Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting

Centanin, Lázaro; Dekanty, Andrés; Romero, Nuria; Irisarri, Maximiliano; Gorr, Thomas A.; Wappner, Pablo

doi:10.1016/j.devcel.2008.01.020

Cited by 111 publications

(181 citation statements)

References 57 publications

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“…During larval stages, in response to hypoxia in surrounding tissues and within the cell itself (Centanin et al, 2008;Jarecki et al, 1999), terminal cells undergo extensive morphogenesis during which the single embryonically generated process undergoes iterative outgrowth and branching events, eventually producing a tree-like network emanating from each cell. By the end of the final larval stage, a typical terminal cell has between 30 and 100 subcellular branches, the longest of which extends over 200 µm (Fig.…”

Section: Introductionmentioning

confidence: 99%

Intracellular lumen formation in Drosophila proceeds via a novel subcellular compartment

Nikolova

Metzstein

2015

Development

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Cellular tubes have diverse morphologies, including multicellular, unicellular and subcellular architectures. Subcellular tubes are found prominently within the vertebrate vasculature, the insect breathing system and the nematode excretory apparatus, but how such tubes form is poorly understood. To characterize the cellular mechanisms of subcellular tube formation, we have refined methods of high pressure freezing/freeze substitution to prepare Drosophila larvae for transmission electron microscopic (TEM) analysis. Using our methods, we have found that subcellular tube formation may proceed through a previously undescribed multimembrane intermediate composed of vesicles bound within a novel subcellular compartment. We have also developed correlative light/TEM procedures to identify labeled cells in TEM-fixed larval samples. Using this technique, we have found that Vacuolar ATPase (V-ATPase) and the V-ATPase regulator Rabconnectin-3 are required for subcellular tube formation, probably in a step resolving the intermediate compartment into a mature lumen. In general, our ultrastructural analysis methods could be useful for a wide range of cellular investigations in Drosophila larvae.

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Section: Introductionmentioning

confidence: 99%

Intracellular lumen formation in Drosophila proceeds via a novel subcellular compartment

Nikolova

Metzstein

2015

Development

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“…Although Drosophila do not breathe discontinuously, they can alter convective oxygen delivery (Lehmann et al, 2000). Further, hypoxic exposure during development causes the induction of Hypoxia Inducible Factor (HIF), a transcription factor that mediates a variety of responses to hypoxia including tracheal proliferation and cell growth (Centanin et al, 2008;Lavista-Llanos et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Lifespan and oxidative stress show a non-linear response to atmospheric oxygen inDrosophila

Rascón

Harrison

2010

Journal of Experimental Biology

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SUMMARYOxygen provides the substrate for most ATP production, but also serves as a source of reactive oxygen species (ROS), which can induce cumulative macromolecular oxidative damage and cause aging. Pure oxygen atmospheres (100kPa) are known to strongly reduce invertebrate lifespan and induce aging-related physiological changes. However, the nature of the relationship between atmospheric oxygen, oxidative stress, and lifespan across a range of oxygen levels is poorly known. Developmental responses are likely to play a strong role, as prior research has shown strong effects of rearing oxygen level on growth, size and respiratory system morphology. In this study, we examined (1) the effect of oxygen on adult longevity and (2) the effect of the oxygen concentration experienced by larvae on adult lifespan by rearing Drosophila melanogaster in three oxygen atmospheres throughout larval development (10, 21 and 40kPa), then measuring the lifespan of adults in five oxygen tensions (2, 10, 21, 40, 100kPa). We also assessed the rate of protein carbonyl production for flies kept at 2, 10, 21, 40 and 100kPa as adults (all larvae reared in normoxia). The rearing of juveniles in varying oxygen treatments affected lifespan in a complex manner, and the effect of different oxygen tensions on adult lifespan was non-linear, with reduced longevity and heightened oxidative stress at extreme high and low atmospheric oxygen levels. Moderate hypoxia (10kPa) extended maximum, but not mean lifespan.

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“…Terminal cells are induced to branch by hypoxia, and normally tile on target tissues. However, terminal cells defective in gas transport permit the compensatory growth of neighboring terminal cells into undersupplied areas (Centanin et al, 2008;Jarecki et al, 1999). Our data uncover an unappreciated ability of autocellular tubeforming stalk cells to undergo ectopic growth and branching to compensate for terminal cells that are unable to sufficiently expand their apical membrane owing to genetic defect or injury.…”

Section: Discussionmentioning

confidence: 75%

Compensatory branching morphogenesis of stalk cells in the Drosophila trachea

Francis

Ghabrial

2015

Development

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Tubes are essential for nutrient transport and gas exchange in multicellular eukaryotes, but how connections between different tube types are maintained over time is unknown. In the Drosophila tracheal system, mutations in oak gall (okg) and conjoined (cnj) confer identical defects, including late onset blockage near the terminal cell-stalk cell junction and the ectopic extension of autocellular, seamed tubes into the terminal cell. We determined that okg and cnj encode the E and G subunits of the vacuolar ATPase (vATPase) and showed that both the V0 and V1 domains are required for terminal cell morphogenesis. Remarkably, the ectopic seamed tubes running along vATPasedeficient terminal cells belonged to the neighboring stalk cells. All vATPase-deficient tracheal cells had reduced apical domains and terminal cells displayed mislocalized apical proteins. Consistent with recent reports that the mTOR and vATPase pathways intersect, we found that mTOR pathway mutants phenocopied okg and cnj. Furthermore, terminal cells depleted for the apical determinants Par6 or aPKC had identical ectopic seamed tube defects. We thus identify a novel mechanism of compensatory branching in which stalk cells extend autocellular tubes into neighboring terminal cells with undersized apical domains. This compensatory branching also occurs in response to injury, with damaged terminal cells being rapidly invaded by their stalk cell neighbor.

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Cell Autonomy of HIF Effects in Drosophila: Tracheal Cells Sense Hypoxia and Induce Terminal Branch Sprouting

Cited by 111 publications

References 57 publications

Intracellular lumen formation in Drosophila proceeds via a novel subcellular compartment

Intracellular lumen formation in Drosophila proceeds via a novel subcellular compartment

Lifespan and oxidative stress show a non-linear response to atmospheric oxygen inDrosophila

Compensatory branching morphogenesis of stalk cells in the Drosophila trachea

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