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Dev Biol. 2015 Jun 15;402(2):162-74. doi: 10.1016/j.ydbio.2015.04.007. Epub 2015 Apr 16.

Distinct effects of Hoxa2 overexpression in cranial neural crest populations reveal that the mammalian hyomandibular-ceratohyal boundary maps within the styloid process.

Author information

1
Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan; Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Chiyoda-ku, Tokyo 102-0076, Japan.
2
Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
3
Evolution des Régulations Endocriniennes, CNRS, UMR7221, Muséum National d'Histoire Naturelle, 7 rue Cuvier, 75231 Paris Cedex 05, France.
4
Laboratory for Systems Biology and Medicine, The University of Tokyo, 4-6-1 Komaba, Meguro, Tokyo 153-8904, Japan; Department of Nephrology and Endocrinology, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
5
Laboratory for Systems Biology and Medicine, The University of Tokyo, 4-6-1 Komaba, Meguro, Tokyo 153-8904, Japan.
6
Laboratory for Systems Biology and Medicine, The University of Tokyo, 4-6-1 Komaba, Meguro, Tokyo 153-8904, Japan; Department of Translational Research for Healthcare and Clinical Science, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
7
Division of Genome Science, Research Center for Advanced Science and Technology, The University of Tokyo, 4-6-1 Komaba, Meguro, Tokyo 153-8904, Japan.
8
Division of Cardiovascular Development and Differentiation, Medical Research Institute, Department of Pediatric Cardiology, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo 162-8666, Japan.
9
Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland; Faculté de chirurgie dentaire, 1, place de l'hôpital, 67 000 Strasbourg, France.
10
Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland; University of Basel, CH-4056 Basel, Switzerland.
11
Department of Physiological Chemistry and Metabolism, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan; Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Chiyoda-ku, Tokyo 102-0076, Japan; Institute for Biology and Mathematics of Dynamical Cell Processes (iBMath), The University of Tokyo, 3-8-1 Komaba, Tokyo 153-8914, Japan. Electronic address: kuri-tky@umin.net.

Abstract

Most gnathostomata craniofacial structures derive from pharyngeal arches (PAs), which are colonized by cranial neural crest cells (CNCCs). The anteroposterior and dorsoventral identities of CNCCs are defined by the combinatorial expression of Hox and Dlx genes. The mechanisms associating characteristic Hox/Dlx expression patterns with the topology and morphology of PAs derivatives are only partially known; a better knowledge of these processes might lead to new concepts on the origin of taxon-specific craniofacial morphologies and of certain craniofacial malformations. Here we show that ectopic expression of Hoxa2 in Hox-negative CNCCs results in distinct phenotypes in different CNCC subpopulations. Namely, while ectopic Hoxa2 expression is sufficient for the morphological and molecular transformation of the first PA (PA1) CNCC derivatives into the second PA (PA2)-like structures, this same genetic alteration does not provoke the transformation of derivatives of other CNCC subpopulations, but severely impairs their development. Ectopic Hoxa2 expression results in the transformation of the proximal Meckel's cartilage and of the malleus, two ventral PA1 CNCCs derivatives, into a supernumerary styloid process (SP), a PA2-derived mammalian-specific skeletal structure. These results, together with experiments to inactivate and ectopically activate the Edn1-Dlx5/6 pathway, indicate a dorsoventral PA2 (hyomandibular/ceratohyal) boundary passing through the middle of the SP. The present findings suggest context-dependent function of Hoxa2 in CNCC regional specification and morphogenesis, and provide novel insights into the evolution of taxa-specific patterning of PA-derived structures.

KEYWORDS:

Craniofacial development; Dlx; Hox; Neural crest cells; Pharyngeal arches; Styloid process

PMID:
25889273
DOI:
10.1016/j.ydbio.2015.04.007
[Indexed for MEDLINE]
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