Organogenesis of the Drosophila Respiratory System

Loganathan, Rajprasad; Cheng, Yim Ling; Andrew, Deborah J.

doi:10.1007/978-3-319-42767-6_6

Cited by 8 publications

(8 citation statements)

References 246 publications

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“…Tracheal system development has been studied extensively in the fruit fly Drosophila (Whitten 1980;Manning and Krasnow 1993;Samakovlis et al 1996a;Affolter and Caussinus 2008;Schottenfeld et al 2010;Loganathan et al 2016). During embryogenesis, the tracheal primordia appear as 10 pairs of tracheal placodes that invaginate into the body cavity while maintaining epithelial integrity, and undergo stereotyped branching and fusion processes to form a network of tubular epithelium (Figure 1).…”

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confidence: 99%

Development and Function of the Drosophila Tracheal System

Hayashi

Kondo

2018

Genetics

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The tracheal system of insects is a network of epithelial tubules that functions as a respiratory organ to supply oxygen to various target organs. Target-derived signaling inputs regulate stereotyped modes of cell specification, branching morphogenesis, and collective cell migration in the embryonic stage. In the postembryonic stages, the same set of signaling pathways controls highly plastic regulation of size increase and pattern elaboration during larval stages, and cell proliferation and reprograming during metamorphosis. Tracheal tube morphogenesis is also regulated by physicochemical interaction of the cell and apical extracellular matrix to regulate optimal geometry suitable for air flow. The trachea system senses both the external oxygen level and the metabolic activity of internal organs, and helps organismal adaptation to changes in environmental oxygen level. Cellular and molecular mechanisms underlying the high plasticity of tracheal development and physiology uncovered through research on are discussed.

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confidence: 99%

Development and Function of the Drosophila Tracheal System

Hayashi

Kondo

2018

Genetics

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“…Epithelial invagination is an important morphogenetic process in which three-dimensional tubular organs are formed from a two-dimensional flat sheet (Andrew and Ewald, 2010; Kondo and Hayashi, 2015; Sawyer et al, 2010), and the Drosophila trachea is a useful model system for analyzing three-dimensional epithelial morphogenesis (Hayashi and Kondo, 2018; Loganathan et al, 2016). Tracheal morphogenesis is initiated by placode specification; ten pairs of tracheal placodes form in the dorsal anterior part of the epidermis in each segment by stage 10, followed by invagination, branching and fusion (Figure 1A).…”

Section: Introductionmentioning

confidence: 99%

Two-step regulation of trachealess ensures tight coupling of cell fate with morphogenesis in the Drosophila trachea

Kondo

Hayashi

2019

eLife

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During organogenesis, inductive signals cause cell differentiation and morphogenesis. However, how these phenomena are coordinated to form functional organs is poorly understood. Here, we show that cell differentiation of the Drosophila trachea is sequentially determined in two steps and that the second step is synchronous with the invagination of the epithelial sheet. The master gene trachealess is dispensable for the initiation of invagination, while it is essential for maintaining the invaginated structure, suggesting that tracheal morphogenesis and differentiation are separately induced. trachealess expression starts in bipotential tracheal/epidermal placode cells. After invagination, its expression is maintained in the invaginated cells but is extinguished in the remaining sheet cells. A trachealess cis-regulatory module that shows both tracheal enhancer activity and silencer activity in the surface epidermal sheet was identified. We propose that the coupling of trachealess expression with the invaginated structure ensures that only invaginated cells canalize robustly into the tracheal fate.

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“…The tracheal (respiratory) system of Drosophila is a paradigm for the analysis of tubular organs [4]. After a morphogenetic phase by branching morphogenesis [5,6] the tracheal tubes mature and become physiologically active [7]. Tube maturation ensures the acquisition of the correct tube diameter and length, and of gas filling, critical steps for organ functional activity [3,8,9].…”

Section: Introductionmentioning

confidence: 99%

Anisotropic Crb accumulation, modulated by Src42A, is coupled to polarised epithelial tube growth in Drosophila

Olivares-Castiñeira

Llimargas

2018

PLoS Genet

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The control of the size of internal tubular organs, such as the lungs or vascular system, is critical for proper physiological activity and to prevent disease or malformations. This control incorporates the intrinsic physical anisotropy of tubes to generate proportionate organs that match their function. The exact mechanisms underlying tube size control and how tubular anisotropy is translated at the cellular level are still not fully understood. Here we investigate these mechanisms using the Drosophila tracheal system. We show that the apical polarity protein Crumbs transiently accumulates anisotropically at longitudinal cell junctions during tube elongation. We provide evidence indicating that the accumulation of Crumbs in specific apical domains correlates with apical surface expansion, suggesting a link between the anisotropic accumulation of Crumbs at the cellular level and membrane expansion. We find that Src42A is required for the anisotropic accumulation of Crumbs, thereby identifying the first polarised cell behaviour downstream of Src42A. Our results indicate that Src42A regulates a mechanism that increases the fraction of Crb protein at longitudinal junctions, and genetic interaction experiments are consistent with Crb acting downstream of Src42A in controlling tube size. Collectively, our results suggest a model in which Src42A would sense the inherent anisotropic mechanical tension of the tube and translate it into a polarised Crumbs accumulation, which may promote a bias towards longitudinal membrane expansion, orienting cell elongation and, as a consequence, longitudinal growth at the tissue level. This work provides new insights into the key question of how organ growth is controlled and polarised and unveils the function of two conserved proteins, Crumbs and Src42A, with important roles in development and homeostasis as well as in disease, in this biological process.

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Organogenesis of the Drosophila Respiratory System

Cited by 8 publications

References 246 publications

Development and Function of the Drosophila Tracheal System

Development and Function of the Drosophila Tracheal System

Two-step regulation of trachealess ensures tight coupling of cell fate with morphogenesis in the Drosophila trachea

Anisotropic Crb accumulation, modulated by Src42A, is coupled to polarised epithelial tube growth in Drosophila

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