Hongxu Meng, Xinyi Wang, Boxuan Wu, Yingqi Jiang, Yuning Dong, Tianyi Zhang, Bingqian Chen, Hanzhang Li, Taozehan Chen, Wenyue Li, Xiaozhao Wang, Xin Lan, Tianrui Zhao, Huan Hu, Wenwen Huang, Núria Gavara, Hongwei Ouyang, Yuan Yuan
Craniosynostosis, resulting from the premature fusion of one or more cranial sutures, often requires invasive surgery for treatment. Currently, the spatiotemporal regulation of calvarial ossification during suture development is largely focused on cellular and molecular patterns. Using physicochemical imaging and nanomechanical mapping, we identified a unidirectional osteo-periosteal interface characterized by calcium phosphate deposition gradient during early postnatal calvarial development. Lineage tracing and dynamic bone formation assays revealed that Mmp13-positive osteoprogenitors, derived from Erg-expressing suture mesenchyme, establish this osteo-periosteal interface and drive asymmetric calvarial osteogenesis in mice. In the Twist1± craniosynostosis model, mineralization patterns initially resembled those of wild-type mice; however, misregulation of the PAK1/MMP13/BMP7 signaling cascade at the dura side triggered bilateral mineralization within the coronal suture, ultimately leading to bone fusion. Importantly, early localized inhibition of MMP13 overactivation, achieved by applying CL-82198 (a small-molecule MMP13 inhibitor) in a thin 20% gelatin methacryloyl (GelMA) hydrogel-based 'Suture Patch', preserved coronal suture patency in Twist1 mutants via a minimally invasive surgical procedure. Our work identifies a unilateral osteo-periosteal interface that is critical for coronal suture patency, reveals the regulatory role of non-cellular components in calvaria development, and proposes a minimally invasive strategy to preserve asymmetric osteogenesis in cranial sutures for the treatment of craniosynostosis. STATEMENT OF SIGNIFICANCE: Craniosynostosis is a premature skull suture fusion that currently requires invasive surgery. We discover a unidirectional mineralization gradient driven by Mmp13+ osteoprogenitors. In a craniosynostosis model, this asymmetric process becomes bilateral and pathological. Leveraging this insight, we engineer a 200-μm hydrogel "Suture Patch" that delivers a small-molecule Mmp13 inhibitor locally. A single application in newborn mice preserves suture patency in 80% of treated animals, corrects skull deformity, and restores progenitor pools-without surgery. Our work integrates advanced materials characterization, single-cell biology, and translational bioengineering to provide both a fundamental revision of suture development and a practical, minimally invasive biomaterial therapy for the debilitating pediatric disorder.