<i>Drosophila</i>as a Model for Neuroendocrine Control of Renal Homeostasis

Dow, Julian A. T.; Halberg, Kenneth A.; Terhzaz, Selim; Davies, Shireen A.

doi:10.1002/9781119391128.ch4

Cited by 13 publications

(15 citation statements)

References 44 publications

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“…The metabolically active principal cell is thus sheltered from these very high, and potentially disruptive, fluxes of water. Given the severe consequences of unregulated fluid loss to a small terrestrial insect, it is not surprising that the tubule is under sophisticated neurohormonal control (53). Whereas cation pumping by the principal cells is under control of DH31 (54), DH44 (55), and Capa (56) neuropeptides, the stellate cells are independently controlled by the neuropeptide kinin (21,57) and by the biogenic amine tyramine (19); both act indistinguishably through intracellular calcium (19,58).…”

Section: Knockdown Of Aqps Reduces Fluid Transport and Impacts Survivalmentioning

confidence: 99%

Specialized stellate cells offer a privileged route for rapid water flux in Drosophila renal tubule

Cabrero

Terhzaz

Dornan

et al. 2020

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

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Insects are highly successful, in part through an excellent ability to osmoregulate. The renal (Malpighian) tubules can secrete fluid faster on a per-cell basis than any other epithelium, but the route for these remarkable water fluxes has not been established. In Drosophila melanogaster, we show that 4 genes of the major intrinsic protein family are expressed at a very high level in the fly renal tissue: the aquaporins (AQPs) Drip and Prip and the aquaglyceroporins Eglp2 and Eglp4. As predicted from their structure, and by their transport function by expressing these proteins in Xenopus oocytes, Drip, Prip, and Eglp2 show significant and specific water permeability, whereas Eglp2 and Eglp4 show very high permeability to glycerol and urea. Knockdowns of any of these genes result in impaired hormone-induced fluid secretion. The Drosophila tubule has 2 main secretory cell types: active cation-transporting principal cells, wherein the aquaglyceroporins localize to opposite plasma membranes, and small stellate cells, the site of the chloride shunt conductance, with these AQPs localizing to opposite plasma membranes. This suggests a model in which osmotically obliged water flows through the stellate cells. Consistent with this model, fluorescently labeled dextran, an in vivo marker of membrane water permeability, is trapped in the basal infoldings of the stellate cells after kinin diuretic peptide stimulation, confirming that these cells provide the major route for transepithelial water flux. The spatial segregation of these components of epithelial water transport may help to explain the unique success of the higher insects in regulating their internal environments.

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Section: Knockdown Of Aqps Reduces Fluid Transport and Impacts Survivalmentioning

confidence: 99%

Specialized stellate cells offer a privileged route for rapid water flux in Drosophila renal tubule

Cabrero

Terhzaz

Dornan

et al. 2020

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

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show abstract

“…Given the severe consequences of unregulated fluid loss to a small terrestrial insect, it is not surprising that the tubule is under sophisticated neurohormonal control (47). Whereas cation pumping by the principal cells is under control of DH31 (48), DH44 (49) and Capa (50) neuropeptides, the stellate cells are independently controlled by the neuropeptide kinin (19, 51) and by the biogenic amine tyramine (17); both act indistinguishably through intracellular calcium (17, 52).…”

Section: Resultsmentioning

confidence: 99%

When two cells are better than one: specialized stellate cells provide a privileged route for uniquely rapid water flux inDrosophilarenal tubule

Cabrero¹,

Terhzaz²,

Dornan³

et al. 2019

Preprint

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Insects are highly successful, in part through an excellent ability to osmoregulate. The renal (Malpighian) tubules can secrete fluid faster on a per-cell basis than any other epithelium, but the route for these remarkable water fluxes has not been established. In Drosophila melanogaster, we show that 4 members of the Major Intrinsic Protein family are expressed at very high level in the fly renal tissue; the aquaporins Drip and Prip, and the aquaglyceroporins Eglp2 and Eglp4. As predicted from their structure and by their transport function by expressing these proteins in Xenopus oocytes, Drip, Prip and Eglp2 show significant and specific water permeability, whereas Eglp2 and Eglp4 show very high permeability to glycerol and urea. Knockdowns of any of these genes impacts tubule performance resulting in impaired hormone-induced fluid secretion. The Drosophila tubule has two main secretory cell types: active cation-transporting principal cells with the aquaglyceroporins localize to opposite plasma membranes and small stellate cells, the site of the chloride shunt conductance, with these aquaporins localising to opposite plasma membranes. This suggests a model in which cations are pumped by the principal cells, causing chloride to follow through the stellate cells in order to balance the charge. As a consequence, osmotically obliged water follows through the stellate cells. Consistent with this model, fluorescently labelled dextran, an in vivo marker of membrane water permeability, is trapped in the basal infoldings of the stellate cells after kinin diuretic peptide stimulation, confirming that these cells provide the major route for transepithelial water flux. The spatial segregation of these components of epithelial water transport may help to explain the unique success of the higher insects.Significance statementThe tiny insect renal (Malpighian) tubule can transport fluid at unparalleled speed, suggesting unique specialisations. Here we show that strategic allocation of Major Intrinsic Proteins (MIPs) to specific cells within the polarized tubule allow the separation of metabolically intense active cation transport from chloride and water conductance. This body plan is general to at least many higher insects, providing a clue to the unique success of the class Insecta.

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“…Furthermore, we demonstrate that at least some of these processes could be modulated by cAMP, as addition of the cAMP-stimulator 8-bromo cAMP greatly increased reabsorption of both fluid and cations, particularly K + . Increased intracellular concentrations of cAMP are a typical response to several forms of neuroendocrine stimulation (Coast et al, 2002;Dow et al, 2018;Phillips and Audsley, 1995) and these findings therefore indicate a potential for humoral regulation of hindgut reabsorption, although a multitude of cellular mechanisms are modulated via this pathway. Nonetheless, we found evidence that at least some of the transporters involved in 5.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, our hindgut assay allows for measurement of bulk fluid transport. The development and optimization of the Ramsay assay paved the way for a multitude of mechanistic and comparative studies of excretory epithelia and we hope this hindgut assay will inspire future research on the role of reabsorptive epithelial function (Beyenbach et al, 2010;Dow and Davies, 2003;Dow et al, 2018;Halberg et al, 2015;Wheeler and Coast, 1990).…”

Section: Discussionmentioning

confidence: 99%

Maintenance of hindgut reabsorption during cold exposure is a key adaptation for Drosophila cold tolerance

Andersen

Overgaard

2020

Journal of Experimental Biology

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Maintaining extracellular osmotic and ionic homeostasis is crucial for organismal function. In insects, hemolymph volume and ion content is regulated by the secretory Malpighian tubules and reabsorptive hindgut. When exposed to stressful cold, homeostasis is gradually disrupted, characterized by a debilitating increase in extracellular K + concentration (hyperkalemia). Accordingly, studies have found a strong link between species-specific cold tolerance and the ability to maintain ion and water homeostasis at low temperature. This is also true for drosophilids where inter-and intra-specific differences in cold tolerance are linked to the secretory capacity of Malpighian tubules. There is, however, little information on the reabsorptive capacity of the hindgut in Drosophila. To address this, we developed a novel method that permits continuous measurements of hindgut ion and fluid reabsorption in Drosophila. We demonstrate that this assay is temporally stable (∼2 h) and responsive to cAMP stimulation and pharmacological intervention in accordance with the current insect hindgut reabsorption model. We then investigated how cold acclimation or cold adaptation affected hindgut reabsorption at benign (24°C) and low temperature (3°C). Cold-tolerant Drosophila species and cold-acclimated D. melanogaster maintain superior fluid and Na + reabsorption at low temperature. Furthermore, cold adaptation and acclimation caused a relative reduction in K + reabsorption at low temperature. These characteristic responses of cold adaptation/ acclimation will promote maintenance of ion and water homeostasis at low temperature. Our study of hindgut function therefore provides evidence that adaptations in the osmoregulatory capacity of insects are critical for their ability to tolerate cold.

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Drosophilaas a Model for Neuroendocrine Control of Renal Homeostasis

Cited by 13 publications

References 44 publications

Specialized stellate cells offer a privileged route for rapid water flux in Drosophila renal tubule

Specialized stellate cells offer a privileged route for rapid water flux in Drosophila renal tubule

When two cells are better than one: specialized stellate cells provide a privileged route for uniquely rapid water flux inDrosophilarenal tubule

Maintenance of hindgut reabsorption during cold exposure is a key adaptation for Drosophila cold tolerance

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