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First published online February 10, 2005
doi: 10.1242/10.1242/dev.01705

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New insights into craniofacial morphogenesis

¹ Department of Plastic and Reconstructive Surgery, Stanford University, Stanford, CA 94305, USA
² Department of Obstetrics and Gynecology, Montefiore Medical Center/Albert Einstein, College of Medicine, Bronx, NY, USA

View larger version (49K): [in a new window]   Fig. 1. Development of the craniofacial primordia. (A-D) A frontal view of the prominences that give rise to the main structures of the face. The frontonasal (or median nasal) prominence (red) contributes to the forehead (A), the middle of the nose (B), the philtrum of the upper lip (C) and the primary palate (D), while the lateral nasal prominence (blue) forms the sides of the nose (B,D). The maxillomandibular prominences (green) give rise to the lower jaw (specifically from the mandibular prominences), to the sides of the middle and lower face, to the lateral borders of the lips, and to the secondary palate (from the maxillary prominences).

View larger version (47K): [in a new window]   Fig. 2. Neurulation in the developing vertebrate embryo. (A) Neurulation begins with a unified layer of ectoderm, underneath which lies the endoderm. A single ectomere is shown in yellow. Ectomeres are discrete regions of superficial ectoderm that exhibit a segmented pattern of gene expression. Fate-mapping experiments suggest that, together with neural crest and neuroectoderm, they define a larger developmental unit (Couly and Le Douarin, 1999). Later, these tissues act on signaling centers in the facial prominences (Hu et al., 2003). (B) The ectoderm begins to fold upwards, giving rise to the neural folds. During this process, interactions between signaling molecules begin to delineate the medial ectoderm as being neural (green) and the lateral regions of ectoderm as being non-neural (blue). The prechordal plate mesendoderm (pcp) and the buccopharyngeal membrane (bpm) become evident at this stage. (C) The neural tube forms upon fusion of the neural folds, giving rise to discrete neuroectoderm (green) and surface ectoderm (blue). Around the same time, the border region between the neuroectoderm and surface ectoderm gives rise to neural crest cells. The surface ectoderm and neuroectoderm of single ectomeres remain aligned during this process. (D) Neurulation completes upon formation of the neural tube, and neural crest cells (nc) lie sandwiched between the facial (surface) ectoderm and the neuroectoderm. Again, the individual neuroectoderm and surface ectoderm components of the ectomere remain in register. (E) Sagittal section through neural tube of a stage 15 chick embryo, showing neural crest (nc) located between surface ectoderm (se) and neuroectoderm (ne). L, lateral; M, medial. (E) Unpublished data from J.A.H.'s laboratory.

View larger version (89K): [in a new window]   Fig. 3. Neural crest migration and ectomere alignment. (A,C,E) Schematics of a developing chick embryo illustrating neural crest migration during craniofacial development. (B,D,F) In situ hybridization showing Fgf8 expression (yellow) during chick craniofacial development. (A-D) As the closed neural tube begins to differentiate into the central nervous system, the neural crest begins to migrate anteriorly from specific rhombomeres (r1-r3) into discrete regions of the face. During this process, the neuroectoderm (ne) and surface ectoderm (se) components of the ectomeres continue to remain aligned (yellow arrows in C). Inset in A shows higher magnification of the boxed area in B (the direct contact between the anterior neuroectoderm and presumptive facial ectoderm, prior to neural crest cell migration between those two epithelial layers). (E,F) As neural crest migration nears completion, the neuroectoderm and facial ectoderm (fe; late-stage term for surface ectoderm) components of the ectomere are no longer aligned. is, isthmus; mn, mandible; PA, pharyngeal arch; pe, pharyngeal endoderm; rp, Rathke's pouch; tel ne, telencephalic neuroectoderm. (B,D,F) Unpublished data from J.A.H.'s laboratory.

View larger version (60K): [in a new window]   Fig. 4. Bmp4 expression levels control beak depth and height. (A,B) Large ground finches have thick, broad and long beaks. (C) The embryonic beak of a ground finch exhibits high Bmp4 expression levels, which promote chondrogenesis and therefore increased beak height, length and depth (red arrow). (D) Misexpression of Bmp4 in the frontonasal process mesenchyme of chick embryos produces a noticeably broader and thicker upper beak, paralleling the beak morphology of the ground finch. (E) Alcian staining of chick embryos injected with RCAS-Bmp4 reveals enlarged skeletal elements in the upper beak. (F,G) Cactus finches have thinner, shorter and narrower beaks. (H) The embryonic beak of a cactus finch exhibits very little Bmp4 expression, and chondrogenesis of the beak is not as pronounced, which leads to an overall smaller beak. (I) Misexpression of noggin, a Bmp4 antagonist, in frontonasal process mesenchyme of chick embryos produces a noticeably thinner and narrower upper beak, paralleling the beak morphology of the cactus finch. (J) Alcian staining reveals stunted upper beak skeletal elements in chicken embryos injected with RCAS-noggin. (B-D,G-I) Reproduced, with permission, from Abzhanov et al. (Abzhanov et al. 2004). (E,J) Reproduced, with permission, from Wu et al. (Wu et al. 2004). (A,F) Courtesy of P. Grant, A. Abzhanov and C. Tabin.

View larger version (75K): [in a new window]   Fig. 5. Morphological differences between jaws of cichlids. (A) The river-dwelling cichlid Metriaclima zebra (left) has a jaw structure (right) that is well-suited for sucking. (B) The Great Lakes cichlid Labeotropheus fuelleborni (left) has a jaw structure (right) that is well-suited for biting. Photographs of Labeotropheus fuelleborni and Metriaclima zebra courtesy of J. Dion and F. Hagblom, respectively. Drawings reproduced, with permission, from Albertson et al. (Albertson et al., 2003a).

View larger version (43K): [in a new window]   Fig. 6. Hox expression in agnathans and gnathostomes. (A) Correlations between Hox expression and jaw development in chordates. The phylum chordata can be subdivided into two groups: jawed gnathostomes (green) and jawless agnathans (red). Some organisms in both groups, including the jawless lamprey and the jawed teleost fish, possess neural crest (blue) that can be acted on by Hox genes. Recent experiments (Ferrier et al., 2000; Cohn, 2002) have demonstrated that Hox expression exists as anterior as the first pharyngeal arch (PA1) in agnathan lampreys and amphioxus. Conversely, in most gnathostome vertebrates, Hox expression is evident only up to the second pharyngeal arch (PA2), and no Hox expression is seen in PA1. As such, loss of Hox expression in PA1 can be correlated with the development of jaws in vertebrates.