Department of Life Sciences, Graduate School of Science, University of Hyogo, Hyogo, Japan.
Department of Biological Sciences, Graduate School of Science, The University of Osaka, Toyonaka, Osaka, Japan.
PLoS Genet. 2024 Oct 7;20(10):e1011422. doi: 10.1371/journal.pgen.1011422. eCollection 2024 Oct.
Complex organ structures are formed with high reproducibility. To achieve such intricate morphologies, the responsible epithelium undergoes multiple simultaneous shape changes, such as elongation and folding. However, these changes have typically been assessed separately. In this study, we revealed how distinct shape changes are controlled during internal organ morphogenesis. The Drosophila embryonic hindgut undergoes left-right asymmetric rotation and anteroposterior elongation in a tissue-autonomous manner driven by cell sliding and convergent extension, respectively, in the hindgut epithelia. However, the regulation of these processes remains unclear. Through genetic analysis and live imaging, we demonstrated that cell sliding and convergent extension are independently regulated by Myosin1D and E-cadherin, and Par-3, respectively, whereas both require MyosinII activity. Using a mathematical model, we demonstrated that independently regulated cellular dynamics can simultaneously cause shape changes in a single mechanical system using anisotropic edge contraction. Our findings indicate that distinct cellular dynamics sharing a common apparatus can be independently and simultaneously controlled to form complex organ shapes. This suggests that such a mechanism may be a general strategy during complex tissue morphogenesis.
复杂的器官结构具有高度的重现性。为了形成如此复杂的形态，负责的上皮组织会经历多次同时发生的形状变化，例如伸长和折叠。然而，这些变化通常是分别评估的。在这项研究中，我们揭示了内部器官形态发生过程中如何控制不同的形状变化。果蝇胚胎后肠以组织自主性的方式发生左右不对称旋转和前后伸长，分别由后肠上皮细胞的滑动和汇聚延伸驱动。然而，这些过程的调节机制尚不清楚。通过遗传分析和活体成像，我们证明细胞滑动和汇聚延伸分别由肌球蛋白 1D 和 E-钙黏蛋白以及 Par-3 独立调节，而这两者都需要肌球蛋白 II 的活性。使用数学模型，我们证明了独立调节的细胞动力学可以使用各向异性边缘收缩在单个机械系统中同时引起形状变化。我们的研究结果表明，共享共同装置的不同细胞动力学可以独立且同时进行控制，从而形成复杂的器官形状。这表明这种机制可能是复杂组织形态发生过程中的一种通用策略。
