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Cranial Neural Crest and Development of the Head Skeleton

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Neural Crest Induction and Differentiation

Part of the book series: Advances in Experimental Medicine and Biology ((volume 589))

Abstract

The skeletal derivatives of the cranial neural crest (CNC) are patterned through a combination of intrinsic differences between crest cells and extrinsic signals from adjacent tissues, including endoderm and ectoderm. In this chapter, we focus on how CNC cells positionally interpret these cues to generate such highly specialized structures as the jaw and ear ossicles. We highlight recent genetic studies of craniofacial development in zebrafish that have revealed new tissue interactions and show that the process of CNC development is highly conserved across the vertebrates.

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References

  1. Northcutt RG, Gans C. The genesis of neural crest and epidermal placodes: A reinterpretation of vertebrate origins. Q Rev Biol 1983; 58:1–28.

    Article  PubMed  CAS  Google Scholar 

  2. deBeer GR. The development of the vertebrate skull. Oxford: Oxford University Press, 1937.

    Google Scholar 

  3. Goodrich ES. Studies on the structure and development of vertebrates. New York: Dover Publications, 1958.

    Google Scholar 

  4. Platt JB. Ectodermic origin of the cartilages of the head. Anat Anz 1893; 8:506–509.

    Google Scholar 

  5. Landacre FL. The fate of the neural crest in the head of the Urodeles. J Comp Neurol 1921; 33:1–43.

    Article  Google Scholar 

  6. Stone LS. Experiments showing the role of migrating neural crest (mesectoderm) in the formation of head skeleton and loose connective tissue. Roux Arch 1929; 118:40–77.

    Article  Google Scholar 

  7. Weston JA, Yoshida H, Robinson V et al. Neural crest and the origin of ectomesenchyme: Neural fold heterogeneity suggests an alternative hypothesis. Dev Dyn 2004; 229:118–30.

    Article  PubMed  Google Scholar 

  8. Johnson MC. A radioautographic study of the migration and fate of cranial neural crest cells in the chick embryo. Anat Rec 1966; 156:143–156.

    Article  Google Scholar 

  9. LeLievre C, LeDouarin NM. Mesenchymal derivatives of the neural crest: Analysis of chimeric quail and chick embryos. J Embryol Exp Morph 1975; 32:445–459.

    Google Scholar 

  10. Couly GF, Coltey PM, Le Douarin NM. The triple origin of the skull in higher vertebrates: A study in quail-chick chimeras. Development 1993; 117:409–29.

    PubMed  CAS  Google Scholar 

  11. Chibon P. Marquage nudeaire par la thymidine tritee des derives de la crete neurale chez l’amphibien urodele Pleurodeles waltii. J Embryol Exp Morph 1967; 18:343–358.

    PubMed  CAS  Google Scholar 

  12. Schilling TF, Kimmel CB. Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 1994; 120:483–94.

    PubMed  CAS  Google Scholar 

  13. Hall BK. Tissue interactions and the initiation of osteogenesis and chondrogenesis in the neural crest-derived mandibular skeleton of the embryonic mouse as seen in isolated murine tissues and in recombinations of murine and avian tissues. J Embryol Exp Morph 1980; 58:251–264.

    PubMed  CAS  Google Scholar 

  14. Cerny R, Lwigale P, Ericsson R et al. Developmental origins and evolution of jaws: New interpretation of “maxillary” and “mandibular”. Dev Biol 2004; 276:225–36.

    Article  PubMed  CAS  Google Scholar 

  15. Lee SH, Bedard O, Buchtova M et al. A new origin for the maxillary jaw. Dev Biol 2004; 276:207–24.

    Article  PubMed  CAS  Google Scholar 

  16. Santagati F, Rijli FM. Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci 2003; 4:806–18.

    Article  PubMed  CAS  Google Scholar 

  17. Rijli FM, Mark M, Lakkaraju S et al. A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 1993; 75:1333–49.

    Article  PubMed  CAS  Google Scholar 

  18. Gendron-Maguire M, Mallo M, Zhang M et al. Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 1993; 75:1317–31.

    Article  PubMed  CAS  Google Scholar 

  19. Noden DM. The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 1983; 96:144–65.

    Article  PubMed  CAS  Google Scholar 

  20. Pasqualetti M, Ori M, Nardi I et al. Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus. Development 2000; 127:5367–78.

    PubMed  CAS  Google Scholar 

  21. Hunter MP, Prince VE. Zebrafish hox paralogue group 2 genes function redundantly as selector genes to pattern the second pharyngeal arch. Dev Biol 2002; 247:367–89.

    Article  PubMed  CAS  Google Scholar 

  22. Schilling TF, Prince V, Ingham PW. Plasticity in zebrafish hox expression in the hindbrain and cranial neural crest. Dev Biol 2001; 231:201–16.

    Article  PubMed  CAS  Google Scholar 

  23. Trainor P, Krumlauf R. Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nat Cell Biol 2000; 2:96–102.

    Article  PubMed  CAS  Google Scholar 

  24. Miller CT, Maves L, Kimmel CB. moz regulates Hox expression and pharyngeal segmental identity in zebrafish. Development 2004; 131:2443–61.

    Article  PubMed  CAS  Google Scholar 

  25. Knight RD, Nair S, Nelson SS et al. lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development 2003; 130:5755–68.

    Article  PubMed  CAS  Google Scholar 

  26. Maconochie M, Krishnamurthy R, Nonchev S et al. Regulation of Hoxa2 in cranial neural crest cells involves members of the AP-2 family. Development 1999; 126:1483–94.

    PubMed  CAS  Google Scholar 

  27. Knight RD, Javidan Y, Nelson S et al. Skeletal and pigment cell defects in the lockjaw mutant reveal multiple roles for zebrafish tfap2a in neural crest development. Dev Dyn 2004; 229:87–98.

    Article  PubMed  CAS  Google Scholar 

  28. Trainor PA, Ariza-McNaughton L, Krumlauf R. Role of the isthmus and FGFs in resolving the paradox of neural crest plasticity and prepatterning. Science 2002; 295:1288–1291.

    Article  PubMed  CAS  Google Scholar 

  29. Schneider RA, Helms JA. The cellular and molecular origins of beak morphology. Science 2003; 299:565–568.

    Article  PubMed  CAS  Google Scholar 

  30. Tucker AS, Lumsden A. Neural crest cells provide species-specific patterning information in the developing branchial skeleton. Evol Dev 2004; 6:32–40.

    Article  PubMed  Google Scholar 

  31. Holder N. Organization of connective tissue patterns by dermal fibroblasts in the regenerating axolotl limb. Development 1989; 105:585–593.

    PubMed  CAS  Google Scholar 

  32. Kontges G, Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 1996; 122:3229–3242.

    PubMed  CAS  Google Scholar 

  33. Schilling TF, Walker C, Kimmel CB. The chinless mutation and neural crest cell interactions in zebrafish jaw development. Development 1996; 122:1417–1426.

    PubMed  CAS  Google Scholar 

  34. Wall NA, Hogan BL. Expression of bone morphogenetic protein-4 (BMP-4), bone morphogenetic protein-7 (BMP-7), fibroblast growth factor-8 (FGF-8) and sonic hedgehog (SHH) during branchial arch development in the chick. Mech Dev 1995; 53:383–392.

    Article  PubMed  CAS  Google Scholar 

  35. Clouthier DE, Schilling TF. Understanding endothelin-1 function during craniofacial development in the mouse and zebrafish. Birth Defects Res 2004; 72:190–199.

    Article  CAS  Google Scholar 

  36. Wada N, Javidan Y, Nelson S et al. Hedgehog signaling is required for cranial neural crest morphogenesis and chondrogenesis at the midline in the zebrafish skull. Development 2005; in press.

    Google Scholar 

  37. Tumarkin A. On the evolution of the auditory conducting apparatus: A new theory based on functional considerations. Evolution 1955; 9:221–243.

    Article  Google Scholar 

  38. Kurihara Y, Kurihara H, Suzuki H et al. Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin-1. Nature 1994; 368:703–710.

    Article  PubMed  CAS  Google Scholar 

  39. Clouthier DE, Hosoda K, Richardson JA et al. Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development 1998; 125:813–824.

    PubMed  CAS  Google Scholar 

  40. Miller CT, Schilling TF, Lee K et al. Sucker encodes a zebrafish Endothelin-1 required for ventral pharyngeal arch development. Development 2000; 127:3815–3828.

    PubMed  CAS  Google Scholar 

  41. Clouthier DE, Williams SC, Hammer RE et al. Cell-autonomous and nonautonomous actions of endothelin-A receptor signaling in craniofacial and cardiovascular development. Dev Biol 2003; 261:506–519.

    Article  PubMed  CAS  Google Scholar 

  42. Kimmel CB, Ullmann B, Walker M et al. Endothelin 1-mediated regulation of pharyngeal bone development in zebrafish. Development 2003; 130:1339–1351.

    Article  PubMed  CAS  Google Scholar 

  43. Ozeki H, Kurihara Y, Tonami K et al. Endothelin-1 regulates the dorsoventral branchial arch patterning in mice. Mech Dev 2004; 121:387–395.

    Article  PubMed  CAS  Google Scholar 

  44. Depew MJ, Lufkin T, Rubenstein JL. Specification of jaw subdivisions by Dlx genes. Science 2002; 298:381–385.

    Article  PubMed  CAS  Google Scholar 

  45. Beverdam A, Merlo GR, Paleari L et al. Jaw transformation with gain of symmetry after Dlx 5/Dlx6 inactivation: Mirror of the past? Genesis 2002; 34:221–227.

    Article  PubMed  CAS  Google Scholar 

  46. Charite J, McFadden DG, Merlo G et al. Role of Dlx6 in regulation of an endothelin-1-dependent, dHAND branchial arch enhancer. Genes Dev 2001; 15:30309–3049.

    Article  Google Scholar 

  47. Yanagisawa H, Clouthier DE, Richardson JA et al. Targeted deletion of a branchial arch-specific enhancer reveals a role of dHAND in craniofacial development. Development 2003; 130:1069–1078.

    Article  PubMed  CAS  Google Scholar 

  48. Hall BK. Tissue interactions and the initiation of osteogenesis and chondrogenesis in the neural crest-derived mandibular skeleton of the embryonic mouse as seen in isolated tissues and in recombinations of murine and avian tissues. J Embryol Exp Morphol 1980; 58:251–264.

    PubMed  CAS  Google Scholar 

  49. Horstadius S, Sellman S. Experimentelle unterschungen uber die Determination des Knorpeligen Kopfskelettes bei Urodelen. Nova Acta R Soc Scient Upsal Ser 1946; 4(13):1–70.

    Google Scholar 

  50. David NB, Saint-Etienne L, Tsang M et al. Requirement for endoderm and FGF3 in ventral head skeleton formation. Development 2002; 129:4457–4468.

    PubMed  CAS  Google Scholar 

  51. Piotrowski T, Nusslein-Volhard C. The endoderm plays an important role in patterning the segmented pharyngeal skeleton in zebrafish (Danio rerio). Dev Biol 2000; 225:339–356.

    Article  PubMed  CAS  Google Scholar 

  52. Piotrowski T, Ahn D-G, Schilling TF et al. The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 2003; 130:5043–5052.

    Article  PubMed  CAS  Google Scholar 

  53. Veitch E, Begbie J, Schilling TF et al. Pharyngeal arch patterning in the absence of neural crest. Curr Biol 1999; 9:1481–1484.

    Article  PubMed  CAS  Google Scholar 

  54. Herzog W, Sonntag C, von der Hardt S et al. Fgf3 signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis. Development 2004; 131:3681–3692.

    Article  PubMed  CAS  Google Scholar 

  55. Walshe J, Mason I. Fgf signaling is required for formation of cartilage in the head. Dev Biol 2003; 264:522–536.

    Article  PubMed  CAS  Google Scholar 

  56. Crump JG, Maves L, Lawson ND et al. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 2004; 131:5703–5716.

    Article  PubMed  CAS  Google Scholar 

  57. Trumpp A, Depew MJ, Rubenstein JL et al. Cremediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev 1999; 13:3136–3148.

    Article  PubMed  CAS  Google Scholar 

  58. Crump JG, Swartz ME, Kimmel CB. An integrin-dependent role of pouch endoderm in hyoid cartilage development. PloS Biol 2004; 2:E244.

    Article  PubMed  Google Scholar 

  59. Couly G, Creuzet S, Bennaceur S et al. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 2002; 129:1061–1073.

    PubMed  CAS  Google Scholar 

  60. Hall BK. The induction of neural crest-derived cartilage and bone by embryonic epithelia: An analysis of the mode of action of an epithelial-mesenchymal interaction. J Embryol Exp Morphol 1981; 64:305–320.

    PubMed  CAS  Google Scholar 

  61. Macatee TL, Hammond BP, Arenkiel BR et al. Ablation of specific expression domains reveals discrete functions of ectoderm-and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 2003; 130:6361–6374.

    Article  PubMed  CAS  Google Scholar 

  62. Frank DU, Fotheringham LK, Brewer JA et al. An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development 2002; 129:4591–4603.

    PubMed  CAS  Google Scholar 

  63. Roehl HH, Nusslein-Volhard C. Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr Biol 2001; 11:503–507.

    Article  PubMed  CAS  Google Scholar 

  64. Schorle H, Meier P, Buchert M et al. Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 1996; 381:235–238.

    Article  PubMed  CAS  Google Scholar 

  65. Zhang J, Hagopian-Donaldson S, Serbedzija G et al. Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 1996; 381:238–241.

    Article  PubMed  CAS  Google Scholar 

  66. Holzschuh J, Barrallo-Gimeno A, Ettl AK et al. Noradrenergic neurons in the zebrafish hindbrain are induced by retinoic acid and require tfap2a for expression of the neurotransmitter phenotype. Development 2004; 130:5741–5754.

    Article  Google Scholar 

  67. Barrallo-Gimeno A, Holtzschuh J, Driever W et al. Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 2004; 131:1463–1477.

    Article  PubMed  CAS  Google Scholar 

  68. Knight RD, Javidan Y, Zhang T et al. AP2-dependent signals from the ectoderm regulate craniofacial development in the zebrafish embryo. Development 2005; 132(13):3127–3138.

    Article  PubMed  CAS  Google Scholar 

  69. Bachler M, Neubuser A. Expression of members of the Fgf family and their receptors during midfacial development. Mech Dev 2001; 100:313–316.

    Article  PubMed  CAS  Google Scholar 

  70. Cobourne MT, Sharpe PT. Tooth and jaw: Molecular mechanisms of patterning in the first branchial arch. Arch Oral Biol 2003; 48:1–14.

    Article  PubMed  CAS  Google Scholar 

  71. Hu D, Helms JA. The role of sonic hedgehog in normal and abnorml craniofacial morphogenesis. Development 1999; 126:4873–4884.

    PubMed  CAS  Google Scholar 

  72. Abzhanov A, Tabin CJ. Shh and Fgf8 act synergistically to drive cartilage outgrowth during cranial development. Dev Biol 2004; 273:134–148.

    Article  PubMed  CAS  Google Scholar 

  73. Haworth KE, Healy C, Morgan P et al. Regionalisation of early head ectoderm is regulated by endoderm and prepatterns the orofacial epithelium. Development 2004; 131:4797–4806.

    Article  PubMed  CAS  Google Scholar 

  74. Shigetani Y, Nobusada Y, Kuratani S. Ectodermally-derived FGF8 defines the maxillomandibular region in the early chick embryo: Epithelial-mesenchymal interactions in the specification of the craniofacial ectomesenchyme. Dev Biol 2000; 228:73–85.

    Article  PubMed  CAS  Google Scholar 

  75. Tucker AS, Al Khamis A, Sharpe PT. Interactions between Bmp-4 and Msx-1 act to restrict gene expression to odontogenic mesenchyme. Dev Dyn 1998; 212:533–539.

    Article  PubMed  CAS  Google Scholar 

  76. Ferguson CA, Tucker AS, Sharpe PT. Temporospatial cell interactions regulating mandibular and maxillary arch patterning. Development 2000; 127:403–412.

    PubMed  CAS  Google Scholar 

  77. Barlow AJ, Bogardi JP, Ladher R et al. Expression of Barx-1 and its differential regulation by FGF-8 and BMP signaling in the maxillary primordia. Dev Dyn 1999; 214:291–302.

    Article  PubMed  CAS  Google Scholar 

  78. Neubüser A, Peters H, Balling R et al. Antagonistic interactions between FGF and BMP signaling pathways: A mechanism for positioning the sites of tooth formation. Cell 1997; 90:247–255.

    Article  PubMed  Google Scholar 

  79. Tucker AS, Matthews K, Sharpe PT. Transformation of tooth type induced by inhibition of BMP signaling. Science 1998; 282:1136–1138.

    Article  PubMed  CAS  Google Scholar 

  80. Schilling TF. Evolution and development: Making jaws. Heredity 2003; 90:3–5.

    Article  PubMed  CAS  Google Scholar 

  81. Kuratani S. Craniofacial development and the evolution of the vertebrates: Old problems on a new background. Zoolog Sci 2005; 22:1–19.

    Article  PubMed  Google Scholar 

  82. Myojin M, Ueki T, Sugahara F et al. Isolation of Dlx and Emx cognates in an agnathan species, Lampetra japonica, and their expression patterns during embryonic and larval development: Conserved and diversified regulatory patterns of homeobox genes in vertebrate head evolution. J Exp Zool 2001; 291:68–84.

    Article  PubMed  CAS  Google Scholar 

  83. Neidert AH, Virupannavar V, Hooker GW et al. Lamprey Dlx genes and early vertebrate evolution. Proc Natl Acad Sci USA 2001; 98:1665–1670.

    Article  PubMed  CAS  Google Scholar 

  84. Grammatopoulos GA, Bell E, Toole L et al. Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development 2000; 127:5355–5366.

    PubMed  CAS  Google Scholar 

  85. Pasqualetti M, Ori M, Nardi I et al. Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus. Development 2000; 127:5367–5378.

    PubMed  CAS  Google Scholar 

  86. Cohn MJ. Evolutionary biology: Lamprey Hox genes and the origin of jaws. Nature 2002; 416:386–387.

    Article  PubMed  CAS  Google Scholar 

  87. Takio Y, Pasqualetti M, Kuraku S et al. Evolutionary biology: Lamprey Hox genes and the evolution of jaws. Nature 2004; 429:6989.

    Article  Google Scholar 

  88. Shigetani Y, Sugahara F, Kawakami Y et al. Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science 2002; 296:1316–1319.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Developmental and Cell Biology, University of California, Irvine, 5210 McGaugh Hall, Irvine, California, 92697, USA

    Thomas F. Schilling

  2. Centre for Developmental and Biomedical Genetics Department of Biomedical Sciences, University of Sheffield, Sheffield, South Yorkshire, UK

    Robert D. Knight

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  1. Robert D. Knight
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  2. Thomas F. Schilling
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Correspondence to Thomas F. Schilling .

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Editors and Affiliations

  1. Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Jean-Pierre Saint-Jeannet Ph.D.

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Knight, R.D., Schilling, T.F. (2006). Cranial Neural Crest and Development of the Head Skeleton. In: Saint-Jeannet, JP. (eds) Neural Crest Induction and Differentiation. Advances in Experimental Medicine and Biology, vol 589. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-46954-6_7

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