{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,3]],"date-time":"2026-08-03T02:28:46Z","timestamp":1785724126038,"version":"3.56.0"},"reference-count":62,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2019,10,8]],"date-time":"2019-10-08T00:00:00Z","timestamp":1570492800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0223569","type":"journal-article","created":{"date-parts":[[2019,10,8]],"date-time":"2019-10-08T13:24:10Z","timestamp":1570541050000},"page":"e0223569","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["Transepithelial transport of P-glycoprotein substrate by the Malpighian tubules of the desert locust"],"prefix":"10.1371","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9178-620X","authenticated-orcid":true,"given":"Marta","family":"Rossi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Davide","family":"De Battisti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeremy Edward","family":"Niven","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2019,10,8]]},"reference":[{"issue":"2","key":"pone.0223569.ref001","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1242\/jeb.61.2.357","article-title":"Active transport by insect Malpighian tubules of acidic dyes and of acylamides","volume":"61","author":"SH Maddrell","year":"1974","journal-title":"J Exp Biol"},{"issue":"4","key":"pone.0223569.ref002","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1242\/jeb.35.4.871","article-title":"Excretion by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae): amino acids, sugars and urea","volume":"35","author":"JA Ramsay","year":"1958","journal-title":"J Exp Biol"},{"key":"pone.0223569.ref003","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1242\/jeb.41.1.15","article-title":"Rectal absorption in the desert locust, Schistocerca gregaria Forskal. I","volume":"41","author":"JE Phillips","year":"1964","journal-title":"J Exp Biol"},{"key":"pone.0223569.ref004","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2806(08)00001-5","article-title":"Insect excretory mechanisms","volume":"35","author":"M O\u2019Donnell","year":"2008","journal-title":"Adv In Insect Phys"},{"issue":"2","key":"pone.0223569.ref005","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1007\/BF00689629","article-title":"Dynamic changes in flow rate and composition of urine during the post-bloodmeal diuresis in Aedes aegypti (L.)","volume":"153","author":"JC Williams","year":"1983","journal-title":"J Comp Physiol B"},{"issue":"7","key":"pone.0223569.ref006","doi-asserted-by":"crossref","first-page":"1369","DOI":"10.1016\/0022-1910(73)90167-4","article-title":"Fluid secretion by in vitro preparations of the Malpighian tubules of the desert locust Schistocerca gregaria","volume":"19","author":"SH Maddrell","year":"1973","journal-title":"J Insect Physiol"},{"issue":"1","key":"pone.0223569.ref007","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1242\/jeb.172.1.335","article-title":"The insect V-ATPase, a plasma membrane proton pump energizing secondary active transport: molecular analysis of electrogenic potassium transport in the tobacco hornworm midgut","volume":"172","author":"HE Wieczorek","year":"1992","journal-title":"J Exp Biol"},{"issue":"2","key":"pone.0223569.ref008","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1242\/jeb.64.2.267","article-title":"Excretion of alkaloids by Malpighian tubules of insects","volume":"64","author":"SH Maddrell","year":"1976","journal-title":"J Exp Biol"},{"issue":"18","key":"pone.0223569.ref009","doi-asserted-by":"crossref","first-page":"2637","DOI":"10.1242\/jeb.201.18.2637","article-title":"Transepithelial transport of nicotine and vinblastine in isolated Malpighian tubules of the tobacco hornworm (Manduca sexta) suggests a P-glycoprotein-like mechanism","volume":"201","author":"LS Gaertner","year":"1998","journal-title":"J Exp Biol"},{"key":"pone.0223569.ref010","first-page":"52","article-title":"Mrp2-like transport of Texas Red by Malpighian tubules of the common American cockroach, Periplaneta americana","volume":"39","author":"KJ Karnaky","year":"2000","journal-title":"Bull Mt Des Isl Biol Lab"},{"issue":"23","key":"pone.0223569.ref011","doi-asserted-by":"crossref","first-page":"4363","DOI":"10.1242\/jeb.01911","article-title":"Transepithelial transport of fluorescent p-glycoprotein and MRP2 substrates by insect Malpighian tubules: confocal microscopic analysis of secreted fluid droplets","volume":"208","author":"JP Leader","year":"2005","journal-title":"J Exp Biol"},{"issue":"3","key":"pone.0223569.ref012","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1002\/arch.20148","article-title":"Changes in fluid secretion rate alter net transepithelial transport of MRP2 and P\u2010glycoprotein substrates in Malpighian tubules of Drosophila melanogaster","volume":"63","author":"MJ O\u2019Donnell","year":"2006","journal-title":"Arch Insect Biochem Physiol: Published in Collaboration with the Entomological Society of America"},{"issue":"3","key":"pone.0223569.ref013","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1152\/physrev.00040.2003","article-title":"Molecular and cellular physiology of renal organic cation and anion transport","volume":"84","author":"SH Wright","year":"2004","journal-title":"Physiol Rev"},{"issue":"11","key":"pone.0223569.ref014","doi-asserted-by":"crossref","first-page":"e26796","DOI":"10.1371\/journal.pone.0026796","article-title":"Killing them with kindness? In-hive medications may inhibit xenobiotic efflux transporters and endanger honey bees","volume":"6","author":"DJ Hawthorne","year":"2011","journal-title":"PLoS One"},{"issue":"5","key":"pone.0223569.ref015","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/j.jinsphys.2006.01.008","article-title":"Tetraethylammonium and nicotine transport by the Malpighian tubules of insects","volume":"52","author":"MR Rheault","year":"2006","journal-title":"J Insect Physiol"},{"issue":"2","key":"pone.0223569.ref016","doi-asserted-by":"crossref","first-page":"e0148242","DOI":"10.1371\/journal.pone.0148242","article-title":"Multi-drug resistance transporters and a mechanism-based strategy for assessing risks of pesticide combinations to honey bees","volume":"11","author":"AJ Guseman","year":"2016","journal-title":"PLoS One"},{"issue":"2","key":"pone.0223569.ref017","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.anbehav.2004.04.018","article-title":"Food choices of solitarious and gregarious locusts reflect cryptic and aposematic antipredator strategies","volume":"69","author":"E Despland","year":"2005","journal-title":"Anim Behav"},{"issue":"3","key":"pone.0223569.ref018","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1046\/j.1570-7458.2000.00632.x","article-title":"Ability of a generalist insect, Schistocerca gregaria, to overcome thioglucoside defense in desert plants: tolerance or adaptation?","volume":"94","author":"AM Mainguet","year":"2000","journal-title":"Entomol Exp Appl"},{"issue":"1438","key":"pone.0223569.ref019","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1098\/rspb.2000.0967","article-title":"Density\u2013dependent aposematism in the desert locust","volume":"267","author":"GA Sword","year":"2000","journal-title":"Proc R Soc Lond B Biol Sci"},{"key":"pone.0223569.ref020","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2806(08)36001-9","article-title":"Locust phase polyphenism: an update","volume":"36","author":"MP Pener","year":"2009","journal-title":"Adv Insect Phys"},{"issue":"3","key":"pone.0223569.ref021","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1007\/s004420100666","article-title":"Tasty on the outside, but toxic in the middle: grasshopper regurgitation and host plant-mediated toxicity to a vertebrate predator","volume":"128","author":"GA Sword","year":"2001","journal-title":"Oecologia"},{"issue":"6716","key":"pone.0223569.ref022","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1038\/16609","article-title":"Density-dependent warning coloration","volume":"397","author":"GA Sword","year":"1999","journal-title":"Nature"},{"issue":"4","key":"pone.0223569.ref023","doi-asserted-by":"crossref","first-page":"e00050","DOI":"10.1002\/prp2.50","article-title":"Characterization of a novel brain barrier ex vivo insect\u2010based P\u2010glycoprotein screening model","volume":"2","author":"O Andersson","year":"2014","journal-title":"Pharmacol Res Perspect"},{"issue":"1","key":"pone.0223569.ref024","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1242\/jeb.31.1.104","article-title":"Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae)","volume":"31","author":"JA Ramsay","year":"1954","journal-title":"J Exp Biol"},{"issue":"1","key":"pone.0223569.ref025","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1111\/j.1432-1033.1997.00104.x","article-title":"Efficiency of P\u2010glycoprotein\u2013mediated exclusion of rhodamine dyes from multidrug\u2010resistant cells is determined by their passive transmembrane movement rate","volume":"248","author":"GD Eytan","year":"1997","journal-title":"Eur J Biochem"},{"issue":"11","key":"pone.0223569.ref026","doi-asserted-by":"crossref","first-page":"3538","DOI":"10.1523\/JNEUROSCI.5564-08.2009","article-title":"Evolutionary conservation of vertebrate blood\u2013brain barrier chemoprotective mechanisms in Drosophila","volume":"29","author":"F Mayer","year":"2009","journal-title":"J Neurosci"},{"key":"pone.0223569.ref027","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.ibmb.2013.11.001","article-title":"The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance","volume":"45","author":"W Dermauw","year":"2014","journal-title":"Insect Biochemi Mol Biol"},{"issue":"11","key":"pone.0223569.ref028","first-page":"2860","article-title":"Phosphorylation of the Mr 170,000 to 180,000 glycoprotein specific to multidrug-resistant tumor cells: effects of verapamil, trifluoperazine, and phorbol esters","volume":"47","author":"H Hamada","year":"1987","journal-title":"Cancer Res"},{"issue":"7","key":"pone.0223569.ref029","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 years of image analysis","volume":"9","author":"CA Schneider","year":"2012","journal-title":"Nature Methods"},{"key":"pone.0223569.ref030","unstructured":"R Core Team. R: A language and environment for statistical computing. R J, 2012."},{"key":"pone.0223569.ref031","doi-asserted-by":"crossref","unstructured":"Bates D, M\u00e4chler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. 2014 Jun 23. https:\/\/arxiv.org\/abs\/1406.5823","DOI":"10.18637\/jss.v067.i01"},{"key":"pone.0223569.ref032","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1007\/978-1-4612-1694-0_15","volume-title":"Selected papers of Hirotugu Akaike","author":"H Akaike","year":"1998"},{"issue":"13","key":"pone.0223569.ref033","doi-asserted-by":"crossref","DOI":"10.18637\/jss.v082.i13","article-title":"lmerTest package: tests in linear mixed effects models","volume":"82","author":"A Kuznetsova","year":"2017","journal-title":"J Stat Softw"},{"issue":"1","key":"pone.0223569.ref034","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1007\/s00265-010-1038-5","article-title":"Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner\u2019s curse","volume":"65","author":"W Forstmeier","year":"2011","journal-title":"Behav Ecol Sociobiol"},{"issue":"4","key":"pone.0223569.ref035","first-page":"216","article-title":"Package \u2018lsmeans\u2019","volume":"34","author":"R Lenth","year":"2018","journal-title":"Am Stat"},{"key":"pone.0223569.ref036","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-24277-4","volume-title":"ggplot2: elegant graphics for data analysis","author":"H Wickham","year":"2016"},{"issue":"2","key":"pone.0223569.ref037","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1124\/jpet.113.205476","article-title":"The grasshopper: a novel model for assessing vertebrate brain uptake","volume":"346","author":"O Andersson","year":"2013","journal-title":"J Pharmacol Exp Ther"},{"issue":"3","key":"pone.0223569.ref038","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1242\/jeb.065987","article-title":"First evidence of epithelial transport in tardigrades: a comparative investigation of organic anion transport","volume":"215","author":"KA Halberg","year":"2012","journal-title":"J Exp Biol"},{"issue":"5","key":"pone.0223569.ref039","first-page":"1967","article-title":"Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil","volume":"41","author":"T Tsuruo","year":"1981","journal-title":"Cancer Res"},{"issue":"12","key":"pone.0223569.ref040","doi-asserted-by":"crossref","first-page":"2439","DOI":"10.1016\/j.bbagen.2015.09.002","article-title":"An invertebrate model for CNS drug discovery: Transcriptomic and functional analysis of a mammalian P-glycoprotein ortholog","volume":"1850","author":"S Al-Qadi","year":"2015","journal-title":"Biochim Biophys Acta Gen Subj"},{"issue":"11\u201312","key":"pone.0223569.ref041","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.drudis.2011.04.004","article-title":"Models for predicting blood\u2013brain barrier permeation","volume":"16","author":"PA Nielsen","year":"2011","journal-title":"Drug Discov Today"},{"issue":"1","key":"pone.0223569.ref042","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1002\/neu.480250103","article-title":"A putative nicotine pump at the metabolic blood\u2013brain barrier of the tobacco hornworm","volume":"25","author":"CL Murray","year":"1994","journal-title":"J Neurobi"},{"key":"pone.0223569.ref043","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.vascn.2016.05.014","article-title":"Organic cation rhodamines for screening organic cation transporters in early stages of drug development","volume":"82","author":"MC Ugwu","year":"2016","journal-title":"J Pharmacol Toxicol Methods"},{"issue":"1","key":"pone.0223569.ref044","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1038\/bjc.1989.9","article-title":"Effect of calcium antagonists on the chemosensitivity of two multidrug-resistant human tumour cell lines which do not overexpress P-glycoprotein","volume":"59","author":"SP Cole","year":"1989","journal-title":"Br J Cancer"},{"issue":"22","key":"pone.0223569.ref045","doi-asserted-by":"crossref","first-page":"12897","DOI":"10.1074\/jbc.271.22.12897","article-title":"The role of passive transbilayer drug movement in multidrug resistance and its modulation","volume":"271","author":"GD Eytan","year":"1996","journal-title":"J Biol Chem"},{"issue":"3","key":"pone.0223569.ref046","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/s002329900305","article-title":"The P-glycoprotein efflux pump: how does it transport drugs?","volume":"160","author":"FJ Sharom","year":"1997","journal-title":"J Membr Biol"},{"issue":"19","key":"pone.0223569.ref047","doi-asserted-by":"crossref","first-page":"1447","DOI":"10.1056\/NEJM199911043411907","article-title":"Calcium-antagonist drugs","volume":"341","author":"DR Abernethy","year":"1999","journal-title":"N Engl J Med"},{"issue":"1","key":"pone.0223569.ref048","doi-asserted-by":"crossref","first-page":"C394","DOI":"10.1152\/ajpcell.2001.280.2.C394","article-title":"Model organisms: new insights into ion channel and transporter function L-type calcium channels regulate epithelial fluid transport in Drosophila melanogaster","volume":"280","author":"MR MacPherson","year":"2001","journal-title":"Am J Physiol"},{"issue":"12","key":"pone.0223569.ref049","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1016\/j.jinsphys.2013.09.005","article-title":"Investigations of the signaling cascade involved in diuretic hormone stimulation of Malpighian tubule fluid secretion in Rhodnius prolixus","volume":"59","author":"JP Paluzzi","year":"2013","journal-title":"J Insect Physiol"},{"issue":"8","key":"pone.0223569.ref050","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1016\/0022-1910(93)90069-4","article-title":"Malpighian tubules of Aedes aegypti: five tubules, one function","volume":"39","author":"KW Beyenbach","year":"1993","journal-title":"J Insect Physiol"},{"issue":"4","key":"pone.0223569.ref051","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1111\/j.1365-3032.1988.tb01120.x","article-title":"Fluid secretion by single isolated Malpighian tubules of the house cricket, Acheta domesticus, and their response to diuretic hormone","volume":"13","author":"GM Coast","year":"1988","journal-title":"Physiol Entomol"},{"issue":"1","key":"pone.0223569.ref052","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1242\/jcs.60.1.117","article-title":"Functional design of microvilli in the Malpighian tubules of the insect Rhodnius prolixus","volume":"60","author":"TJ Bradley","year":"1983","journal-title":"J Cell Sci"},{"issue":"1","key":"pone.0223569.ref053","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1242\/jeb.175.1.1","article-title":"A comparison of the effects of two putative diuretic hormones from Locusta migratoria on isolated locust Malpighian tubules","volume":"175","author":"GM Coast","year":"1993","journal-title":"J Exp Biol"},{"issue":"10","key":"pone.0223569.ref054","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/0022-1910(88)90127-8","article-title":"Diuretic activity of a newly identified neuropeptide\u2014the arginine-vasopressin-like insect diuretic hormone: use of an improved bioassay","volume":"34","author":"JP Proux","year":"1988","journal-title":"J Insect Physiol"},{"issue":"9","key":"pone.0223569.ref055","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1016\/0022-1910(93)90056-W","article-title":"Inhibition of desert locust (Schistocerca gregaria) Malpighian tubule fluid secretion by destruxins, cyclic peptide toxins from the insect pathogenic fungus Metarhizium anisopliae","volume":"39","author":"PJ James","year":"1993","journal-title":"J Insect Physiol"},{"issue":"3","key":"pone.0223569.ref056","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s00049-009-0018-6","article-title":"Plant chemistry and insect sequestration","volume":"19","author":"SE Opitz","year":"2009","journal-title":"Chemoecology"},{"issue":"1","key":"pone.0223569.ref057","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1379\/CSC-67R.1","article-title":"Expression of mdr49 and mdr65 multidrug resistance genes in larval tissues of Drosophila melanogaster under normal and stress conditions","volume":"10","author":"MG Tapadia","year":"2005","journal-title":"Cell stress Chaperones"},{"issue":"23","key":"pone.0223569.ref058","doi-asserted-by":"crossref","first-page":"2407","DOI":"10.1016\/j.cub.2013.10.016","article-title":"Phenotypic transformation affects associative learning in the desert locust","volume":"23","author":"PM Sim\u00f5es","year":"2013","journal-title":"Curr Biol"},{"issue":"2","key":"pone.0223569.ref059","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/0304-4165(96)00060-8","article-title":"Tobacco budworm P-glycoprotein: biochemical characterization and its involvement in pesticide resistance","volume":"1291","author":"CL Lanning","year":"1996","journal-title":"Biochim Biophys Acta Gen Subj"},{"issue":"3","key":"pone.0223569.ref060","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.cca.2004.02.002","article-title":"Identification of factors responsible for insecticide resistance in Helicoverpa armigera","volume":"137","author":"R Srinivas","year":"2004","journal-title":"Comp Biochem Physiol C Toxicol Pharmacol"},{"issue":"1","key":"pone.0223569.ref061","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1007\/s12013-014-9969-5","article-title":"Mitochondrial P-glycoprotein ATPase contributes to insecticide resistance in the cotton bollworm, Helicoverpa armigera (Noctuidae: Lepidoptera)","volume":"70","author":"SM Akbar","year":"2014","journal-title":"Cell Biochem Biophys"},{"key":"pone.0223569.ref062","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1007\/978-1-4020-6059-5_27","volume-title":"Area-wide control of insect pests. From research to field implementation","author":"A Van Huis","year":"2007"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0223569","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,1]],"date-time":"2022-10-01T02:51:14Z","timestamp":1664592674000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0223569"}},"subtitle":[],"editor":[{"given":"Subba Reddy","family":"Palli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2019,10,8]]},"references-count":62,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2019,10,8]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0223569","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/529750","asserted-by":"object"}]},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,8]]}}}