Programmed disassembly of a microtubule-based membrane protrusion network coordinates 3D epithelial morphogenesis in Drosophila

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. Synopsis During Drosophila pupal wing development, the dorsal and ventral epithelial layers form cytoskeleton-based protrusions that interconnect the two tissue layers. Here, in vivo live imaging of the pupal wing links the dynamics of these protrusions, named here Interplanar Amida Network (IPAN), to the coordination of cell divisions across the two epithelial leaflets. Basal microtubule-based protrusions of the IPAN sustain cell–cell contacts between the dorsal and ventral epithelia. IPAN disassembly at the G2/M transition releases cell–cell contacts. Loss of cell–cell contact affects mitosis in both the dorsal and ventral epithelia in a coordinated manner. Microtubule-rich protrusions form contacts between two epithelial leaflets to coordinate mitosis in the developing Drosophila wing.