Khouri-Farah Nagham, Winchester Emma Wentworth, Schilder Brian M, Robinson Kelsey, Curtis Sarah W, Skene Nathan G, Leslie-Clarkson Elizabeth J, Cotney Justin
Graduate Program in Genetics and Developmental Biology, UConn Health.
Department of Brain Sciences, Faculty of Medicine, Imperial College London, London, W12 0BZ, UK.
bioRxiv. 2025 Feb 5:2025.01.18.633396. doi: 10.1101/2025.01.18.633396.
Craniofacial development gives rise to the complex structures of the face and involves the interplay of diverse cell types. Despite its importance, our understanding of human-specific craniofacial developmental mechanisms and their genetic underpinnings remains limited. Here, we present a comprehensive single-nucleus RNA sequencing (snRNA-seq) atlas of human craniofacial development from craniofacial tissues of 24 embryos that span six key time points during the embryonic period (4-8 post-conception weeks). This resource resolves the transcriptional dynamics of seven major cell types and uncovers distinct major cell types, including muscle progenitors and cranial neural crest cells (CNCCs), as well as dozens of subtypes of ectoderm and mesenchyme. Comparative analyses reveal substantial conservation of major cell types, alongside human biased differences in gene expression programs. CNCCs, which play a crucial role in craniofacial morphogenesis, exhibit the lowest marker gene conservation, underscoring their evolutionary plasticity. Spatial transcriptomics further localizes cell populations, providing a detailed view of their developmental roles and anatomical context. We also link these developmental processes to genetic variation, identifying cell type-specific enrichments for common variants associated with facial morphology and rare variants linked to orofacial clefts. Intriguingly, Neanderthal-introgressed sequences are enriched near genes with biased expression in cartilage and specialized ectodermal subtypes, suggesting their contribution to modern human craniofacial features. This atlas offers unprecedented insights into the cellular and genetic mechanisms shaping the human face, highlighting conserved and distinctly human aspects of craniofacial biology. Our findings illuminate the developmental origins of craniofacial disorders, the genetic basis of facial variation, and the evolutionary legacy of ancient hominins. This work provides a foundational resource for exploring craniofacial biology, with implications for developmental genetics, evolutionary biology, and clinical research into congenital anomalies.
颅面发育产生了面部的复杂结构,并涉及多种细胞类型的相互作用。尽管其很重要,但我们对人类特有的颅面发育机制及其遗传基础的理解仍然有限。在这里,我们展示了一个全面的人类颅面发育单核RNA测序(snRNA-seq)图谱,该图谱来自24个胚胎的颅面组织,这些胚胎跨越胚胎期的六个关键时间点(受孕后4 - 8周)。这个资源解析了七种主要细胞类型的转录动态,并揭示了不同的主要细胞类型,包括肌肉祖细胞和颅神经嵴细胞(CNCCs),以及外胚层和间充质的数十种亚型。比较分析揭示了主要细胞类型的大量保守性,以及基因表达程序中的人类偏向性差异。在颅面形态发生中起关键作用的CNCCs表现出最低的标记基因保守性,突出了它们的进化可塑性。空间转录组学进一步定位了细胞群体,提供了它们发育作用和解剖背景的详细视图。我们还将这些发育过程与遗传变异联系起来,确定了与面部形态相关的常见变异和与口面部裂隙相关的罕见变异的细胞类型特异性富集。有趣的是,尼安德特人渗入序列在软骨和特殊外胚层亚型中偏向表达的基因附近富集,表明它们对现代人类颅面特征的贡献。这个图谱为塑造人类面部的细胞和遗传机制提供了前所未有的见解,突出了颅面生物学中保守和独特的人类方面。我们的发现阐明了颅面疾病的发育起源、面部变异的遗传基础以及古代人类的进化遗产。这项工作为探索颅面生物学提供了基础资源,对发育遗传学、进化生物学和先天性异常的临床研究具有重要意义。