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Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust

Marta Rossi, Davide De Battisti, Jeremy Edward Niven

PLOS ONE, Volume: 14, Issue: 10, Start page: e0223569

Swansea University Author: Davide De Battisti

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DOI (Published version): 10.1371/journal.pone.0223569

Abstract

Extrusion of xenobiotics is essential for allowing animals to remove toxic substances present in their diet or generated as a biproduct of their metabolism. By transporting a wide range of potentially noxious substrates, active transporters of the ABC transporter family play an important role in xen...

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Published in: PLOS ONE
ISSN: 1932-6203
Published: Public Library of Science (PLoS) 2019
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URI: https://cronfa.swan.ac.uk/Record/cronfa52757
first_indexed 2019-11-15T19:14:02Z
last_indexed 2025-04-29T03:47:16Z
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spelling 2025-04-28T13:11:59.9694677 v2 52757 2019-11-15 Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust dda80a3c7c8b7fe4af0f4bbd8eb91f15 Davide De Battisti Davide De Battisti true false 2019-11-15 BGPS Extrusion of xenobiotics is essential for allowing animals to remove toxic substances present in their diet or generated as a biproduct of their metabolism. By transporting a wide range of potentially noxious substrates, active transporters of the ABC transporter family play an important role in xenobiotic extrusion. One such class of transporters are the multidrug resistance P-glycoprotein transporters. Here, we investigated P-glycoprotein transport in the Malpighian tubules of the desert locust (Schistocerca gregaria), a species whose diet includes plants that contain toxic secondary metabolites. To this end, we studied transporter physiology using a modified Ramsay assay in which ex vivo Malpighian tubules are incubated in different solutions containing the P-glycoprotein substrate dye rhodamine B in combination with different concentrations of the P-glycoprotein inhibitor verapamil. To determine the quantity of the P-glycoprotein substrate extruded we developed a simple and cheap method as an alternative to liquid chromatography–mass spectrometry, radiolabelled alkaloids or confocal microscopy. Our evidence shows that: (i) the Malpighian tubules contain a P-glycoprotein; (ii) tubule surface area is positively correlated with the tubule fluid secretion rate; and (iii) as the fluid secretion rate increases so too does the net extrusion of rhodamine B. We were able to quantify precisely the relationships between the fluid secretion, surface area, and net extrusion. We interpret these results in the context of the life history and foraging ecology of desert locusts. We argue that P-glycoproteins contribute to the removal of xenobiotic substances from the haemolymph, thereby enabling gregarious desert locusts to maintain toxicity through the ingestion of toxic plants without suffering the deleterious effects themselves. Journal Article PLOS ONE 14 10 e0223569 Public Library of Science (PLoS) 1932-6203 8 10 2019 2019-10-08 10.1371/journal.pone.0223569 COLLEGE NANME Biosciences Geography and Physics School COLLEGE CODE BGPS Swansea University Another institution paid the OA fee M.R. was financially supported by a graduate studentship from the School of Life Sciences, University of Sussex. D.D.B. was financially supported by the Welsh government/HEFCW RESILCOAST project. 2025-04-28T13:11:59.9694677 2019-11-15T16:23:23.1649007 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Marta Rossi 1 Davide De Battisti 2 Jeremy Edward Niven 3 52757__15901__d7a59ad2639e4d2e9ad0ca6013bc4978.pdf 52757.pdf 2019-11-15T16:25:00.6011694 Output 1933459 application/pdf Version of Record true Released under the terms of a Creative Commons Attribution License (CC-BY). true https://creativecommons.org/licenses/by/4.0/
title Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust
spellingShingle Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust
Davide De Battisti
title_short Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust
title_full Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust
title_fullStr Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust
title_full_unstemmed Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust
title_sort Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust
author_id_str_mv dda80a3c7c8b7fe4af0f4bbd8eb91f15
author_id_fullname_str_mv dda80a3c7c8b7fe4af0f4bbd8eb91f15_***_Davide De Battisti
author Davide De Battisti
author2 Marta Rossi
Davide De Battisti
Jeremy Edward Niven
format Journal article
container_title PLOS ONE
container_volume 14
container_issue 10
container_start_page e0223569
publishDate 2019
institution Swansea University
issn 1932-6203
doi_str_mv 10.1371/journal.pone.0223569
publisher Public Library of Science (PLoS)
college_str Faculty of Science and Engineering
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hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
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description Extrusion of xenobiotics is essential for allowing animals to remove toxic substances present in their diet or generated as a biproduct of their metabolism. By transporting a wide range of potentially noxious substrates, active transporters of the ABC transporter family play an important role in xenobiotic extrusion. One such class of transporters are the multidrug resistance P-glycoprotein transporters. Here, we investigated P-glycoprotein transport in the Malpighian tubules of the desert locust (Schistocerca gregaria), a species whose diet includes plants that contain toxic secondary metabolites. To this end, we studied transporter physiology using a modified Ramsay assay in which ex vivo Malpighian tubules are incubated in different solutions containing the P-glycoprotein substrate dye rhodamine B in combination with different concentrations of the P-glycoprotein inhibitor verapamil. To determine the quantity of the P-glycoprotein substrate extruded we developed a simple and cheap method as an alternative to liquid chromatography–mass spectrometry, radiolabelled alkaloids or confocal microscopy. Our evidence shows that: (i) the Malpighian tubules contain a P-glycoprotein; (ii) tubule surface area is positively correlated with the tubule fluid secretion rate; and (iii) as the fluid secretion rate increases so too does the net extrusion of rhodamine B. We were able to quantify precisely the relationships between the fluid secretion, surface area, and net extrusion. We interpret these results in the context of the life history and foraging ecology of desert locusts. We argue that P-glycoproteins contribute to the removal of xenobiotic substances from the haemolymph, thereby enabling gregarious desert locusts to maintain toxicity through the ingestion of toxic plants without suffering the deleterious effects themselves.
published_date 2019-10-08T04:40:10Z
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