<i>Drosophila</i>Knickkopf and Retroactive are needed for epithelial tube growth and cuticle differentiation through their specific requirement for chitin filament organization

Moussian, Bernard; Tång, Erika; Tonning, Anna; Helms, Sigrun; Schwarz, Heinz; Nüsslein‐Volhard, Christiane; Uv, Anne

doi:10.1242/dev.02177

Cited by 152 publications

(164 citation statements)

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“…Because the chitin matrix requires renewal during larval molting, we analyzed essential modulators for chitin maturation and protection. It was shown that newly synthesized chitin is protected by the conserved glycosylphosphatidylinositol-anchored Knk (Knickkopf) protein for organization of the body wall cuticle in Tribolium and for cuticle texture in Drosophila trachea and epidermis (4,24,25). In wild type first instar larvae, Knk was found in the cuticle matrix, showing strong co-localization with chitin.…”

Section: Resultsmentioning

confidence: 99%

“…The antibodies used are ␣-Spectrin (1:10, mouse, Developmental Studies Hybridoma Bank), Knk (1:333; rabbit) (24), Obst-A (1:300; rabbit) (19), Serp (1:175; rabbit), and Verm (1:175; rabbit) (10). Primary antibodies were detected by secondary antibodies linked with fluorescent dyes (Dianova, Hamburg, Germany and Jackson ImmunoResearch Laboratories, West Grove, PA) and mounted in Vectashield (Vector Laboratories, Burlingame, CA).…”

Section: Methodsmentioning

confidence: 99%

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Obstructor A Organizes Matrix Assembly at the Apical Cell Surface to Promote Enzymatic Cuticle Maturation in Drosophila

Pesch

Riedel

Behr

2015

Journal of Biological Chemistry

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Background:The apical extracellular matrix (aECM) protects against environmental stresses that attack organisms throughout lifetime. Results: Epidermal cells secrete obstructor A into a core organizer region for controlling aECM assembly at the apical cell surface. Conclusion: Normal aECM assembly is mediated by obstructor A and regulates cuticle stability at the epidermis. Significance: Cuticle formation of the insect epidermis is genetically conserved.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Obstructor A Organizes Matrix Assembly at the Apical Cell Surface to Promote Enzymatic Cuticle Maturation in Drosophila

Pesch

Riedel

Behr

2015

Journal of Biological Chemistry

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“…Knk has subsequently been found to be essential for the normal laminar organization of endocuticle at embryonic stages of growth (10). However, the possible contributions of Knk to postembryonic cuticle morphogenesis were unknown.…”

Section: Resultsmentioning

confidence: 99%

Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton

Chaudhari

Arakane

Specht

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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During each molting cycle of insect development, synthesis of new cuticle occurs concurrently with the partial degradation of the overlying old exoskeleton. Protection of the newly synthesized cuticle from molting fluid enzymes has long been attributed to the presence of an impermeable envelope layer that was thought to serve as a physical barrier, preventing molting fluid enzymes from accessing the new cuticle and thereby ensuring selective degradation of only the old one. In this study, using the red flour beetle, Tribolium castaneum, as a model insect species, we show that an entirely different and unexpected mechanism accounts for the selective action of chitinases and possibly other molting enzymes. The molting fluid enzyme chitinase, which degrades the matrix polysaccharide chitin, is not excluded from the newly synthesized cuticle as previously assumed. Instead, the new cuticle is protected from chitinase action by the T. castaneum Knickkopf (TcKnk) protein. TcKnk colocalizes with chitin in the new cuticle and organizes it into laminae. Down-regulation of TcKnk results in chitinase-dependent loss of chitin, severe molting defects, and lethality at all developmental stages. The conservation of Knickkopf across insect, crustacean, and nematode taxa suggests that its critical roles in the laminar ordering and protection of exoskeletal chitin may be common to all chitinous invertebrates.RNAi | nikkomycin | phylogenetic tree | transmission electron microscopy | chitin synthase D uring development, insects must undergo periodic molting to accommodate growth and to overcome the rigid constraints imposed by portions of their chitinous exoskeletons (1, 2). This process entails the complete replacement of the entire outer shell of the insect, including digestion; resorption and recycling of the inner, more pliable layers; and shedding of the outer, more highly sclerotized and waterproofed layers, which are either discarded or, in some cases, ingested for further recycling (1-4). The molting process is hormonally initiated by 20-hydroxyecdysone and begins with the epidermis secreting what will become the outer layers of the new cuticle that separate the epidermal layer from the overlying old cuticle. An "apolytic space" then forms, separating new (inner) from old (outer) cuticles (5). With the delicate epidermis now protected by the first layers of new cuticle, the molting fluid in the apolytic space can digest the inner layers of the outer (old) cuticle. According to long-held dogma, protection of the new cuticle from degradation by molting fluid enzymes is conferred by a thin, nonchitinous envelope (previously termed the "cuticulin" layer or the "outer epicuticle") deposited by the epidermal cells just before the secretion of new cuticular chitin underneath (3). This envelope was believed to form a protective barrier against proteolytic and chitinolytic enzymes of the molting fluid, thereby confining their actions to the proximal layers of the old (outer) exoskeleton while preventing digestion of the newly deposit...

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“…The uniform expansion of tube diameter requires the formation of a transient luminal chitin-based matrix (Araujo et al, 2005;Moussian et al, 2006;Tonning et al, 2005;Devine et al, 2005) (reviewed by Swanson and Beitel, 2006) (see Fig. 6).…”

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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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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DrosophilaKnickkopf and Retroactive are needed for epithelial tube growth and cuticle differentiation through their specific requirement for chitin filament organization

Cited by 152 publications

References 42 publications

Obstructor A Organizes Matrix Assembly at the Apical Cell Surface to Promote Enzymatic Cuticle Maturation in Drosophila

Obstructor A Organizes Matrix Assembly at the Apical Cell Surface to Promote Enzymatic Cuticle Maturation in Drosophila

Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton

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

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