Drug resistance is affected by colocalization of P-glycoproteins in raft-like structures unexpected in eggshells of the nematode Haemonchus contortus

Biochemistry and Cell Biology

Volumn 88, Issue 3, 2010, Pages 459-467

  Riou, Mickaël ^a,d   Guégnard, Fabrice ^a   Sizaret, Pierre Yves ^b   Le Vern, Yves ^c   Kerboeuf, Dominique ^a,c  

^a UR1282   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c CEMAGREF   (France)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Drug resistance; Nematodes; P glycoprotein; Rafts; Xenobiotic transport

Indexed keywords

BIOLOGICAL FEATURES; CELLULAR TARGETS; CHOLESTEROL CONTENT; COLOCALIZATION; COLOCALIZE; DRUG RESISTANCE; EFFLUX PUMPS; MEMBRANE CHOLESTEROL; MICRO-DOMAINS; P-GLYCOPROTEIN;

ANIMALS; CELL MEMBRANES; CHOLESTEROL; CYTOLOGY; DETOXIFICATION; PROTEINS; PUMPS;

GLYCOPROTEINS;

GLYCOPROTEIN P; TIABENDAZOLE; XENOBIOTIC AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; CONCENTRATION RESPONSE; CUTICLE; DRUG TRANSPORT; EGG SHELL; FLOW CYTOMETRY; HAEMONCHUS CONTORTUS; LC 50; PARASITE IDENTIFICATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; VERTEBRATE;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; DRUG RESISTANCE; FLOW CYTOMETRY; HAEMONCHUS; MEMBRANE FLUIDITY; MEMBRANE MICRODOMAINS; MICROSCOPY, FLUORESCENCE; OVUM; P-GLYCOPROTEIN;

EUKARYOTA; HAEMONCHUS CONTORTUS; NEMATODA; VERTEBRATA;

EID: 77952733646     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O09-126     Document Type: Article

References (48)

1. Aumont, G., Gruner, L., and Hostache, G. 2003. Comparison of the resistance to sympatric and allopatric isolates of Haemonchus contortus of Black Belly sheep in Guadeloupe (FWI) and of INRA 401 sheep in France. Vet. Parasitol. 116(2): 139-150. doi:10.1016/S0304-4017(03)00259-0. PMID:14519318.
2. Bacso, Z., Nagy, H., Goda, K., Bene, L., Fenyvesi, F., Matkó, J., and Szabó, G. 2004. Raft and cytoskeleton associations of an ABC transporter: P-glycoprotein. Cytometry A, 61(2): 105-116. doi:10.1002/cyto.a. 20081. PMID:15382145. (Pubitemid 39362285)
3. Beaumont-Schwartz, C., Kerboeuf, D., and Hubert, J. 1987. Méthodes de mise en évidence de souche de strongles gastro-intestinaux resistantes aux anthelminthiques. Rec. Méd. Vét. 163: 683-688.
4. Blackhall, W.J., Liu, H.Y., Xu, M., Prichard, R.K., and Beech, R.N. 1998. Selection at a P-glycoprotein gene in ivermectinand moxidectin-selected strains of Haemonchus contortus. Mol. Biochem. Parasitol. 95(2): 193-201. doi:10.1016/S0166-6851(98)00087-5. PMID:9803412.
5. Brown, D.A., and London, E. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275(23): 17221-17224. doi:10.1074/jbc.R000005200. PMID:10770957.
6. Fra, A.M., Williamson, E., Simons, K., and Parton, R.G. 1994. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269(49): 30745-30748. PMID:7982998.
7. Galmiche, A., and Boquet, P. 2001. Toxines bactériennes: facteurs de virulence et outils de biologie cellulaire. Méd. Sci. (Paris), 17: 691-700.
8. Garrigues, A., Escargueil, A.E., and Orlowski, S. 2002. The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc. Natl. Acad. Sci. U.S.A. 99(16): 10347-10352. doi:10.1073/pnas.162366399. PMID:12145328.
9. Gilleard, J.S. 2006. Understanding anthelmintic resistance: the need for genomics and genetics. Int. J. Parasitol. 36(12): 1227-1239. doi:10.1016/j.ijpara.2006.06.010. PMID:16889782.
10. Gottesman, M.M. 2002. Mechanisms of cancer drug resistance. Annu. Rev. Med. 53(1): 615-627. doi:10.1146/annurev.med.53.082901.103929. PMID:11818492.
11. Gottesman, M.M., Fojo, T., and Bates, S.E. 2002. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer, 2(1): 48-58. doi:10.1038/nrc706. PMID:11902585.
12. Harder, T., Scheiffele, P., Verkade, P., and Simons, K. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141(4): 929-942. doi:10.1083/jcb.141.4.929. PMID:9585412. (Pubitemid 28243961)
13. Kaplan, R.M. 2004. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol. 20(10): 477-481. doi:10.1016/j.pt.2004.08. 001. PMID:15363441.
14. Kelly, J.D., Whitlock, H.V., Thompson, H.G., Hall, C.A., Martin, I.C., and Le Jambre, L.F. 1978. Physiological characteristics of free-living and parasitic stages of strains of Haemonchus contortus, susceptible or resistant to benzimidazole anthelmintics. Res. Vet. Sci. 25(3): 376-385. PMID:749089.
15. Kerboeuf, D., and Riou, M. 2006. Nematodes as models for the study of the regulation of activity of P-glycoproteins in multidrug resistance (MDR). Anti-Infect. Agents Med. Chem. 5: 389-402.
16. Kerboeuf, D., Aycardi, J., and Soubieux, D. 1996. Flow-cytometry analysis of sheep-nematode egg populations. Parasitol. Res. 82(4): 358-363. doi:10.1007/s004360050126. PMID:8740553.
17. Kerboeuf, D., Chambrier, P., Le Vern, Y., and Aycardi, J. 1999. Flow cytometry analysis of drug transport mechanisms in Haemonchus contortus susceptible or resistant to anthelmintics. Parasitol. Res. 85(2): 118-123. doi:10.1007/s004360050519. PMID:9934960.
18. Kerboeuf, D., Guégnard, F., and Vern, Y.L. 2003. Detection of P-glycoprotein-mediated multidrug resistance against anthelmintics in Haemonchus contortus using anti-human mdr1 monoclonal antibodies. Parasitol. Res. 91(1): 79-85. doi:10.1007/s00436-003-0942-2. PMID:12898231.
19. Klein, C., Pillot, T., Chambaz, J., and Drouet, B. 2003. Determination of plasma membrane fluidity with a fluorescent analogue of sphingomyelin by FRAP measurement using a standard confocal microscope. Brain Res. Brain Res. Protoc. 11(1): 46-51. doi:10.1016/S1385-299X(03)00016-3. PMID:12697262.
20. Kwa, M.S., Okoli, M.N., Schulz-Key, H., Okongkwo, P.O., and Roos, M.H. 1998. Use of P-glycoprotein gene probes to investigate anthelmintic resistance in Haemonchus contortus and comparison with Onchocerca volvulus. Int. J. Parasitol. 28(8): 1235-1240. doi:10.1016/S0020-7519(98)00071-X. PMID:9762570. (Pubitemid 28386920)
21. Lacey, E., and Prichard, R.K. 1986. Interactions of benzimidazoles (BZ) with tubulin from BZ-sensitive and BZ-resistant isolates of Haemonchus contortus. Mol. Biochem. Parasitol. 19(2): 171-181. doi:10.1016/0166-6851(86) 90122-2. PMID:3755220. (Pubitemid 16076530)
22. Lavie, Y., Fiucci, G., and Liscovitch, M. 1998. Up-regulation of caveolae and caveolar constituents in multidrug-resistant cancer cells. J. Biol. Chem. 273(49): 32380-32383. doi:10.1074/jbc.273.49.32380. PMID:9829965.
23. Lincke, C.R., The, I., van Groenigen, M., and Borst, P. 1992. The P-glycoprotein gene family of Caenorhabditis elegans. Cloning and characterization of genomic and complementary DNA sequences. J. Mol. Biol. 228(2): 701-711. doi:10.1016/0022-2836(92)90855-E. PMID:1360540.
24. Lincke, C.R., Broeks, A., The, I., Plasterk, R.H., and Borst, P. 1993. The expression of two P-glycoprotein (pgp) genes in transgenic Caenorhabditis elegans is confined to intestinal cells. EMBO J. 12(4): 1615-1620. PMID:8096815.
25. Luker, G.D., Pica, C.M., Kumar, A.S., Covey, D.F., and 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. doi:10.1021/bi9928593. PMID:10869171. (Pubitemid 30439594)
26. Mechetner, E.B., and Roninson, I.B. 1992. Efficient inhibition of P-glycoprotein-mediated multidrug resistance with a monoclonal antibody. Proc. Natl. Acad. Sci. U.S.A. 89(13): 5824-5828. doi:10.1073/pnas.89.13.5824. PMID:1352877.
27. Modok, S., Heyward, C., and Callaghan, R. 2004. P-glycoprotein retains function when reconstituted into a sphingolipid- and cholesterol-rich environment. J. Lipid Res. 45(10): 1910-1918. doi:10.1194/jlr.M400220-JLR200. PMID:15258203. (Pubitemid 40990884)
28. Mukhopadhyay, K., Kohli, A., and Prasad, R. 2002. Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrob. Agents Chemother. 46(12): 3695-3705. doi:10.1128/AAC.46.12.3695-3705.2002. PMID:12435664.
29. Pallarés-Trujillo, J., López-Soriano, F.J., and Argilés, J.M. 2000. Lipids: A key role in multidrug resistance? (Review). Int. J. Oncol. 16(4): 783-798. [Review.] PMID:10717249.
30. Prichard, R. 1994. Anthelmintic resistance. Vet. Parasitol. 54(1-3): 259-268. doi:10.1016/0304-4017(94)90094-9. PMID:7846855.
31. Prichard, R., and Tait, A. 2001. The role of molecular biology in veterinary parasitology. Vet. Parasitol. 98(1-3): 169-194. doi:10.1016/S0304- 4017(01)00429-0. PMID:11516585.
32. Riou, M., Guégnard, F., Le Vern, Y., and Kerboeuf, D. 2003. Modulation of the multidrug resistance (MDR) system in the nematode Haemonchus contortus by changing cholesterol content: effects on resistance to anthelmintics. J. Antimicrob. Chemother. 52(2): 180-187. doi:10.1093/jac/dkg332. PMID:12865394.
33. Riou, M., Koch, C., Delaleu, B., Berthon, P., and Kerboeuf, D. 2005. Immunolocalisation of an ABC transporter, P-glycoprotein, in the eggshells and cuticles of free-living and parasitic stages of Haemonchus contortus. Parasitol. Res. 96(3): 142-148. doi:10.1007/s00436-005-1345-3. PMID:15856301.
34. Riou, M., Grasseau, I., Blesbois, E., and Kerboeuf, D. 2007. Relationships between sterol/phospholipid composition and xenobiotic transport in nematodes. Parasitol. Res. 100(5): 1125-1134. doi:10.1007/s00436-006-0455-x. PMID:17294217.
35. Romsicki, Y., and Sharom, F.J. 2001. Phospholipid flippase activity of the reconstituted P-glycoprotein multidrug transporter. Biochemistry, 40(23): 6937-6947. doi:10.1021/bi0024456. PMID: 11389609. (Pubitemid 32538241)
36. Rothnie, A., Theron, D., Soceneantu, L., Martin, C., Traikia, M., Berridge, G., et al. 2001. The importance of cholesterol in maintenance of P-glycoprotein activity and its membrane perturbing influence. Eur. Biophys. J. 30(6): 430-442. doi:10.1007/s002490100156. PMID:11718296.
37. Sangster, N.C. 1994. P-glycoproteins in nematodes. Parasitol. Today, 10(8): 319-322. doi:10.1016/0169-4758(94)90088-4. PMID:15275432.
38. Schinkel, A.H., Arceci, R.J., Smit, J.J., Wagenaar, E., Baas, F., Dollé, M., et al. 1993. Binding properties of monoclonal antibodies recognizing external epitopes of the human MDR1 P-glycoprotein. Int. J. Cancer, 55(3): 478-484. doi:10.1002/ijc.2910550326. PMID:8104165.
39. Simons, K., and Ikonen, E. 1997. Functional rafts in cell membranes. Nature, 387(6633): 569-572. doi:10.1038/42408. PMID: 9177342.
40. Simons, K., and Toomre, D. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1(1): 31-39. doi:10.1038/35036052. PMID:11413487.
41. Smit, J.J., Schinkel, A.H., Mol, C.A., Majoor, D., Mooi, W.J., Jongsma, A.P., et al. 1994. Tissue distribution of the human MDR3 P-glycoprotein. Lab. Invest. 71(5): 638-649. PMID: 7734012.
42. Taylor, M.A. 1990. A larval development test for the detection of anthelmintic resistance in nematodes of sheep. Res. Vet. Sci. 49(2): 198-202. PMID:2236917.
43. Troost, J., Lindenmaier, H., Haefeli, W.E., and Weiss, J. 2004. Modulation of cellular cholesterol alters P-glycoprotein activity in multidrug-resistant cells. Mol. Pharmacol. 66(5): 1332-1339. doi:10.1124/mol.104.002329. PMID:15308763.
44. van Wyk, J.A., and Malan, F.S. 1988. Resistance of field strains of Haemonchus contortus to ivermectin, closantel, rafoxanide and the benzimidazoles in South Africa. Vet. Rec. 123(9): 226-228. PMID:3176284.
45. Wojtal, K.A., de Vries, E., Hoekstra, D., and van Ijzendoorn, S.C. 2006. Efficient trafficking of MDR1/P-glycoprotein to apical canalicular plasma membranes in HepG2 cells requires PKA-RIIalpha anchoring and glucosylceramide. Mol. Biol. Cell, 17(8): 3638-3650. doi:10.1091/mbc.E06-03-0230. PMID: 16723498.
46. Wolstenholme, A.J., Fairweather, I., Prichard, R., von Samson-Himmelstjerna, G., and Sangster, N.C. 2004. Drug resistance in veterinary helminths. Trends Parasitol. 20(10): 469-476. doi:10.1016/j.pt.2004.07.010. PMID:15363440.
47. Xu, M., Molento, M., Blackhall, W., Ribeiro, P., Beech, R., and Prichard, R. 1998. Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Mol. Biochem. Parasitol. 91(2): 327-335. doi:10.1016/S0166-6851(97)00215-6. PMID:9566525.
48. Zimniak, P., Pikula, S., Bandorowicz-Pikula, J., and Awasthi, Y.C. 1999. Mechanisms for xenobiotic transport in biological membranes. Toxicol. Lett. 106(2-3): 107-118. doi:10.1016/S0378-4274(99)00061-2. PMID:10403654.