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Molecular Biology

, Volume 53, Issue 2, pp 227–236 | Cite as

Neural Crest—An Unusual Population of Embryonic Cells

  • E. S. PshennikovaEmail author
  • A. S. Voronina
REVIEWS
  • 4 Downloads

Abstract

The neural crest (NC) in embryos of vertebrates represents a cell population formed at the border of the neural plate. These cells retain pluripotency, express a set of specific markers, and become multipotent upon their migration away from the neural tube to give rise to numerous derivatives. The genes specific for vertebrate NC appeared in evolution long before vertebrates. Abnormal development of NC cells causes numerous pathologies in humans.

Keywords:

neural crest gene regulatory networks pluripotency stem cells 

Notes

REFERENCES

  1. 1.
    His W. 1868. Untersuchungen über die erste Anlage des Wirbeltierleibes: die erste Entwickelung des Hühnchens im Ei. Leipzig: Vogel FCW.CrossRefGoogle Scholar
  2. 2.
    Horstadius S. 1950. The Neural Crest: Its Properties and Derivatives in the Light of Experimental Research. London: Oxford Univ. Press.Google Scholar
  3. 3.
    Katschenko N. 1888. Zur Entwicklungsgeschichte der Selachierembryos. Anat. Anz. 3, 445–467.Google Scholar
  4. 4.
    Muñoz W.A., Trainor P.A. 2015. Neural crest cell evolution: How and when did a neural crest cell become a neural crest cell. Curr. Top. Dev. Biol. 111, 3–26.CrossRefGoogle Scholar
  5. 5.
    Stone L.S. 1928. Problems concerning the origin and development of the neural crest and cranial ganglia in the vertebrates. Yale J. Biol. Med. 1, 7–14.Google Scholar
  6. 6.
    Stone L.S. 1929. Experiments showing the role of migrating neural crest (mesectoderm) in the formation of head skeleton and loose connective tissue in Rana palustris. Wilhelm Roux Arch. EntwMech Org. 118, 40–77.CrossRefGoogle Scholar
  7. 7.
    Saint-Jeannet J.P., Moody S.A. 2014. Establishing the pre-placodal region and breaking it into placodes with distinct identities. Dev. Biol. 389, 13–27.CrossRefGoogle Scholar
  8. 8.
    Graham A., Shimeld S.M. 2013. The origin and evolution of the ectodermal placodes. J. Anat. 222, 32–40.CrossRefGoogle Scholar
  9. 9.
    Northcutt R.G., Gans C. 1983. The genesis of neural crest and epidermal placodes: A reinterpretation of vertebrate origins. Q. Rev. Biol. 58, 1–28.CrossRefGoogle Scholar
  10. 10.
    Abitua P.B., Gainous T.B., Kaczmarczyk A.N., Winchell C.J., Hudson C., Kamata K., Nakagawa M., Tsuda M., Kusakabe T.G., Levine M. 2015. The pre-vertebrate origins of neurogenic placodes. Nature. 524, 462‒465.CrossRefGoogle Scholar
  11. 11.
    Couly G.F., Coltey P.M., Le Douarin N.M. 1993. The triple origin of skull in higher vertebrates: A study in quail–chick chimeras. Development. 117, 409–429.Google Scholar
  12. 12.
    Le Douarin N.M., Dupin E. 2012. The neural crest in vertebrate evolution. Curr. Opin. Genet. Dev. 22, 381–389.CrossRefGoogle Scholar
  13. 13.
    Le Douarin N.M., Couly G., Creuzet S.E. 2012. The neural crest is a powerful regulator of pre-otic brain development. Dev. Biol. 366, 74–82.CrossRefGoogle Scholar
  14. 14.
    Mongera A., Singh A.P, Levesque M.P., Chen Y.Y., Konstantinidis P., Nüsslein-Volhard C. 2013. Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development. 140, 916–925.CrossRefGoogle Scholar
  15. 15.
    Hall B.K. 1997. Germ layers and the germ-layer theory revisited: Primary and secondary germ layers, neural crest as a fourth germ layer, homology, demise of the germ-layer theory. Evol. Biol. 30, 121–186.Google Scholar
  16. 16.
    Hall B.K. 2000. The neural crest as a fourth germ layer and vertebrates as quadroblastic not triploblastic. Evol. Dev. 2, 3–5.CrossRefGoogle Scholar
  17. 17.
    Hall B.K. 2018. Germ layers, the neural crest and emergent organization in development and evolution. Genesis. e23103.  https://doi.org/10.1002/dvg.23103
  18. 18.
    Meulemans D., Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev. Cell. 7, 291–299.CrossRefGoogle Scholar
  19. 19.
    DeRobertis E.M., Kuroda H. 2004. Dorsal–ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285–308.CrossRefGoogle Scholar
  20. 20.
    Duband J.L., Dady A., Fleury V. 2015. Resolving time and space constraints during neural crest formation and delamination. Curr. Top. Dev. Biol. 111, 27–67.CrossRefGoogle Scholar
  21. 21.
    Green S.A., Simões-Costa M., Bronner M.E. 2015. Evolution of vertebrates as viewed from the crest. Nature. 520, 474–482.CrossRefGoogle Scholar
  22. 22.
    Simões-Costa M., Bronner M.E. 2015. Establishing neural crest identity: A gene regulatory recipe. Development. 142, 242–257.CrossRefGoogle Scholar
  23. 23.
    Halbleib J.M., Nelson W. J. 2006. Cadherins in development: Cell adhesion, sorting, and tissue morphogenesis. Gen. Dev. 20, 3199–3214.CrossRefGoogle Scholar
  24. 24.
    Kalcheim C. 2015. Epithelial–mesenchymal transitions during neural crest and somite development. J. Clin. Med. 5, pii: E1.  https://doi.org/10.3390/jcm5010001 CrossRefGoogle Scholar
  25. 25.
    Taneyhill L.A., Schiffmacher A.T. 2013. Cadherin dynamics during neural crest cell ontogeny. Prog. Mol. Biol. Transl. Sci. 116, 291–315.CrossRefGoogle Scholar
  26. 26.
    York J.R., Yuan T., Zehnder K., McCauley D.W. 2017. Lamprey neural crest migration is Snail-dependent and occurs without a differential shift in cadherin expression. Dev. Biol. 428, 176–187.CrossRefGoogle Scholar
  27. 27.
    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.  https://doi.org/10.1002/dvg.23028 CrossRefGoogle Scholar
  28. 28.
    Ezin A.M., Fraser S.E., Bronner-Fraser M. 2009. Fate map and morphogenesis of presumptive neural crest and dorsal neural tube. Dev. Biol. 330, 221–236.CrossRefGoogle Scholar
  29. 29.
    Beloussov L.V., Luchinskaia N.N., Stein A.A. 2000. Tension-dependent collective cell movements in the early gastrula ectoderm of Xenopus laevis embryos. Dev. Genes Evol. 210, 92–104.CrossRefGoogle Scholar
  30. 30.
    Evstifeeva A.Yu., Belousov L.V. 2016. Surface microdeformations and regulation of cell movements in Xenopus development. Russ. J. Dev. Biol. 47 (1), 1–10.CrossRefGoogle Scholar
  31. 31.
    Eroshkin F.M., Zaraisky A.G. 2017. Mechano-sensitive regulation of gene expression during the embryonic development. Genesis. 55, e23026.  https://doi.org/10.1002/dvg.23026 CrossRefGoogle Scholar
  32. 32.
    Xiong F., Tentner A.R., Huang P., Gelas A., Mosaliganti K.R., Souhait L., Rannou N., Swinburne I.A., Obholzer N.D., Cowgill P.D., Schier A.F., Megason S.G. 2013. Specified neural progenitors sort to form sharp domains after noisy Shh signaling. Cell. 153, 550–561.CrossRefGoogle Scholar
  33. 33.
    Stuhlmiller T.J., Garcia-Castro M.I. 2012. FGF/MAPK signaling is required in the gastrula epiblast for avian neural crest induction. Development. 139, 289–300.CrossRefGoogle Scholar
  34. 34.
    Buitrago-Delgado E., Nordin K., Rao A., Geary L., LaBonne C. 2015. Shared regulatory programs suggest retention of blastula-stage potential in neural crest cells. Science. 348, 1332–1335.CrossRefGoogle Scholar
  35. 35.
    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.CrossRefGoogle Scholar
  36. 36.
    Liu Y., Labosky P.A. 2008. Regulation of embryonic stem cell self-renewal and pluripotency by Foxd3. Stem Cells. 26, 2475–2484.CrossRefGoogle Scholar
  37. 37.
    Lin Y., Li X. Y., Willis A.L., Liu C., Chen G., Weiss S.J. 2014. Snail1-dependent control of embryonic stem cell pluripotency and lineage commitment. Nat. Commun. 5, 3070. pmid: 24401905 https://doi.org/10.1038/ncomms4070
  38. 38.
    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.CrossRefGoogle Scholar
  39. 39.
    Jeffery W.R., Strickler A.G., Yamamoto Y. 2004. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature. 431, 696–699.CrossRefGoogle Scholar
  40. 40.
    Jeffery W.R., Chiba T., Krajka F.R., Deyts C., Satoh N., Joly J.S. 2008. Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: Insights into the ancestry and evolution of the neural crest. Dev. Biol. 324, 152–160.CrossRefGoogle Scholar
  41. 41.
    Pshennikova E., Voronina A. 2012. Expression of the transcription factor Xvent-2 in Xenopus laevis embryogenesis. Am. J. Mol. Biol. 2, 124–131.CrossRefGoogle Scholar
  42. 42.
    Pshennikova E.S., Voronina A.S. 2016. The proteins of Vent-family and their mRNAs are located in different areas of the tails of zebrafish and Xenopus embryos. Int. J. Biochem. Cell Biol. 79, 388–392.CrossRefGoogle Scholar
  43. 43.
    Gans C., Northcutt R.G. 1983. Neural crest and the origin of vertebrates. A new head. Science. 20, 268–274.CrossRefGoogle Scholar
  44. 44.
    Meulemans D., Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev. Cell. 7, 291–299.CrossRefGoogle Scholar
  45. 45.
    Jeffery W.R. 2006. Ascidian neural crest-like cells: Phylogenetic distribution, relationship to larval complexity, and pigment cell fate. J. Exp. Zool. B: Mol. Dev. 306, 470–480.CrossRefGoogle Scholar
  46. 46.
    Bourlat S.J., Juliusdottir T., Lowe C.J. Freeman R., Aronowicz J., Kirschner M., Lander E.S., Thorndyke M., Nakano H., Kohn A.B., Heyland A., Moroz L.L., Copley R.R., Telford M.J. 2006. Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature. 444, 85–88.CrossRefGoogle Scholar
  47. 47.
    Putnam N., Butts T., Ferrier D.E.K., Furlong R.F., Hellsten U., Kawashima T., Robinson-Rechavi M., Shoguchi E., Terry A., Yu J.K., Benito-Gutiérrez E.L., Dubchak I., Garcia-Fernàndez J., Gibson-Brown J.J., Grigoriev I.V., et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature. 453, 1064–1071.CrossRefGoogle Scholar
  48. 48.
    Yu J.K., Meulemans D., McKeown S.J., Bronner-Fraser M. 2008. Insights from the amphioxus genome on the origin of vertebrate neural crest. Genome Res. 18, 1127–1132.CrossRefGoogle Scholar
  49. 49.
    Yu J.-K. 2010. The evolutionary origin of the vertebrate neural crest and its developmental gene regulatory network: Insights from amphioxus. Zoology (Jena). 113, 1–9.CrossRefGoogle Scholar
  50. 50.
    Holland P.W., Garcia-Fernandez J., Williams N.A., Sidow A. 1994. Gene duplications and the origins of vertebrate development. Dev. Suppl. 125–133.Google Scholar
  51. 51.
    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.CrossRefGoogle Scholar
  52. 52.
    Sauka-Spengler T., Meulemans D., Jones M., Bronner-Fraser M. 2007. Ancient evolutionary origin of the neural crest gene regulatory network. Dev. Cell. 13, 405‒420.CrossRefGoogle Scholar
  53. 53.
    Green S.A., Bronner M.E. 2014. The lamprey: A jawless vertebrate model system for examining origin of the neural crest and other vertebrate traits. Differentiation. 87, 44–51.CrossRefGoogle Scholar
  54. 54.
    Smith J.J. 2015. The sea lamprey meiotic map resolves ancient vertebrate genome duplications. Genome Res. 25, 1081–1090.CrossRefGoogle Scholar
  55. 55.
    Ono H., Kozmik Z., Yu J.-K., Wada H. 2014. A novel N-terminal motif is responsible for the evolution of neural crest-specific gene-regulatory activity in vertebrate FoxD3. Dev. Biol. 385, 396–404.CrossRefGoogle Scholar
  56. 56.
    Kim Y.J., Lim H., Li Z., Oh Y., Kovlyagina I., Choi I.Y., Dong X., Lee G. 2014. Generation of multipotent induced neural crest by direct reprogramming of human postnatal fibroblasts with a single transcription factor. Cell Stem Cell. 15, 497–506.CrossRefGoogle Scholar
  57. 57.
    Bronner M.E., LeDouarin N.M. 2012. Development and evolution of the neural crest: An overview. Dev. Biol. 366, 2–9.CrossRefGoogle Scholar
  58. 58.
    Kim J., Lo L., Dormand E., Anderson D.J. 2003. OX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron. 38, 17–31.CrossRefGoogle Scholar
  59. 59.
    Simoes-Costa M., Bronner M.E. 2013. Insights into neural crest development and evolution from genomic analysis. Genome Res. 23, 1069–1080.CrossRefGoogle Scholar
  60. 60.
    Kirillova A., Genikhovich G., Pukhlyakova E. 2018. Germ-layer commitment and axis formation in sea anemone embryonic cell aggregates. Proc. Natl. Acad. Sci. U. S. A. 115, 1813–1818.CrossRefGoogle Scholar
  61. 61.
    Martindale M.Q., Pang K., Finnerty J.R. 2004. Investigating the origins of triploblasty: ‘Mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development. 131, 2463–2474.CrossRefGoogle Scholar
  62. 62.
    Steinmetz P.R.H., Aman A., Kraus J.E.M., Technau U. 2017. Gut-like ectodermal tissue in a sea anemone challenges germ layer homology. Nat. Ecol. Evol. 1, 1535–1542.CrossRefGoogle Scholar
  63. 63.
    Fritzenwanker J.H., Saina M., Technau U. 2004. Analysis of forkhead and snail expression reveals epithelial–mesenchymal transitions during embryonic and larval development of Nematostella vectensis. Dev. Biol. 275, 389–402.CrossRefGoogle Scholar
  64. 64.
    Busengdal H., Rentzsch F. 2017. Unipotent progenitors contribute to the generation of sensory cell types in the nervous system of the cnidarian Nematostella vectensis. Dev. Biol. 431, 59–68.CrossRefGoogle Scholar
  65. 65.
    Hörstadius S. 1973. Experimental Embryology of Echinoderms. Oxford, England: Clarendon.Google Scholar
  66. 66.
    Le Douarin N.M. 2004. The avian embryo as a model to study the development of the neural crest: A long and still ongoing story. Mech. Dev. 121, 1089–1102.CrossRefGoogle Scholar
  67. 67.
    Le Douarin N.M., Dupin E. 2018. The “beginnings” of the neural crest. Dev. Biol. pii: S0012-1606(17)30882-5.  https://doi.org/10.1016/j.ydbio.2018.07.019
  68. 68.
    Green S.A., Uy B.R., Bronner M.E. 2017. Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest. Nature. 544, 88–91.CrossRefGoogle Scholar
  69. 69.
    Coelho-Aguiar J.M., Le Douarin N.M., Dupin E. 2013. Environmental factors unveil dormant developmental capacities in multipotent progenitors of the trunk neural crest. Dev. Biol. 384, 3–25.CrossRefGoogle Scholar
  70. 70.
    John N., Cinelli P., Wegner M., Sommer L. 2011. Transforming growth factor β-mediated Sox10 suppression controls mesenchymal progenitor generation in neural crest stem cells. Stem Cells. 29, 689–699.CrossRefGoogle Scholar
  71. 71.
    Donoghue P.C.J., Graham A., Kelsh R.N. 2008. The origin and evolution of the neural crest. Bioessays. 30, 530–541.CrossRefGoogle Scholar
  72. 72.
    Dupin E., Coelho-Aguiar J.M. 2013. Isolation and differentiation properties of neural crest stem cells. Cytometry A. 83, 38‒47.CrossRefGoogle Scholar
  73. 73.
    Jinno H., Morozova O., Jones K.L., Biernaskie J.A., Paris M., Hosokawa R., Rudnicki M.A., Chai Y., Rossi F., Marra M.A., Miller F.D. 2010. Convergent genesis of an adult neural crest-like dermal stem cell from distinct developmental origins. Stem Cells. 28, 2027–2040.CrossRefGoogle Scholar
  74. 74.
    Morrison S.J., White P.M., Zock C., Anderson D.J. 1999. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell. 96, 737–749.CrossRefGoogle Scholar
  75. 75.
    Dyachuk V., Furlan A., Shahidi M.K., Giovenco M., Kaukua N., Konstantinidou C., Pachnis V., Memic F., Marklund U., Müller T., Birchmeier C., Fried K., Ernfors P., Adameyko I. 2014. Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science. 345, 82–87.CrossRefGoogle Scholar
  76. 76.
    Espinosa-Medina I., Outin E., Picard C.A., Chettouh Z., Dymecki S., Consalez G.G., Coppola E., Brunet J.F. 2014. Neurodevelopment. Parasympathetic ganglia derive from Schwann cell precursors. Science. 345, 87–90.CrossRefGoogle Scholar
  77. 77.
    Espinosa-Medina I., Jevans B., Boismoreau F. 2017. Dual origin of enteric neurons in vagal Schwann cell precursors and the sympathetic neural crest. Proc. Natl. Acad. Sci. U. S. A. 114, 11980–11985.CrossRefGoogle Scholar
  78. 78.
    Adameyko I., Lallemend F., Aquino J.B., Pereira J.A., Topilko P., Müller T., Fritz N., Beljajeva A., Mochii M., Liste I., Usoskin D., Suter U., Birchmeier C., Ernfors P. 2009. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell. 139, 366–379.CrossRefGoogle Scholar
  79. 79.
    Adameyko I., Lallemend F., Furlan A.Y. 2012. Sox2 and Mitf cross-regulatory interactions consolidate progenitor and melanocyte lineages in the cranial neural crest. Development. 139, 397–410.CrossRefGoogle Scholar
  80. 80.
    Krause M.P., Dworski S., Feinberg K., Jones K., Johnston A.P., Paul S., Paris M., Peles E., Bagli D., Forrest C.R., Kaplan D.R., Miller F.D. 2014. Direct genesis of functional rodent and human Schwann cells from skin mesenchymal precursors. Stem Cell Rep. 3, 85–100.CrossRefGoogle Scholar
  81. 81.
    Butler Tjaden N.E., Trainor P.A. 2013. The developmental etiology and pathogenesis of Hirschsprung disease. Transl. Res. 162, 1–15.CrossRefGoogle Scholar
  82. 82.
    Zhang D., Ighaniyan S., Stathopoulos L., Rollo B., Landman K., Hutson J., Newgreen D. 2014. The neural crest: A versatile organ system. Birth Defects Res. C: Embryo Today. 102, 275–298.CrossRefGoogle Scholar
  83. 83.
    Bolande R.P. 1974. The neurocristopathies: A unifying concept of disease arising in neural crest maldevelopment. Hum. Pathol. 5, 409–429.CrossRefGoogle Scholar
  84. 84.
    Hall B.K. 2009. The Neural Crest and Neural Crest Cells in Vertebrate Development and Evolution, 2nd ed. New York: Springer.CrossRefGoogle Scholar
  85. 85.
    Harris M.L., Fufa T.D., Palmer J.W., Joshi S.S., Larson D.M., Incao A., Gildea D.E., Trivedi N.S., Lee A.N., Day C.P., Michael H.T., Hornyak T.J., Merlino G.; NISC Comparative Sequencing Program, Pavan W.J. 2018. A direct link between MITF, innate immunity, and hair graying. PLoS Biol. 16, e2003648.  https://doi.org/10.1371/journal.pbio.2003648 CrossRefGoogle Scholar
  86. 86.
    Rodrigues M., Ezzedine K., Hamzavi I., Pandya A.G., Harris J.E.; Vitiligo Working Group. 2017. New discoveries in the pathogenesis and classification of vitiligo. J. Am. Acad. Dermatol. 77, 1–13.CrossRefGoogle Scholar

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© Pleiades Publishing, Inc. 2019

Authors and Affiliations

  1. 1.Bach Institute of Biochemistry, Research Center of Biotechnology, Russian Academy of SciencesMoscowRussia

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