Development, Vol 125, Issue 17 3445-3459, Copyright © 1998 by Company of Biologists

JOURNAL ARTICLES

Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development

G Couly, A Grapin-Botton, P Coltey, B Ruhin and NM Le Douarin
Institut d'Embryologie Cellulaire et Moleculaire du CNRS et du College de France, 94736 Nogent-sur-Marne Cedex, France.

In addition to pigment cells, and neural and endocrine derivatives, the neural crest is characterized by its ability to yield mesenchymal cells. In amniotes, this property is restricted to the cephalic region from the mid-diencephalon to the end of rhombomere 8 (level of somites 4/5). The cephalic neural crest is divided into two domains: an anterior region corresponding to the diencephalon, mesencephalon and metencephalon (r1, r2) in which expression of Hox genes is never observed, and a posterior domain in which neural crest cells exhibit (with a few exceptions) the same Hox code as the rhombomeres from which they originate. By altering the normal distribution of neural crest cells in the branchial arches through appropriate embryonic manipulations, we have investigated the relationships between Hox gene expression and the level of plasticity that neural crest cells display when they are led to migrate to an ectopic environment. We made the following observations. (i) Hox gene expression is not altered in neural crest cells by their transposition to ectopic sites. (ii) Expression of Hox genes by the BA ectoderm does not depend upon an induction by the neural crest. This second finding further supports the concept of segmentation of the cephalic ectoderm into ectomeres (Couly and Le Douarin, 1990). According to this concept, metameres can be defined in large bands of ectoderm including not only the CNS and the neural crest but also the corresponding superficial ectoderm fated to cover craniofacial primordia. (iii) The construction of a lower jaw requires the environment provided by the ectomesodermal components of BA1 or BA2 associated with the Hox gene non-expressing neural crest cells. Hox gene-expressing neural crest cells are unable to yield the lower jaw apparatus including the entoglossum and basihyal even in the BA1 environment. In contrast, the posterior part of the hyoid bone can be constructed by any region of the neural crest cells whether or not they are under the regulatory control of Hox genes. Such is also the case for the neural and connective tissues (including those comprising the cardiovascular system) of neural crest origin, upon which no segmental restriction is imposed. The latter finding confirms the plasticity observed 24 years ago (Le Douarin and Teillet, 1974) for the precursors of the PNS.

This article has been cited by other articles:

				P. Leucht, J.-B. Kim, R. Amasha, A. W. James, S. Girod, and J. A. Helms Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration Development, September 1, 2008; 135(17): 2845 - 2854. [Abstract] [Full Text] [PDF]

				G. W. Calloni, C. Glavieux-Pardanaud, N. M. Le Douarin, and E. Dupin Sonic Hedgehog promotes the development of multipotent neural crest progenitors endowed with both mesenchymal and neural potentials PNAS, December 11, 2007; 104(50): 19879 - 19884. [Abstract] [Full Text] [PDF]

				S. E. Creuzet, S. Martinez, and N. M. Le Douarin The cephalic neural crest exerts a critical effect on forebrain and midbrain development PNAS, September 19, 2006; 103(38): 14033 - 14038. [Abstract] [Full Text] [PDF]

				J. G. Crump, M. E. Swartz, J. K. Eberhart, and C. B. Kimmel Moz-dependent Hox expression controls segment-specific fate maps of skeletal precursors in the face Development, July 15, 2006; 133(14): 2661 - 2669. [Abstract] [Full Text] [PDF]

				F. Santagati, M. Minoux, S.-Y. Ren, and F. M. Rijli Temporal requirement of Hoxa2 in cranial neural crest skeletal morphogenesis Development, November 15, 2005; 132(22): 4927 - 4936. [Abstract] [Full Text] [PDF]

				P. Kang and K.K.H. Svoboda Epithelial-Mesenchymal Transformation during Craniofacial Development J. Dent. Res., August 1, 2005; 84(8): 678 - 690. [Abstract] [Full Text] [PDF]

				T. Aberg, R. Rice, D. Rice, I. Thesleff, and J. Waltimo-Siren Chondrogenic Potential of Mouse Calvarial Mesenchyme J. Histochem. Cytochem., May 1, 2005; 53(5): 653 - 663. [Abstract] [Full Text] [PDF]

				N. M. Le Douarin, S. Creuzet, G. Couly, and E. Dupin Neural crest cell plasticity and its limits Development, October 1, 2004; 131(19): 4637 - 4650. [Abstract] [Full Text] [PDF]

				L.-B. Ruest, X. Xiang, K.-C. Lim, G. Levi, and D. E. Clouthier Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity Development, September 15, 2004; 131(18): 4413 - 4423. [Abstract] [Full Text] [PDF]

				W. Y. Chan, C. S. Cheung, K. M. Yung, and A. J. Copp Cardiac neural crest of the mouse embryo: axial level of origin, migratory pathway and cell autonomy of the splotch (Sp2H) mutant effect Development, July 15, 2004; 131(14): 3367 - 3379. [Abstract] [Full Text] [PDF]

				M. Schubert, N. D. Holland, H. Escriva, L. Z. Holland, and V. Laudet Retinoic acid influences anteroposterior positioning of epidermal sensory neurons and their gene expression in a developing chordate (amphioxus) PNAS, July 13, 2004; 101(28): 10320 - 10325. [Abstract] [Full Text] [PDF]

				P. Y. Lwigale, G. W. Conrad, and M. Bronner-Fraser Graded potential of neural crest to form cornea, sensory neurons and cartilage along the rostrocaudal axis Development, May 1, 2004; 131(9): 1979 - 1991. [Abstract] [Full Text] [PDF]

				Y. Mori-Akiyama, H. Akiyama, D. H. Rowitch, and B. de Crombrugghe Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest PNAS, August 5, 2003; 100(16): 9360 - 9365. [Abstract] [Full Text] [PDF]

				D. Hu, R. S. Marcucio, and J. A. Helms A zone of frontonasal ectoderm regulates patterning and growth in the face Development, May 1, 2003; 130(9): 1749 - 1758. [Abstract] [Full Text] [PDF]

				S. Creuzet, G. Couly, C. Vincent, and N. M. Le Douarin Negative effect of Hox gene expression on the development of the neural crest-derived facial skeleton Development, March 11, 2003; 129(18): 4301 - 4313. [Abstract] [Full Text] [PDF]

				G. Grammatopoulos, E Bell, L Toole, A Lumsden, and A. Tucker Homeotic transformation of branchial arch identity after Hoxa2 overexpression Development, January 12, 2000; 127(24): 5355 - 5365. [Abstract] [PDF]

				M Pasqualetti, M Ori, I Nardi, and F. Rijli Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus Development, January 12, 2000; 127(24): 5367 - 5378. [Abstract] [PDF]

				O Wendling, C Dennefeld, P Chambon, and M Mark Retinoid signaling is essential for patterning the endoderm of the third and fourth pharyngeal arches Development, January 4, 2000; 127(8): 1553 - 1562. [Abstract] [PDF]

				C. Ferguson, A. Tucker, and P. Sharpe Temporospatial cell interactions regulating mandibular and maxillary arch patterning Development, January 1, 2000; 127(2): 403 - 412. [Abstract] [PDF]

				J. Barrow and M. Capecchi Compensatory defects associated with mutations in Hoxa1 restore normal palatogenesis to Hoxa2 mutants Development, January 11, 1999; 126(22): 5011 - 5026. [Abstract] [PDF]

				M Rossel and M. Capecchi Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development Development, January 11, 1999; 126(22): 5027 - 5040. [Abstract] [PDF]

				H. Etchevers, G Couly, C Vincent, and N. Le Douarin Anterior cephalic neural crest is required for forebrain viability Development, January 8, 1999; 126(16): 3533 - 3543. [Abstract] [PDF]

				M. Lu, H. Cheng, M. Kern, S. Potter, B Tran, T. Diekwisch, and J. Martin prx-1 functions cooperatively with another paired-related homeobox gene, prx-2, to maintain cell fates within the craniofacial mesenchyme Development, January 2, 1999; 126(3): 495 - 504. [Abstract] [PDF]