Abstract
Multicellular tubes consist of polarized cells wrapped around a central lumen and are essential structures underlying many developmental and physiological functions. In Drosophila compound eyes, each ommatidium forms a luminal matrix, the inter-rhabdomeral space, to shape and separate the key phototransduction organelles, the rhabdomeres, for proper visual perception. In an enhancer screen to define mechanisms of retina lumen formation, we identified Actin5C as a key molecule. Our results demonstrate that the disruption of lumen formation upon the reduction of Actin5C is not linked to any discernible defect in microvillus formation, the rhabdomere terminal web (RTW), or the overall morphogenesis and basal extension of the rhabdomere. Second, the failure of proper lumen formation is not the result of previously identified processes of retinal lumen formation: Prominin localization, expansion of the apical membrane, or secretion of the luminal matrix. Rather, the phenotype observed with Actin5C is phenocopied upon the decrease of the individual components of non-muscle myosin II (MyoII) and its upstream activators. In photoreceptor cells MyoII localizes to the base of the rhabdomeres, overlapping with the actin filaments of the RTW. Consistent with the well-established roll of actomyosin-mediated cellular contraction, reduction of MyoII results in reduced distance between apical membranes as measured by a decrease in lumen diameter. Together, our results indicate the actomyosin machinery coordinates with the localization of apical membrane components and the secretion of an extracellular matrix to overcome apical membrane adhesion to initiate and expand the retinal lumen.
Highlights
Multicellular tubes are fundamental structures required for the transport of gases, liquids, or cells and are necessary for the generation and function of tissues and organs such as lung, kidney, blood vessels, neural tubes, and mammary gland
In an effort to investigate the mechanisms of Drosophila retinal lumen formation, we identified a contractile machinery that was present at the apical portion of photoreceptor cells
Our data is consistent with the idea that a contractile force contributes to the initial separation of the juxtaposed apical membranes and subsequent enlargement of the luminal space
Summary
Multicellular tubes are fundamental structures required for the transport of gases, liquids, or cells and are necessary for the generation and function of tissues and organs such as lung, kidney, blood vessels, neural tubes, and mammary gland. To construct a functional tube, there needs to be mechanisms to first generate a luminal space and regulate the expansion and determination of the final diametrical size of the lumen. Cells utilize multiple pathways to organize themselves to form an initial tubular network (reviewed in [1,2,3]) and likewise diametric luminal growth appears to be under precise genetic control [4]. To date lumen growth has been characterized as a process of directed and regulated apical secretion of components into a central space and a reorganization of the apical membrane. Secretion likely provides a mechanical expansion force that drives the diametrical growth of the tube lumen [5,6,7]. The fusion of secretory vesicles with apical plasma membranes often changes the cells apical domain antigens, which in return drive the expansion of apical membrane permitting an increase in the diameter of the lumen [4,11,12]
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
