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

Pesch, Yanina-Yasmin; Riedel, Dietmar; Behr, Matthias

doi:10.1074/jbc.m114.614933

Cited by 61 publications

(83 citation statements)

References 39 publications

(73 reference statements)

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“…In this light, it is noteworthy that other exoskeleton components have recently been implicated in the regulation of tissue and body shapes. For example, some cuticular proteins are involved in the regulation of tracheal morphology and/or larval body shapes in Drosophila [6][21][22], and the control of the Drosophila adult wing shape requires the function of cuticle-related molecules, such as a transmembrane protein mediating the cell-cuticle attachment, an enzyme potentially involved in cross-linking of cuticle components, and genes specifically expressed during cuticle formation [23][24][25][26]. Changes in sequences or expression patterns of patterning genes (encoding morphogens and transcription factors) should often have pleiotropic effects that affect viability of the organism.…”

Section: Discussionmentioning

confidence: 99%

Mechanical Control of Whole Body Shape by a Single Cuticular Protein Obstructor-E in Drosophila melanogaster

et al. 2017

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Body shapes are much more variable than body plans. One way to alter body shapes independently of body plans would be to mechanically deform bodies. To what extent body shapes are regulated physically, or molecules involved in physical control of morphogenesis, remain elusive. During fly metamorphosis, the cuticle (exoskeleton) covering the larval body contracts longitudinally and expands laterally to become the ellipsoidal pupal case (puparium). Here we show that Drosophila melanogaster Obstructor-E (Obst-E) is a protein constituent of the larval cuticle that confers the oriented contractility/expandability. In the absence of obst-E function, the larval cuticle fails to undergo metamorphic shape change and finally becomes a twiggy puparium. We present results indicating that Obst-E regulates the arrangement of chitin, a long-chain polysaccharide and a central component of the insect cuticle, and directs the formation of supracellular ridges on the larval cuticle. We further show that Obst-E is locally required for the oriented shape change of the cuticle during metamorphosis, which is associated with changes in the morphology of those ridges. Thus, Obst-E dramatically affects the body shape in a direct, physical manner by controlling the mechanical property of the exoskeleton.

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Section: Discussionmentioning

confidence: 99%

Mechanical Control of Whole Body Shape by a Single Cuticular Protein Obstructor-E in Drosophila melanogaster

et al. 2017

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“…Here, nascent chitin fibres are deposited where they are supposed to interact with the chitin-organizing factor Knk, the chitin-binding protein Obst-A and the CDAs Serp and Verm (Petkau et al, 2012;Pesch et al, 2015;. Here, nascent chitin fibres are deposited where they are supposed to interact with the chitin-organizing factor Knk, the chitin-binding protein Obst-A and the CDAs Serp and Verm (Petkau et al, 2012;Pesch et al, 2015;.…”

Section: Site-autonomous Function Of Cdas In the Locustmentioning

confidence: 99%

“…In the fruit fly, Drosophila melanogaster, the putative CDAs Serpentine (Serp, CDA1) and Vermiform (Verm, CDA2) are expressed and secreted in the tracheal system, where they are involved in the assembly of a luminal chitin rod and the regulation of tracheal tube length (Luschnig et al, 2006;Wang et al, 2006). In this context, Serp and Verm localize to the extracellular region adjacent to the apical plasma membrane of epidermal cells called the assembly zone, where they cooperate with the chitin-binding proteins Obst-A and Knickkopf (Knk) to organize chitin fibres (Petkau et al, 2012;Pesch et al, 2015;. In this context, Serp and Verm localize to the extracellular region adjacent to the apical plasma membrane of epidermal cells called the assembly zone, where they cooperate with the chitin-binding proteins Obst-A and Knickkopf (Knk) to organize chitin fibres (Petkau et al, 2012;Pesch et al, 2015;.…”

Section: Introductionmentioning

confidence: 99%

LmCDA1 organizes the cuticle by chitin deacetylation in Locusta migratoria

Liu

Zhao

et al. 2018

Insect Molecular Biology

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Cells produce an extracellular matrix (ECM) with a stereotypic organization that is important for tissue function. The insect cuticle is a layered ECM that mainly consists of the polysaccharide chitin and associated proteins adopting a quasi‐crystalline structure. Our understanding of the molecular mechanisms deployed during construction of the highly ordered protein–chitin ECM so far is limited. In this study, we report on the role of the chitin deacetylase 1 (LmCDA1) in the organization of the protein–chitin ECM in the migratory locust Locusta migratoria, and LmCDA1 localizes predominantly to the apical tier of the protein–chitin ECM, but it is also found in lower regions. Reduction of LmCDA1 function correlates with lower amounts of chitin and impedes conversion of chitin to chitosan by deacetylation. Establishment of the quasi‐crystalline architecture of the protein–chitin ECM is, however, independent of LmCDA1 activity, but it is dependent on another chitin deacetylase, LmCDA2, which has no detectable effects on chitin deacetylation and, as shown previously, no influence on chitin content. Our data reveal that LmCDA1 and LmCDA2 act in parallel and independently from each other in defining the dimensions of the cuticle. Both enzymes are non‐uniformly distributed within the protein–chitin matrix, suggesting a site‐autonomous function.

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“…Obstructor‐A is a secretory protein produced by epidermal cells and enriched in the apical assembly zone. Its ability to interact with chitin, the cuticle modifier protein Knickkopf, and chitin deacetylase suggests the formation of a matrix‐scaffold that coordinates the trafficking and localization of proteins in the assembly zone, leading to the maturation and stabilization of the apical cell matrix (Petkau et al ., ; Pesch et al ., ). Mutations to obstructor‐A result in severe defects in moulting, wound protection, tube expansion and assembly zone formation (Tiklová et al ., ; Pesch et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Studies on the chitin/chitosan binding properties of six cuticular proteins analogous to peritrophin 3 from Bombyx mori

Ren

Liu

et al. 2017

Insect Molecular Biology

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Chitin deacetylation is required to make the cuticle rigid and compact through chitin chain crosslinking. Thus it is presumed that specialized proteins are required to bind deacetylated chitin chains together. However, deacetylated-chitin binding proteins have not ever been reported. In a previous work, six cuticular proteins analogous to peritrophin 3 (CPAP3s) were found to be abundant in the moulting fluid of Bombyx mori. In this study, these BmCPAP3s (BmCPAP3-A1, BmCPAP3-A2, BmCPAP3-B, BmCPAP3-C, BmCPAP3-D1 and BmCPAP3-D2) were cloned and expressed in Escherichia coli and purified using metal-chelating affinity chromatography. Their binding activities demonstrated that although all of the BmCPAP3s showed similar binding abilities toward crystalline chitin and colloidal chitin, they differed in their affinities toward partially and fully deacetylated chitin. Amongst them, BmCPAP3-D1 exhibited the highest binding activity toward deacetylated chitin. The gene expression pattern of BmCPAP3-D1 was similar to BmCPAP3-A1 and BmCPAP3-C at most stages except that it was dramatically upregulated at the beginning of the pupa to adult transition stage. This work is the first report of a chitin-binding protein, BmCPAP3-D1, which exhibits high binding affinity to deacetylated chitin.

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

Cited by 61 publications

References 39 publications

Mechanical Control of Whole Body Shape by a Single Cuticular Protein Obstructor-E in Drosophila melanogaster

Mechanical Control of Whole Body Shape by a Single Cuticular Protein Obstructor-E in Drosophila melanogaster

LmCDA1 organizes the cuticle by chitin deacetylation in Locusta migratoria

Studies on the chitin/chitosan binding properties of six cuticular proteins analogous to peritrophin 3 from Bombyx mori

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