Institute of Molecular and Cell Biology, University of Tartu, 51010, Tartu, Estonia.
Institute of Biotechnology, University of Helsinki, 00014, Helsinki, Finland.
EMBO J. 2024 Feb;43(4):568-594. doi: 10.1038/s44318-023-00025-w. Epub 2024 Jan 23.
Comprehensive analysis of cellular dynamics during the process of morphogenesis is fundamental to understanding the principles of animal development. Despite recent advancements in light microscopy, how successive cell shape changes lead to complex three-dimensional tissue morphogenesis is still largely unresolved. Using in vivo live imaging of Drosophila wing development, we have studied unique cellular structures comprising a microtubule-based membrane protrusion network. This network, which we name here the Interplanar Amida Network (IPAN), links the two wing epithelium leaflets. Initially, the IPAN sustains cell-cell contacts between the two layers of the wing epithelium through basal protrusions. Subsequent disassembly of the IPAN involves loss of these contacts, with concomitant degeneration of aligned microtubules. These processes are both autonomously and non-autonomously required for mitosis, leading to coordinated tissue proliferation between two wing epithelia. Our findings further reveal that a microtubule organization switch from non-centrosomal to centrosomal microtubule-organizing centers (MTOCs) at the G2/M transition leads to disassembly of non-centrosomal microtubule-derived IPAN protrusions. These findings exemplify how cell shape change-mediated loss of inter-tissue contacts results in 3D tissue morphogenesis.
全面分析形态发生过程中的细胞动态对于理解动物发育的原理至关重要。尽管近年来在光学显微镜方面取得了进展，但连续的细胞形状变化如何导致复杂的三维组织形态发生仍然在很大程度上未得到解决。我们使用活体成像研究了果蝇翅膀发育过程中的独特细胞结构，包括一个基于微管的膜突起网络。我们将这个网络命名为平面间阿玛达网络（IPAN），它连接着两个翅膀上皮层。最初，IPAN 通过基底突起维持着两层翅膀上皮细胞之间的细胞间接触。随后，IPAN 的解体涉及到这些接触的丧失，伴随着排列整齐的微管的退化。这些过程对于有丝分裂都是自主和非自主所必需的，从而导致两个翅膀上皮之间的组织协调增殖。我们的发现进一步表明，在 G2/M 转换期间，从非中心体微管到中心体微管组织中心（MTOC）的微管组织转换导致非中心体微管衍生的 IPAN 突起的解体。这些发现说明了细胞形状变化介导的组织间接触的丧失如何导致 3D 组织形态发生。
