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

TY - JOUR

T1 - Distinct effects of Hoxa2 overexpression in cranial neural crest populations reveal that the mammalian hyomandibular-ceratohyal boundary maps within the styloid process

AU - Kitazawa, Taro

AU - Fujisawa, Kou

AU - Narboux-Nême, Nicolas

AU - Arima, Yuichiro

AU - Kawamura, Yumiko

AU - Inoue, Tsuyoshi

AU - Wada, Youichiro

AU - Kohro, Takahide

AU - Aburatani, Hiroyuki

AU - Kodama, Tatsuhiko

AU - Kim, Ki-Sung

AU - Sato, Takahiro

AU - Uchijima, Yasunobu

AU - Maeda, Kazuhiro

AU - Miyagawa-Tomita, Sachiko

AU - Minoux, Maryline

AU - Rijli, Filippo M

AU - Levi, Giovanni

AU - Kurihara, Yukiko

AU - Kurihara, Hiroki

N1 - Copyright © 2015 Elsevier Inc. All rights reserved.

PY - 2015/6/15

Y1 - 2015/6/15

N2 - 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.

AB - 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.

KW - Alcian Blue

KW - Animals

KW - Anthraquinones

KW - Branchial Region/embryology

KW - DNA Primers/genetics

KW - Gene Expression Profiling

KW - Gene Expression Regulation, Developmental/genetics

KW - Homeodomain Proteins/metabolism

KW - In Situ Hybridization

KW - Mice

KW - Mice, Mutant Strains

KW - Morphogenesis/genetics

KW - Neural Crest/embryology

KW - Real-Time Polymerase Chain Reaction

U2 - 10.1016/j.ydbio.2015.04.007

DO - 10.1016/j.ydbio.2015.04.007

M3 - Journal article

C2 - 25889273

SN - 0012-1606

VL - 402

SP - 162

EP - 174

JO - Developmental Biology

JF - Developmental Biology

IS - 2

ER -