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

Cabrero, P. , Terhzaz, S. , Dornan, A. J. , Ghimire, S., Holmes, H. L., Turin, D. R., Romero, M. F., Davies, S. and Dow, J. A.T. (2020) Specialized stellate cells offer a privileged route for rapid water flux in Drosophila renal tubule. Proceedings of the National Academy of Sciences of the United States of America, 117(3), pp. 1779-1787. (doi: 10.1073/pnas.1915943117) (PMID:31907321)

[img]
Preview
Text
205426.pdf - Published Version
Available under License Creative Commons Attribution.

1MB

Abstract

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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Cabrero, Mr Pablo and Dow, Professor Julian and Dornan, Dr Anthony and Ghimire, Mr Saurav and Terhzaz, Dr Selim and Davies, Professor Shireen
Authors: Cabrero, P., Terhzaz, S., Dornan, A. J., Ghimire, S., Holmes, H. L., Turin, D. R., Romero, M. F., Davies, S., and Dow, J. A.T.
College/School:College of Medical Veterinary and Life Sciences > Institute of Molecular Cell and Systems Biology
Journal Name:Proceedings of the National Academy of Sciences of the United States of America
Publisher:National Academy of Sciences
ISSN:0027-8424
ISSN (Online):1091-6490
Published Online:06 January 2020
Copyright Holders:Copyright © 2020 the Authors
First Published:First published in Proceedings of the National Academy of Sciences of the United States of America 117(3):1779-1787
Publisher Policy:Reproduced under a Creative Commons license

University Staff: Request a correction | Enlighten Editors: Update this record

Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
168614Functional Genomics of the enigmatic stellate cell.Shireen DaviesBiotechnology and Biological Sciences Research Council (BBSRC)BB/L002647/1MCSB - Integrative & Systems Biology
173817Functional analysis of insect neuropeptide G protein-coupled receptorsShireen DaviesBiotechnology and Biological Sciences Research Council (BBSRC)BB/P008097/1MCSB - Integrative & Systems Biology
169260Improving stone disease treatment by accurate phenotyping and risk stratificationJulian DowNational Institutes of Health (NIH)1U54DK100227-01MCSB - Integrative & Systems Biology