Open Access
Research Article
Issue
Parasite
Volume 27, 2020
Article Number 3
Number of page(s) 13
DOI https://doi.org/10.1051/parasite/2019079
Published online 14 January 2020
  • Abu-Qare AW, Elmasry E, Abou-Donia MB. 2003. A role for P-glycoprotein in environmental toxicology. Journal of Toxicology and Environmental Health, Part B Critical Reviews, 6(3), 279–288. [CrossRef] [Google Scholar]
  • Ambudkar SV, Dey S, Hrycyna CA, Ramachandra M, Pastan I, Gottesman MM. 1999. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annual Review of Pharmacology and Toxicology, 39, 361–398. [CrossRef] [PubMed] [Google Scholar]
  • Barrett J. 1997. Helminth detoxification mechanisms. Journal of Helminthology, 71(2), 85–89. [CrossRef] [PubMed] [Google Scholar]
  • Beaumont-Schwartz C, Kerboeuf D, Hubert J. 1987. Méthodes de mise en évidence de souche de strongles gastro-intestinaux resistantes aux anthelminthiques. Recueil de Médecine Vétérinaire, 163, 683–688. [Google Scholar]
  • Beech RN, Prichard RK, Scott ME. 1994. Genetic variability of the beta-tubulin genes in benzimidazole- susceptible and -resistant strains of Haemonchus contortus. Genetics, 138(1), 103–110. [PubMed] [Google Scholar]
  • Bessa LJ, Ferreira M, Gameiro P. 2018. Evaluation of membrane fluidity of multidrug-resistant isolates of Escherichia coli and Staphylococcus aureus in presence and absence of antibiotics. Journal of Photochemistry and Photobiology B, 181, 150–156. [CrossRef] [Google Scholar]
  • Beugnet F, Gauthey M, Kerboeuf D. 1997. Partial in vitro reversal of benzimidazole resistance by the free- living stages of Haemonchus contortus with verapamil. Veterinary Research, 141(22), 575–576. [Google Scholar]
  • Blanchard A, Guegnard F, Charvet CL, Crisford A, Courtot E, Sauve C, Harmache A, Duguet T, O’Connor V, Castagnone-Sereno P, Reaves B, Wolstenholme AJ, Beech RN, Holden-Dye L, Neveu C. 2018. Deciphering the molecular determinants of cholinergic anthelmintic sensitivity in nematodes: when novel functional validation approaches highlight major differences between the model Caenorhabditis elegans and parasitic species. PLoS Pathogens, 14(5), e1006996. [CrossRef] [PubMed] [Google Scholar]
  • Blesbois E, Grasseau I, Hermier D. 1999. Changes in lipid content of fowl spermatozoa after liquid storage at 2 to 5 degrees C. Theriogenology, 52(2), 325–334. [CrossRef] [PubMed] [Google Scholar]
  • Borst P, Schinkel AH, Smit JJ, Wagenaar E, Van Deemter L, Smith AJ, Eijdems EW, Baas Zaman GJ. 1993. Classical and novel forms of multidrug resistance and the physiological functions of P-glycoproteins in mammals. Pharmacology and Therapeutics, 60(2), 289–299. [CrossRef] [Google Scholar]
  • Borst P, Zelcer N, van Helvoort A. 2000. ABC transporters in lipid transport. Biochimical and Biophysical Acta, 1486(1), 128–144. [CrossRef] [Google Scholar]
  • Canitrot Y, Lautier D. 1995. Use of rhodamine 123 for the detection of multidrug resistance. Bulletin du Cancer, 82(9), 687–697. [PubMed] [Google Scholar]
  • Castaing M, Loiseau A, Djoudi L. 2003. Effects of cholesterol on dye leakage induced by multidrug-resistance modulators from anionic liposomes. European Journal of Pharmacological Sciences, 18(1), 81–88. [CrossRef] [Google Scholar]
  • Charvet CL, Guegnard F, Courtot E, Cortet J, Neveu C. 2018. Nicotine-sensitive acetylcholine receptors are relevant pharmacological targets for the control of multidrug resistant parasitic nematodes. International Journal of Parasitology – Drugs and Drug Resistance, 8(3), 540–549. [CrossRef] [Google Scholar]
  • Christian AE, Haynes MP, Phillips MC, Rothblat GH. 1997. Use of cyclodextrins for manipulating cellular cholesterol content. Journal of Lipid Researchs, 38(11), 2264–2272. [Google Scholar]
  • Dey S, Ramachandra M, Pastan I, Gottesman MM, Ambudkar SV. 1998. Photoaffinity labeling of human P-glycoprotein: effect of modulator interaction and ATP hydrolysis on substrate binding. Methods of Enzymology, 292, 318–328. [Google Scholar]
  • Eytan GD, Regev R, Oren G, Assaraf YG. 1996. The role of passive transbilayer drug movement in multidrug resistance and its modulation. Journal of Biological Chemistry, 271(22), 12897–12902. [CrossRef] [Google Scholar]
  • Feller N, Kuiper CM, Lankelma J, Ruhdal JK, Scheper RJ, Pinedo HM, Broxterman HJ. 1995. Functional detection of MDR1/P170 and MRP/P190-mediated multidrug resistance in tumour cells by flow cytometry. British Journal of Cancer, 72(3), 543–549. [CrossRef] [PubMed] [Google Scholar]
  • Garnier-Suillerot A, Marbeuf-Gueye C, Salerno M, Loetchutinat C, Fokt I, Krawczyk M, Kowalczyk T, Priebe W. 2001. Analysis of drug transport kinetics in multidrug-resistant cells: implications for drug action. Current Medicinal Chemistry, 8(1), 51–64. [CrossRef] [PubMed] [Google Scholar]
  • Gimpl G, Burger K, Fahrenholz F. 1997. Cholesterol as modulator of receptor function. Biochemistry, 36(36), 10959–10974. [CrossRef] [PubMed] [Google Scholar]
  • Giraud MN, Motta C, Boucher D, Grizard G. 2000. Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa. Human Reproduction, 15(10), 2160–2164. [CrossRef] [Google Scholar]
  • Godoy P, Che H, Beech RN, Prichard RK. 2015. Characterization of Haemonchus contortus P-glycoprotein-16 and its interaction with the macrocyclic lactone anthelmintics. Molecular and Biochemical Parasitology, 204(1), 11–15. [CrossRef] [PubMed] [Google Scholar]
  • Godoy P, Lian J, Beech RN, Prichard RK. 2015. Haemonchus contortus P-glycoprotein-2: in situ localisation and characterisation of macrocyclic lactone transport. International Journal for Parasitology, 45(1), 85–93. [CrossRef] [PubMed] [Google Scholar]
  • Godoy P, Che H, Beech RN, Prichard RK. 2016. Characterisation of P-glycoprotein-9.1 in Haemonchus contortus. Parasites and Vectors, 9, 52. [CrossRef] [Google Scholar]
  • Hoste H, Torres-Acosta JF, Quijada J, Chan-Perez I, Dakheel MM, Kommuru DS, Mueller-Harvey I, Terrill TH. 2016. Interactions between nutrition and infections with Haemonchus contortus and related gastrointestinal nematodes in small ruminants. Advances in Parasitology, 93, 239–351. [CrossRef] [PubMed] [Google Scholar]
  • Ilangumaran S, Hoessli DC. 1998. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochemical Journal, 335(Pt 2), 433–440. [CrossRef] [Google Scholar]
  • Issouf M, Guegnard F, Koch C, Le Vern Y, Blanchard-Letort A, Che H, Beech RN, Kerboeuf D, Neveu C. 2014. Haemonchus contortus P-glycoproteins interact with host eosinophil granules: a novel insight into the role of ABC transporters in host-parasite interaction. PLoS One, 9(2), e87802. [CrossRef] [PubMed] [Google Scholar]
  • Kaschny M, Demeler J, Janssen IJ, Kuzmina TA, Besognet B, Kanellos T, Kerboeuf D, von Samson-Himmelstjerna G, Krucken J. 2015. Macrocyclic lactones differ in interaction with recombinant P-glycoprotein 9 of the parasitic nematode Cylicocylus elongatus and ketoconazole in a yeast growth assay. PLoS Pathogens, 11(4), e1004781. [CrossRef] [PubMed] [Google Scholar]
  • Kerboeuf D, Aycardi J. 1999. Unexpected increased thiabendazole tolerance in Haemonchus contortus resistant to anthelmintics by modulation of glutathione activity. Parasitology Research, 85(8–9), 713–718. [CrossRef] [PubMed] [Google Scholar]
  • Kerboeuf D, Aycardi J, Soubieux D. 1996. Flow-cytometry analysis of sheep-nematode egg populations. Parasitology Research, 82(4), 358–363. [CrossRef] [PubMed] [Google Scholar]
  • Kerboeuf D, Chambrier P, Le Vern Y, Aycardi J. 1999. Flow cytometry analysis of drug transport mechanisms in Haemonchus contortus susceptible or resistant to anthelmintics. Parasitology Research, 85(2), 118–123. [CrossRef] [PubMed] [Google Scholar]
  • Kerboeuf D, Guegnard F, Le Vern Y. 2002. Analysis and partial reversal of multidrug resistance to anthelmintics due to P-glycoprotein in Haemonchus contortus eggs using Lens culinaris lectin. Parasitology Research, 88(9), 816–821. [CrossRef] [PubMed] [Google Scholar]
  • Kerboeuf D, Blackhall W, Kaminsky R, von Samson-Himmelstjerna G. 2003. P-glycoprotein in helminths: function and perspectives for anthelmintic treatment and reversal of resistance. International Journal of Antimicrobial Agents, 22(3), 332–346. [CrossRef] [PubMed] [Google Scholar]
  • Kerboeuf D, Guegnard F, Vern YL. 2003. Detection of P-glycoprotein-mediated multidrug resistance against anthelmintics in Haemonchus contortus using anti-human mdr1 monoclonal antibodies. Parasitology Research, 91(1), 79–85. [CrossRef] [PubMed] [Google Scholar]
  • Kerboeuf D, Riou M, Neveu C, Issouf M. 2010. Membrane drug transport in helminths. Anti-Infective Agent in Medicinal Chemistry, 9, 113–129. [CrossRef] [Google Scholar]
  • Kim RB. 2002. Transporters and xenobiotic disposition. Toxicology, 181–182, 291–297. [CrossRef] [PubMed] [Google Scholar]
  • Kimura Y, Kioka N, Kato H, Matsuo M, Ueda K. 2007. Modulation of drug-stimulated ATPase activity of human MDR1/P-glycoprotein by cholesterol. Biochemical Journal, 401(2), 597–605. [CrossRef] [Google Scholar]
  • Klein U, Gimpl G, Fahrenholz F. 1995. Alteration of the myometrial plasma membrane cholesterol content with beta-cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry, 34(42), 13784–13793. [CrossRef] [PubMed] [Google Scholar]
  • Klein C, Pillot T, Chambaz J, Drouet B. 2003. Determination of plasma membrane fluidity with a fluorescent analogue of sphingomyelin by FRAP measurement using a standard confocal microscope. Brain Research Protocols, 11(1), 46–51. [CrossRef] [Google Scholar]
  • Kohler P. 2001. The biochemical basis of anthelmintic action and resistance. International Journal of Parasitology, 31(4), 336–345. [CrossRef] [Google Scholar]
  • Kwa MS, Kooyman FN, Boersema JH, Roos MH. 1993. Effect of selection for benzimidazole resistance in Haemonchus contortus on beta-tubulin isotype 1 and isotype 2 genes. Biochemical and Biophysical Research Communications, 191(2), 413–419. [CrossRef] [PubMed] [Google Scholar]
  • Kwa MS, Veenstra JG, Roos MH. 1994. Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype 1. Molecular and Biochemical Parasitology, 63(2), 299–303. [CrossRef] [PubMed] [Google Scholar]
  • Laberge RM, Ambadipudi R, Georges E. 2014. P-glycoprotein mediates the collateral sensitivity of multidrug resistant cells to steroid hormones. Biochemical and Biophysical Research Communications, 447(4), 574–579. [CrossRef] [PubMed] [Google Scholar]
  • Le Jambre LF, Dobson RJ, Lenane IJ, Barnes EH. 1999. Selection for anthelmintic resistance by macrocyclic lactones in Haemonchus contortus. International Journal of Parasitology, 29(7), 1101–1111. [CrossRef] [Google Scholar]
  • Lee EY, Jeong PY, Kim SY, Shim YH, Chitwood DJ, Paik YK. 2009. Effects of sterols on the development and aging of Caenorhabditis elegans. Methods in Molecular Biology, 462, 167–179. [Google Scholar]
  • Lespine A. 2013. Lipid-like properties and pharmacology of the anthelmintic macrocyclic lactones. Expert Opinion on Drug Metabolism and Toxicology, 9(12), 1581–1595. [CrossRef] [Google Scholar]
  • Lespine A, Menez C, Bourguinat C, Prichard RK. 2012. P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. International Journal of Parasitology – Drugs and Drug Resistances, 2, 58–75. [CrossRef] [Google Scholar]
  • Lu P, Liu R, Sharom FJ. 2001. Drug transport by reconstituted P-glycoprotein in proteoliposomes. Effect of substrates and modulators, and dependence on bilayer phase state. European Journal of Biochemistry, 268(6), 1687–1697. [CrossRef] [PubMed] [Google Scholar]
  • Luker GD, Pica CM, Kumar AS, Covey DF, Piwnica-Worms D. 2000. Effects of cholesterol and enantiomeric cholesterol on P-glycoprotein localization and function in low-density membrane domains. Biochemistry, 39(26), 7651–7661. [CrossRef] [PubMed] [Google Scholar]
  • Marechal E, Riou M, Kerboeuf D, Beugnet F, Chaminade P, Loiseau PM. 2011. Membrane lipidomics for the discovery of new antiparasitic drug targets. Trends in Parasitology, 27(11), 496–504. [CrossRef] [PubMed] [Google Scholar]
  • Marques HMC. 2010. A review on cyclodextrin encapsulation of essential oils and volatiles. Flavour and Fragrance Journal., 25(5), 313–326. [Google Scholar]
  • Menez C, Mselli-Lakhal L, Foucaud-Vignault M, Balaguer P, Alvinerie M, Lespine A. 2012. Ivermectin induces P-glycoprotein expression and function through mRNA stabilization in murine hepatocyte cell line. Biochemical Pharmacology, 83(2), 269–278. [CrossRef] [PubMed] [Google Scholar]
  • Menez C, Alberich M, Courtot E, Guegnard F, Blanchard A, Aguilaniu H, Lespine A. 2019. The transcription factor NHR-8: a new target to increase ivermectin efficacy in nematodes. PLoS Pathogens, 15(2), e1007598. [CrossRef] [PubMed] [Google Scholar]
  • Mora MP, Tourne-Peteilh C, Charveron M, Fabre B, Milon A, Muller I. 1999. Optimisation of plant sterols incorporation in human keratinocyte plasma membrane and modulation of membrane fluidity. Chemistry Physics Lipids, 101(2), 255–265. [CrossRef] [Google Scholar]
  • Mukhopadhyay K, Kohli A, Prasad R. 2002. Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrobial Agents Chemotherapy, 46(12), 3695–3705. [CrossRef] [Google Scholar]
  • Oldfield E, Chapman D. 1972. Dynamics of lipids in membranes: heterogeneity and the role of cholesterol. FEBS Letters, 23(3), 285–297. [CrossRef] [PubMed] [Google Scholar]
  • Page AP, Stepek G, Winter AD, Pertab D. 2014. Enzymology of the nematode cuticle: a potential drug target? International Journal of Parasitology – Drugs and Drug Resistances, 4(2), 133–141. [CrossRef] [Google Scholar]
  • Pallares-Trujillo J, Lopez-Soriano FJ, Argiles JM. 2000. Lipids: a key role in multidrug resistance? (Review). International Journal of Oncology, 16(4), 783–798. [PubMed] [Google Scholar]
  • Peelman F, Labeur C, Vanloo B, Roosbeek S, Devaud C, Duverger N, Denefle P, Rosier M, Vandekerckhove J, Rosseneu M. 2003. Characterization of the ABCA transporter subfamily: identification of prokaryotic and eukaryotic members, phylogeny and topology. Journal of Molecular Biology, 325(2), 259–274. [CrossRef] [PubMed] [Google Scholar]
  • Prichard RK, Hall CA, Kelly JD, Martin IC, Donald AD. 1980. The problem of anthelmintic resistance in nematodes. Australian Veterinary Journal, 56(5), 239–251. [CrossRef] [PubMed] [Google Scholar]
  • Qu Q, Sharom FJ. 2002. Proximity of bound Hoechst 33342 to the ATPase catalytic sites places the drug binding site of P-glycoprotein within the cytoplasmic membrane leaflet. Biochemistry, 41(14), 4744–4752. [CrossRef] [PubMed] [Google Scholar]
  • Qu Q, Chu JW, Sharom FJ. 2003. Transition state P-glycoprotein binds drugs and modulators with unchanged affinity, suggesting a concerted transport mechanism. Biochemistry, 42(5), 1345–1353. [CrossRef] [PubMed] [Google Scholar]
  • Qu Q, Russell PL, Sharom FJ. 2003. Stoichiometry and affinity of nucleotide binding to P-glycoprotein during the catalytic cycle. Biochemistry, 42(4), 1170–1177. [CrossRef] [PubMed] [Google Scholar]
  • Ramos F, Portella LP, Rodrigues Fde S, Reginato CZ, Potter L, Cezar AS, Sangioni LA, Vogel FS. 2016. Anthelmintic resistance in gastrointestinal nematodes of beef cattle in the state of Rio Grande do Sul, Brazil. International Journal of Parasitology – Drugs and Drug Resistances, 6(1), 93–101. [CrossRef] [Google Scholar]
  • Riou M. 2008. “From eggs per gram to genes”–21st International Conference of the World Association for the Advancement of Veterinary Parasitology (WAAVP 2007). Parasite, 15(2), 183–184. [PubMed] [Google Scholar]
  • Riou M, Guegnard F, Le Vern Y, Kerboeuf D. 2003. Modulation of the multidrug resistance (MDR) system in the nematode Haemonchus contortus by changing cholesterol content: effects on resistance to anthelmintics. Journal of Antimicrobial Chemotherapy, 52(2), 180–187. [CrossRef] [Google Scholar]
  • Riou M, Koch C, Kerboeuf D. 2005. Increased resistance to anthelmintics of Haemonchus contortus eggs associated with changes in membrane fluidity of eggshells during embryonation. Parasitology Reseach, 95(4), 266–272. [CrossRef] [Google Scholar]
  • Riou M, Grasseau I, Blesbois E, Kerboeuf D. 2007. Relationships between sterol/phospholipid composition and xenobiotic transport in nematodes. Parasitology Research, 100(5), 1125–1134. [CrossRef] [PubMed] [Google Scholar]
  • Riou M, Guegnard F, Sizaret PY, Le Vern Y, Kerboeuf D. 2010. Drug resistance is affected by colocalization of P-glycoproteins in raft-like structures unexpected in eggshells of the nematode Haemonchus contortus. Biochemical Cell and Biology, 88(3), 459–467. [CrossRef] [Google Scholar]
  • Rothnie A, Theron D, Soceneantu L, Martin C, Traikia M, Berridge G, Higgins CF, Devaux PF, Callaghan R. 2001. The importance of cholesterol in maintenance of P-glycoprotein activity and its membrane perturbing influence. European Biophysical Journal, 30(6), 430–442. [CrossRef] [Google Scholar]
  • Schinkel AH. 1997. The physiological function of drug-transporting P-glycoproteins. Seminars in Cancer Biology, 8(3), 161–170. [CrossRef] [PubMed] [Google Scholar]
  • Schinkel AH, Mol CA, Wagenaar E, van Deemter L, Smit JJ, Borst P. 1995. Multidrug resistance and the role of P-glycoprotein knockout mice. European Journal of Cancer, 31A(7–8), 1295–1298. [CrossRef] [PubMed] [Google Scholar]
  • Shechter E, Rossignol B. 1997. Biochimie et biophysique des membranes. Aspects structuraux et fonctionnels. Paris (France): Dunod, 459 p. [Google Scholar]
  • Shinitzky M, Barenholz Y. 1974. Dynamics of the hydrocarbon layer in liposomes of lecithin and sphingomyelin containing dicetylphosphate. Journal of Biological Chemistry, 249(8), 2652–2657. [Google Scholar]
  • Shinitzky M, Barenholz Y. 1978. Fluidity parameters of lipid regions determined by fluorescence polarization. Biochimical and Biophysical Acta, 515(4), 367–394. [CrossRef] [Google Scholar]
  • Sinicrope FA, Dudeja PK, Bissonnette BM, Safa AR, Brasitus TA. 1992. Modulation of P-glycoprotein-mediated drug transport by alterations in lipid fluidity of rat liver canalicular membrane vesicles. Journal of Biological Chemistry, 267(35), 24995–25002. [Google Scholar]
  • Smit JJ, Schinkel AH, Oude Elferink RPJ, Groen AK, Wagenaar E, van Deemter L, Mol CAAM, Ottenhoff R, van der Lugt NMT, van Roon MA, van der Valk MA, Offerhaus JA, Berns AJM, Borst P. 1993. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell, 75(3), 451–462. [CrossRef] [PubMed] [Google Scholar]
  • Smit JJ, Schinkel AH, Mol CA, Majoor D, Mooi WJ, Jongsma AP, Lincke CR, Borst P. 1994. Tissue distribution of the human MDR3 P-glycoprotein. Laboratory Investigation, 71(5), 638–649. [Google Scholar]
  • Varadyova Z, Pisarčíková J, Babják M, Hodges A, Mravčáková D, Kišidayová S, Königová A, Vadlejch J, Várady M. 2018. Ovicidal and larvicidal activity of extracts from medicinal-plants against Haemonchus contortus. Experimental Parasitology, 195, 71–77. [CrossRef] [PubMed] [Google Scholar]
  • Waller PJ. 1999. International approaches to the concept of integrated control of nematode parasites of livestock. International Journal of Parasitology, 29(1), 155–164; discussion 183–184. [CrossRef] [Google Scholar]
  • Yoshimoto H, Takeo T, Irie T, Nakagata N. 2017. Fertility of cold-stored mouse sperm is recovered by promoting acrosome reaction and hyperactivation after cholesterol efflux by methyl-beta-cyclodextrin. Biology and Reproduction, 96(2), 446–455. [CrossRef] [Google Scholar]
  • Yunomae K, Arima H, Hirayama F, Uekama K. 2003. Involvement of cholesterol in the inhibitory effect of dimethyl-beta-cyclodextrin on P-glycoprotein and MRP2 function in Caco-2 cells. FEBS Letters, 536(1–3), 225–231. [CrossRef] [PubMed] [Google Scholar]
  • Zimniak P, Pikula S, Bandorowicz-Pikula J, Awasthi YC. 1999. Mechanisms for xenobiotic transport in biological membranes. Toxicology Letters, 106(2–3), 107–118. [CrossRef] [PubMed] [Google Scholar]