Neural crest cells: Evolution, embryonic bases and craniofacial development. Systematic literature review
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The neural crest cells are a population of embryonic stem cells that differentiate from the neuro-ectoderm and whose appearance constitutes an evolutionary innovation allowed vertebrates develop different morpho-functional structures to adapt from asuspensivorous eating style to a predatory style, much more efficient. This systematic literature review describes the essential role of neural crest cells in the evolutionary and embryonic development of the craniofacial structures of the vertebrates.For this purpose we searched PubMed through the Medical Subject Headings (MeSh) “neural crest” combined with the terms “neurulation, evolution, embryonic and fetal development,
craniofacial development” through the Boolean connectors“AND” y “+”.
Key words: Neurulation, neutral plata, neural crest cells, embryonic and fetal development, craniofacial development.
Moreno-Gómez, F. A., & Pachajoa, H. (2017). Neural crest cells: Evolution, embryonic bases and craniofacial development. Systematic literature review. Revista Estomatología, 23(2). https://doi.org/10.25100/re.v23i2.5787
1. Gilbert SF. Biología del desarrollo. Séptima edición. Editorial Médica Panamericana: Buenos Aires; 2006.
2. Sadler TW. Embriología médica de Langman. Décimosegunda edición. WoltersKluwer: Barcelona; 2012.
3. Moore KL, Persaud TVN, Torchia MG. Embriología clínica. Novena edición. Elsevier Saunders: Barcelona; 2013.
4. Rychel AL, Smith SE, Shimamoto HT, Swalla BJ. Evolution and development of the chordates: collagen and pharyngeal cartilage. Mol Biol Evol. 2006; 23(3):541-9.
5. Cameron CB, Garey JR, Swalla BJ. Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. PNAS. 2000; 97(9):4469-74.
6. Gerhart J, Lowe C,Kirschner M. Hemichordates and the origin of chordates. CurrOpin Genet Dev 2005, 15(4):461-7.
7. Winchel CJ, Sullivam J, Cameron CB, Swalla BJ, Mallatt. Evaluating hypotheses of deuterostome phylogeny and Chordate
Evolution with new LSU and SSU ribosomal DNA data. Mol Biol Evol. 2002; 19(5):762-76.
8. Kardong KV. Vertebrates: comparative anatomy, function and evolution. Sixth edition. Mc. Graw Hill: New York; 2012.
9. Forey PL, Janvier P. Agnathans and the origin of jawed vertebrates. Nature. 1993; 361:129-34.
10. Shimeld SM, Holland PWH. Vertebrate innovations. PNAS. 2000; 97(9):4449-52.
11. Durand JF. Major African contributions to Palaeozoic and Mesozoic vertebrate palaeontology. J Afr Earth Sci. 2005; 43:53-82.
12. Smith MM, Hall BK. Developmentand evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev CambPhilosSoc 1990; 65(3):277-373.
13. Donoghue PCJ, Samsom IJ. Origin and early evolution of vertebrate skeletonization. Microsc Res Tech. 2000; 59:352-72.
14. Duque JF. Crestas neurales, placodas y arcos branquiales: una revisión evolutiva y embriológica de datos básicos y recientes. Rev Acad Colomb Cienc. 2003; 27(103): 291-307.
15. Gans C, Northcutt RG. Neural crest and the origin of vertebrates: a new head. Science 1983; 220:268-74.
16. Hall BK. Evolutionary Origins of the Neural Crest and Neural Crest Cells. Evol Biol. 2008; 35:248-66.
17. Trainor PA, Melton KR, Manzanares M. Origins and plasticity of neural crest cells and their roles in jaw and craniofacial evolution. Int J Dev Biol. 2003; 47:541-53.
18. Nanci A. Ten Cate´s oral histology. Eighth edition. Elsevier Mosby. St. Louis; 2013.
19. Green SA, Simoes-Costa M, Bronner ME. Evolution of vertebrates as viewed from the crest. Nature. 2015; 520(7548):47482.
20. Technau U, Scholz CB. Origin and evolution of endoderm and mesoderm.Int J Dev Biol. 2003; 47:531-39.
21. Sauka-Spengler T, Meulemans D, Jones M, Bronner-Fraser M. Ancient Evolutionary Origin of the neural crest gene regulatory network. Dev Cell. 2007; 13:405-20.
22. Lang D, Brown CB, Epstein JA. Neural crest formation and craniofacial development. In: Inborn errors of development: The molecular basis of clinical disorders of morphogenesis. Epstein ChJ, Erikson RP, Wynshaw-Boris A, Editors. Oxford University Press: New York; 2004. p. 67-74.
23. Graveson AC. Contributions to the Development of the Vertebrate Head. Am Zool. 1993; 33(4):424-33.
24. Holland LZ, Holland ND. Evolution of Neural Crest and Placodes: Amphioxus as a Model for the Ancestral Vertebrate?
J Anat. 2001; 199(1-2):85-98. 25. Dupin E, Le Douarin NM. The neural crest, a multifaceted structure of the vertebrates. Birth Defects Res C Embryo Today. 2014; 102(3):187-209.
26. Hunt P, Ferretti P, Krumlauf R, Thorogood. Restoration of normal hox code and branquial arch morphogenesis after extensive deletion of hindbrain neural crest. Dev Biol. 1995; 168:584-97.
27. Meulemans D, Bronner-Fraser M. Generegulatory interactions in neural crest evolution and development. Dev Cell. 2004; 7:291-9.
28. Baker CV, Bronner-Fraser M. The origins of the neural crest. Part I: Embryonic induction. Mech Dev. 1997; 69(1-2):3-11.
29. SantagatiF, Minoux M, Ren S-Y, Rijli FM. Temporal requirement of Hoxa2 in cranial neural crest skeletal Morphogenesis. Development. 2005; 132: 4927-36.
30. Muñoz WA, Trainor PA. Neural crest cell evolution: how and when did a neural crest cell become a neural crest cell. Curr Top Dev Biol. 2015; 111:3-26.
31. Trainor PA, Tan SS, Tam PP. Cranial Paraxial Mesoder: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development. 1994; 120(9):2397-408.
32. McCauley DW, Bronner-Fraser M. Neural crest contributions to the lamprey head. Development. 2003; 130:2317-27.
33. Sauka-Spengler T, Bronner-Fraser M. Development and evolution of the migratory neural crest: a gene regulatory perspective. Curr Opin Genet Dev. 2006;16:360-6.
34. Meulemans D, Bronner-Fraser M. Amphioxus and lamprey AP-2 genes: implications for neural crest evolution and migration patterns. Development. 2002; 129:4953-4962.
35. Kuratani S. Cephalic neural crest cells and the evolution of craniofacial structures in vertebrates: morphological and embryological significance of the premandibular-mandibular boundary. Zoology. 2005; 108:13-25.
36. Sarkar L, Cobourne M, Naylor S, Smalley M, Dale T, Sharpe PT. Wnt/Shh interactions regulate ectodermal boundary formation during mammalian tooth development. PNAS. 2000; 97(9):4520-4.
37. Barembaum M, Bronner-Fraser M. Early steps in neural crest specification.Semin Cell Dev Biol. 2005; 16:642-6.
38. KalcheimCh, Burstyn-Cohen T. Early stages of neural crest ontogeny: formation and regulation of cell delamination. Int J Dev Biol. 2005; 49:105-16.
39. Raible DW, Ragland JW. Reiterated Wnt and BMP signals in neural crest development.Semin Cell Dev Biol. 2005; 16:673-82.
40. Marcucio RS, Cordero DR, Hu D, Helms JA. Molecular interactions coordinating the development of the forebrain and face. DevBiol. 2005; 284:48-61.
41. Lister JA, Cooper C, Nguyen K, Modrell M, Grant K, Raible DW. Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Dev Biol. 2006; 290:92-104.
42. Nie X, Luukko K, Kettunen P. BMP signalling in craniofacial development. Int J Dev Biol. 2006; 50:511-21.
43. Huang X, Saint-Jeannet JP. Induction of the neural crest and the opportunities of life on the edge. DevBiol. 2004; 275: 1-11.
44. Morales AV, Barbas JA, Nieto MA. How to become neural crest: From segregation to delamination. Semin Cell Dev Biol. 2005; 16:655-662.
45. Bhatt S, Diaz R, Trainor PA. Signals and switches in Mammalian neural crest cell differentiation. Cold Spring HarbPerspect Biol. 2013; 5(2):a008326.
46. Jones NC, Trainos PA. Role of Morphogens in Neural Crest Cell Determination. J Neurobiol. 2005; 64(4):388-404.
47. Monsoro-Burq AH. PAX transcription factors in neural crest development. Semin Cell Dev Biol. 2015; S1084- 9521(15):175-5.
48. Nichols DH. Ultrastructure of neural crest formation in the midbrain/rostral hindbrain and preotic hindbrain regions of the mouse embryo. Am J Anat. 1987; 179(2):143- 154.
49. Weston JA. Sequential Segregation and Fate of Developmentally Restricted Intermediate Cell Populations in the
Neural Crest Lineage. Curr Top Dev Biol. 1991; 25:133-153.
50. Wang Ch-Ch. Development of the rhombencephalon:molecular evolution and geneticregulation.NeuroembryolAging. 2004; 3:78-91.
51. Graham A. The Development and Evolution of the Pharyngeal Arches. J Anat. 2001; 199: 133-141.
52. TrainorPA, Krumlauf R. Hox genes, neural crest cells and branchial arch patterning. Curr Top DevBiol. 2001; 13: 698-705.
53. Trokovic N, Trokovic R, Partanen J. Fibroblast growth factor signalling and regional specification of the pharyngeal ectoderm. Int J DevBiol. 2005; 49:797-805.
54. Graham A, Richardson J. Developmental and evolutionary origins of the pharyngeal apparatus. Evodevo. 2012;3(1):24.
55. Neidert AH, Virupannavar V, Hooker GW, Langeland JA. Lamprey Dlxgenes and early vertebrate evolution. PNAS. 2001; 98(4):1665-70.
56. Cobourne MT, Sharpe PT. Tooth and jaw: molecular mechanisms of patterning in the first branchial arch. Arch Oral Biol. 2003; 48:1-14.
57. Lumsden A, Sprawson N, Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the
chick embryo. Development. 1991; 113: 1281-91.
58. Sechrist J, Serbedzija GN, Scherson T, Fraser SE, Bronner-Fraser M. Segmental migration of the hindbrain neural crest does
not arise from its segmental generation. Development. 1993; 118:691-703.
59. Kontges G, Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996; 122:3229-42.
60. Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development. 2002; 129:1061-73.
61. Manzanares M, Wada H, Itasaki N, Trainor PA, Krumlauf R, Holland PW. Conservation and elaboration of Hox gene regulation during evolution of the vertebrate head. Nature. 2000; 408:854-7.
62. Alappati S, Zhang ZY, Chen YP. Msx homeobox gene family and craniofacial development. Cell Res. 2003; 13(6):429-42.
63. Diogo R, Kelly RG, Christiaen L, Levine M, Ziermann JM, Molnar JL, et al. A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature. 2015; 520(7548):466-73.
64. Frisdal A, Trainor PA. Development and evolution of the pharyngeal apparatus. Wiley Interdiscip Rev Dev Biol. 2014;
3(6):403-18.
65. Shigetani Y. Heterotopic shift of epithelialmesenchymal interactions in vertebrate jaw evolution. Science. 2002; 296 (5571):
1316-9.
66. Couly G, Grapin-Botton A, Coltey P, Ruhin B, Le Douarin NM. Determination of the identity of the derivates of the cephalic neural crest: incompatibility between Hox gene expression and lower
jaw development. Development. 1998; 125(17):3445-59.
67. Cobourne MT. Construction for the Modern Head: current concepts in craniofacial development. J Orthod. 2000;27:307-14.
2. Sadler TW. Embriología médica de Langman. Décimosegunda edición. WoltersKluwer: Barcelona; 2012.
3. Moore KL, Persaud TVN, Torchia MG. Embriología clínica. Novena edición. Elsevier Saunders: Barcelona; 2013.
4. Rychel AL, Smith SE, Shimamoto HT, Swalla BJ. Evolution and development of the chordates: collagen and pharyngeal cartilage. Mol Biol Evol. 2006; 23(3):541-9.
5. Cameron CB, Garey JR, Swalla BJ. Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. PNAS. 2000; 97(9):4469-74.
6. Gerhart J, Lowe C,Kirschner M. Hemichordates and the origin of chordates. CurrOpin Genet Dev 2005, 15(4):461-7.
7. Winchel CJ, Sullivam J, Cameron CB, Swalla BJ, Mallatt. Evaluating hypotheses of deuterostome phylogeny and Chordate
Evolution with new LSU and SSU ribosomal DNA data. Mol Biol Evol. 2002; 19(5):762-76.
8. Kardong KV. Vertebrates: comparative anatomy, function and evolution. Sixth edition. Mc. Graw Hill: New York; 2012.
9. Forey PL, Janvier P. Agnathans and the origin of jawed vertebrates. Nature. 1993; 361:129-34.
10. Shimeld SM, Holland PWH. Vertebrate innovations. PNAS. 2000; 97(9):4449-52.
11. Durand JF. Major African contributions to Palaeozoic and Mesozoic vertebrate palaeontology. J Afr Earth Sci. 2005; 43:53-82.
12. Smith MM, Hall BK. Developmentand evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev CambPhilosSoc 1990; 65(3):277-373.
13. Donoghue PCJ, Samsom IJ. Origin and early evolution of vertebrate skeletonization. Microsc Res Tech. 2000; 59:352-72.
14. Duque JF. Crestas neurales, placodas y arcos branquiales: una revisión evolutiva y embriológica de datos básicos y recientes. Rev Acad Colomb Cienc. 2003; 27(103): 291-307.
15. Gans C, Northcutt RG. Neural crest and the origin of vertebrates: a new head. Science 1983; 220:268-74.
16. Hall BK. Evolutionary Origins of the Neural Crest and Neural Crest Cells. Evol Biol. 2008; 35:248-66.
17. Trainor PA, Melton KR, Manzanares M. Origins and plasticity of neural crest cells and their roles in jaw and craniofacial evolution. Int J Dev Biol. 2003; 47:541-53.
18. Nanci A. Ten Cate´s oral histology. Eighth edition. Elsevier Mosby. St. Louis; 2013.
19. Green SA, Simoes-Costa M, Bronner ME. Evolution of vertebrates as viewed from the crest. Nature. 2015; 520(7548):47482.
20. Technau U, Scholz CB. Origin and evolution of endoderm and mesoderm.Int J Dev Biol. 2003; 47:531-39.
21. Sauka-Spengler T, Meulemans D, Jones M, Bronner-Fraser M. Ancient Evolutionary Origin of the neural crest gene regulatory network. Dev Cell. 2007; 13:405-20.
22. Lang D, Brown CB, Epstein JA. Neural crest formation and craniofacial development. In: Inborn errors of development: The molecular basis of clinical disorders of morphogenesis. Epstein ChJ, Erikson RP, Wynshaw-Boris A, Editors. Oxford University Press: New York; 2004. p. 67-74.
23. Graveson AC. Contributions to the Development of the Vertebrate Head. Am Zool. 1993; 33(4):424-33.
24. Holland LZ, Holland ND. Evolution of Neural Crest and Placodes: Amphioxus as a Model for the Ancestral Vertebrate?
J Anat. 2001; 199(1-2):85-98. 25. Dupin E, Le Douarin NM. The neural crest, a multifaceted structure of the vertebrates. Birth Defects Res C Embryo Today. 2014; 102(3):187-209.
26. Hunt P, Ferretti P, Krumlauf R, Thorogood. Restoration of normal hox code and branquial arch morphogenesis after extensive deletion of hindbrain neural crest. Dev Biol. 1995; 168:584-97.
27. Meulemans D, Bronner-Fraser M. Generegulatory interactions in neural crest evolution and development. Dev Cell. 2004; 7:291-9.
28. Baker CV, Bronner-Fraser M. The origins of the neural crest. Part I: Embryonic induction. Mech Dev. 1997; 69(1-2):3-11.
29. SantagatiF, Minoux M, Ren S-Y, Rijli FM. Temporal requirement of Hoxa2 in cranial neural crest skeletal Morphogenesis. Development. 2005; 132: 4927-36.
30. Muñoz WA, Trainor PA. Neural crest cell evolution: how and when did a neural crest cell become a neural crest cell. Curr Top Dev Biol. 2015; 111:3-26.
31. Trainor PA, Tan SS, Tam PP. Cranial Paraxial Mesoder: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development. 1994; 120(9):2397-408.
32. McCauley DW, Bronner-Fraser M. Neural crest contributions to the lamprey head. Development. 2003; 130:2317-27.
33. Sauka-Spengler T, Bronner-Fraser M. Development and evolution of the migratory neural crest: a gene regulatory perspective. Curr Opin Genet Dev. 2006;16:360-6.
34. Meulemans D, Bronner-Fraser M. Amphioxus and lamprey AP-2 genes: implications for neural crest evolution and migration patterns. Development. 2002; 129:4953-4962.
35. Kuratani S. Cephalic neural crest cells and the evolution of craniofacial structures in vertebrates: morphological and embryological significance of the premandibular-mandibular boundary. Zoology. 2005; 108:13-25.
36. Sarkar L, Cobourne M, Naylor S, Smalley M, Dale T, Sharpe PT. Wnt/Shh interactions regulate ectodermal boundary formation during mammalian tooth development. PNAS. 2000; 97(9):4520-4.
37. Barembaum M, Bronner-Fraser M. Early steps in neural crest specification.Semin Cell Dev Biol. 2005; 16:642-6.
38. KalcheimCh, Burstyn-Cohen T. Early stages of neural crest ontogeny: formation and regulation of cell delamination. Int J Dev Biol. 2005; 49:105-16.
39. Raible DW, Ragland JW. Reiterated Wnt and BMP signals in neural crest development.Semin Cell Dev Biol. 2005; 16:673-82.
40. Marcucio RS, Cordero DR, Hu D, Helms JA. Molecular interactions coordinating the development of the forebrain and face. DevBiol. 2005; 284:48-61.
41. Lister JA, Cooper C, Nguyen K, Modrell M, Grant K, Raible DW. Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Dev Biol. 2006; 290:92-104.
42. Nie X, Luukko K, Kettunen P. BMP signalling in craniofacial development. Int J Dev Biol. 2006; 50:511-21.
43. Huang X, Saint-Jeannet JP. Induction of the neural crest and the opportunities of life on the edge. DevBiol. 2004; 275: 1-11.
44. Morales AV, Barbas JA, Nieto MA. How to become neural crest: From segregation to delamination. Semin Cell Dev Biol. 2005; 16:655-662.
45. Bhatt S, Diaz R, Trainor PA. Signals and switches in Mammalian neural crest cell differentiation. Cold Spring HarbPerspect Biol. 2013; 5(2):a008326.
46. Jones NC, Trainos PA. Role of Morphogens in Neural Crest Cell Determination. J Neurobiol. 2005; 64(4):388-404.
47. Monsoro-Burq AH. PAX transcription factors in neural crest development. Semin Cell Dev Biol. 2015; S1084- 9521(15):175-5.
48. Nichols DH. Ultrastructure of neural crest formation in the midbrain/rostral hindbrain and preotic hindbrain regions of the mouse embryo. Am J Anat. 1987; 179(2):143- 154.
49. Weston JA. Sequential Segregation and Fate of Developmentally Restricted Intermediate Cell Populations in the
Neural Crest Lineage. Curr Top Dev Biol. 1991; 25:133-153.
50. Wang Ch-Ch. Development of the rhombencephalon:molecular evolution and geneticregulation.NeuroembryolAging. 2004; 3:78-91.
51. Graham A. The Development and Evolution of the Pharyngeal Arches. J Anat. 2001; 199: 133-141.
52. TrainorPA, Krumlauf R. Hox genes, neural crest cells and branchial arch patterning. Curr Top DevBiol. 2001; 13: 698-705.
53. Trokovic N, Trokovic R, Partanen J. Fibroblast growth factor signalling and regional specification of the pharyngeal ectoderm. Int J DevBiol. 2005; 49:797-805.
54. Graham A, Richardson J. Developmental and evolutionary origins of the pharyngeal apparatus. Evodevo. 2012;3(1):24.
55. Neidert AH, Virupannavar V, Hooker GW, Langeland JA. Lamprey Dlxgenes and early vertebrate evolution. PNAS. 2001; 98(4):1665-70.
56. Cobourne MT, Sharpe PT. Tooth and jaw: molecular mechanisms of patterning in the first branchial arch. Arch Oral Biol. 2003; 48:1-14.
57. Lumsden A, Sprawson N, Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the
chick embryo. Development. 1991; 113: 1281-91.
58. Sechrist J, Serbedzija GN, Scherson T, Fraser SE, Bronner-Fraser M. Segmental migration of the hindbrain neural crest does
not arise from its segmental generation. Development. 1993; 118:691-703.
59. Kontges G, Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996; 122:3229-42.
60. Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development. 2002; 129:1061-73.
61. Manzanares M, Wada H, Itasaki N, Trainor PA, Krumlauf R, Holland PW. Conservation and elaboration of Hox gene regulation during evolution of the vertebrate head. Nature. 2000; 408:854-7.
62. Alappati S, Zhang ZY, Chen YP. Msx homeobox gene family and craniofacial development. Cell Res. 2003; 13(6):429-42.
63. Diogo R, Kelly RG, Christiaen L, Levine M, Ziermann JM, Molnar JL, et al. A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature. 2015; 520(7548):466-73.
64. Frisdal A, Trainor PA. Development and evolution of the pharyngeal apparatus. Wiley Interdiscip Rev Dev Biol. 2014;
3(6):403-18.
65. Shigetani Y. Heterotopic shift of epithelialmesenchymal interactions in vertebrate jaw evolution. Science. 2002; 296 (5571):
1316-9.
66. Couly G, Grapin-Botton A, Coltey P, Ruhin B, Le Douarin NM. Determination of the identity of the derivates of the cephalic neural crest: incompatibility between Hox gene expression and lower
jaw development. Development. 1998; 125(17):3445-59.
67. Cobourne MT. Construction for the Modern Head: current concepts in craniofacial development. J Orthod. 2000;27:307-14.
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