How to cite this WIREs title:
WIREs Dev Biol

Impact Factor: 3.883

Specifying neural crest cells: From chromatin to morphogens and factors in between

Advanced Review

Crystal D. Rogers, Shuyi Nie

Published Online: May 03 2018

DOI: 10.1002/wdev.322

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

Neural crest (NC) cells are a stem‐like multipotent population of progenitor cells that are present in vertebrate embryos, traveling to various regions in the developing organism. Known as the “fourth germ layer,” these cells originate in the ectoderm between the neural plate (NP), which will become the brain and spinal cord, and nonneural tissues that will become the skin and the sensory organs. NC cells can differentiate into more than 30 different derivatives in response to the appropriate signals including, but not limited to, craniofacial bone and cartilage, sensory nerves and ganglia, pigment cells, and connective tissue. The molecular and cellular mechanisms that control the induction and specification of NC cells include epigenetic control, multiple interactive and redundant transcriptional pathways, secreted signaling molecules, and adhesion molecules. NC cells are important not only because they transform into a wide variety of tissue types, but also because their ability to detach from their epithelial neighbors and migrate throughout developing embryos utilizes mechanisms similar to those used by metastatic cancer cells. In this review, we discuss the mechanisms required for the induction and specification of NC cells in various vertebrate species, focusing on the roles of early morphogenesis, cell adhesion, signaling from adjacent tissues, and the massive transcriptional network that controls the formation of these amazing cells. This article is categorized under: Nervous System Development > Vertebrates: General Principles Gene Expression and Transcriptional Hierarchies > Regulatory Mechanisms Gene Expression and Transcriptional Hierarchies > Gene Networks and Genomics Signaling Pathways > Cell Fate Signaling

Morphogenesis and NC specification. (a, a′) In chicken embryos, the NPB (green) is specified by Hamburger Hamilton stage 5 (HH5) prior to the onset of definitive neural crest (NC) markers and expresses transcription factors such as MSX1, ZIC1, and PAX7. (b, b′) As neurulation proceeds at HH7‐HH8, the neural folds rise and bend toward the midline. At this stage the neural folds are being specified as definitive NC cells. (c, c′) By HH8, definitive NC markers are expressed in the dorsal neural tube (SOX9, SOX10, SNAI2, and FOXD3), the neural tube is closed, and the ectodermal cells are converging on the midline to cover the neural tube. (d, d′) By HH9, the NC cells are beginning to undergo EMT and start detaching from the neural tube. ECT, ectoderm; NC, neural crest; NF, neural folds; NPB, neural plate border; NP, neural plate

[ Normal View | Magnified View ]

The NC gene regulatory network (GRN) is constantly evolving. This GRN was compiled from gene perturbation studies from multiple species including chick, frog, mouse and zebrafish. The GRN displays the regulatory interactions between signaling factors (top level) and their intracellular effectors and downstream transcriptional targets. The NP (left) and epidermis (right) are depicted on either side of the NC as they would be in a developing embryo. NPB specification (green), premigratory NC specification (blue), and NC EMT factors (yellow) are shown. Pax3/7, Tfap2 are both represented twice because they have been identified as both border specifiers and NC specifiers. Solid lines indicate direct regulatory interactions based on promoter and cis‐regulatory analysis. Verified animal models are marked next to each direct interaction (c, chick; m, mouse; x, frog, f, fish). Signaling factors are represented as proteins in all capitals while GRN transcription factors are lower case and capitalized, but not italicized, to demonstrate that they represent both functional proteins and gene targets. Dashed lines represent functional interactions without evidence of direct interaction so far. Bubble nodes: Protein–protein interactions

[ Normal View | Magnified View ]

Recent technological advances have allowed more in depth study of the NC regulatory levels. Diagram shows the different intracellular control levels that regulate how and when NC cells form and the assays that can be used to perform systems analysis of NC formation. (Left) Depiction of a cell with multiple levels of genetic and proteomic regulation and where in the cell these processes take place (cytoplasm vs. nucleus). Specific types of cellular regulation are identified at three different levels: The general levels of regulation starting from extracellular morphogens that activate intercellular cascades followed by regulation of DNA transcription, mRNA availability, stability and translation, and protein stability, modification and degradation. Column 2 shows the types of analyses used to identify the changes at the previous levels. Finally, specific examples of genes, mRNAs, microRNAs and proteins that are regulated at these levels during NC development with references

[ Normal View | Magnified View ]

Embryonic NC cells vs. human induced NC cells (HiNCs). Schematic comparing (a) the development and isolation of embryonic NC cells versus (b) the technique used to create human induced NC cells from differentiated fibroblasts. To create human induced pluripotent NC cells, fibroblasts must first be de‐differentiated by reprogramming them using the Yamanaka stem cell factors, Oct4, Sox2, Nanog, and Klf4. Then by using the appropriate media (various), those stem cells can be differentiated into NC cells in vitro

[ Normal View | Magnified View ]

Developmental stages and molecules involved in NC specification and migration. Prior to differentiation, NC cells go through three stages (left column), neural plate border (NPB), premigratory NC (PNC), and migratory NC (MNC). The nonneural ectoderm (NNE) develops lateral to the NPB cells during neurulation as the neural folds (NF) rise to form the neural tube (NT). At these early stages, signaling from WNTs, FGFs, BMPs, and BMP antagonists (Noggin, Chordin) (middle column) drives the specification of the NPB specifiers (right column). As the NT closes, NC cells are specified in the dorsal NT, and are marked by NC specifier transcription factors. Along with signaling from WNTs, BMPs, RA, and FGFs, the NC specifiers down regulate adhesive cadherins, upregulate migratory cadherins and the cells leave the neural tube. The neural and nonneural ectoderm is pink and green, premigratory and migratory NC are orange

[ Normal View | Magnified View ]

Comparative gene expression of morphogens and NC transcription factors in frog and chick. Diagrams depicting the expression of NC transcription factors Pax3/7 and Snai2 compared to various genes coding for morphogens that regulate their early expression (Bmp2/4, Wnt1/8A, and Fgf2/4/8). (a, b) In the frog embryo, Pax3 is expressed by late gastrula stage (stage 12.5) in the presumptive NC region adjacent to the NP. Its expression is broader than Snai2, which is also in the presumptive NC region. At this stage, Bmp4, Fgf2, and Wnt8 transcripts are expressed posteriorly near the blastopore. At neurula stage (stage 17), the NC cells are preparing to migrate ventrolaterally away from the midline, and the expression of both Pax7 and Snai2 remains adjacent to the rising neural folds. At this stage, BMPs remain in the nonneural ectoderm and mesoderm while Fgf8 is expressed in the anterior region, in the brain, and Fgf2 and Fgf4 are in the posterior mesoderm. By stage 17, Wnt8 is expressed in the developing neural folds. (c, d) At late gastrula stage (HH5) in the chicken embryo, Pax7 is expressed in the NPB, but Snai2 is limited to the primitive streak/mesoderm. Bmp4 is expressed in the ectoderm and NPB, Fgf8 is expressed in the mesoderm, and Wnt8 is expressed in the NPB and the mesoderm. At neurula stage (HH8), Pax7 is expressed in the definitive NC as well as the dorsal neural tube, and the NPB in the posterior region. Snai2 is expressed in the definitive NC cells in the head. Bmp4 is expressed in the neural folds and the mesoderm, and Wnt1 is expressed in the dorsal neural folds and Wnt8A is expressed in the paraxial mesoderm. The differences in expression of these morphogens may explain some of the differences in NC induction between organisms. Embryos are depicted as follows: (a, c) Anterior to the top, posterior to the bottom, dorsal out. (b, d) Dorsal up, ventral down. All expression patterns (a–d) were found in Xenbase and Geisha

[ Normal View | Magnified View ]

References

Abitua,, P. B., Wagner,, E., Navarrete,, I. A., & Levine,, M. (2012). Identification of a rudimentary neural crest in a non‐vertebrate chordate. Nature, 492, 104–107.
Acloque,, H., Ocana,, O. H., Abad,, D., Stern,, C. D., & Nieto,, M. A. (2017). Snail2 and Zeb2 repress P‐cadherin to define embryonic territories in the chick embryo. Development, 144, 649–656.
Aguero,, T. H., Fernandez,, J. P., Lopez,, G. A., Tribulo,, C., & Aybar,, M. J. (2012). Indian hedgehog signaling is required for proper formation, maintenance and migration of Xenopus neural crest. Developmental Biology, 364, 99–113.
Anderson,, M. J., Schimmang,, T., & Lewandoski,, M. (2016). An FGF3‐BMP signaling axis regulates caudal neural tube closure, neural crest specification and anterior‐posterior axis extension. PLoS Genetics, 12, e1006018.
Andree,, B., Duprez,, D., Vorbusch,, B., Arnold,, H. H., & Brand,, T. (1998). BMP‐2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mechanisms of Development, 70, 119–131.
Aoki,, Y., Saint‐Germain,, N., Gyda,, M., Magner‐Fink,, E., Lee,, Y. H., Credidio,, C., & Saint‐Jeannet,, J. P. (2003). Sox10 regulates the development of neural crest‐derived melanocytes in Xenopus. Developmental Biology, 259, 19–33.
Aruga,, J., Tohmonda,, T., Homma,, S., & Mikoshiba,, K. (2002). Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Developmental Biology, 244, 329–341.
Avery,, J., & Dalton,, S. (2016). Methods for derivation of multipotent neural crest cells derived from human pluripotent stem cells. Methods in Molecular Biology, 1341, 197–208.
Aybar,, M. J., Nieto,, M. A., & Mayor,, R. (2003). Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development, 130, 483–494.
Bae,, C. J., Park,, B. Y., Lee,, Y. H., Tobias,, J. W., Hong,, C. S., & Saint‐Jeannet,, J. P. (2014). Identification of Pax3 and Zic1 targets in the developing neural crest. Developmental Biology, 386, 473–483.
Bajpai,, R., Chen,, D. A., Rada‐Iglesias,, A., Zhang,, J., Xiong,, Y., Helms,, J., … Wysocka,, J. (2010). CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature, 463, 958–962.
Bajpai,, V. K., Kerosuo,, L., Tseropoulos,, G., Cummings,, K. A., Wang,, X., Lei,, P., … Andreadis,, S. T. (2017). Reprogramming postnatal human epidermal keratinocytes toward functional neural crest fates. Stem Cells, 35, 1402–1415.
Banerjee,, P., Dutta,, S., & Pal,, R. (2016). Dysregulation of Wnt‐signaling and a candidate set of miRNAs underlie the effect of metformin on neural crest cell development. Stem Cells, 34, 334–345.
Bang,, A. G., Papalopulu,, N., Goulding,, M. D., & Kintner,, C. (1999). Expression of Pax‐3 in the lateral neural plate is dependent on a Wnt‐mediated signal from posterior nonaxial mesoderm. Developmental Biology, 212, 366–380.
Barembaum,, M., & Bronner,, M. E. (2013). Identification and dissection of a key enhancer mediating cranial neural crest specific expression of transcription factor, Ets‐1. Developmental Biology, 382, 567–575.
Barriga,, E. H., Maxwell,, P. H., Reyes,, A. E., & Mayor,, R. (2013). The hypoxia factor Hif‐1alpha controls neural crest chemotaxis and epithelial to mesenchymal transition. The Journal of Cell Biology, 201, 759–776.
Barriga,, E. H., & Mayor,, R. (2015). Embryonic cell‐cell adhesion: A key player in collective neural crest migration. Current Topics in Developmental Biology, 112, 301–323.
Basch,, M. L., Bronner‐Fraser,, M., & Garcia‐Castro,, M. I. (2006). Specification of the neural crest occurs during gastrulation and requires Pax7. Nature, 441, 218–222.
Bell,, G. W., Yatskievych,, T. A., & Antin,, P. B. (2004). GEISHA, a whole‐mount in situ hybridization gene expression screen in chicken embryos. Developmental Dynamics, 229, 677–687.
Bell,, K. M., Western,, P. S., & Sinclair,, A. H. (2000). SOX8 expression during chick embryogenesis. Mechanisms of Development, 94, 257–260.
Bellmeyer,, A., Krase,, J., Lindgren,, J., & LaBonne,, C. (2003). The protooncogene c‐myc is an essential regulator of neural crest formation in xenopus. Developmental Cell, 4, 827–839.
Betancur,, P., Bronner‐Fraser,, M., & Sauka‐Spengler,, T. (2010a). Assembling neural crest regulatory circuits into a gene regulatory network. Annual Review of Cell and Developmental Biology, 26, 581–603.
Betancur,, P., Bronner‐Fraser,, M., & Sauka‐Spengler,, T. (2010b). Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. Proceedings of the National Academy of Sciences of the United States of America, 107, 3570–3575.
Bhat,, N., Kwon,, H. J., & Riley,, B. B. (2013). A gene network that coordinates preplacodal competence and neural crest specification in zebrafish. Developmental Biology, 373, 107–117.
Bildsoe,, H., Fan,, X., Wilkie,, E. E., Ashoti,, A., Jones,, V. J., Power,, M., … Loebel,, D. A. (2016). Transcriptional targets of TWIST1 in the cranial mesoderm regulate cell‐matrix interactions and mesenchyme maintenance. Developmental Biology, 418, 189–203.
Bonano,, M., Tribulo,, C., De Calisto,, J., Marchant,, L., Sanchez,, S. S., Mayor,, R., & Aybar,, M. J. (2008). A new role for the Endothelin‐1/Endothelin‐A receptor signaling during early neural crest specification. Developmental Biology, 323, 114–129.
Bonstein,, L., Elias,, S., & Frank,, D. (1998). Paraxial‐fated mesoderm is required for neural crest induction in Xenopus embryos. Developmental Biology, 193, 156–168.
Borchers,, A., David,, R., & Wedlich,, D. (2001). Xenopus cadherin‐11 restrains cranial neural crest migration and influences neural crest specification. Development, 128, 3049–3060.
Bowes,, J. B., Snyder,, K. A., Segerdell,, E., Jarabek,, C. J., Azam,, K., Zorn,, A. M., & Vize,, P. D. (2010). Xenbase: Gene expression and improved integration. Nucleic Acids Research, 38, D607–D612.
Brugger,, S. M., Merrill,, A. E., Torres‐Vazquez,, J., Wu,, N., Ting,, M. C., Cho,, J. Y., … Maxson,, R. (2004). A phylogenetically conserved cis‐regulatory module in the Msx2 promoter is sufficient for BMP‐dependent transcription in murine and Drosophila embryos. Development, 131, 5153–5165.
Bugner,, V., Tecza,, A., Gessert,, S., & Kuhl,, M. (2011). Peter Pan functions independently of its role in ribosome biogenesis during early eye and craniofacial cartilage development in Xenopus laevis. Development, 138, 2369–2378.
Cajal,, M., Creuzet,, S. E., Papanayotou,, C., Saberan‐Djoneidi,, D., Chuva de Sousa Lopes,, S. M., Zwijsen,, A., … Camus,, A. (2014). A conserved role for non‐neural ectoderm cells in early neural development. Development, 141, 4127–4138.
Carmona‐Fontaine,, C., Acuna,, G., Ellwanger,, K., Niehrs,, C., & Mayor,, R. (2007). Neural crests are actively precluded from the anterior neural fold by a novel inhibitory mechanism dependent on Dickkopf1 secreted by the prechordal mesoderm. Developmental Biology, 309, 208–221.
Chapman,, S. C., Schubert,, F. R., Schoenwolf,, G. C., & Lumsden,, A. (2002). Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Developmental Biology, 245, 187–199.
Chawla,, B., Schley,, E., Williams,, A. L., & Bohnsack,, B. L. (2016). Retinoic acid and Pitx2 regulate early neural crest survival and migration in craniofacial and ocular development. Birth Defects Research. Part B, Developmental and Reproductive Toxicology, 107, 126–135.
Cheng,, Y., Cheung,, M., Abu‐Elmagd,, M. M., Orme,, A., & Scotting,, P. J. (2000). Chick sox10, a transcription factor expressed in both early neural crest cells and central nervous system. Brain Research. Developmental Brain Research, 121, 233–241.
Cheung,, M., Chaboissier,, M. C., Mynett,, A., Hirst,, E., Schedl,, A., & Briscoe,, J. (2005). The transcriptional control of trunk neural crest induction, survival, and delamination. Developmental Cell, 8, 179–192.
Christian,, J. L., McMahon,, J. A., McMahon,, A. P., & Moon,, R. T. (1991). Xwnt‐8, a Xenopus Wnt‐1/int‐1‐related gene responsive to mesoderm‐inducing growth factors, may play a role in ventral mesodermal patterning during embryogenesis. Development, 111, 1045–1055.
Ciarlo,, C., Kaufman,, C. K., Kinikoglu,, B., Michael,, J., Yang,, S., D Amato,, C., … Zon,, L. I. (2017). A chemical screen in zebrafish embryonic cells establishes that Akt activation is required for neural crest development. Elife, 6.
Coles,, E. G., Taneyhill,, L. A., & Bronner‐Fraser,, M. (2007). A critical role for Cadherin6B in regulating avian neural crest emigration. Developmental Biology, 312, 533–544.
Darnell,, D. K., Kaur,, S., Stanislaw,, S., Davey,, S., Konieczka,, J. H., Yatskievych,, T. A., & Antin,, P. B. (2007). GEISHA: An in situ hybridization gene expression resource for the chicken embryo. Cytogenetic and Genome Research, 117, 30–35.
Davenport,, C., Diekmann,, U., Budde,, I., Detering,, N., & Naujok,, O. (2016). Anterior‐posterior patterning of definitive endoderm generated from human embryonic stem cells depends on the differential signaling of retinoic acid, Wnt‐, and BMP‐signaling. Stem Cells, 34, 2635–2647.
de Croze,, N., Maczkowiak,, F., & Monsoro‐Burq,, A. H. (2011). Reiterative AP2a activity controls sequential steps in the neural crest gene regulatory network. Proceedings of the National Academy of Sciences of the United States of America, 108, 155–160.
Deichmann,, C., Link,, M., Seyfang,, M., Knotz,, V., Gradl,, D., & Wedlich,, D. (2015). Neural crest specification by Prohibitin1 depends on transcriptional regulation of prl3 and vangl1. Genesis, 53, 627–639.
Ding,, H. L., Hooper,, J. E., Batzel,, P., Eames,, B. F., Postlethwait,, J. H., Artinger,, K. B., & Clouthier,, D. E. (2016). MicroRNA profiling during craniofacial development: Potential roles for Mir23b and Mir133b. Frontiers in Physiology, 7, 281.
Dixon,, J., Jones,, N. C., Sandell,, L. L., Jayasinghe,, S. M., Crane,, J., Rey,, J. P., … Trainor,, P. A. (2006). Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proceedings of the National Academy of Sciences of the United States of America, 103, 13403–13408.
Duband,, J. L., Dady,, A., & Fleury,, V. (2015). Resolving time and space constraints during neural crest formation and delamination. Current Topics in Developmental Biology, 111, 27–67.
Duester,, G. (2008). Retinoic acid synthesis and signaling during early organogenesis. Cell, 134, 921–931.
Fairchild,, C. L., Conway,, J. P., Schiffmacher,, A. T., Taneyhill,, L. A., & Gammill,, L. S. (2014). FoxD3 regulates cranial neural crest EMT via downregulation of tetraspanin18 independent of its functions during neural crest formation. Mechanisms of Development, 132, 1–12.
Fairchild,, C. L., & Gammill,, L. S. (2013). Tetraspanin18 is a FoxD3‐responsive antagonist of cranial neural crest epithelial‐to‐mesenchymal transition that maintains cadherin‐6B protein. Journal of Cell Science, 126, 1464–1476.
Feledy,, J. A., Beanan,, M. J., Sandoval,, J. J., Goodrich,, J. S., Lim,, J. H., Matsuo‐Takasaki,, M., … Sargent,, T. D. (1999). Inhibitory patterning of the anterior neural plate in Xenopus by homeodomain factors Dlx3 and Msx1. Developmental Biology, 212, 455–464.
Ferronha,, T., Rabadan,, M. A., Gil‐Guinon,, E., Le Dreau,, G., de Torres,, C., & Marti,, E. (2013). LMO4 is an essential cofactor in the Snail2‐mediated epithelial‐to‐mesenchymal transition of neuroblastoma and neural crest cells. The Journal of Neuroscience, 33, 2773–2783.
Gallik,, K. L., Treffy,, R. W., Nacke,, L. M., Ahsan,, K., Rocha,, M., Green‐Saxena,, A., & Saxena,, A. (2017). Neural crest and cancer: Divergent travelers on similar paths. Mechanisms of Development, 148, 89–99.
Gammill,, L. S., & Bronner‐Fraser,, M. (2002). Genomic analysis of neural crest induction. Development, 129, 5731–5741.
Garcia‐Castro,, M. I., Marcelle,, C., & Bronner‐Fraser,, M. (2002). Ectodermal Wnt function as a neural crest inducer. Science, 297, 848–851.
Garnett,, A. T., Square,, T. A., & Medeiros,, D. M. (2012). BMP, Wnt and FGF signals are integrated through evolutionarily conserved enhancers to achieve robust expression of Pax3 and Zic genes at the zebrafish neural plate border. Development, 139, 4220–4231.
Gaur,, S., Mandelbaum,, M., Herold,, M., Majumdar,, H. D., Neilson,, K. M., Maynard,, T. M., … Moody,, S. A. (2016). Neural transcription factors bias cleavage stage blastomeres to give rise to neural ectoderm. Genesis, 54, 334–349.
Gee,, S. T., Milgram,, S. L., Kramer,, K. L., Conlon,, F. L., & Moody,, S. A. (2011). Yes‐associated protein 65 (YAP) expands neural progenitors and regulates Pax3 expression in the neural plate border zone. PLoS One, 6, e20309.
Gessert,, S., Bugner,, V., Tecza,, A., Pinker,, M., & Kuhl,, M. (2010). FMR1/FXR1 and the miRNA pathway are required for eye and neural crest development. Developmental Biology, 341, 222–235.
Glavic,, A., Silva,, F., Aybar,, M. J., Bastidas,, F., & Mayor,, R. (2004). Interplay between notch signaling and the homeoprotein Xiro1 is required for neural crest induction in Xenopus embryos. Development, 131, 347–359.
Goulding,, M. D., Chalepakis,, G., Deutsch,, U., Erselius,, J. R., & Gruss,, P. (1991). Pax‐3, a novel murine DNA binding protein expressed during early neurogenesis. The EMBO Journal, 10, 1135–1147.
Green,, S. A., Simoes‐Costa,, M., & Bronner,, M. E. (2015). Evolution of vertebrates as viewed from the crest. Nature, 520, 474–482.
Griffin,, J. N., Sondalle,, S. B., Del Viso,, F., Baserga,, S. J., & Khokha,, M. K. (2015). The ribosome biogenesis factor Nol11 is required for optimal rDNA transcription and craniofacial development in Xenopus. PLoS Genetics, 11, e1005018.
Groves,, A. K., & LaBonne,, C. (2014). Setting appropriate boundaries: Fate, patterning and competence at the neural plate border. Developmental Biology, 389, 2–12.
Hatch,, V. L., Marin‐Barba,, M., Moxon,, S., Ford,, C. T., Ward,, N. J., Tomlinson,, M. L., … Wheeler,, G. N. (2016). The positive transcriptional elongation factor (P‐TEFb) is required for neural crest specification. Developmental Biology, 416, 361–372.
Hernandez‐Lagunas,, L., Powell,, D. R., Law,, J., Grant,, K. A., & Artinger,, K. B. (2011). prdm1a and olig4 act downstream of Notch signaling to regulate cell fate at the neural plate border. Developmental Biology, 356, 496–505.
Hindley,, C. J., Condurat,, A. L., Menon,, V., Thomas,, R., Azmitia,, L. M., Davis,, J. A., & Pruszak,, J. (2016). The hippo pathway member YAP enhances human neural crest cell fate and migration. Scientific Reports, 6, 23208.
Hong,, C. S., Devotta,, A., Lee,, Y. H., Park,, B. Y., & Saint‐Jeannet,, J. P. (2014). Transcription factor AP2 epsilon (Tfap2e) regulates neural crest specification in Xenopus. Developmental Neurobiology, 74, 894–906.
Hong,, C. S., Park,, B. Y., & Saint‐Jeannet,, J. P. (2008). Fgf8a induces neural crest indirectly through the activation of Wnt8 in the paraxial mesoderm. Development, 135, 3903–3910.
Hong,, C. S., & Saint‐Jeannet,, J. P. (2007). The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border. Molecular Biology of the Cell, 18, 2192–2202.
Hu,, N., Strobl‐Mazzulla,, P., Sauka‐Spengler,, T., & Bronner,, M. E. (2012). DNA methyltransferase3A as a molecular switch mediating the neural tube‐to‐neural crest fate transition. Genes %26 Development, 26, 2380–2385.
Hu,, N., Strobl‐Mazzulla,, P. H., & Bronner,, M. E. (2014). Epigenetic regulation in neural crest development. Developmental Biology, 396, 159–168.
Hu,, N., Strobl‐Mazzulla,, P. H., Simoes‐Costa,, M., Sanchez‐Vasquez,, E., & Bronner,, M. E. (2014). DNA methyltransferase 3B regulates duration of neural crest production via repression of Sox10. Proceedings of the National Academy of Sciences of the United States of America, 111, 17911–17916.
Hurtado,, C., & De Robertis,, E. M. (2007). Neural induction in the absence of organizer in salamanders is mediated by MAPK. Developmental Biology, 307, 282–289.
Ikeya,, M., Lee,, S. M., Johnson,, J. E., McMahon,, A. P., & Takada,, S. (1997). Wnt signalling required for expansion of neural crest and CNS progenitors. Nature, 389, 966–970.
Ishimura,, A., Maeda,, R., Takeda,, M., Kikkawa,, M., Daar,, I. O., & Maeno,, M. (2000). Involvement of BMP‐4/msx‐1 and FGF pathways in neural induction in the Xenopus embryo. Development, Growth %26 Differentiation, 42, 307–316.
Jacques‐Fricke,, B. T., & Gammill,, L. S. (2014). Neural crest specification and migration independently require NSD3‐related lysine methyltransferase activity. Molecular Biology of the Cell, 25, 4174–4186.
James‐Zorn,, C., Ponferrada,, V. G., Jarabek,, C. J., Burns,, K. A., Segerdell,, E. J., Lee,, J., … Vize,, P. D. (2013). Xenbase: Expansion and updates of the Xenopus model organism database. Nucleic Acids Research, 41, D865–D870.
Jaroonwitchawan,, T., Muangchan,, P., & Noisa,, P. (2016). Inhibition of FGF signaling accelerates neural crest cell differentiation of human pluripotent stem cells. Biochemical and Biophysical Research Communications, 481, 176–181.
Jimenez,, L., Wang,, J., Morrison,, M. A., Whatcott,, C., Soh,, K. K., Warner,, S., … Stewart,, R. A. (2016). Phenotypic chemical screening using a zebrafish neural crest EMT reporter identifies retinoic acid as an inhibitor of epithelial morphogenesis. Disease Models %26 Mechanisms, 9, 389–400.
Joubin,, K., & Stern,, C. D. (2001). Formation and maintenance of the organizer among the vertebrates. The International Journal of Developmental Biology, 45, 165–175.
Karpinka,, J. B., Fortriede,, J. D., Burns,, K. A., James‐Zorn,, C., Ponferrada,, V. G., Lee,, J., … Vize,, P. D. (2015). Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes. Nucleic Acids Research, 43, D756–D763.
Kee,, Y., & Bronner‐Fraser,, M. (2005). To proliferate or to die: Role of Id3 in cell cycle progression and survival of neural crest progenitors. Genes %26 Development, 19, 744–755.
Kerosuo,, L., & Bronner,, M. E. (2016). cMyc regulates the size of the premigratory neural crest stem cell pool. Cell Reports, 17, 2648–2659.
Kerosuo,, L., Nie,, S., Bajpai,, R., & Bronner,, M. E. (2015). Crestospheres: Long‐term maintenance of multipotent, Premigratory neural crest stem cells. Stem Cell Reports, 5, 499–507.
Khudyakov,, J., & Bronner‐Fraser,, M. (2009). Comprehensive spatiotemporal analysis of early chick neural crest network genes. Developmental Dynamics, 238, 716–723.
Kiecker,, C., Bates,, T., & Bell,, E. (2016). Molecular specification of germ layers in vertebrate embryos. Cellular and Molecular Life Sciences, 73, 923–947.
Kimura‐Yoshida,, C., Mochida,, K., Ellwanger,, K., Niehrs,, C., & Matsuo,, I. (2015). Fate specification of neural plate border by canonical Wnt signaling and Grhl3 is crucial for neural tube closure. eBioMedicine, 2, 513–527.
Knight,, R. D., Nair,, S., Nelson,, S. S., Afshar,, A., Javidan,, Y., Geisler,, R., … Schilling,, T. F. (2003). lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development, 130, 5755–5768.
Koehler,, A., Schlupf,, J., Schneider,, M., Kraft,, B., Winter,, C., & Kashef,, J. (2013). Loss of Xenopus cadherin‐11 leads to increased Wnt/beta‐catenin signaling and up‐regulation of target genes c‐myc and cyclin D1 in neural crest. Developmental Biology, 383, 132–145.
LaBonne,, C., & Bronner‐Fraser,, M. (1998). Neural crest induction in Xenopus: Evidence for a two‐signal model. Development, 125, 2403–2414.
Ladher,, R. K., Church,, V. L., Allen,, S., Robson,, L., Abdelfattah,, A., Brown,, N. A., … Francis‐West,, P. H. (2000). Cloning and expression of the Wnt antagonists Sfrp‐2 and Frzb during chick development. Developmental Biology, 218, 183–198.
Lamb,, T. M., Knecht,, A. K., Smith,, W. C., Stachel,, S. E., Economides,, A. N., Stahl,, N., … Harland,, R. M. (1993). Neural induction by the secreted polypeptide noggin. Science, 262, 713–718.
Lander,, R., Nasr,, T., Ochoa,, S. D., Nordin,, K., Prasad,, M. S., & Labonne,, C. (2013). Interactions between Twist and other core epithelial‐mesenchymal transition factors are controlled by GSK3‐mediated phosphorylation. Nature Communications, 4, 1542.
Lander,, R., Nordin,, K., & LaBonne,, C. (2011). The F‐box protein Ppa is a common regulator of core EMT factors Twist, Snail, Slug, and Sip1. The Journal of Cell Biology, 194, 17–25.
Laue,, K., Pogoda,, H. M., Daniel,, P. B., van Haeringen,, A., Alanay,, Y., von Ameln,, S., … Robertson,, S. P. (2011). Craniosynostosis and multiple skeletal anomalies in humans and zebrafish result from a defect in the localized degradation of retinoic acid. American Journal of Human Genetics, 89, 595–606.
Lee,, P. C., Taylor‐Jaffe,, K. M., Nordin,, K. M., Prasad,, M. S., Lander,, R. M., & LaBonne,, C. (2012). SUMOylated SoxE factors recruit Grg4 and function as transcriptional repressors in the neural crest. The Journal of Cell Biology, 198, 799–813.
Lee,, R. T., Nagai,, H., Nakaya,, Y., Sheng,, G., Trainor,, P. A., Weston,, J. A., & Thiery,, J. P. (2013). Cell delamination in the mesencephalic neural fold and its implication for the origin of ectomesenchyme. Development, 140, 4890–4902.
Lee,, S. Y., Lim,, S. K., Cha,, S. W., Yoon,, J., Lee,, S. H., Lee,, H. S., … Kim,, J. (2011). Inhibition of FGF signaling converts dorsal mesoderm to ventral mesoderm in early Xenopus embryos. Differentiation, 82, 99–107.
Leung,, A. W., Murdoch,, B., Salem,, A. F., Prasad,, M. S., Gomez,, G. A., & Garcia‐Castro,, M. I. (2016). WNT/beta‐catenin signaling mediates human neural crest induction via a pre‐neural border intermediate. Development, 143, 398–410.
Li,, B., Kuriyama,, S., Moreno,, M., & Mayor,, R. (2009). The posteriorizing gene Gbx2 is a direct target of Wnt signalling and the earliest factor in neural crest induction. Development, 136, 3267–3278.
Light,, W., Vernon,, A. E., Lasorella,, A., Iavarone,, A., & LaBonne,, C. (2005). Xenopus Id3 is required downstream of Myc for the formation of multipotent neural crest progenitor cells. Development, 132, 1831–1841.
Linker,, C., Bronner‐Fraser,, M., & Mayor,, R. (2000). Relationship between gene expression domains of Xsnail, Xslug, and Xtwist and cell movement in the prospective neural crest of Xenopus. Developmental Biology, 224, 215–225.
Litsiou,, A., Hanson,, S., & Streit,, A. (2005). A balance of FGF, BMP and WNT signalling positions the future placode territory in the head. Development, 132, 4051–4062.
Liu,, J. A., Wu,, M. H., Yan,, C. H., Chau,, B. K., So,, H., Ng,, A., … Cheung,, M. (2013). Phosphorylation of Sox9 is required for neural crest delamination and is regulated downstream of BMP and canonical Wnt signaling. Proceedings of the National Academy of Sciences of the United States of America, 110, 2882–2887.
Liu,, Y., Helms,, A. W., & Johnson,, J. E. (2004). Distinct activities of Msx1 and Msx3 in dorsal neural tube development. Development, 131, 1017–1028.
Luan,, Z., Liu,, Y., Stuhlmiller,, T. J., Marquez,, J., & Garcia‐Castro,, M. I. (2013). SUMOylation of Pax7 is essential for neural crest and muscle development. Cellular and Molecular Life Sciences, 70, 1793–1806.
Lumb,, R., Buckberry,, S., Secker,, G., Lawrence,, D., & Schwarz,, Q. (2017). Transcriptome profiling reveals expression signatures of cranial neural crest cells arising from different axial levels. BMC Developmental Biology, 17, 5.
Luo,, T., Matsuo‐Takasaki,, M., Lim,, J. H., & Sargent,, T. D. (2001). Differential regulation of Dlx gene expression by a BMP morphogenetic gradient. The International Journal of Developmental Biology, 45, 681–684.
Macri,, S., Simula,, L., Pellarin,, I., Pegoraro,, S., Onorati,, M., Sgarra,, R., … Vignali,, R. (2016). Hmga2 is required for neural crest cell specification in Xenopus laevis. Developmental Biology, 411, 25–37.
Maj,, E., Kunneke,, L., Loresch,, E., Grund,, A., Melchert,, J., Pieler,, T., … Borchers,, A. (2016). Controlled levels of canonical Wnt signaling are required for neural crest migration. Developmental Biology, 417, 77–90.
Mansouri,, A., & Gruss,, P. (1998). Pax3 and Pax7 are expressed in commissural neurons and restrict ventral neuronal identity in the spinal cord. Mechanisms of Development, 78, 171–178.
Marchal,, L., Luxardi,, G., Thome,, V., & Kodjabachian,, L. (2009). BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proceedings of the National Academy of Sciences of the United States of America, 106, 17437–17442.
Marchant,, L., Linker,, C., Ruiz,, P., Guerrero,, N., & Mayor,, R. (1998). The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Developmental Biology, 198, 319–329.
Martik,, M. L., & Bronner,, M. E. (2017). Regulatory logic underlying diversification of the neural crest. Trends in Genetics, 33, 715–727.
Martinez‐Morales,, P. L., Diez del Corral,, R., Olivera‐Martinez,, I., Quiroga,, A. C., Das,, R. M., Barbas,, J. A., … Morales,, A. V. (2011). FGF and retinoic acid activity gradients control the timing of neural crest cell emigration in the trunk. The Journal of Cell Biology, 194, 489–503.
Masek,, J., Machon,, O., Korinek,, V., Taketo,, M. M., & Kozmik,, Z. (2016). Tcf7l1 protects the anterior neural fold from adopting the neural crest fate. Development, 143, 2206–2216.
Matsukawa,, S., Miwata,, K., Asashima,, M., & Michiue,, T. (2015). The requirement of histone modification by PRDM12 and Kdm4a for the development of pre‐placodal ectoderm and neural crest in Xenopus. Developmental Biology, 399, 164–176.
Matsuo‐Takasaki,, M., Matsumura,, M., & Sasai,, Y. (2005). An essential role of Xenopus Foxi1a for ventral specification of the cephalic ectoderm during gastrulation. Development, 132, 3885–3894.
Mayor,, R., Guerrero,, N., & Martinez,, C. (1997). Role of FGF and noggin in neural crest induction. Developmental Biology, 189, 1–12.
Mayor,, R., Morgan,, R., & Sargent,, M. G. (1995). Induction of the prospective neural crest of Xenopus. Development, 121, 767–777.
McLarren,, K. W., Litsiou,, A., & Streit,, A. (2003). DLX5 positions the neural crest and preplacode region at the border of the neural plate. Developmental Biology, 259, 34–47.
McLennan,, R., Bailey,, C. M., Schumacher,, L. J., Teddy,, J.M., Morrison,, J. A., Kasemeier‐Kulesa,, J. C., … Kulesa,, P. M,. (2017). DAN (NBL1) promotes collective neural crest migration by restraining uncontrolled invasion. J Cell Biol, 216, 3339–3354.
McMahon,, A. R., & Merzdorf,, C. S. (2010). Expression of the zic1, zic2, zic3, and zic4 genes in early chick embryos. BMC Research Notes, 3, 167.
Menendez,, L., Kulik,, M. J., Page,, A. T., Park,, S. S., Lauderdale,, J. D., Cunningham,, M. L., & Dalton,, S. (2013). Directed differentiation of human pluripotent cells to neural crest stem cells. Nature Protocols, 8, 203–212.
Meulemans,, D., & Bronner‐Fraser,, M. (2002). Amphioxus and lamprey AP‐2 genes: Implications for neural crest evolution and migration patterns. Development, 129, 4953–4962.
Meulemans,, D., & Bronner‐Fraser,, M. (2005). Central role of gene cooption in neural crest evolution. Journal of Experimental Biology Part B: Molecular and Developmental Evolution, 304, 298–303.
Mikawa,, T., Poh,, A. M., Kelly,, K. A., Ishii,, Y., & Reese,, D. E. (2004). Induction and patterning of the primitive streak, an organizing center of gastrulation in the amniote. Developmental Dynamics, 229, 422–432.
Milet,, C., Maczkowiak,, F., Roche,, D. D., & Monsoro‐Burq,, A. H. (2013). Pax3 and Zic1 drive induction and differentiation of multipotent, migratory, and functional neural crest in Xenopus embryos. Proceedings of the National Academy of Sciences of the United States of America, 110, 5528–5533.
Minoux,, M., Holwerda,, S., Vitobello,, A., Kitazawa,, T., Kohler,, H., Stadler,, M. B., & Rijli,, F. M. (2017). Gene bivalency at Polycomb domains regulates cranial neural crest positional identity. Science, 355, eaal2913.
Monsoro‐Burq,, A. H., Fletcher,, R. B., & Harland,, R. M. (2003). Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development, 130, 3111–3124.
Monsoro‐Burq,, A. H., Wang,, E., & Harland,, R. (2005). Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Developmental Cell, 8, 167–178.
Moury,, J. D., & Jacobson,, A. G. (1990). The origins of neural crest cells in the axolotl. Developmental Biology, 141, 243–253.
Murko,, C., Lagger,, S., Steiner,, M., Seiser,, C., Schoefer,, C., & Pusch,, O. (2013). Histone deacetylase inhibitor Trichostatin A induces neural tube defects and promotes neural crest specification in the chicken neural tube. Differentiation, 85, 55–66.
Naylor,, R. W., Skvarca,, L. B., Thisse,, C., Thisse,, B., Hukriede,, N. A., & Davidson,, A. J. (2016). BMP and retinoic acid regulate anterior‐posterior patterning of the non‐axial mesoderm across the dorsal‐ventral axis. Nature Communications, 7, 12197.
Nichane,, M., Ren,, X., Souopgui,, J., & Bellefroid,, E. J. (2008). Hairy2 functions through both DNA‐binding and non DNA‐binding mechanisms at the neural plate border in Xenopus. Developmental Biology, 322, 368–380.
Nikitina,, N., Sauka‐Spengler,, T., & Bronner‐Fraser,, M. (2008). Dissecting early regulatory relationships in the lamprey neural crest gene network. Proceedings of the National Academy of Sciences of the United States of America, 105, 20083–20088.
Nordin,, K., & LaBonne,, C. (2014). Sox5 is a DNA‐binding cofactor for BMP R‐Smads that directs target specificity during patterning of the early ectoderm. Developmental Cell, 31, 374–382.
Northrop,, J., Woods,, A., Seger,, R., Suzuki,, A., Ueno,, N., Krebs,, E., & Kimelman,, D. (1995). BMP‐4 regulates the dorsal‐ventral differences in FGF/MAPKK‐mediated mesoderm induction in Xenopus. Developmental Biology, 172, 242–252.
Ochoa,, S. D., Salvador,, S., & LaBonne,, C. (2012). The LIM adaptor protein LMO4 is an essential regulator of neural crest development. Developmental Biology, 361, 313–325.
O`Donnell,, M., Hong,, C. S., Huang,, X., Delnicki,, R. J., & Saint‐Jeannet,, J. P. (2006). Functional analysis of Sox8 during neural crest development in Xenopus. Development, 133, 3817–3826.
Oonuma,, K., Tanaka,, M., Nishitsuji,, K., Kato,, Y., Shimai,, K., & Kusakabe,, T. G. (2016). Revised lineage of larval photoreceptor cells in Ciona reveals archetypal collaboration between neural tube and neural crest in sensory organ formation. Developmental Biology, 420, 178–185.
Ossipova,, O., & Sokol,, S. Y. (2011). Neural crest specification by noncanonical Wnt signaling and PAR‐1. Development, 138, 5441–5450.
Patthey,, C., & Gunhaga,, L. (2014). Signaling pathways regulating ectodermal cell fate choices. Experimental Cell Research, 321, 11–16.
Pegoraro,, C., & Monsoro‐Burq,, A. H. (2013). Signaling and transcriptional regulation in neural crest specification and migration: Lessons from xenopus embryos. WIREs Developmental Biology, 2, 247–259.
Pera,, E. M., Ikeda,, A., Eivers,, E., & De Robertis,, E. M. (2003). Integration of IGF, FGF, and anti‐BMP signals via Smad1 phosphorylation in neural induction. Genes %26 Development, 17, 3023–3028.
Plouhinec,, J. L., Medina‐Ruiz,, S., Borday,, C., Bernard,, E., Vert,, J. P., Eisen,, M. B., … Monsoro‐Burq,, A. H. (2017). A molecular atlas of the developing ectoderm defines neural, neural crest, placode, and nonneural progenitor identity in vertebrates. PLoS Biology, 15, e2004045.
Plouhinec,, J. L., Roche,, D. D., Pegoraro,, C., Figueiredo,, A. L., Maczkowiak,, F., Brunet,, L. J., … Monsoro‐Burq,, A. H. (2014). Pax3 and Zic1 trigger the early neural crest gene regulatory network by the direct activation of multiple key neural crest specifiers. Developmental Biology, 386, 461–472.
Podleschny,, M., Grund,, A., Berger,, H., Rollwitz,, E., & Borchers,, A. (2015). A PTK7/Ror2 Co‐receptor complex affects xenopus neural crest migration. PLoS One, 10, e0145169.
Powell,, D. R., Hernandez‐Lagunas,, L., LaMonica,, K., & Artinger,, K. B. (2013). Prdm1a directly activates foxd3 and tfap2a during zebrafish neural crest specification. Development, 140, 3445–3455.
Powell,, D. R., Williams,, J. S., Hernandez‐Lagunas,, L., Salcedo,, E., O`Brien,, J. H., & Artinger,, K. B. (2015). Cdon promotes neural crest migration by regulating N‐cadherin localization. Developmental Biology, 407, 289–299.
Prasad,, M. S., Sauka‐Spengler,, T., & LaBonne,, C. (2012). Induction of the neural crest state: Control of stem cell attributes by gene regulatory, post‐transcriptional and epigenetic interactions. Developmental Biology, 366, 10–21.
Pyrgaki,, C., Liu,, A., & Niswander,, L. (2011). Grainyhead‐like 2 regulates neural tube closure and adhesion molecule expression during neural fold fusion. Developmental Biology, 353, 38–49.
Rabadán,, M. A., Herrera,, A., Fanlo,, L., Usieto,, S., Carmona‐Fontaine,, C., Barriga,, E. H., … Martí,, E. (2016). Delamination of neural crest cells requires transient and reversible Wnt inhibition mediated by Dact1/2. Development, 143, 2194–2205.
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, 633–648.
Ray,, H. J., & Niswander,, L. A. (2016). Grainyhead‐like 2 downstream targets act to suppress epithelial‐to‐mesenchymal transition during neural tube closure. Development, 143, 1192–1204.
Rinon,, A., Molchadsky,, A., Nathan,, E., Yovel,, G., Rotter,, V., Sarig,, R., & Tzahor,, E. (2011). p53 coordinates cranial neural crest cell growth and epithelial‐mesenchymal transition/delamination processes. Development, 138, 1827–1838.
Roellig,, D., Tan‐Cabugao,, J., Esaian,, S., & Bronner,, M. E. (2017). Dynamic transcriptional signature and cell fate analysis reveals plasticity of individual neural plate border cells. eLife, 6.
Rogers,, C. D., Archer,, T. C., Cunningham,, D. D., Grammer,, T. C., & Casey,, E. M. (2008). Sox3 expression is maintained by FGF signaling and restricted to the neural plate by vent proteins in the Xenopus embryo. Developmental Biology, 313, 307–319.
Rogers,, C. D., Jayasena,, C. S., Nie,, S., & Bronner,, M. E. (2012). Neural crest specification: Tissues, signals, and transcription factors. WIREs Developmental Biology, 1, 52–68.
Rogers,, C. D., Moody,, S. A., & Casey,, E. S. (2009). Neural induction and factors that stabilize a neural fate. Birth Defects Research. Part C, Embryo Today, 87, 249–262.
Rogers,, C. D., Saxena,, A., & Bronner,, M. E. (2013). Sip1 mediates an E‐cadherin‐to‐N‐cadherin switch during cranial neural crest EMT. The Journal of Cell Biology, 203, 835–847.
Sakai,, D., Suzuki,, T., Osumi,, N., & Wakamatsu,, Y. (2006). Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development, 133, 1323–1333.
Sanchez‐Ferras,, O., Bernas,, G., Farnos,, O., Toure,, A. M., Souchkova,, O., & Pilon,, N. (2016). A direct role for murine Cdx proteins in the trunk neural crest gene regulatory network. Development, 143, 1363–1374.
Sanchez‐Ferras,, O., Bernas,, G., Laberge‐Perrault,, E., & Pilon,, N. (2014). Induction and dorsal restriction of paired‐box 3 (Pax3) gene expression in the caudal neuroectoderm is mediated by integration of multiple pathways on a short neural crest enhancer. Biochimica et Biophysica Acta, 1839, 546–558.
Sasai,, N., Mizuseki,, K., & Sasai,, Y. (2001). Requirement of FoxD3‐class signaling for neural crest determination in Xenopus. Development, 128, 2525–2536.
Sasai,, N., Kutejova,, E., & Briscoe,, J. (2014). Integration of signals along orthogonal axes of the vertebrate neural tube controls progenitor competence and increases cell diversity. PLoS Biol, 12, e1001907.
Sato,, T., Sasai,, N., & Sasai,, Y. (2005). Neural crest determination by co‐activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development, 132, 2355–2363.
Schiffmacher,, A. T., Xie,, V., & Taneyhill,, L. A. (2016). Cadherin‐6B proteolysis promotes the neural crest cell epithelial‐to‐mesenchymal transition through transcriptional regulation. The Journal of Cell Biology, 215, 735–747.
Schille,, C., Bayerlova,, M., Bleckmann,, A., & Schambony,, A. (2016). Ror2 signaling is required for local upregulation of GDF6 and activation of BMP signaling at the neural plate border. Development, 143, 3182–3194.
Schille,, C., Heller,, J., & Schambony,, A. (2016). Differential requirement of bone morphogenetic protein receptors Ia (ALK3) and Ib (ALK6) in early embryonic patterning and neural crest development. BMC Developmental Biology, 16(1), 1.
Schille,, C., & Schambony,, A. (2017). Signaling pathways and tissue interactions in neural plate border formation. Neurogenesis (Austin), 4, e1292783.
Schlosser,, G. (2014). Early embryonic specification of vertebrate cranial placodes. WIREs Developmental Biology, 3, 349–363.
Schmidt,, C., McGonnell,, I. M., Allen,, S., Otto,, A., & Patel,, K. (2007). Wnt6 controls amniote neural crest induction through the non‐canonical signaling pathway. Developmental Dynamics, 236, 2502–2511.
Schorle,, H., Meier,, P., Buchert,, M., Jaenisch,, R., & Mitchell,, P. J. (1996). Transcription factor AP‐2 essential for cranial closure and craniofacial development. Nature, 381, 235–238.
Schwend,, T., & Ahlgren,, S. C. (2009). Zebrafish con/disp1 reveals multiple spatiotemporal requirements for hedgehog‐signaling in craniofacial development. BMC Developmental Biology, 9, 59.
Schwend,, T., Loucks,, E. J., & Ahlgren,, S. C. (2010). Visualization of Gli activity in craniofacial tissues of hedgehog‐pathway reporter transgenic zebrafish. PLoS One, 5, e14396.
Shi,, J., Severson,, C., Yang,, J., Wedlich,, D., & Klymkowsky,, M. W. (2011). Snail2 controls mesodermal BMP/Wnt induction of neural crest. Development, 138, 3135–3145.
Shigetani,, Y., Wakamatsu,, Y., Tachibana,, T., & Okabe,, M. (2016). Conversion of neural plate explants to pre‐placodal ectoderm‐like tissue in vitro. Biochemical and Biophysical Research Communications, 477, 807–813.
Shih,, H. Y., Hsu,, S. Y., Ouyang,, P., Lin,, S. J., Chou,, T. Y., Chiang,, M. C., & Cheng,, Y. C. (2017). Bmp5 regulates neural crest cell survival and proliferation via two different signaling pathways. Stem Cells, 35, 1003–1014.
Shyamala,, K., Yanduri,, S., Girish,, H. C., & Murgod,, S. (2015). Neural crest: The fourth germ layer. Journal of Oral and Maxillofacial Pathology, 19, 221–229.
Simoes‐Costa,, M., & Bronner,, M. E. (2015). Establishing neural crest identity: A gene regulatory recipe. Development, 142, 242–257.
Simoes‐Costa,, M., & Bronner,, M. E. (2016). Reprogramming of avian neural crest axial identity and cell fate. Science, 352, 1570–1573.
Simoes‐Costa,, M., Stone,, M., & Bronner,, M. E. (2015). Axud1 integrates Wnt signaling and transcriptional inputs to drive neural crest formation. Developmental Cell, 34, 544–554.
Simoes‐Costa,, M., Tan‐Cabugao,, J., Antoshechkin,, I., Sauka‐Spengler,, T., & Bronner,, M. E. (2014). Transcriptome analysis reveals novel players in the cranial neural crest gene regulatory network. Genome Research, 24(2), 281–290. https://doi.org/10.1101/gr.161182.113
Simoes‐Costa,, M. S., McKeown,, S. J., Tan‐Cabugao,, J., Sauka‐Spengler,, T., & Bronner,, M. E. (2012). Dynamic and differential regulation of stem cell factor FoxD3 in the neural crest is encrypted in the genome. PLoS Genetics, 8, e1003142.
Sive,, H. L., Draper,, B. W., Harland,, R. M., & Weintraub,, H. (1990). Identification of a retinoic acid‐sensitive period during primary axis formation in Xenopus laevis. Genes %26 Development, 4, 932–942.
Spokony,, R. F., Aoki,, Y., Saint‐Germain,, N., Magner‐Fink,, E., & Saint‐Jeannet,, J. P. (2002). The transcription factor Sox9 is required for cranial neural crest development in Xenopus. Development, 129, 421–432.
Stolfi,, A., Ryan,, K., Meinertzhagen,, I. A., & Christiaen,, L. (2015). Migratory neuronal progenitors arise from the neural plate borders in tunicates. Nature, 527, 371–374.
Streit,, A., Lee,, K. J., Woo,, I., Roberts,, C., Jessell,, T. M., & Stern,, C. D. (1998). Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development, 125, 507–519.
Strobl‐Mazzulla,, P. H., & Bronner,, M. E. (2012a). Epithelial to mesenchymal transition: New and old insights from the classical neural crest model. Seminars in Cancer Biology, 22, 411–416.
Strobl‐Mazzulla,, P. H., & Bronner,, M. E. (2012b). A PHD12‐Snail2 repressive complex epigenetically mediates neural crest epithelial‐to‐mesenchymal transition. The Journal of Cell Biology, 198, 999–1010.
Strobl‐Mazzulla,, P. H., Sauka‐Spengler,, T., & Bronner‐Fraser,, M. (2010). Histone demethylase JmjD2A regulates neural crest specification. Developmental Cell, 19, 460–468.
Stuhlmiller,, T. J., & Garcia‐Castro,, M. I. (2012a). Current perspectives of the signaling pathways directing neural crest induction. Cellular and Molecular Life Sciences, 69, 3715–3737.
Stuhlmiller,, T. J., & Garcia‐Castro,, M. I. (2012b). FGF/MAPK signaling is required in the gastrula epiblast for avian neural crest induction. Development, 139, 289–300.
Tai,, A., Cheung,, M., Huang,, Y. H., Jauch,, R., Bronner,, M. E., & Cheah,, K. S. (2016). SOXE neofunctionalization and elaboration of the neural crest during chordate evolution. Scientific Reports, 6, 34964.
Takahashi,, K., & Yamanaka,, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663–676.
Takahashi,, Y., Tonegawa,, A., Matsumoto,, K., Ueno,, N., Kuroiwa,, A., Noda,, M., & Nifuji,, A. (1996). BMP‐4 mediates interacting signals between the neural tube and skin along the dorsal midline. Genes to Cells, 1, 775–783.
Taneyhill,, L. A., Coles,, E. G., & Bronner‐Fraser,, M. (2007). Snail2 directly represses cadherin6B during epithelial‐to‐mesenchymal transitions of the neural crest. Development, 134, 1481–1490.
Taneyhill,, L. A., & Schiffmacher,, A. T. (2017). Should I stay or should I go? Cadherin function and regulation in the neural crest. Genesis, 55, e23028.
Taylor,, K. M., & Labonne,, C. (2005). SoxE factors function equivalently during neural crest and inner ear development and their activity is regulated by SUMOylation. Developmental Cell, 9, 593–603.
Testaz,, S., Jarov,, A., Williams,, K. P., Ling,, L. E., Koteliansky,, V. E., Fournier‐Thibault,, C., & Duband,, J. L. (2001). Sonic hedgehog restricts adhesion and migration of neural crest cells independently of the patched‐smoothened‐Gli signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 98, 12521–12526.
Theveneau,, E., Duband,, J. L., & Altabef,, M. (2007). Ets‐1 confers cranial features on neural crest delamination. PLoS One, 2, e1142.
Theveneau,, E., Steventon,, B., Scarpa,, E., Garcia,, S., Trepat,, X., Streit,, A., & Mayor,, R. (2013). Chase‐and‐run between adjacent cell populations promotes directional collective migration. Nature Cell Biology, 15, 763–772.
Tien,, C. L., Jones,, A., Wang,, H., Gerigk,, M., Nozell,, S., & Chang,, C. (2015). Snail2/Slug cooperates with Polycomb repressive complex 2 (PRC2) to regulate neural crest development. Development, 142, 722–731.
Tolosa,, E. J., Fernandez‐Zapico,, M. E., Battiato,, N. L., & Rovasio,, R. A. (2016). Sonic hedgehog is a chemotactic neural crest cell guide that is perturbed by ethanol exposure. European Journal of Cell Biology, 95, 136–152.
Trainor,, P. A., Tan,, S. S., & Tam,, P. P. (1994). Cranial paraxial mesoderm: Regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development, 120, 2397–2408.
Tremblay,, P., Pituello,, F., & Gruss,, P. (1996). Inhibition of floor plate differentiation by Pax3: Evidence from ectopic expression in transgenic mice. Development, 122, 2555–2567.
Tribulo,, C., Aybar,, M. J., Nguyen,, V. H., Mullins,, M. C., & Mayor,, R. (2003). Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. Development, 130, 6441–6452.
Trinh,, L. A., Chong‐Morrison,, V., Gavriouchkina,, D., Hochgreb‐Hagele,, T., Senanayake,, U., Fraser,, S. E., & Sauka‐Spengler,, T. (2017). Biotagging of specific cell populations in zebrafish reveals gene regulatory logic encoded in the nuclear transcriptome. Cell Reports, 19, 425–440.
Uribe,, R. A., Hong,, S. S., & Bronner,, M. E. (2017). Retinoic acid temporally orchestrates colonization of the gut by vagal neural crest cells. Developmental Biology.
Vallin,, J., Thuret,, R., Giacomello,, E., Faraldo,, M. M., Thiery,, J. P., & Broders,, F. (2001). Cloning and characterization of three Xenopus slug promoters reveal direct regulation by Lef/beta‐catenin signaling. The Journal of Biological Chemistry, 276, 30350–30358.
Van Otterloo,, E., Li,, W., Garnett,, A., Cattell,, M., Medeiros,, D. M., & Cornell,, R. A. (2012). Novel Tfap2‐mediated control of soxE expression facilitated the evolutionary emergence of the neural crest. Development, 139, 720–730.
Varley,, J. E., & Maxwell,, G. D. (1996). BMP‐2 and BMP‐4, but not BMP‐6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Experimental Neurology, 140, 84–94.
Vega‐Lopez,, G. A., Bonano,, M., Tribulo,, C., Fernandez,, J. P., Aguero,, T. H., & Aybar,, M. J. (2015). Functional analysis of Hairy genes in Xenopus neural crest initial specification and cell migration. Developmental Dynamics, 244, 988–1013.
Villanueva,, S., Glavic,, A., Ruiz,, P., & Mayor,, R. (2002). Posteriorization by FGF, Wnt, and retinoic acid is required for neural crest induction. Developmental Biology, 241, 289–301.
von Bubnoff,, A., Schmidt,, J. E., & Kimelman,, D. (1996). The Xenopus laevis homeobox gene Xgbx‐2 is an early marker of anteroposterior patterning in the ectoderm. Mechanisms of Development, 54, 149–160.
Wai,, H. A., Kawakami,, K., Wada,, H., Muller,, F., Vernallis,, A. B., Brown,, G., & Johnson,, W. E. (2015). The development and growth of tissues derived from cranial neural crest and primitive mesoderm is dependent on the ligation status of retinoic acid receptor gamma: Evidence that retinoic acid receptor gamma functions to maintain stem/progenitor cells in the absence of retinoic acid. Stem Cells and Development, 24, 507–519.
Wakamatsu,, Y., Nomura,, T., Osumi,, N., & Suzuki,, K. (2014). Comparative gene expression analyses reveal heterochrony for Sox9 expression in the cranial neural crest during marsupial development. Evolution %26 Development, 16, 197–206.
Wang,, C., Kam,, R. K., Shi,, W., Xia,, Y., Chen,, X., Cao,, Y., … Zhao,, H. (2015). The proto‐oncogene transcription factor Ets1 regulates neural crest development through histone deacetylase 1 to mediate output of bone morphogenetic protein signaling. The Journal of Biological Chemistry, 290, 21925–21938.
Wang,, W. D., Melville,, D. B., Montero‐Balaguer,, M., Hatzopoulos,, A. K., & Knapik,, E. W. (2011). Tfap2a and Foxd3 regulate early steps in the development of the neural crest progenitor population. Developmental Biology, 360, 173–185.
Wang,, X. D., Morgan,, S. C., & Loeken,, M. R. (2011). Pax3 stimulates p53 ubiquitination and degradation independent of transcription. PLoS One, 6, e29379.
Watanabe,, T., Goulding,, E. H., & Pratt,, R. M. (1988). Alterations in craniofacial growth induced by isotretinoin (13‐cis‐retinoic acid) in mouse whole embryo and primary mesenchymal cell culture. Journal of Craniofacial Genetics and Developmental Biology, 8, 21–33.
Watanabe,, T., Kanai,, Y., Matsukawa,, S., & Michiue,, T. (2015). Specific induction of cranial placode cells from Xenopus ectoderm by modulating the levels of BMP, Wnt, and FGF signaling. Genesis, 53, 652–659.
Watanabe,, T., & Pratt,, R. M. (1991). Effects of retinoic acid on embryonic development of mice in culture. Experientia, 47, 493–497.
Wei,, D., & Loeken,, M. R. (2014). Increased DNA methyltransferase 3b (Dnmt3b)‐mediated CpG island methylation stimulated by oxidative stress inhibits expression of a gene required for neural tube and neural crest development in diabetic pregnancy. Diabetes, 63, 3512–3522.
Wei,, K., Chen,, J., Akrami,, K., Galbraith,, G. C., Lopez,, I. A., & Chen,, F. (2007). Neural crest cell deficiency of c‐myc causes skull and hearing defects. Genesis, 45, 382–390.
Werner,, A., Iwasaki,, S., McGourty,, C. A., Medina‐Ruiz,, S., Teerikorpi,, N., Fedrigo,, I., … Rape,, M. (2015). Cell‐fate determination by ubiquitin‐dependent regulation of translation. Nature, 525, 523–527.
Wilde,, J. J., Petersen,, J. R., & Niswander,, L. (2014). Genetic, epigenetic, and environmental contributions to neural tube closure. Annual Review of Genetics, 48, 583–611.
Wiszniak,, S., Kabbara,, S., Lumb,, R., Scherer,, M., Secker,, G., Harvey,, N., … Schwarz,, Q. (2013). The ubiquitin ligase Nedd4 regulates craniofacial development by promoting cranial neural crest cell survival and stem‐cell like properties. Developmental Biology, 383, 186–200.
Woda,, J. M., Pastagia,, J., Mercola,, M., & Artinger,, K. B. (2003). Dlx proteins position the neural plate border and determine adjacent cell fates. Development, 130, 331–342.
Xi,, J., Wu,, Y., Li,, G., Ma,, L., Feng,, K., Guo,, X., … Kang,, J. (2017). Mir‐29b mediates the neural tube versus neural crest fate decision during embryonic stem cell neural differentiation. Stem Cell Reports, 9, 571–586.
Yan,, Y. L., Willoughby,, J., Liu,, D., Crump,, J. G., Wilson,, C., Miller,, C. T., … Postlethwait,, J. H. (2005). A pair of Sox: Distinct and overlapping functions of zebrafish sox9 co‐orthologs in craniofacial and pectoral fin development. Development, 132, 1069–1083.
Yang,, X., Li,, J., Zeng,, W., Li,, C., & Mao,, B. (2016). Elongator protein 3 (Elp3) stabilizes Snail1 and regulates neural crest migration in Xenopus. Scientific Reports, 6, 26238.
Yardley,, N., & Garcia‐Castro,, M. I. (2012). FGF signaling transforms non‐neural ectoderm into neural crest. Developmental Biology, 372, 166–177.
Zhang,, C., & Klymkowsky,, M. W. (2009). Unexpected functional redundancy between Twist and Slug (Snail2) and their feedback regulation of NF‐kappaB via Nodal and Cerberus. Developmental Biology, 331, 340–349.
Zhang,, Z., Shi,, Y., Zhao,, S., Li,, J., Li,, C., & Mao,, B. (2014). Xenopus Nkx6.3 is a neural plate border specifier required for neural crest development. PLoS One, 9, e115165.
Zhao,, C., Andreeva,, V., Gibert,, Y., LaBonty,, M., Lattanzi,, V., Prabhudesai,, S., … Yelick,, P. C. (2014). Tissue specific roles for the ribosome biogenesis factor Wdr43 in zebrafish development. PLoS Genetics, 10, e1004074.
Zhou,, B. P., Deng,, J., Xia,, W., Xu,, J., Li,, Y. M., Gunduz,, M., & Hung,, M. C. (2004). Dual regulation of snail by GSK‐3beta‐mediated phosphorylation in control of epithelial‐mesenchymal transition. Nature Cell Biology, 6, 931–940.

Further Reading

Green,, S. A., Simoes‐Costa,, M., & Bronner,, M. E. (2015). Evolution of vertebrates as viewed from the crest. Nature, 520(7,548), 474–482. https://doi.org/10.1038/nature14436

Society Partners

	Free online access to WIREs Developmental Biology is a member benefit. Learn More
	SDB Collaborative Resources
	Society for Developmental Biology Homepage

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

The latest WIREs articles in your inbox

Sign Up for Article Alerts