells. Each image represents 10 confocal sections separated by 10 microns.

Movie Source: Original Neural Crest movies kindly provided by Paul Kulesa.[16]

Neural crest migration Chicken Head (movies overview)
Chicken-neural-crest-migration-01.jpg
 ‎‎Neural Crest 1
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 ‎‎Neural Crest 2
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 ‎‎Neural Crest 3
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Chicken-neural-crest-migration-04.jpg
 ‎‎Neural Crest 4
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 ‎‎Neural Crest 5
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 ‎‎Neural Crest 6
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Chicken-neural-crest-migration-07.jpg
 ‎‎Neural Crest 7
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Neural Crest Movies: Migration 01 | Migration 02 | Migration 03 | Migration 04 | Migration 05 | Migration 06 | Migration 07

Textbooks

Pharyngeal arch cartilages.jpg
Logo.png Hill, M.A. (2018). UNSW Embryology (18th ed.) Retrieved September 25, 2018, from https://embryology.med.unsw.edu.au
Neural Crest Links: neural crest | Lecture - Early Neural | Lecture - Neural Crest Development | Lecture Movie | Schwann cell | adrenal | melanocyte | peripheral nervous system | enteric nervous system | cornea | cranial nerve neural crest | head | skull | cardiac neural crest | Nicole Le Douarin | Neural Crest Movies | neural crest abnormalities | Category:Neural Crest
Historic Embryology - Neural Crest  
1879 Olfactory Organ | 1905 Cranial and Spinal Nerves | 1908 10 mm Peripheral | 1910 Mammal Sympathetic | 1920 Human Sympathetic | 1939 10 Somite Embryo | 1942 Origin | 1957 Adrenal
The Developing Human, 8th edn.jpg Moore, K.L. & Persuad, T.V.N. (2008). The Developing Human: clinically oriented embryology (8th ed.). Philadelphia: Saunders. (chapter links only work with a UNSW connection).
Larsen's human embryology 4th edn.jpg Schoenwolf, G.C., Bleyl, S.B., Brauer, P.R. and Francis-West, P.H. (2009). Larsen’s Human Embryology (4th ed.). New York; Edinburgh: Churchill Livingstone. The following chapter links only work with a UNSW Library subscription
  • Chapter 10 - Development of the Peripheral Nervous System
  • Chapter 16 - Development of the Pharyngeal Apparatus and Face
Additional Resources

Objectives

Mouse neural crest (E10.5 ganglia Sox10)
  • Understand the structures derived from ectoderm.
  • Understand the formation of neural folds.
  • Identify the initial location of neural crest cells in the trilaminar embryo.
  • Identify pathways of neural crest migration throughout the embryo.
  • To know the major tissues to which neural crest cells contribute.
  • To know how abnormalities in development that result from abnormal neural crest cell migration.
  • Understand how neural crest cells contribute to the pharyngeal arches and the head structures they form.

Neural Crest Derivatives

A key feature of neural crest is the migration into other embryonic tissues to form specific neural and non-neural populations and structures.

Cranial neural crest

  • migration - dorsolaterally and into pharyngeal arches
  • craniofacial mesenchyme - cartilage, bone, cranial neurons, glia, and connective tissues of the face
  • pharyngeal arches and pouches - thymic cells, tooth odontoblasts, middle ear bones (ossicles), stria vascularis cells, and jaw (mandible)
Cochlea - Stria Vascularis
Mouse organ of corti 02.jpg Mouse organ of corti 04.jpg
Inner ear cochlea, showing the stria vascularis intermediate cells that are derived from neural crest.


Hearing - Inner Ear Development

Eye - Cornea
Human embryonic cornea Mouse eye neural crest cornea 01.jpg
Human embryonic cornea detail (Week 8, Carnegie stage 22)]] Mouse cornea layers
The adult eye cornea has three layers: an outer epithelium layer (ectoderm), a middle stromal layer of collagen-rich extracellular matrix between stromal keratocytes (neural crest) and an inner layer of endothelial cells (neural crest)


Vision - Cornea Development

Carotid body are chemoreceptors in the wall of the common carotid (3rd pharyngeal arch) [17][18]

Cardiac neural crest

  • migration - located between the cranial and trunk neural crests, overlapping the anterior portion of the vagal neural crest.
  • pharyngeal arches - (3,4,6) melanocytes, neurons, cartilage, and connective tissue
  • heart outflow tract - aortic arch/pulmonary artery septum, large arteries wall musculoconnective tissue


Neural Crest - Cardiac

Cardiac Neural Crest Migration

Cardiac Neural Crest Migration

Trunk neural crest

  • migration - two major pathways over somites (dorsolaterally) and between somite and neural tube (ventrolaterally)
  • dorsolateral - skin melanocytes
  • ventrolaterally - dorsal root ganglia, sympathetic ganglia, adrenal medulla, aortic nerve clusters

para-aortic body

(organ of Zuckerkandl, OZ) A neural crest derived chromaffin body, anatomically located at the bifurcation of the aorta or at the origin of the inferior mesenteric artery. Thought to act as a fetal regulator of blood pressure, secreting catecholamines into the fetal circulation.[19] In human, reaches its maximal size at 3 years of age and then regresses either by death, dispersion or differentiation.[20]

Named in 1901 by Emil Zuckerkandl (1849-1910) a Hungarian-Austrian anatomist at the University of Vienna.

Links: Cardiovascular System Development

Development Overview

The following cranial and trunk data is based upon 185 serially sectioned staged (Carnegie) human embryos.[21]

Cranial Neural Crest

Human Eye Neural Crest Timeline
Carnegie Stage Event
9 an indication of mesencephalic neural crest
10 trigeminal, facial, and postotic components
11 crest-free zones are soon observable in rhombomere 1, 3, and 5
12 rhombomeres 6 and 7 neural crest migrate to pharyngeal arch 3 and then rostrad to the truncus arteriosus
13 nasal crest and the terminalis-vomeronasal complex are last of the cranial crest to appear
9 to 14 otic vesicle primordium descends
Week: 1 2 3 4 5 6 7 8
Carnegie stage: 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
Data from a study of 185 serially sectioned staged (Carnegie) human embryos.[21] Links: vision | neural crest | timeline |     Category:Timeline

Trunk Neural Crest

Spinal ganglia increase in number over time and are in phase with the somites, though not their centre. There are 3 migratory pathways: ventrolateral between dermatomyotome and sclerotome, ventromedial between neural tube and sclerotomes, and lateral between surface ectoderm and dermatomyotome.

Vagal Neural Crest

  • Vagal segment arise at the level of somites 1–7
    • leave neural crest at week 4 and also populate the pharyngeal arches.
    • enter posterior wall of anterior gut, then surround and continue their rostrocaudal migration route
    • migrate into external gut wall just beneath the serosa
    • form an uninterrupted chain of cells that continues migration in the caudal direction
    • mitotically divide during migration
    • differentiate into neurons and glial cells of the myenteric plexus
  • migration - ventrally into surrounding splanchnic mesenchyme of gastrointestinal tract
  • splanchnic mesenchyme - parasympathetic (enteric) ganglia of the gut


Recent research suggests that the vagal neural crest cells are a transitional population that has evolved between the head and the trunk, taking separate pathways to the both the heart and to the gut.[22][23]

Sacral Neural Crest

  • Sacral segment arises caudally to somite 28
    • contributes to the enteric nervous system along the postumbilical gut


Neck and Shoulder

A mouse study using individually labelled cells of postotic neural crest followed the development of the shoulder girdle (clavicle and scapula) that connects the upper limb to the axial skeleton.[24]

  • Clavicle is a neural crest-mesodermal structure, posterior dermal clavicle mesoderm.
  • Cryptic cell boundaries traverse apparently homogeneous skeleton of the neck and shoulders.
  • Bones and muscles code of connectivity that mesenchymal stem cells of both neural crest and mesodermal origin obey
  • Neural crest anchors the head onto the anterior lining of the shoulder girdle
  • Hox-gene-controlled mesoderm links trunk muscles to the posterior neck and shoulder skeleton.
  • Skeleton identified as neural crest-derived is affected in human Klippel-Feil syndrome, Sprengel's deformity and Arnold-Chiari I/II malformation.

Skin Melanocytes

Melanoblast migration.png Mouse-melanoblast migration icon.jpg
Mouse melanocyte migration[25] Movie Mouse Skin - Melanoblast Migration E14.5[26]

Neural Crest Migration

A key event in neural crest development is migration from the original site that neural crest cells are generated (edge of the neural plate) to the different anatomical regions within the embryo.

Stimulators

  • complement component C3a - (C3a) acts as an autocrine diffusible chemotactic agent attracting NCC toward the self-secreted source.

Inhibitors

  • versican - (VCAN, Chondroitin Sulfate Proteoglycan 2; Cspg2) an extracellular matrix proteoglycan that acts as both an inhibitor of NCC migration and as a guiding cue by forming exclusionary boundaries.[27]


Links: OMIM 118661

Historic

The paper by Marshall, Morphology of the Vertebrate Olfactory Organ (1879)[2], was historically the first time the term "neural crest" was used. In his own earlier papers he had referred to this as a "neural ridge" in describing development of the chicken embryo neural tube.

See paper text and his referenced comment:

"I take this opportunity to make a slight alteration in the nomenclature adopted in my former paper. I have there suggested the term neural ridge for the longitudinal ridge of cells which grows out from the reentering angle between the external epiblast and the neural canal, and from which the nerves, whether cranial or spinal, arise. Since this ridge appears before closure of the neural canal is effected, there are manifestly two neural ridges, one on either side ; but I have also applied the same term, neural ridge, to the single outgrowth formed by the fusion of the neural ridges of the two sides after complete closure of the neural canal is effected, and after the external epiblast has become completely separated from the neural canal. I propose in future to speak of this single median outgrowth as the neural crest, limiting the term neural ridge to the former acceptation. Thus, while there are two neural ridges, there is only one neural crest, a distinction that will be at once evident on reference to my former figures."


Links: Embryology History

References

  1. 1.0 1.1 Thomas S, Thomas M, Wincker P, Babarit C, Xu P, Speer MC, Munnich A, Lyonnet S, Vekemans M & Etchevers HC. (2008). Human neural crest cells display molecular and phenotypic hallmarks of stem cells. Hum. Mol. Genet. , 17, 3411-25. PMID: 18689800 DOI.
  2. 2.0 2.1 Marshall A. The morphology of the vertebrate olfactory organ. (1879) Quarterly Journal of Microscopic Science. 19: 300–340.
  3. 3.0 3.1 Cox SG, Kim H, Garnett AT, Medeiros DM, An W & Crump JG. (2012). An essential role of variant histone H3.3 for ectomesenchyme potential of the cranial neural crest. PLoS Genet. , 8, e1002938. PMID: 23028350 DOI.
  4. Odelin G, Faure E, Coulpier F, Di Bonito M, Bajolle F, Studer M, Avierinos JF, Charnay P, Topilko P & Zaffran S. (2018). Krox20 defines a subpopulation of cardiac neural crest cells contributing to arterial valves and bicuspid aortic valve. Development , 145, . PMID: 29158447 DOI.
  5. Pla P & Monsoro-Burq AH. (2018). The neural border: Induction, specification and maturation of the territory that generates neural crest cells. Dev. Biol. , , . PMID: 29852131 DOI.
  6. Radenkovic G, Radenkovic D & Velickov A. (2018). Development of interstitial cells of Cajal in the human digestive tract as the result of reciprocal induction of mesenchymal and neural crest cells. J. Cell. Mol. Med. , 22, 778-785. PMID: 29193736 DOI.
  7. Uribe RA, Hong SS & Bronner ME. (2018). Retinoic acid temporally orchestrates colonization of the gut by vagal neural crest cells. Dev. Biol. , 433, 17-32. PMID: 29108781 DOI.
  8. Mimura S, Suga M, Okada K, Kinehara M, Nikawa H & Furue MK. (2016). Bone morphogenetic protein 4 promotes craniofacial neural crest induction from human pluripotent stem cells. Int. J. Dev. Biol. , 60, 21-8. PMID: 26934293 DOI.
  9. Causeret F, Ensini M, Teissier A, Kessaris N, Richardson WD, Lucas de Couville T & Pierani A. (2011). Dbx1-expressing cells are necessary for the survival of the mammalian anterior neural and craniofacial structures. PLoS ONE , 6, e19367. PMID: 21552538 DOI.
  10. Betters E, Liu Y, Kjaeldgaard A, Sundström E & García-Castro MI. (2010). Analysis of early human neural crest development. Dev. Biol. , 344, 578-92. PMID: 20478300 DOI.
  11. Kulesa PM, Bailey CM, Kasemeier-Kulesa JC & McLennan R. (2010). Cranial neural crest migration: new rules for an old road. Dev. Biol. , 344, 543-54. PMID: 20399765 DOI.
  12. Lee G, Chambers SM, Tomishima MJ & Studer L. (2010). Derivation of neural crest cells from human pluripotent stem cells. Nat Protoc , 5, 688-701. PMID: 20360764 DOI.
  13. Green SA, Simoes-Costa M & Bronner ME. (2015). Evolution of vertebrates as viewed from the crest. Nature , 520, 474-482. PMID: 25903629 DOI.
  14. Barraud P, Seferiadis AA, Tyson LD, Zwart MF, Szabo-Rogers HL, Ruhrberg C, Liu KJ & Baker CV. (2010). Neural crest origin of olfactory ensheathing glia. Proc. Natl. Acad. Sci. U.S.A. , 107, 21040-5. PMID: 21078992 DOI.
  15. Woodhoo A & Sommer L. (2008). Development of the Schwann cell lineage: from the neural crest to the myelinated nerve. Glia , 56, 1481-90. PMID: 18803317 DOI.
  16. Kulesa PM & Fraser SE. (2000). In ovo time-lapse analysis of chick hindbrain neural crest cell migration shows cell interactions during migration to the branchial arches. Development , 127, 1161-72. PMID: 10683170
  17. Smith P, Scraggs M & Heath D. (1993). The development of the nerve network in the fetal human carotid body and its subsequent function in cardiac disease. Cardioscience , 4, 143-9. PMID: 8400021
  18. Hempleman SC & Warburton SJ. (2013). Comparative embryology of the carotid body. Respir Physiol Neurobiol , 185, 3-8. PMID: 22902512 DOI.
  19. WEST GB, SHEPHERD DM, HUNTER RB & MACGREGOR AR. (1953). The function of the organs of Zuckerkandl. Clin Sci , 12, 317-25. PMID: 13107111
  20. Schober A, Parlato R, Huber K, Kinscherf R, Hartleben B, Huber TB, Schütz G & Unsicker K. (2013). Cell loss and autophagy in the extra-adrenal chromaffin organ of Zuckerkandl are regulated by glucocorticoid signalling. J. Neuroendocrinol. , 25, 34-47. PMID: 23078542 DOI.
  21. 21.0 21.1 O'Rahilly R & Müller F. (2007). The development of the neural crest in the human. J. Anat. , 211, 335-51. PMID: 17848161 DOI.
  22. Kuo BR & Erickson CA. (2010). Regional differences in neural crest morphogenesis. Cell Adh Migr , 4, 567-85. PMID: 20962585
  23. Kuo BR & Erickson CA. (2011). Vagal neural crest cell migratory behavior: a transition between the cranial and trunk crest. Dev. Dyn. , 240, 2084-100. PMID: 22016183 DOI.
  24. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP & Koentges G. (2005). Neural crest origins of the neck and shoulder. Nature , 436, 347-55. PMID: 16034409 DOI.
  25. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP & Koentges G. (2005). Neural crest origins of the neck and shoulder. Nature , 436, 347-55. PMID: 16034409 DOI.
  26. Mort RL, Hay L & Jackson IJ. (2010). Ex vivo live imaging of melanoblast migration in embryonic mouse skin. Pigment Cell Melanoma Res , 23, 299-301. PMID: 20067551 DOI.
  27. Szabó A, Melchionda M, Nastasi G, Woods ML, Campo S, Perris R & Mayor R. (2016). In vivo confinement promotes collective migration of neural crest cells. J. Cell Biol. , 213, 543-55. PMID: 27241911 DOI.


Books

Trainor, P. (ed) Neural crest cells: evolution, development and disease. ISBN: 978-0-12-401730-6 ScienceDirect Nelms BL, Labosky PA. Transcriptional Control of Neural Crest Development. San Rafael (CA): Morgan & Claypool Life Sciences; 2010. PMID 21452438

Reviews

Martik ML & Bronner ME. (2017). Regulatory Logic Underlying Diversification of the Neural Crest. Trends Genet. , 33, 715-727. PMID: 28851604 DOI.

Bronner ME & Simões-Costa M. (2016). The Neural Crest Migrating into the Twenty-First Century. Curr. Top. Dev. Biol. , 116, 115-34. PMID: 26970616 DOI.

Green SA, Simoes-Costa M & Bronner ME. (2015). Evolution of vertebrates as viewed from the crest. Nature , 520, 474-482. PMID: 25903629 DOI.

Lee YH & Saint-Jeannet JP. (2011). Sox9 function in craniofacial development and disease. Genesis , 49, 200-8. PMID: 21309066 DOI.

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Cite this page: Hill, M.A. (2018, September 25) Embryology Neural Crest Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Neural_Crest_Development

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