The<i>Drosophila</i>formin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton

Matusek, Tamás; Djiane, Alexandre; Jankovics, Ferenc; Brunner, Damian; Mlodzik, Marek; Mihály, József

doi:10.1242/dev.02266

Cited by 139 publications

(197 citation statements)

References 42 publications

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

confidence: 55%

“…Pri is essential for the formation of the specific F-actin bundles that prefigure the formation of the taenidial fold pattern of the tracheal cuticle. A novel formin with a similar role in actin organization has also been reported recently (Matusek et al, 2006).Although the accumulation of discrete apical luminal matrices has clearly emerged as a key feature in the proper regulation of branching morphogenesis in the developing tracheal system, it is also clear that these matrices have to be removed or remodelled before the tracheal system can take over its assigned function. 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).…”

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confidence: 57%

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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 Spacesupporting

confidence: 55%

mentioning

confidence: 57%

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

2008

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“…The dDAAM excision alleles, the UAS-FL-DAAM and UAS-C-DAAM transgenic flies were created as described by Matusek et al (2006). For the aims of the dominant interaction studies, we first created the following double mutant stocks: (1) CA and Sca-Gal4.…”

Section: Methodsmentioning

confidence: 99%

“…DNA constructs for transgenic flies and transfection experiments were created by standard cloning techniques. Whole-mount embryo RNA in situ hybridization was performed as described by Matusek et al (2006).…”

Section: Methodsmentioning

confidence: 99%

Formin Proteins of the DAAM Subfamily Play a Role during Axon Growth

Matusek¹,

Gombos²,

Szécsényi³

et al. 2008

J. Neurosci.

130

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The regulation of growth cone actin dynamics is a critical aspect of axonal growth control. Among the proteins that are directly involved in the regulation of actin dynamics, actin nucleation factors play a pivotal role by promoting the formation of novel actin filaments. However, the essential nucleation factors in developing neurons have so far not been clearly identified. Here, we show expression data, and use true loss-of-function analysis and targeted expression of activated constructs to demonstrate that the Drosophila formin DAAM plays a critical role in axonal morphogenesis. In agreement with this finding, we show that dDAAM is required for filopodia formation at axonal growth cones. Our genetic interaction, immunoprecipitation and protein localization studies argue that dDAAM acts in concert with Rac GTPases, Profilin and Enabled during axonal growth regulation. We also show that mouse Daam1 rescues the CNS defects observed in dDAAM mutant flies to a high degree, and vice versa, that Drosophila DAAM induces the formation of neurite-like protrusions when expressed in mouse P19 cells, strongly suggesting that the function of DAAM in developing neurons has been conserved during evolution.

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“…Hannemann et al (2008) described that FHOD1, associated to ROCK1 is required for the membrane blebbing, which is dependent on F-actin integrity. Also, mammalian and Drosophila formins perform different roles during development and differentiated cells (Homem and Pfeifer, 2009;Massarwa et al, 2009;Matusek et al, 2006Matusek et al, , 2008. Based on sequence similarity, it is reasonable to think that FHOS represents a new formin and that Fhos might be a new component of the FHOD subfamily, along with FHOS1/ FHOD1, both of them involved in cell death processes (Ménard et al, 2006).…”

Section: Fhos's Persistent Salivary Glands Exhibit Changes In the Actmentioning

confidence: 99%

Fhos encodes a Drosophila Formin‐Like Protein participating in autophagic programmed cell death

Anhezini

Saita

Costa

et al. 2012

Genesis

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Summary: Larval tissues undergo programmed cell death (PCD) during Drosophila metamorphosis. PCD is triggered in a stage and tissue-specific fashion in response to ecdysone pulses. The understanding of how ecdysone induces the stage and tissue-specificity of cell death remains obscure. Several steroid-regulated primary response genes have been shown to act as key regulators of cellular responses to ecdysone by inducing a cascade of transcriptional regulation of late responsive genes. In this article, the authors identify Fhos as a gene that is required for Drosophila larval salivary gland destruction. Animals with a P-element mutation in Fhos possess persistent larval salivary glands, and precise excisions of this P-element insertion resulted in reversion of this salivary gland mutant phenotype. Fhos encodes the Drosophila homolog of mammalian Formin Fhos. Fhos is differentially transcribed during development and responds to ecdysone in a method that is similar to other cell death genes. Similarly to what has been shown for its mammalian counterpart, FHOS protein is translocated to the nucleus at later stages of cell death. Fhos mutants posses disrupted actin cytoskeleton dynamics in persistent salivary glands. Together, our data indicate that Fhos is a new ecdysone-regulated gene that is crucial for changes in the actin cytoskeleton during salivary gland elimination in Drosophila. genesis 50:672-684, 2012. V V C 2012 Wiley Periodicals, Inc.

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TheDrosophilaformin DAAM regulates the tracheal cuticle pattern through organizing the actin cytoskeleton

Cited by 139 publications

References 42 publications

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

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

Formin Proteins of the DAAM Subfamily Play a Role during Axon Growth

Fhos encodes a Drosophila Formin‐Like Protein participating in autophagic programmed cell death

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