A cell surface protein controls endocrine ring gland morphogenesis and steroid production

Pesch, Yanina-Yasmin; Hesse, Ricarda; Ali, Tariq; Behr, Matthias

doi:10.1016/j.ydbio.2018.10.007

Cited by 8 publications

(12 citation statements)

References 72 publications

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“…To further investigate which of the tracheal chitinases play a role in tube size expansion, we analyzed chitin in the trachea by using the Alexa488-linked chitin-binding probe (cbp). Besides, we used the Alexa633-linked wheat germ agglutinin (WGA), which is a lectin that detects sugar residues and therefore labels both chitinous structures and surfaces of tracheal cell membranes 8,9 . The tracheal-specific knockdown of cht2, cht5, cht6 genes, but not of cht7 and cht12, resulted in tubes with a sinusoidal appearance in the early stage of 17 embryos ( Figs.…”

Section: Resultsmentioning

confidence: 99%

“…After tube length determination has been completed, tracheal cells of embryos of stage 17 internalize the intraluminal chitin-cable contents 27,28,46 . This process requires the DnaJ domain protein Wurst for Clathrin heavy chain recruitment and the clathrin-mediated endocytosis of chitin-associated proteins 9,26,46 . In endocytosis mutant embryos, tubes do not remove extracellular proteins, such as Obst-A, Verm, Knk as well as chitin, from the lumen 9,26,27 .…”

Section: Resultsmentioning

confidence: 99%

“…This process requires the DnaJ domain protein Wurst for Clathrin heavy chain recruitment and the clathrin-mediated endocytosis of chitin-associated proteins 9,26,46 . In endocytosis mutant embryos, tubes do not remove extracellular proteins, such as Obst-A, Verm, Knk as well as chitin, from the lumen 9,26,27 . When expressing tracheal-specific RNAi of the cht2, cht5, and cht6 genes in embryos, we did not observe any luminal residues of Knk, Obst-A or Verm at the end of stage 17 as found in wurst or clathrin mutants (Figs.…”

Section: Resultsmentioning

confidence: 99%

“…Individual domain arrangement, which includes signal-peptides, catalytic-, and transmembrane-domains and chitin-binding domains, may cause functional differences among insect glycosylhydrolases family 18. Thus, members can be classified into eight groups 34 : The Drosophila Chitinases contain single (Cht2, 4,5,6,8,9,11,12) or more (Cht7, Cht1/Cht3/Cht10) catalytic Glyco18 domains, some possess a chitin-binding domain (Cht5,7,12) others a transmembrane domain (Cht7). In contrast, as Idgf proteins (group V) contain one Glyco18 domain, which lacks a critical glutamate residue, they do not possess chitinolytic activity 40 .…”

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confidence: 99%

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Glycosylhydrolase genes control respiratory tubes sizes and airway stability

Behr

Riedel

2020

Sci Rep

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tight barriers are crucial for animals. insect respiratory cells establish barriers through their extracellular matrices. These chitinous-matrices must be soft and flexible to provide ventilation, but also tight enough to allow oxygen flow and protection against dehydration, infections, and environmental stresses. However, genes that control soft, flexible chitin-matrices are poorly known. We investigated the genes of the chitinolytic glycosylhydrolase-family 18 in the tracheal system of Drosophila melanogaster. Our findings show that five chitinases and three chitinase-like genes organize the tracheal chitin-cuticles. Most of the chitinases degrade chitin from airway lumina to enable oxygen delivery. They further improve chitin-cuticles to enhance tube stability and integrity against stresses. Unexpectedly, some chitinases also support chitin assembly to expand the tube lumen properly. Moreover, Chitinase2 plays a decisive role in the chitin-cuticle formation that establishes taenidial folds to support tube stability. Chitinase2 is apically enriched on the surface of tracheal cells, where it controls the chitin-matrix architecture independently of other known cuticular proteins or chitinases. We suppose that the principle mechanisms of chitin-cuticle assembly and degradation require a set of critical glycosylhydrolases for flexible and not-flexible cuticles. The same glycosylhydrolases support thick laminar cuticle formation and are evolutionarily conserved among arthropods. Oxygen uptake is vital for all animals and an essential factor responsible for the limitation of fitness 1. Arthropods, especially insects, actively perform tracheal ventilation and diffusion to oxygenate their organs 2. The tracheal system is a hallmark of insects limiting their sizes, even in terms of giant evolutionary insects when hyperoxia occurred during the late Carboniferous and early Permian 3. The Drosophila respiratory system consists of multicellular and unicellular tubes. They together form a complex airway network that transfers oxygen to target tissues 4,5. Oxygen transport requires barriers to multicellular tracheal tubes. The intercellular diffusion barriers form at the lateral membrane by tight junctions analogous septate junctions (SJs), which prevent the paracellular flow of fluids across the tracheal epithelium into the lumina of the airways 6,7. Chitin-containing cuticles establish extracellular barriers against infections and to withstand tension forces 8,9. These include hydrophobic layers facing the lumen, which are impermeable to in-and outflux of fluids 10. Importantly, tracheal chitin-cuticles assemble to assist tube maturation and partially degrade in subsequent steps to support airway clearance during late embryogenesis 11. A crucial but less understood aspect is how the assembly and degradation of chitin-cuticles can occur 12 while maintaining protective barriers and integrity of the tubular system. Tracheal branching is genetically highly controlled and often evolutionarily conserved 13-17. After initial branc...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Glycosylhydrolase genes control respiratory tubes sizes and airway stability

Behr

Riedel

2020

Sci Rep

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“…Developmental changes are controlled by the endocrine system, and many hormones interact to regulate insect growth and development [ 3 ]. Among these, the ecdysteroid hormone ecdysone, produced by the prothoracic gland (PG), regulates molting and metamorphosis in its active form [ 4 , 5 , 6 ]. The function of ecdysone has also been studied in relation to embryonic development [ 7 ], ovary development [ 8 ], and silk gland development [ 9 ].…”

Section: Introductionmentioning

confidence: 99%

BmFoxO Gene Regulation of the Cell Cycle Induced by 20-Hydroxyecdysone in BmN-SWU1 Cells

Zhang

Yang

Chen

et al. 2020

Insects

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Ecdysteroid titer determines the state of the cell cycle in silkworm (Bombyxmori) metamorphosis. However, the mechanism of this process is unclear. In this study, we demonstrated that the BmFoxO gene participates in the regulation of the cell cycle induced by 20-Hydroxyecdysone (20E) in BmN-SWU1 cells. The 20E blocks the cell cycle in the G2/M phase through the ecdysone receptor (EcR) and inhibits DNA replication. The 20E can promote BmFoxO gene expression. Immunofluorescence and Western blot results indicated that 20E can induce BmFoxO nuclear translocation in BmN-SWU1 cells. Overexpression of the BmFoxO gene affects cell cycle progression, which results in cell cycle arrest in the G0/G1 phase as well as inhibition of DNA replication. Knockdown of the BmFoxO gene led to cell accumulation at the G2/M phase. The effect of 20E was attenuated after BmFoxO gene knockdown. These findings increase our understanding of the function of 20E in the regulation of the cell cycle in B. mori.

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The biology of insect chitinases and their roles at chitinous cuticles

Rabadiya,

Behr

2024

Insect Biochemistry and Molecular Biology

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A cell surface protein controls endocrine ring gland morphogenesis and steroid production

Cited by 8 publications

References 72 publications

Glycosylhydrolase genes control respiratory tubes sizes and airway stability

Glycosylhydrolase genes control respiratory tubes sizes and airway stability

BmFoxO Gene Regulation of the Cell Cycle Induced by 20-Hydroxyecdysone in BmN-SWU1 Cells

The biology of insect chitinases and their roles at chitinous cuticles

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