Research Article

You have full text access to this OnlineOpen article

Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells

  1. Darrell J.R. Evans1,
  2. Drew M. Noden2,*

Article first published online: 4 JAN 2006

DOI: 10.1002/dvdy.20663

Issue

Developmental Dynamics

Developmental Dynamics

Special Issue: Craniofacial Development Special Issue

Volume 235, Issue 5, pages 1310–1325, May 2006

Additional Information

How to Cite

Evans, D. J.R. and Noden, D. M. (2006), Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev. Dyn., 235: 1310–1325. doi: 10.1002/dvdy.20663

Author Information

  1. 1

    Brighton and Sussex Medical School, University of Sussex, Falmer, Brighton, United Kingdom

  2. 2

    Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

*Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853-6401

Publication History

  1. Issue published online: 19 APR 2006
  2. Article first published online: 4 JAN 2006
  3. Manuscript Accepted: 11 NOV 2005

Funded by

  • Wellcome Trust
  • NIDCR. Grant Numbers: DE06632, DE014597, EY015917
  • NEI

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (1902K)

REFERENCES

  • Anakwe K, Robson L, Hadley J, Buxton P, Church V, Allen S, Hartmann C, Harfe B, Nohno T, Brown AM, Evans DJ, Francis-West P. 2003. Wnt signalling regulates myogenic differentiation in the developing avian wing. Development 130: 3503–3514.
  • Boot MJ, Gittenberger-de Groot AC, van Iperen L, Poelmann RE. 2003. The myth of ventrally emigrating neural tube VENT cells and their contribution to the developing cardiovascular system. Anat Embryol (Berl) 206: 327–333.
  • Borue X, Noden DM. 2004. Normal and aberrant craniofacial myogenesis by grafted trunk somitic and segmental plate mesoderm. Development 131: 3967–3980.
  • Burke AC, Nowicki JL. 2003. A new view of patterning domains in the vertebrate mesoderm. Dev Cell 4: 159–165.
  • Carvajal JJ, Cox D, Summerbell D, Rigby PW. 2001. A BAC transgenic analysis of the Mrf4/Myf5 locus reveals interdigitated elements that control activation and maintenance of gene expression during muscle development. Development 128: 1859–1868.
  • Cerny R, Meulemans D, Berger J, Wilsch-Brauninger M, Kurth T, Bronner-Fraser M, Epperlein HH. 2004a. Combined intrinsic and extrinsic influences pattern cranial neural crest migration and pharyngeal arch morphogenesis in axolotl. Dev Biol 266: 252–269.
  • Cerny R, Lwigale P, Ericsson R, Meulemans D, Epperlein HH, Bronner-Fraser M. 2004b. Developmental origins and evolution of jaws: new interpretation of “maxillary” and “mandibular”. Dev Biol 276: 225–236.
  • Cochard P, Coltey P. 1983. Cholinergic traits in the neural crest: acetylcholinesterase in crest cells of the chick embryo. Dev Biol 98: 221–238.
  • Couly GF, Colte PM, Le Douarin NM. 1992. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114: 1–15.
  • Couly GF, Coltey PM, Le Douarin NM. 1993. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117: 409–429.
  • Couly GF, Coltey PM, Eichmann A, Le Douarin NM. 1995. The angiogenic potentials of the cephalic mesoderm and the origin of brain and head blood vessels. Mech Dev 53: 97–112.
  • Couly G, Creuzet S, Bennaceur S, Vincent C, Le Douarin NM. 2002. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129: 1061–1073.
  • Duprez D. 2002. Signals regulating muscle formation in the limb during embryonic development. Int J Dev Biol 46: 915–925.
  • Duprez D, Lapointe F, Edom-Vovard F, Kostakopoulou K, Robson L. 1999. Sonic hedgehog (SHH) specifies muscle pattern at tissue and cellular chick level, in the chick limb bud. Mech Dev 82: 151–163.
  • Eames BF, Helms JA. 2004. Conserved molecular program regulating cranial and appendicular skeletogenesis. Dev Dyn 231: 4–13.
    Direct Link:
  • Erdmann K. 1940. Zur entwicklunsgeschichte der knochen im schädel des huhnes bis zum zeitpunktdes ausschlüpfen aus dem ei. Zeit Morphol Okol Tiere Berlin 36: 315–400.
  • Evans DJR. 2003. Origins and re-segmentation of the thoracic ribs. Dev Biol 256: 115–127.
  • Feinberg RN, Noden DM. 1991. Experimental analysis of blood vessel development in the avian wing bud. Anat Rec 231: 136–144.
    Direct Link:
  • Francis-West PH, Robson L, Evans DJR. 2003. Craniofacial development: the tissue and molecular interactions that control development of the head. Adv Anat Embryol Cell Biol 169: 1–138.
  • Gage PJ, Rhoades W, Prucka SK, Hjalt T. 2005. Fate maps of neural crest and mesoderm in the mammalian eye. Invest Ophthalmol Vis Sci 46: 4200–4208.
  • Gans C, Northcutt RG. 1983. Neural crest and the origin of vertebrates: a new head. Science 220: 268–274.
  • Gasser RF. 1967. Development of the facial muscles in man. Am J Anat 120: 357–376.
    Direct Link:
  • Graham A, Begbie J, McGonnell I. 2004. Significance of the cranial neural crest. Dev Dyn 229: 5–13.
    Direct Link:
  • Gross JB, Hanken J. 2005. Cranial neural crest contributes to the bony skull vault in adult Xenopus laevis: insights from cell labeling studies. J Exp Zool B Mol Dev Evol 304: 169–176.
    Direct Link:
  • Hacker A, Guthrie S. 1998. A distinct developmental programme for the cranial paraxial mesoderm in the chick embryo. Development 125: 3461–3472.
  • Hall BK. 1999. The neural crest in development and evolution. New York: Springer-Verlag.
  • Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88: 49–92.
    Direct Link:
  • Helms JA, Schneider RA. 2003. Cranial skeletal biology. Nature 423: 326–331.
  • Hörstadius S, Sellman S. 1946. Experimentelle Untersuchungen uber die Determination des knorpeligen Kopfskelettes bei Urodelen. Nov Act Reg Soc Scient Ups Ser 13: 1–170.
  • Huang R, Zhi Q, Ordahl CP, Christ B. 1997. The fate of the first avian somite. Anat Embryol (Berl) 195: 435–449.
  • Huang R, Zhi Q, Ispisua-Belmonte J-C, Christ B, Patel K. 1999. Origin and development of the avian tongue muscles. Anat Embryol (Berl) 200: 137–152.
  • Huang R, Zhi Q, Patel K, Wilting J, Christ B. 2000. Contribution of single somites to the skeleton and muscles of the occipital and cervical regions in avian embryos. Anat Embryol (Berl) 202: 375–383.
  • Jaskoll T, Melnick M, MacDougall M, Brownell AG, Slavkin HC. 1981. Spatiotemporal patterns of fibronectin distribution during embryonic development. II. Chick branchial arches. J Craniofac Genet Dev Biol 1: 203–212.
  • Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. 2002. Tissue origins and interactions in the mammalian skull vault. Dev Biol 241: 106–116.
  • Kasperk C, Wergedal J, Strong D, Farley J, Wangerin K, Gropp H, Ziegler R, Baylink DJ. 1995. Human bone cell phenotypes differ depending on their skeletal site of origin. J Clin Endocrinol Metab 80: 2511–2517.
  • Kardon G. 1998. Muscle and tendon morphogenesis in the avian hind limb. Development 125: 4019–4032.
  • Kardon G, Campbell JK, Tabin CJ. 2002. Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev Cell 3: 533–545.
  • Kardon G, Harfe BD, Tabin CJ. 2003. A Tcf4-positive mesodermal population provides a prepattern for vertebrate limb muscle patterning. Dev Cell 5: 937–944.
  • Kimmel CB, Miller CT, Keynes RJ. 2001. Neural crest patterning and the evolution of the jaw. J Anat 199: 105–120.
    Direct Link:
  • Köntges G, Lumsden A. 1996. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122: 3229–3242.
  • Kuratani S. 2003. Evolutionary developmental biology and vertebrate head segmentation: a perspective from developmental constraint. Theor Biosci 122: 230–251.
  • Kuratani S. 2004. Evolution of the verterbrate jaw: comparative embryology and molecular developmental biology reveal the factors behind evolutionary novelty. J Anat 205: 335–347.
    Direct Link:
  • Kuratani S. 2005. Craniofacial development and the evolution of the vertebrates: the old problems on a new background. Zool Sci 22: 1–19.
  • Lance-Jones C. 1979. The morphogenesis of the thigh of the mouse with special reference to tetrapos muscle homologies. J Morphol 162: 275–309.
    Direct Link:
  • Le Douarin NM. 1973. A Feulgen-positive nucleolus. Exp Cell Res 77: 459–468.
  • Le Douarin NM, Kalcheim C. 1999. Neural crest. 2nd ed. Cambridge: Cambridge University Press.
  • Le Douarin NM, Ziller C, Couly GF. 1993. Patterning of neural crest derivatives in the avian embryo: in vivo and in vitro studies. Dev Biol 159: 24–49.
  • LeLiévre C. 1978. Participation of neural crest-derived cells in the genesis of the skull in birds. J Embryol Exp Morphol 47: 17–37.
  • LeLiévre CS, Le Douarin NM. 1975. Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morphol 34: 125–154.
  • Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP, Koentges G. 2005. Neural crest origins of the neck and shoulder. Nature 436: 347–355.
  • McClearn D, Noden DM. 1988. Ontogeny of architectural complexity in embryonic quail visceral arch muscles. Am J Anat 183: 277–293.
    Direct Link:
  • Meier S. 1979. Development of the chick embryo mesoblast. Formation of the embryonic axis and establishment of the metameric pattern. Dev Biol 73: 24–45.
  • Mikawa T, Gourdie RG. 1996. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol 174: 221–232.
  • Mikawa T, Fischman DA, Dougherty JP, Brown AMC. 1991. In vivo analysis of a new lacZ retrovirus vector suitable for cell lineage marking in avian and other species. Exp Cell Res 195: 516–523.
  • Mikawa T, Borisov A, Brown AMC, Fischman D. 1992. Clonal analysis of cardiac morphogenesis in the chicken embryo using a replication-defective retrovirus: I. Formation of the ventricular myocardium. Dev Dyn 193: 11–23.
  • Mootoosamy RC, Dietrich S. 2002. Distinct regulatory cascades for head and trunk myogenesis. Development 129: 573–583.
  • Morriss-Kay GM. 2001. Derivation of the mammalian skull vault. J Anat 199: 143–151.
  • Noden DM. 1975. An analysis of migratory behavior of avian cephalic neural crest cells. Dev Biol 42: 106–130.
  • Noden DM. 1978. The control of avian cephalic neural crest cytodifferentiation. I. Skeletal and connective tissues. Dev Biol 67: 296–312.
  • Noden DM. 1983a. The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96: 144–165.
  • Noden DM. 1983b. The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat 168: 257–276.
    Direct Link:
  • Noden DM. 1984. The use of chimeras in analyses of craniofacial development. In: Le DouarinNM, McLarenD, editors. Chimeras in developmental biology. London: Academic Press. p 241–280.
  • Noden DM. 1986. Patterning of avian craniofacial muscles. Dev Biol 116: 347–356.
  • Noden DM. 1988. Interactions and fates of avian craniofacial mesenchyme. Development 103: 121–140.
  • Noden DM. 1990. Origins and assembly of avian embryonic blood vessels. Ann N Y Acad Sci 588: 236–249.
    Direct Link:
  • Noden DM. 1991a. Origins and patterning of avian outflow tract endocardium. Development 111: 867–876.
  • Noden DM. 1991b. Vertebrate craniofacial development: the relation between ontogenetic process and morphological outcome. Brain Behav Evol 38: 190–225.
  • Noden DM. 1991c. The development of craniofacial blood vessels. In: FeinbergRN, ShererG, AuerbachR, editors. Development of the vascular system. Basel: Karger. p 1–24.
  • Noden DM, Trainor PA. 2005. Relations and interactions between cranial mesoderm and neural crest populations. J Anat (in press).
    Direct Link:
  • Noden DM, Francis-West P. 2006. The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235.
    Direct Link:
  • Noden DM, Marcucio R, Borycki A, Emerson CP Jr. 1999. Differentiation of avian craniofacial muscles: I. Patterns of early regulatory gene expression and myosin heavy chain synthesis. Dev Dyn 216: 96–112.
    Direct Link:
  • Northcutt RG. 2005. The new head hypothesis revisited. J Exp Zool 304: 274–297.
    Direct Link:
  • O'Gorman S. 2005. Second branchial arch lineages of the middle ear of wild-type and Hoxa2 mutant mice. Dev Dyn 234: 124–131.
    Direct Link:
  • Olsson L, Falck P, Lopez K, Cobb J, Hanken J. 2001. Cranial neural crest cells contribute to connective tissue in cranial muscles in the anuran amphibian, Bombina orientalis. Dev Biol 237: 354–367.
  • Rees E, Young RD, Evans DJR. 2003. Spatial and temporal contribution of somitic myoblasts to avian limb muscles. Dev Biol 253: 264–278.
  • Ruberte J, Carretero A, Navarro M, Marcucio RS, Noden DM. 2003. Morphogenesis of blood vessels in the head muscles of the avian embryo: spatial, temporal, and VEGF expression analysis. Dev Dyn 227: 470–483.
    Direct Link:
  • Ruhin B, Creuzet S, Vincent C, Benouaiche L, Le Douarin NM, Couly G. 2003. Patterning of the hyoid cartilage depends upon signals arising from the ventral foregut endoderm. Dev Dyn 228: 239–246.
    Direct Link:
  • Santagati F, Rijli FM. 2003. Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci 4: 806–818.
  • Schneider RA. 1999. Neural crest can form cartilages normally derived from mesoderm during development of the avian head skeleton. Dev Biol 208: 441–455.
  • Sohal GS, Ali MM, Galileo DS, Ali AA. 1998. Emigration of neuroepithelial cells from the hindbrain neural tube in the chick embryo. Int J Dev Neurosci 16: 477–481.
  • Stone JR, Hall BK. 2004. Latent homologues for the neural crest as an evolutionary novelty. Evol Dev 6: 123–129.
    Direct Link:
  • Thompson KS. 1993. Segmentation, the adult skull, and the problem of homology. In: HankenJ, HallBK, editors. The skull. Vol. 2. Patterns of structural and systematic diversity. Chicago: University of Chicago Press. p 36–68.
  • Thorogood P. 1993. Differentiation and morphogenesis of cranial skeletal tissues. In: HankenJ, HallBK, editors. The skull. Vol. 1. Chicago: University of Chicago Press. p 112–152.
  • Tosney KW. 1982. The segregation and early migration of cranial neural crest cells in the avian embryo. Dev Biol 89: 13–24.
  • Tosney KW. 2004. Long-distance cue from emerging dermis stimulates neural crest melanoblast migration. Dev Dyn 229: 99–108.
    Direct Link:
  • Trainor PA, Krumlauf R. 2001. Hox genes, neural crest cells and branchial arch patterning. Curr Opin Cell Biol 13: 698–705.
  • Trainor PA, Tam PPL. 1995. Cranial paraxial mesoderm and neural crest of the mouse embryo-codistribution in the craniofacial mesenchyme but distinct segregation in the branchial arches. Development 121: 2569–2582.
  • Trainor PA, Tan SS, Tam PPL. 1994. Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development 120: 2397–23408.
  • Trainor PA, Sobieszczuk D, Wilkinson D, Krumlauf R. 2002. Signalling between the hindbrain and paraxial tissues dictates neural crest migration pathways. Development 129: 433–442.
  • Tzahor E, Kempf H, Mootoosamy RC, Poon AC, Abzhanov A, Tabin CJ, Dietrich S, Lassar AB. 2003. Antagonists of Wnt and BMP signaling promote the formation of vertebrate head muscle. Genes Dev 17: 3087–3099.
  • Venters SJ, Argent RE, Deegan FM, Perez-Baron G, Wong TS, Tidyman WE, Denetclaw WF Jr, Marcelle C, Bronner-Fraser M, Ordahl CP. 2004. Precocious terminal differentiation of premigratory limb muscle precursor cells requires positive signalling. Dev Dyn 229: 591–599.
    Direct Link:
  • Wagner G. 1949. Die bedeutung der neuralleiste für die kopgestaltung der amphibienlarven: Untersuchungen an chimaeren von Triton und Bombinator. Rev Suisse Zool 56: 519–620.
  • Wagner GP. 1989. The origin of morphological characters and the biological basis of homology. Evolution 43: 1157–1171.
  • Wahl CM, Noden DM, Baker R. 1994. Developmental relations between sixth nerve motor neurons and their targets in the chick embryo. Dev Dyn 201: 191–202.
  • Wei Y, Mikawa T. 2000. Fate diversity of primitive streak cells during heart field formation in ovo. Dev Dyn 219: 505–513.
    Direct Link:
  • Wigmore PM, Evans DJR. 2002. Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis. Int Rev Cytol 216: 175–232.
  • Yaneza M, Gilthorpe JD, Lumsden A, Tucker AS. 2002. No evidence for ventrally migrating neural tube cells from the mid- and hindbrain. Dev Dyn 223: 163–167.
    Direct Link:
View Full Article (HTML) Get PDF (1902K)