Shaping of biological tubes by mechanical interaction of cell and extracellular matrix

Dong, Bo; Hayashi, Shigeo

doi:10.1016/j.gde.2015.02.009

Cited by 31 publications

(39 citation statements)

References 50 publications

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“…It has been shown in other tissues that different endosomal sorting pathways control Crb trafficking regulating its activity. While a fraction of the pool of internalised Crb protein undergoes degradation [8], Crb is also recycled back to the apical membrane through Rab11/ [39] Exo84 [40] or the Retromer complex [41,42] dependent pathways. We asked whether any of these pathways is required for Crb trafficking and recycling during tracheal development.…”

Section: Resultsmentioning

confidence: 99%

“…aECM) are coordinated rather than being two independent mechanisms controlling the same morphogenetic event. Indeed, some reports propose that the aECM may be anchored to the apical cell membrane through connecting proteins such as ZP proteins [7,8,61–63]. In such case, it still remains to be explained if these proteins transduce the signal to regulate Crb-mediated apical membrane growth.…”

Section: Discussionmentioning

confidence: 99%

“…Diametric/circumferential growth of tracheal tubes occurs at stage 14 and correlates with a pulse of secretion that ensures apical membrane growth and secretion of contents into the lumen [4,6]. This secreted luminal material, which includes chitin, chitin-associated proteins and ZP proteins like Pio-Pio and Dumpy, forms an apical extracellular matrix (aECM) that organises into an elastic filament [7,8]. This filament plays an important role in the control of the size and stability of the tracheal tubes [9,10].…”

Section: Introductionmentioning

confidence: 99%

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EGFR controls Drosophila tracheal tube elongation by intracellular trafficking regulation

Olivares-Castiñeira

Llimargas

2017

PLoS Genet

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Development is governed by a few conserved signalling pathways. Amongst them, the EGFR pathway is used reiteratively for organ and tissue formation, and when dysregulated can lead to cancer and metastasis. Given its relevance, identifying its downstream molecular machinery and understanding how it instructs cellular changes is crucial. Here we approach this issue in the respiratory system of Drosophila. We identify a new role for EGFR restricting the elongation of the tracheal Dorsal Trunk. We find that EGFR regulates the apical determinant Crb and the extracellular matrix regulator Serp, two factors previously known to control tube length. EGFR regulates the organisation of endosomes in which Crb and Serp proteins are loaded. Our results are consistent with a role of EGFR in regulating Retromer/WASH recycling routes. Furthermore, we provide new insights into Crb trafficking and recycling during organ formation. Our work connects cell signalling, trafficking mechanisms and morphogenesis and suggests that the regulation of cargo trafficking can be a general outcome of EGFR activation.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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EGFR controls Drosophila tracheal tube elongation by intracellular trafficking regulation

Olivares-Castiñeira

Llimargas

2017

PLoS Genet

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“…An area that warrants further attention is native matrix biology during tissue development, homeostasis and regeneration, including, but not limited to, dynamic properties, biological tubes and the active site architecture. Insights into this area will facilitate the generation of in vitro systems that accurately recapitulate the in vivo microenvironment and the subsequent the biomimetic design of biomaterials that can adapt to, or dynamically interact with, surrounding tissue, thereby promoting desirable cellular processes to ensure that natural function can be immediately replicated after the biomaterials' in vivo implantation [293,756,757]. Meanwhile, a fundamental understanding of ECM storage (cues and growth factors) could offer important cues about the nature of molecule–matrix interactions and improve the potency of current biopolymers in the presentation and delivery of multiple therapeutic agents for tissue engineering [101,102].…”

Section: Future Directions and Outlookmentioning

confidence: 99%

Advancing biomaterials of human origin for tissue engineering

Chen

Liu

2016

Progress in Polymer Science

925

513

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Biomaterials have played an increasingly prominent role in the success of biomedical devices and in the development of tissue engineering, which seeks to unlock the regenerative potential innate to human tissues/organs in a state of deterioration and to restore or reestablish normal bodily function. Advances in our understanding of regenerative biomaterials and their roles in new tissue formation can potentially open a new frontier in the fast-growing field of regenerative medicine. Taking inspiration from the role and multi-component construction of native extracellular matrices (ECMs) for cell accommodation, the synthetic biomaterials produced today routinely incorporate biologically active components to define an artificial in vivo milieu with complex and dynamic interactions that foster and regulate stem cells, similar to the events occurring in a natural cellular microenvironment. The range and degree of biomaterial sophistication have also dramatically increased as more knowledge has accumulated through materials science, matrix biology and tissue engineering. However, achieving clinical translation and commercial success requires regenerative biomaterials to be not only efficacious and safe but also cost-effective and convenient for use and production. Utilizing biomaterials of human origin as building blocks for therapeutic purposes has provided a facilitated approach that closely mimics the critical aspects of natural tissue with regard to its physical and chemical properties for the orchestration of wound healing and tissue regeneration. In addition to directly using tissue transfers and transplants for repair, new applications of human-derived biomaterials are now focusing on the use of naturally occurring biomacromolecules, decellularized ECM scaffolds and autologous preparations rich in growth factors/non-expanded stem cells to either target acceleration/magnification of the body's own repair capacity or use nature's paradigms to create new tissues for restoration. In particular, there is increasing interest in separating ECMs into simplified functional domains and/or biopolymeric assemblies so that these components/constituents can be discretely exploited and manipulated for the production of bioscaffolds and new biomimetic biomaterials. Here, following an overview of tissue auto-/allo-transplantation, we discuss the recent trends and advances as well as the challenges and future directions in the evolution and application of human-derived biomaterials for reconstructive surgery and tissue engineering. In particular, we focus on an exploration of the structural, mechanical, biochemical and biological information present in native human tissue for bioengineering applications and to provide inspiration for the design of future biomaterials.

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“…However, this filament is a transient structure and toward the end of embryogenesis it is completely cleared from the lumen (Moussian et al, ; Tsarouhas et al, ). Recent studies have identified the chitin filament as an elastic material coupled to the apical cell membrane and have reported that this coupling is required for tube length regulation (Dong and Hayashi, ). Overall, it has been proposed that the aECM, composed of the chitin filament and its associated proteins, participates in coordinating apical membrane growth and cell contractility.…”

Section: Different Stages Of Aecm Formation During Tube Morphogenesismentioning

confidence: 99%

Drosophilachitinous aECM and its cellular interactions during tracheal development

Öztürk-Çolak

Moussian

Araújo

2015

Developmental Dynamics

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The morphology of organs, and hence their proper physiology, relies to a considerable extent on the extracellular matrix (ECM) secreted by their cells. The ECM is a structure contributed to and commonly shared by many cells in an organism that plays an active role in morphogenesis. Increasing evidence indicates that the ECM not only provides a passive contribution to organ shape but also impinges on cell behaviour and genetic programmes. The ECM is emerging as a direct modulator of many aspects of cell biology, rather than as a mere physical network that supports cells. Here, we review how the apical chitinous ECM is generated in Drosophila trachea and how cells participate in the formation of this supracellular structure. We discuss recent findings on the molecular and cellular events that lead to the formation of this apical ECM (aECM) and how it is influenced and affects tracheal cell biology. Drosophila Cuticle, a Specialised ECM Apical extracellular matrices (aECMs) play crucial roles in organ physiology and morphogenesis and protect the animal against physical and chemical damage, infection, and dehydration. As in all insects, the cuticle of Drosophila is an aECM produced by the epidermis, and the tracheal, hind-, and foregut epithelia. This ECM is shed off and replaced during moulting and metamorphosis to accommodate growth and body and organ shape changes. Composed of chitin, proteins, lipids, and small organic molecules, the insect epidermal cuticle is formed by several plain horizontal layers, namely the outermost envelope, the protein-rich epicuticle, and the innermost chitinous procuticle (Locke, 2001;Moussian, 2010). The envelope consists of lipids and proteins of unknown sequence. The epicuticle harbours proteins that, likewise, are yet unexplored. In contrast, the procuticle has been studied extensively in the last decade. It contains chitin filaments that are arranged in parallel to form flat sheets, the so-called laminae. Laminae are stacked either helicoidally or not, depending the body region. Chitin organisation is considered to depend on chitin-binding proteins that are coded by several genes that differ between species. Recently, it was reported that the putative chitin-binding protein Obstructor-A (ObstA) recruits the chitin deacetlyses Verm, Serp, and Knk to the extracellular region adjacent to the apical plasma membrane for chitin organisation (Pesch et al., 2015).In the Drosophila tracheae, cuticle architecture is quite different. Instead of being plain, the tracheal cuticle runs as a spiral perpendicular to the tube axis. Layering of the spiral ridges, called taenidia, is simpler. Beneath the envelope, there is a very thin epicuticle. The chitinous procuticle does not have any visible ordered texture. In 1958, Michael Locke, based on extensive work on tracheal development in the bug Rhodnius prolixus, proposed that excessive expansion of the tracheal tubes and space restriction in the developing animal may cause a mechanical force that is responsible for tracheal cuticle taenidial foma...

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Shaping of biological tubes by mechanical interaction of cell and extracellular matrix

Cited by 31 publications

References 50 publications

EGFR controls Drosophila tracheal tube elongation by intracellular trafficking regulation

EGFR controls Drosophila tracheal tube elongation by intracellular trafficking regulation

Advancing biomaterials of human origin for tissue engineering

Drosophilachitinous aECM and its cellular interactions during tracheal development

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