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First published online January 23, 2009
doi: 10.1242/10.1242/dev.028621

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Rostral and caudal pharyngeal arches share a common neural crest ground pattern

Maryline Minoux^1,*, Gregory S. Antonarakis^2,*, Marie Kmita^2,3, Denis Duboule^2,4, and Filippo M. Rijli^1,5,

¹ Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP, UMR 7104, Strasbourg, France.
² Department of Zoology and Animal Biology and National Research Centre Frontiers in Genetics, University of Geneva, Switzerland.
³ Laboratory of Genetics and Development, Institut de Recherches Cliniques de Montréal (IRCM), 110 avenue des Pins Ouest, H2W1R7, Montréal Quebec, Canada.
⁴ School of Life Sciences, Ecole Polytechnique Fédérale, Lausanne, Switzerland.
⁵ Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland.

View larger version (131K): [in this window] [in a new window]   Fig. 1. Pre-otic and post-otic NCC contribution to the hyoid complex. (A-F) Alkaline phosphatase (AP) (A-C) and cresyl violet (D-F) staining on adjacent frontal cryosections through the hyoid bone complex of E15.5 R4::Cre;Z/AP mouse fetuses. (G) Whole-mount AP staining of E11.5 R4::Cre;Z/AP mouse embryos. AP is expressed in rhombomere 4 (R4) as well as in PA2 NCCs. PA3 NCCs are devoid of AP expression (arrow). (H) Schematic drawing representing the composite origin of the hyoid bone. Rhombomere 4-derived AP+ NCCs contribute to the lesser horns (LH), the central part of the body (Bo) and two symmetrical regions articulating with the lesser horns. The greater horns (GH) are entirely AP negative, thus derived by post-otic NCCs. PA2, second pharyngeal arch; PA3, third pharyngeal arch; To, tongue.

View larger version (55K): [in this window] [in a new window]   Fig. 2. Homeosis of second, third and fourth arch skeletal derivatives in Hoxa-deleted mouse mutants (A-H) Ventrolateral views of whole-mount head skeletal preparations (A,C,E,G) and their schematic diagrams representing hyoid bone complex, middle ear skeletal elements, dentary bones and skull base elements (B,D,F,H) from wild-type (A,B), Hoxa2-/- (C,D), Wnt1::Cre/Hoxaflox/flox (E,F) or Wnt1::Cre/Hoxaflox/flox/Hoxddel/+ (G,H) newborns. The orientation of the skeletal preparations is shown in B; A, anterior; P, posterior; D, dorsal; V, ventral. (C,D) Homeotic change of PA2 towards PA1 morphology includes absence of styloid process, stapes (S) and lesser horn (LH) of hyoid bone, and appearance of partially duplicated Meckel's cartilage (MC2), incus (I2), malleus (M2), tympanic (T2) and pterygoid (P2) bones, as well as transformed gonial (G*) and ectopic squamosal (SQ2) bones. (E-H) Additional ectopic skeletal elements are present, indicating homeosis of PA3 and PA4, in addition to PA2, structures towards PA1 morphology. The greater horn (GH) of the hyoid bone is abnormally extended dorsally, resembling a partially triplicated Meckel's cartilage (MC3). MC2 (arrow) is also further extended when compared with D. The dorsal end of MC3 displayed a morphology resembling a supernumerary malleus (M3). In addition, ectopic membranous bone elements near MC3 and M3 may represent supernumerary dentary (DB2) and tympanic (T3) bones. Note that, in order to provide a better magnification for MC3 and M3, SQ2 and SQ3 are outside of the visible field of the picture in E and G. Arrowheads in G,H show fusions between the hyoid and thyroid cartilages. (I,J) Dissected middle ear and hyoid cartilage elements from a Wnt1::Cre/Hoxaflox/flox mutant newborn (I) and their representation in diagram (J). Morphological transformation of the thyroid cartilage (TC) results in an additional ectopic cartilage resembling partial quadruplication of Meckel's jaw cartilage (MC4). Note that MC4 and MC3 directly fuse with an unusually extended MC2, supporting their identity as supernumerary jaw cartilages. (I) The ectopic pterygoid bone (P2) has been dissected out from the basiphenoid (BS) bone. AS, alisphenoid bone; BO, basioccipital bone; DB, dentary bone; EX, exoccipital bone; G, gonial bone; H, hyoid bone; I, incus; M, malleus; MC, Meckel's cartilage; O, otic capsule; P, pterygoid bone; Q, quadrate bone; S, stapes; SQ, squamosal bone; T, tympanic bone. Asterisk indicates absence of lesser horn.

View larger version (46K): [in this window] [in a new window]   Fig. 3. Transformation of thyroid cartilage into supernumerary jaw element. (A,B) Frontal view of hyoid (H) and thyroid (TC) skeletal preparations from wild-type (A) and Wnt1::Cre/Hoxaflox/flox (B) mutant newborns. The orientation of the skeletal preparations is shown in A. (B) Asterisk represents absence of the lateral process (LP) of TC and morphological transformation in an additional ectopic cartilage resembling partial quadruplication of Meckel's jaw cartilage (MC4). Note that MC4 projects dorsally and fuses to a transformed greater horn of the hyoid bone (MC3). LH, lesser horn of hyoid bone; GH, greater horn of hyoid bone.

View larger version (112K): [in this window] [in a new window]   Fig. 4. Ectopic membranous bones in Hoxa and Hoxa/Hoxd deleted mutants. (A-D) Lateral views of head skeletal preparations from wild-type (A), Wnt1::Cre/Hoxaflox/flox (B), Wnt1::Cre/Hoxaflox/del (C) and Wnt1::Cre/Hoxaflox/flox/Hoxddel/+ (D) newborns. Orientation is shown in A. Whereas an ectopic partial squamosal bone (SQ2) is a feature of Hoxa2-/- mutants (Fig. 2C), additional supernumerary ectopic membranous bones appear in B-D that may reflect partial duplication of dentary (DB2) bone as well as triplication of squamosal (SQ3) bone. DB, dentary bone; SQ, squamosal bone.

View larger version (77K): [in this window] [in a new window]   Fig. 5. Molecular changes in Hoxa-deleted embryos support homeosis of post-otic NCCs. (A-D) Whole-mount in situ hybridization on wild-type (A,C) and Wnt1::Cre/Hoxaflox/flox/Hoxddel/del (B,D) embryos with antisense CRABP1 (A,B) and Pax1 (C,D) probes. Arrows show NCC migration into third and fourth pharyngeal arches. Pax1 expression marks pharyngeal pouches (pp)1-3. Normal NCC migration and arch segmentation is observed in B,D. (E-M) Whole-mount in situ hybridization on wild-type (E,H,K), Hoxa2-/- (F,I,L) and Wnt1::Cre/Hoxaflox/flox (G,J,M) E10.5 embryos using antisense Pitx1 (E-G), Alx4 (H-J) and Barx1 (K-M) probes. The arrowhead in K represents a small Barx1 expression domain at the dorsoanterior margin of PA2. The arrows indicate Barx1 ectopic expressions in second (PA2), third (PA3), and fourth (PA4) arches. PA1, first pharyngeal arch.

View larger version (46K): [in this window] [in a new window]   Fig. 6. Hox-free ground pattern for skeletogenic NCC contributing to pharyngeal arches. Vertical colored bars represent Hox gene expression patterns in NCC subpopulations contributing to pharyngeal arch (PA) mesenchyme. On the left side of the drawing, each pharyngeal arch is endowed with a specific Hox expression code represented by a distinct color, with the exception of PA1, which is devoid of Hox expression (yellow). Conditional deletion of Hoxa genes in NCCs reveals that rostral and caudal pharyngeal arches share the same Hox-free ground patterning program corresponding to the mandibular PA1 program. On the right-hand side, all arches are now depicted in yellow.

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