ArticleProceedings of the National Academy of Sciences of the United States of America2013
Rotational motion during three-dimensional morphogenesis of mammary epithelial acini relates to laminin matrix assembly.
Article in Proceedings of the National Academy of Sciences of the United States of America, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 76 papers.
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Who cites it
76 citing papers in PubMed.
- Initiation of rotational collective migration inProceedings of the National Academy of Sciences of the United States of America · 2026Article
- Combinatorial regulation of cellular rotation by CUL-3-actomyosin-dependent oriented division, eggshell geometry, and Ras-MAPK signaling during dorsal-ventral axis establishment inbioRxiv : the preprint server for biology · 2026Article
- Adhesion and polarity-driven morphogenesis: Mechanisms and constraints in tissue formation.PLoS computational biology · 2026Article
- Single-cell chiral symmetry breaking under confinement.bioRxiv : the preprint server for biology · 2026Article
- Rotational migration in human pancreatic ductal organoids depends on actin and myosin activity.Communications biology · 2025Article
- Cell-mediated matrix deformations and cell-cell adhesions determine epithelial collective cell migration phenotypes.APL bioengineering · 2025Article
- Collective migration modes in development, tissue repair and cancer.Nature reviews. Molecular cell biology · 2025Review
- Rotational migration in human pancreatic ductal organoids depends on actin and myosin activity.ArXiv · 2025Article
- Tissue geometry and mechanochemical feedback initiate rotational migration inbioRxiv : the preprint server for biology · 2025Article
- Dynamic Organization of Cells in Colonic Epithelium is Encoded by Five Biological Rules.Biology of the cell · 2025Article
- Global versus local matrix remodeling drives rotational versus invasive collective migration of epithelial cells.Developmental cell · 2025Article
- Surface Acoustic Wave-Enhanced Multi-View Acoustofluidic Rotation Cytometry (MARC) for Pre-Cytopathological Screening.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2024Article
- RNAi-directed knockdown in the cnidarian fish blood parasite Sphaerospora molnari.Scientific reports · 2024Article
- Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo.Development (Cambridge, England) · 2023Article
- Curvature induces active velocity waves in rotating spherical tissues.Nature communications · 2023Article
- Collective cell migration during human mammary gland organoid morphogenesis.Biophysics reviews · 2022Article
- The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces.Science advances · 2022Article
- High-throughput formation and image-based analysis of basal-in mammary organoids in 384-well plates.Scientific reports · 2022Article
- Human Breast Extracellular Matrix Microstructures and Protein Hydrogel 3D Cultures of Mammary Epithelial Cells.Cancers · 2021Article
- Configurational fingerprints of multicellular living systems.Proceedings of the National Academy of Sciences of the United States of America · 2021Article
16 more citing papers are in PubMed but not listed here.
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5 authors.
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Abstract
Our understanding of the mechanisms by which ducts and lobules develop is derived from model organisms and three-dimensional (3D) cell culture models wherein mammalian epithelial cells undergo morphogenesis to form multicellular spheres with a hollow central lumen. However, the mechanophysical properties associated with epithelial morphogenesis are poorly understood. We performed multidimensional live-cell imaging analysis to track the morphogenetic process starting from a single cell to the development of a multicellular, spherical structure composed of polarized epithelial cells surrounding a hollow lumen. We report that in addition to actively maintaining apicobasal polarity, the structures underwent rotational motions at rates of 15-20 μm/h and the structures rotated 360° every 4 h during the early phase of morphogenesis. Rotational motion was independent of the cell cycle, but was blocked by loss of the epithelial polarity proteins Scribble or Pard3, or by inhibition of dynein-based microtubule motors. Interestingly, none of the structures derived from human cancer underwent rotational motion. We found a direct relationship between rotational motion and assembly of endogenous basement membrane matrix around the 3D structures, and that structures that failed to rotate were defective in weaving exogenous laminin matrix. Dissolution of basement membrane around mature, nonrotating acini restored rotational movement and the ability to assemble exogenous laminin. Thus, coordinated rotational movement is a unique mechanophysical process observed during normal 3D morphogenesis that regulates laminin matrix assembly and is lost in cancer-derived epithelial cells.
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