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First published online September 9, 2004
doi: 10.1242/10.1242/dev.01350

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Neural crest cell plasticity and its limits

Institut d'Embryologie cellulaire et moléculaire du CNRS et du Collège de France (UMR CNRS 7128), 49bis Avenue de la Belle Gabrielle, 94736 Nogent-sur-Marne Cedex, France

View larger version (42K): [in a new window]   Fig. 1. Fate map of the neural crest-derived phenotypes along the neural axis. The various cell phenotypes yielded by neural crest (NC) cells at different anteroposterior levels of the neural fold (light blue) are shown in chick embryos of 7 (left) and 28 (right) somites (S). Left, tissues that arise from the cephalic NC; right, tissues that arise from the trunk NC in cervical, thoracic and lumbosacral regions of the spinal cord. The region that gives rise to mesectoderm (green) extends from the level of mid-diencephalon down to rhombomere (r) 8 (corresponding to S4). Melanocytes (grey) are produced along the entire length of the neural axis. The parasympathetic ciliary ganglion (yellow) derives from the mesencephalic NC. Enteric ganglia (orange) arise from both vagal (S1-S7) and lumbosacral (posterior to S28) NC. Caudal to S4, the trunk NC yields PNS sympathetic ganglia (red), whereas the sensory ganglia (dark blue) are generated by the mes-metencephalic NC and by the NC from posterior rhombencephalic to lumbosacral levels. Endocrine cells (violet) originate from the NC of S2-S4 and S18-S24 levels.

View larger version (52K): [in a new window]   Fig. 2. Cephalic neural crest contribution to head skeleton, vasculature and to conotruncal structures of the heart. (A) Fate map of the cephalic neural crest (NC) in five-somite stage (ss) chick embryo. The anterior neural fold domain extending from mid-diencephalon down to rhombomere (r) 2 (in light blue) yields Hox-negative NC cells (NCCs) only, while the posterior one (in pink), generates Hox-positive NCCs [reproduced, with permission, from Couly et al. (Couly et al., 1996)]. Both are present in r3. (B) Respective contribution of Hox-negative and Hox-positive NC domains to the craniofacial and hypobranchial skeleton. (C) Refined colour-coded map of the cephalic NC levels at 5 ss and (D) their contribution to the musculo-connective wall of the head vascular tree. Prosencephalic meninges (pink) derive from diencephalic-mesencephalic (Di-Mes) NCCs, whereas meninges in the mesencephalon and more caudal CNS (light grey) originate from the mesoderm (light grey in C). (E) Relative contribution to the conotruncal structures of the heart of r6 to r8 cardiac NCCs [reproduced, with permission, from Etchevers et al. (Etchevers et al., 1999; Etchevers et al., 2001)]. A, aorta; An, angular; Ar, articular; AV, atrioventricular valve; Bb, basibranchial; Bh, basihyal; C, columella; Cb, ceratobranchial; D, dentary; Di, diencephalon; Eb, epibranchial; En, entoglossum; F, frontal; Io, interorbital septum; IVS, intraventricular septum; J, jugal; Mc, Meckel's cartilage; Mes, anterior mesencephalon; Mx, maxillary; N, nasal; Nc, nasal capsule; O, opercular; P, parietal; PA, pulmonary artery; Pl, palate; Pm, premaxilla; Pt, pterygoid; Q, quadrate; Qj, quadratojugal; r, rhombomere; SA, sinoatrial valve; Sa, supra-angular; SL, semilunar valve; So, sclerotic ossicles; Sq, squamosal.

View larger version (55K): [in a new window]   Fig. 3. Hox gene expression restricts skeletogenic properties of the cephalic neural crest. (A) In a 5-somite stage (ss) chick embryo, the cephalic neural crest (NC) is divided into an anterior Hox-negative (Hox–) domain (red) and a posterior Hox-positive (Hox+) domain (blue). The transition between these two domains corresponds to rhombomere (r) 3 (orange). The neural fold rostral to the mid-diencephalon does not produce NC cells (NCCs). (B) Postmigratory Hox– NCCs (red) yield cartilages, as well as endochondral and membrane bones of the entire upper face and jaws. By contrast, skeletogenic functions of Hox+ NCCs (blue) are limited to chondrogenesis and endochondral ossification in the hyoid structure. (C-H) Facial development at embryonic day (E) 7 after resection and/or exchange of cephalic NC domains in 5 ss chick embryo. The removal of Hox– FSNC (facial skeletogenic neural crest; broken lines) (C) abolishes head development (D). Replacement of FSNC by Hox+ neural fold (E) severely hampers head morphogenesis (F). Following removal of whole FSNC (as in E) (G), implantation of only a fragment of the FSNC (from either di-, mes- or metencephalic level) restores normal development of complete face and forebrain (H). Reproduced, with permission, from Couly et al. (Couly et al., 2002).

View larger version (104K): [in a new window]   Fig. 4. FGF8 promotes facial regeneration. (A) In a normal chick, at embryonic day 2 (E2), Fgf8 is expressed in the branchial arches (BAs, arrows) and nasofrontal (arrowheads) ectoderm, as well as in the neuroectoderm of the isthmus (Is) and prosencephalon. (B,C) After ablation of the FSNC (facial skeletogenic neural crest) at the 5-somite stage (ss) (B), Fgf8 expression is dramatically reduced both in BA1 (arrow) and forehead territories (arrowheads) (C). (D) Implantation of FGF8-soaked beads at the presumptive level of BA1 ectoderm following ablation of FSNC (D) induces regeneration of facial and cephalic structures. (E-G) Role of the rhombomere (r) 3-derived neural crest (NC) in regenerating the jaws. (E) Replacement of the r3-NC by its quail counterpart in a 5 ss chick embryo and FGF8-soaked bead implantation. (F) Skeletogenic cells in Meckel's cartilage (Mc) are exclusively quail derived, as shown in G, which shows a higher magnification of quail cell-specific antibody against a perinuclear antigen (QCPN) staining. Mdp, mandibular process; T, tongue.

View larger version (81K): [in a new window]   Fig. 5. The foregut endoderm patterns the neural crest-derived skeleton. (A) Transplantation of endodermal zone II from quail into stage-matched chick neurula. (B,C) Sections of the operated embryonic day (E) 6 host after detection of quail cells [quail cell-specific antibody against a perinuclear antigen (QCPN), brown] and cartilage staining (Alcian Blue). (B) Laterally engrafted endodermal cells have induced ectopic differentiation of chondrogenic cells, which all derive from host mesectoderm (see enlargement in C). (D) Bilateral grafting of quail endodermal stripe (II) implanted ventrally into a stage-matched chick embryo. (E) At E9, the host shows an additional lower beak apparatus (lb*) interposed between the endogenous upper (ub) and lower (lb) components of the host bill. (F) This supernumerary structure is accompanied by an additional Meckel's cartilage (Mc*) (Alcian Blue staining). Reproduced, with permission, from Couly et al. (Couly et al., 2002). A, articular; Ey, eye; NaCa, nasal capsule; Q, quadrate.

View larger version (85K): [in a new window]   Fig. 6. Neural crest cells impart morphological features to skeletal and ectodermal structures. Sagittal sections of the beaks of control duck (A) and quail (B) embryos. (C,D) Beak sections of duck-quail chimeras after orthotopic replacement of quail neural crest (NC) into duck host (`Quck' chimera) (C), and reciprocal graft of duck NC into quail embryo (`Duail') (D), showing that the host upper bill morphology is modified according to the species origin of the NC [reproduced, with permission, from Schneider and Helms (Schneider and Helms, 2003)]. (E) Chimeric hyoid skeletal structures of a quail at embryonic day (E) 9, after unilateral replacement by duck NC (Alcian Blue staining). (F) Higher magnification of the entoglossum: on grafted side, the ipsilateral half has acquired a duck-shaped morphology [reproduced, with permission, from Tucker and Lumsden (Tucker and Lumsden, 2004)]. Arrows indicate the proximal limit of the cartilages on both sides. d, dentary; et, egg tooth; ey, eye; Mk, Meckel's cartilage; nc, nasal capsule; np, nasal passage; pm, premaxilla; pp, prenasal process; V, trigeminal sensory neurons.

View larger version (41K): [in a new window]   Fig. 7. Model for neural crest lineage segregation. Neural crest (NC) progenitors identified by in vitro clonal analysis are ordered according to their number of developmental potentials [data taken from elsewhere (Baroffio et al., 1991; Trentin et al., 2004)]. In the cephalic NC, neurons (N), glia (G), melanocytes (M) and mesectodermal derivatives – myofibroblasts (F) and cartilage (C) – arise from diverse `intermediate' pluripotent and bipotent progenitors, which suggest that committed cells are generated through progressive restrictions in the potentialities of a putative `totipotent-like' NC stem cell (broken circle). In the trunk NC, clonogenic cells endowed with chondrogenic potential (blue) are not recovered; however, various myofibroblastic (non-chondrogenic) progenitors (pink) are present as in the cephalic NC. Self-renewal was demonstrated for rat trunk GNF-like cells (Stemple and Anderson, 1992), and for quail trunk and cephalic GM and GF progenitors (Trentin et al., 2004).