A cellular process that includes asymmetric cytokinesis remodels the dorsal tracheal branches in Drosophila larvae

Abstract

Tubular networks are central to the structure and function of many organs, such as the vertebrate lungs or the Drosophila tracheal system. Their component epithelial cells are able to proliferate and to undergo complex morphogenetic movements, while maintaining their barrier function. Little is known about the details of the mitotic process in tubular epithelia. Our study presents a comprehensive model of cellular remodeling and proliferation in the dorsal branches of third-instar Drosophila larvae. Through a combination of immunostaining and novel live imaging techniques, we identify the key steps in the transition from a unicellular to a multicellular tube. Junctional remodeling precedes mitosis and, as the cells divide, new junctions are formed through several variations of what we refer to as 'asymmetric cytokinesis'. Depending on the spacing of cells along the dorsal branch, mitosis can occur either before or after the transition to a multicellular tube. In both instances, cell separation is accomplished through asymmetric cytokinesis, a process that is initiated by the ingression of the cytokinetic ring. Unequal cell compartments are a possible but rare outcome of completing mitosis through this mechanism. We also found that the Dpp signaling pathway is required but not sufficient for cell division in the dorsal branches.

Cell cycle dependent TGFβ-BMP antagonism regulates neural tube closure by modulating tight junctions

“…Thus, shifts in polarity, which facilitate shape changes might occur during mitosis and involve specific mitotic phases. But how polarity shifts might affect events during subsequent phases of the cell cycle is not understood, although novel mechanisms that correlate junctional remodeling with cytokinesis have been recently proposed (Denes et al, 2015).…”

Endothelial cell division in angiogenic sprouts of differing cellular architecture

“…Because of their three-dimensional structure, tubular networks have a more complex morphology than epithelial sheets. Therefore, the division of elongated and lumenized cells may require some adaptations of the mitotic machinery in order to accommodate their peculiar geometry as was recently shown in a study of the Drosophila larval trachea system ( Denes et al, 2015 ). While the actomyosin rings that drive cytokinesis in the Drosophila epithelia are able to symmetrically deform the AJs of the two cells that flank the emerging junction ( Founounou et al, 2013 ; Guillot and Lecuit, 2013 ; Herszterg et al, 2013 ), during cytokinesis in tracheal tubes, the membrane furrows asymmetrically on the side of the cell that is proximal to the nucleus, and the new junction then extends around the lumen until it connects and fuses with another membrane.…”

“…While the actomyosin rings that drive cytokinesis in the Drosophila epithelia are able to symmetrically deform the AJs of the two cells that flank the emerging junction ( Founounou et al, 2013 ; Guillot and Lecuit, 2013 ; Herszterg et al, 2013 ), during cytokinesis in tracheal tubes, the membrane furrows asymmetrically on the side of the cell that is proximal to the nucleus, and the new junction then extends around the lumen until it connects and fuses with another membrane. We found that in the remodeling dorsal tracheal branches, such asymmetric de novo junction formation is the norm, presumably because the specific geometry and the rigidity of the tubes favor this outcome ( Denes et al, 2015 ).…”

Tricellular junction proteins promote disentanglement of daughter and neighbour cells during epithelial cytokinesis

“…The coordination between de novo junction formation and cell division is a general feature of monolayered tissues (Denes et al, 2015; Firmino et al, 2016; Founounou et al, 2013; Herszterg et al, 2013; Higashi et al, 2016; Jinguji and Ishikawa, 1992; Lau et al, 2015; Morais-De-Sá and Sunkel, 2013; Pinheiro et al, 2017; Reinsch and Karsenti, 1994). The coordination of TCJ formation and cytokinesis leading to the formation of a neighbour-neighbour interface has been elegantly studied in the epithelium of the gastrulating Xenopus embryo.…”