Sequential Pulses of Apical Epithelial Secretion and Endocytosis Drive Airway Maturation in Drosophila

Tsarouhas, Vasilios; Senti, Kirsten-André; Jayaram, Satish Arcot; Tiklová, Katarína; Hemphälä, Johanna; Adler, Jeremy; Samakovlis, Christos

doi:10.1016/j.devcel.2007.06.008

Cited by 180 publications

(262 citation statements)

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“…Based on an elegant study combining live imaging and genetic analysis, it has been proposed that tube maturation comprises three distinct epithelial transitions (Tsarouhas et al, 2007). First, a secretion burst deposits luminal proteins into the luminal space, leading to the rapid expansion described above.…”

Section: From Branches To Functional Tubes: Regulating the Luminal Spacementioning

confidence: 99%

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Tracheal branching morphogenesis inDrosophila: new insights into cell behaviour and organ architecture

2008

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2055Our understanding of the molecular control of morphological processes has increased tremendously over recent years through the development and use of high resolution in vivo imaging approaches, which have enabled cell behaviour to be linked to molecular functions. Here we review how such approaches have furthered our understanding of tracheal branching morphogenesis in Drosophila, during which the control of cell invagination, migration, competition and rearrangement is accompanied by the sequential secretion and resorption of proteins into the apical luminal space, a vital step in the elaboration of the trachea's complex tubular network. We also discuss the similarities and differences between flies and vertebrates in branched organ formation that are becoming apparent from these studies. IntroductionBranching morphogenesis restructures epithelial sheets to give rise to organs of fascinating three-dimensional architecture, as exemplified by the adult lung, the kidney and the vasculature in humans. In Drosophila melanogaster, genetic studies have provided much insight into the regulatory networks that regulate the ordered formation of tracheal branches in the embryo, and into how the different branches coordinate their relative sizes, an issue that is of importance to the physical aspects of branched organ function (Affolter et al., 2003;Ghabrial et al., 2003;Uv et al., 2003). More recently, the development of live-imaging approaches in Drosophila have allowed researchers to take a deeper look at the behaviour of cells during the branching process, and have enabled events at the molecular level to be linked to the behaviour of individual cells or groups of cells.This combination of molecular genetics and live-imaging techniques has provided investigators with a unique opportunity to understand the morphological processes that occur during branching morphogenesis. This review focuses and builds on some of these recent insights, and assesses how they have led to a better understanding of the cellular and molecular processes that contribute to the transformation of simple, two-dimensional epithelial sheets into fascinating, three-dimensional tubular structures that can perform important functions in development and homeostasis. We focus here on the Drosophila tracheal system because several cellular and molecular paradigms, such as cell migration, competition and rearrangement, as well as the elaboration of a complex apical luminal environment, have recently been uncovered in this system that might serve related roles in the formation of other branched organs or tissues; these similarities might help us in the future to gain an even better understanding of how morphogenesis in general is regulated during development. Tracheal development in the fly embryoThe complex structure of the tracheal system consists of interconnected, metameric units of different-sized tubes that extend over the entire embryo shortly before hatching (Samakovlis et al., 1996b) (see Fig. 1, see also Movie 1 in the supplementary material)....

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Section: From Branches To Functional Tubes: Regulating the Luminal Spacementioning

confidence: 99%

“…In a second step, the solid luminal material is rapidly cleared from the lumen, and, shortly afterwards, the liquid is removed. Genetic studies implicate exo-and endocytosis components in lumen expansion and solid matrix clearance, respectively (Tsarouhas et al, 2007;Behr et al, 2007).…”

Section: From Branches To Functional Tubes: Regulating the Luminal Spacementioning

confidence: 99%

Tracheal branching morphogenesis inDrosophila: new insights into cell behaviour and organ architecture

2008

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“…2A). During this period, new apical membrane is added through apical secretion, and animals with impaired secretion fail to expand the tracheal lumen while completing many other morphogenetic processes [1,2]. Tracheal tube elongation is controlled independently of diametric expansion and requires the tyrosine kinase Src42 for polarized cell shape changes in the axial dimension of the tubes [4,5].…”

Section: Introductionmentioning

confidence: 99%

“…For instance, the addition of apical membrane to accommodate rapid lumen diameter expansion can be driven by exocytosis, as in the Drosophila tracheae [1,2], or by reshuffling of intracellular membrane to the apical surface, as in the excretory organ in C. elegans [3]. Oriented cell intercalation, cell division and cell elongation also participate in regulating lumen dimensions during size-maturation of the organ.…”

Section: Introductionmentioning

confidence: 99%

Luminal matrices: An inside view on organ morphogenesis

Luschnig

2014

Experimental Cell Research

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Tubular epithelia come in various shapes and sizes to accommodate the specific needs for transport, excretion and absorption in multicellular organisms. The intestinal tract, glandular organs and conduits for liquids and gases are all lined by a continuous layer of epithelial cells, which form the boundary of the luminal space. Defects in epithelial architecture and lumen dimensions will impair transport and can lead to serious organ malfunctions. Not surprisingly, multiple cellular and molecular mechanisms participate in controlling size and form of tubular epithelial structures. One intriguing aspect of epithelial organ formation is the coordinate behavior of individual cells as they mold the mature lumen. Here, we focus on recent findings, primarily from Drosophila, demonstrating that informative cues can emanate from the developing organ lumen in the form of solid luminal material. The luminal material is produced by the surrounding epithelium and helps to coordinate changes in shape and arrangement of the very same cells, resulting in correct lumen dimensions.

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“…Apical secretion of luminal contents precedes expansion of tube diameter and occurs in a sudden burst through COPI-, COPII-and Sec24-dependent membrane transport (Forster et al, 2010;Grieder et al, 2008;Jayaram et al, 2008;Tsarouhas et al, 2007) and is dependent on RhoDiaphanous-Myosin V transport (Massarwa et al, 2009). In addition to secretion of chitin, apical secretion may also play a role in tube length by contributing to apical membrane growth and/or targeting other as of yet unidentified, regulators of tube size to the luminal surface.…”

Section: Regulation Of Tracheal Tube/lumen Size and Shapementioning

confidence: 99%