Single-cell branching morphogenesis in the Drosophila trachea

Best, Benedikt T.

doi:10.1016/j.ydbio.2018.12.001

Cited by 23 publications

(34 citation statements)

References 93 publications

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“…This led us to a quantitative 505 approach, scoring the frequency of morphological abnormalities/features per 506 branch. 507 Those Rabs whose depletion caused strong reductions in branch numbers (Rab6 508 and Rab8) were also associated with the most severe phenotypes in their 509 subcellular tubes, consistent with our previous conclusion that TCs' ability to form 510 branches depends on their ability to form proper tubes (reviewed in Best, 2019). 511…”

Section: Involvement Of Rabs In Terminal Cell Morphogenesis 497supporting

confidence: 79%

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Multiple requirements for Rab GTPases in the development ofDrosophilatracheal dorsal branches and terminal cells

Best

Leptin

2019

Preprint

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14Biosciences 15 Correspondence to M.L., Abstract 18The tracheal epithelium in fruit fly larvae is a popular model for multi-and unicellular 19 migration and morphogenesis. Like all epithelial cells, tracheal cells use Rab 20GTPases to organise their internal membrane transport, resulting in the specific 21 localisation or secretion of proteins on the apical or basal membrane compartments. 22Some contributions of Rabs to junctional remodelling and governance of tracheal 23 lumen contents are known, but it is reasonable to assume that they play important 24 further roles in morphogenesis. This pertains in particular to terminal tracheal cells, 25 specialised branch-forming cells that drastically reshape both their apical and basal 26 membrane during the larval stages. We performed a loss-of-function screen in the 27 tracheal system, knocking down endogenously tagged alleles of 26 Rabs by 28 targeting the tag via RNAi. This revealed that at least 14 Rabs are required to 29 ensure proper cell fate specification and migration of the dorsal branches, as well as 30 their epithelial fusion with the contralateral dorsal branch. The screen implicated four 31 Rabs in the subcellular morphogenesis of terminal cells themselves. Further tests 32suggested residual gene function after knockdown, leading us to discuss the 33 limitations of this approach. We conclude that more Rabs than identified here may 34 be important for tracheal morphogenesis, and that the tracheal system offers great 35 opportunities for studying several Rabs that have barely been characterised so far. 36

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Section: Involvement Of Rabs In Terminal Cell Morphogenesis 497supporting

confidence: 79%

“…Virtually every cellular pathway that has been studied in TCs, when perturbed, is 318 associated with changes in the number of branches (Best, 2019). We therefore 319 consider branch number an unspecific phenotype that reflects overall TC "health".…”

Section: Rabs Required For Terminal Cell Morphogenesis 309mentioning

confidence: 99%

Multiple requirements for Rab GTPases in the development ofDrosophilatracheal dorsal branches and terminal cells

Best

Leptin

2019

Preprint

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“…neurons or trachea) in regulating tracheal dynamics. Surprisingly, we found the transcription factor Sima/Hif-1, which promotes tracheal growth in response to changing O 2 conditions (Best, 2019), is also required for normal levels of astrocyte microdomain Ca 2+ transients. It appears that one effect of astrocyte microdomain Ca 2+ signaling is to feed back to suppress overall tracheal filopodial growth, perhaps thereby lowering O 2 delivery and avoiding hyperoxia.…”

Section: Discussionmentioning

confidence: 71%

TrpML-mediated astrocyte microdomain Ca²⁺ transients regulate astrocyte-tracheal interactions

Freeman

2019

Preprint

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Astrocytes exhibit spatially-restricted near membrane microdomain Ca 2+ transients in their fine processes. How these transients are generated, and how they regulate brain function in vivo remain unclear. Here we show that Drosophila astrocytes exhibit spontaneous, activity-independent microdomain Ca 2+ transients in their fine processes.Astrocyte microdomain Ca 2+ transients are mediated by the TRP channel TrpML, stimulated by reactive oxygen species (ROS), and can be enhanced in frequency by tyramine via the TyrRII receptor. Interestingly, astrocyte microdomain Ca 2+ transients are closely associated with tracheal elements, which dynamically extend filopodia throughout the nervous system, and astrocyte microdomain Ca 2+ transients precede retraction of tracheal filopodia. Loss of TrpML leads to increased tracheal filopodial numbers and growth, and increased ROS in the CNS. Basal levels of astrocyte microdomain Ca 2+ transient signaling were regulated by the hypoxia-sensitive factor Sima/Hif-1, providing a link between astrocyte-tracheal interactions and the molecular control of CNS gas exchange. We propose that local ROS production regulates tracheal dynamics through TrpML-dependent modulation of astrocyte microdomain Ca 2+ transients, and in turn CNS gas exchange.

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“…Virtually every cellular pathway that has been studied in TCs, when perturbed, is associated with changes in the number of branches (Best 2019). We therefore consider branch number an unspecific phenotype that reflects overall TC "health".…”

Section: Rabs Required For Terminal Cell Morphogenesismentioning

confidence: 99%

“…We counted the number of branches per TC depleted for each Rab via YRab-YFPi. This reflects overall cell health (Best 2019). Left: Dotplots with one dot for each TC and bars showing mean 6 SD.…”

Section: Rabs Required For Terminal Cell Morphogenesismentioning

confidence: 99%

Multiple Requirements for Rab GTPases in the Development ofDrosophilaTracheal Dorsal Branches and Terminal Cells

Best

Leptin

2020

G3 Genes|Genomes|Genetics

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The tracheal epithelium in fruit fly larvae is a popular model for multi- and unicellular migration and morphogenesis. Like all epithelial cells, tracheal cells use Rab GTPases to organize their internal membrane transport, resulting in the specific localization or secretion of proteins on the apical or basal membrane compartments. Some contributions of Rabs to junctional remodelling and governance of tracheal lumen contents are known, but it is reasonable to assume that they play important further roles in morphogenesis. This pertains in particular to terminal tracheal cells, specialized branch-forming cells that drastically reshape both their apical and basal membrane during the larval stages. We performed a loss-of-function screen in the tracheal system, knocking down endogenously tagged alleles of 26 Rabs by targeting the tag via RNAi. This revealed that at least 14 Rabs are required to ensure proper cell fate specification and migration of the dorsal branches, as well as their epithelial fusion with the contralateral dorsal branch. The screen implicated four Rabs in the subcellular morphogenesis of terminal cells themselves. Further tests suggested residual gene function after knockdown, leading us to discuss the limitations of this approach. We conclude that more Rabs than identified here may be important for tracheal morphogenesis, and that the tracheal system offers great opportunities for studying several Rabs that have barely been characterized so far.

show abstract

Single-cell branching morphogenesis in the Drosophila trachea

Cited by 23 publications

References 93 publications

Multiple requirements for Rab GTPases in the development ofDrosophilatracheal dorsal branches and terminal cells

Multiple requirements for Rab GTPases in the development ofDrosophilatracheal dorsal branches and terminal cells

TrpML-mediated astrocyte microdomain Ca²⁺ transients regulate astrocyte-tracheal interactions

Multiple Requirements for Rab GTPases in the Development ofDrosophilaTracheal Dorsal Branches and Terminal Cells

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Single-cell branching morphogenesis in the Drosophila trachea

Cited by 23 publications

References 93 publications

Multiple requirements for Rab GTPases in the development ofDrosophilatracheal dorsal branches and terminal cells

Multiple requirements for Rab GTPases in the development ofDrosophilatracheal dorsal branches and terminal cells

TrpML-mediated astrocyte microdomain Ca2+ transients regulate astrocyte-tracheal interactions

Multiple Requirements for Rab GTPases in the Development ofDrosophilaTracheal Dorsal Branches and Terminal Cells

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TrpML-mediated astrocyte microdomain Ca²⁺ transients regulate astrocyte-tracheal interactions