Masaryk University, Faculty of Medicine, Department of Histology and Embryology, Brno, Czech Republic.
Institut Curie, Laboratory of Genetics and Developmental Biology, INSERM U934, CNRS UMR3215, PSL Université Paris, Paris, France.
PLoS Biol. 2024 Jan 10;22(1):e3002093. doi: 10.1371/journal.pbio.3002093. eCollection 2024 Jan.
Epithelial branching morphogenesis is an essential process in living organisms, through which organ-specific epithelial shapes are created. Interactions between epithelial cells and their stromal microenvironment instruct branching morphogenesis but remain incompletely understood. Here, we employed fibroblast-organoid or fibroblast-spheroid co-culture systems and time-lapse imaging to reveal that physical contact between fibroblasts and epithelial cells and fibroblast contractility are required to induce mammary epithelial branching. Pharmacological inhibition of ROCK or non-muscle myosin II, or fibroblast-specific knock-out of Myh9 abrogate fibroblast-induced epithelial branching. The process of fibroblast-induced branching requires epithelial proliferation and is associated with distinctive epithelial patterning of yes associated protein (YAP) activity along organoid branches, which is dependent on fibroblast contractility. Moreover, we provide evidence for the in vivo existence of contractile fibroblasts specifically surrounding terminal end buds (TEBs) of pubertal murine mammary glands, advocating for an important role of fibroblast contractility in branching in vivo. Together, we identify fibroblast contractility as a novel stromal factor driving mammary epithelial morphogenesis. Our study contributes to comprehensive understanding of overlapping but divergent employment of mechanically active fibroblasts in developmental versus tumorigenic programs.
上皮分支形态发生是生物体内的一个基本过程,通过这个过程形成了特定于器官的上皮形状。上皮细胞与其基质微环境之间的相互作用指导分支形态发生,但仍不完全清楚。在这里,我们采用成纤维细胞类器官或成纤维细胞球体共培养系统和延时成像来揭示,成纤维细胞与上皮细胞之间的物理接触和成纤维细胞收缩性是诱导乳腺上皮分支所必需的。用 ROCK 或非肌肉肌球蛋白 II 的药理学抑制剂处理,或成纤维细胞特异性敲除 Myh9,均可消除成纤维细胞诱导的上皮分支。成纤维细胞诱导的分支过程需要上皮细胞的增殖,并与沿类器官分支的 yes 相关蛋白 (YAP) 活性的独特上皮模式有关,这依赖于成纤维细胞的收缩性。此外,我们还提供了证据表明,在青春期小鼠乳腺的终末芽(TEB)周围存在具有收缩性的成纤维细胞,这表明成纤维细胞的收缩性在体内分支中起着重要作用。总之,我们确定了成纤维细胞收缩性是驱动乳腺上皮形态发生的一种新的基质因子。我们的研究有助于全面了解机械活性成纤维细胞在发育和肿瘤发生程序中重叠但不同的作用。