Hox/Meis-dependent gene-regulatory transition underlies cardiopharyngeal neural crest diversification

Abstract Neural crest cells (NCCs) are multipotent migratory cells essential for cardiac development, yet the lineage trajectories and gene regulatory networks underlying their differentiation in the cardiopharyngeal region remain unclear. Here, we integrate single-cell RNA-seq, spatial transcriptomics, and multiomic analyses to construct a comprehensive map of NCC lineages in developing mouse cardiopharyngeal tissues. We identify a transition from Hox -positive pharyngeal NCCs to Hox -negative intracardiac populations associated with the outflow tract cushion, accompanied by a shift in Meis transcription factor binding and gene-regulatory network architecture. By contrast, NCCs forming the aorticopulmonary septum and great vessel smooth muscle retain distinct Hox -codes. A Meis2 – Sox9 – Scx gene-regulatory network defines a skeletogenic progenitor-like intermediate state that gives rise to coronary artery smooth muscle and semilunar valves. Our findings suggest that the loss of Hox -dependent regional identity enables pharyngeal NCCs to acquire new fates upon entering the cardiac cushion, providing insight into the developmental origins of coronary and valvular calcification.

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Publication Details

Journal
The EMBO Journal
Published
2026-09-15
DOI
https://doi.org/10.1038/s44318-026-00886-x
Primary Topic
Congenital heart defects research
Type
article
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article

Hox/Meis-dependent gene-regulatory transition underlies cardiopharyngeal neural crest diversification

Hiroyuki Aburatani, Kazuhiro Matsui, Yunce Wang, Haruhiko Akiyama et al.
The EMBO Journal
Congenital heart defects research
article

Hox/Meis-dependent gene-regulatory transition underlies cardiopharyngeal neural crest diversification

Hiroyuki Aburatani, Kazuhiro Matsui, Yunce Wang, Haruhiko Akiyama, Shiro Fukuda, Chisa Shukunami, Yasunobu Uchijima, Masahide Seki, Youichiro Wada, Mayuko Kida, Daiki Seya, Teruhisa Kawamura, Hiroki Kurihara, Takahide Kohro, Yukihiro Harada, Hiroki Higashiyama, Akinori Kanai, Hiroto Katoh, Akiyasu Iwase, Sachiko Miyagawa‐Tomita, Yukiko Kurihara, Osamu Nakagawa, Shumpei Ishikawa, Akashi Taguchi, Shogo Yamamoto, Seitaro Nomura, Yutaka Suzuki
article en

Abstract

Abstract Neural crest cells (NCCs) are multipotent migratory cells essential for cardiac development, yet the lineage trajectories and gene regulatory networks underlying their differentiation in the cardiopharyngeal region remain unclear. Here, we integrate single-cell RNA-seq, spatial transcriptomics, and multiomic analyses to construct a comprehensive map of NCC lineages in developing mouse cardiopharyngeal tissues. We identify a transition from Hox -positive pharyngeal NCCs to Hox -negative intracardiac populations associated with the outflow tract cushion, accompanied by a shift in Meis transcription factor binding and gene-regulatory network architecture. By contrast, NCCs forming the aorticopulmonary septum and great vessel smooth muscle retain distinct Hox -codes. A Meis2 – Sox9 – Scx gene-regulatory network defines a skeletogenic progenitor-like intermediate state that gives rise to coronary artery smooth muscle and semilunar valves. Our findings suggest that the loss of Hox -dependent regional identity enables pharyngeal NCCs to acquire new fates upon entering the cardiac cushion, providing insight into the developmental origins of coronary and valvular calcification.

The EMBO Journal
Hiroshima University (JP), Teikyo Heisei University (JP), Ritsumeikan University (JP), Jichi Medical University (JP), Tokyo University of Science (JP), Kagawa Nutrition University (JP), National Cerebral and Cardiovascular Center (JP), Chiba Cancer Center (JP), National Cancer Center Hospital East (JP), Kumamoto Medical Center (JP), Gifu University (JP), The University of Tokyo (JP), Kumamoto University (JP)
Partnerships for the goals
Openalex Percentile: Top 18%
Congenital heart defects research
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