Chloride channels in stellate cells are essential for uniquely high secretion rates in neuropeptide-stimulated Drosophila diuresis

Cabrero, P. , Terhzaz, S. , Romero, M. F., Davies, S. A. , Blumenthal, E. M. and Dow, J. A. T. (2014) Chloride channels in stellate cells are essential for uniquely high secretion rates in neuropeptide-stimulated Drosophila diuresis. Proceedings of the National Academy of Sciences of the United States of America, 111(39), pp. 14301-14306. (doi:10.1073/pnas.1412706111) (PMID:25228763) (PMCID:PMC4191759)

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Abstract

Epithelia frequently segregate transport processes to specific cell types, presumably for improved efficiency and control. The molecular players underlying this functional specialization are of particular interest. In Drosophila, the renal (Malpighian) tubule displays the highest per-cell transport rates known and has two main secretory cell types, principal and stellate. Electrogenic cation transport is known to reside in the principal cells, whereas stellate cells control the anion conductance, but by an as-yet-undefined route. Here, we resolve this issue by showing that a plasma membrane chloride channel, encoded by ClC-a, is exclusively expressed in the stellate cell and is required for Drosophila kinin-mediated induction of diuresis and chloride shunt conductance, evidenced by chloride ion movement through the stellate cells, leading to depolarization of the transepithelial potential. By contrast, ClC-a knockdown had no impact on resting secretion levels. Knockdown of a second CLC gene showing highly abundant expression in adult Malpighian tubules, ClC-c, did not impact depolarization of transepithelial potential after kinin stimulation. Therefore, the diuretic action of kinin in Drosophila can be explained by an increase in ClC-a–mediated chloride conductance, over and above a resting fluid transport level that relies on other (ClC-a–independent) mechanisms or routes. This key segregation of cation and anion transport could explain the extraordinary fluid transport rates displayed by some epithelia.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Cabrero, Mr Pablo and Dow, Professor Julian and Terhzaz, Dr Selim and Davies, Professor Shireen
Authors: Cabrero, P., Terhzaz, S., Romero, M. F., Davies, S. A., Blumenthal, E. M., and Dow, J. A. T.
College/School:College of Medical Veterinary and Life Sciences > Institute of Molecular Cell and Systems Biology
College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
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
Copyright Holders:Copyright © 2014 The Authors
First Published:First published in Proceedings of the National Academy of Sciences of the United States of America 111(39):14301-14306
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
503711Epithelial stress sensors: novel roles for cytochrome P450s and organellar calcium in integrated stress and immune responses.Shireen DaviesBiotechnology and Biological Sciences Research Council (BBSRC)BB/G020620/1RI MOLECULAR CELL & SYSTEMS BIOLOGY
626691Functional Genomics of the enigmatic stellate cell.Shireen DaviesBiotechnology and Biological Sciences Research Council (BBSRC)BB/L002647/1RI MOLECULAR CELL & SYSTEMS BIOLOGY