Characterization of an ABCG-like transporter from the protozoan parasite Leishmania with a role in drug resistance and transbilayer lipid movement

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 10, 2008, Pages 3573-3579

  Castanys Muñoz, Esther ^a   Pérez Victoria, José María ^a   Gamarro, Francisco ^a   Castanys, Santiago ^a  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABCG TRANSPORTER; AMPHOTERICIN B; ANTILEISHMANIAL AGENT; CAMPTOTHECIN; CARBON 14; CHLOROQUINE; EDELFOSINE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; KETOCONAZOLE; MEFLOQUINE; MILTEFOSINE; PAROMOMYCIN; PERIFOSINE; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE; PHOSPHOLIPID; PRIMAQUINE; SITAMAQUINE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; DRUG ACCUMULATION; DRUG STRUCTURE; ENDOCYTOSIS; GENE EXPRESSION; INTERNALIZATION; ISOTOPE LABELING; LEISHMANIA; LEISHMANIASIS; LIPID BILAYER; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VISCERAL LEISHMANIASIS;

AMINOQUINOLINES; ANIMALS; ANTIPROTOZOAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CHLOROQUINE; DNA, PROTOZOAN; DRUG RESISTANCE; FLUORESCENT DYES; GENES, PROTOZOAN; HUMANS; LEISHMANIA INFANTUM; LEISHMANIASIS, VISCERAL; LIPID BILAYERS; PHOSPHORYLCHOLINE; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; TRANSFORMATION, GENETIC;

EID: 54049089634     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00587-08     Document Type: Article

References (38)

1. Araújo-Santos, J. M., F. Gamarro, S. Castanys, A. Herrmann, and T. Pomorski. 2003. Rapid transport of phospholipids across the plasma membrane of Leishmania infantum. Biochem. Biophys. Res. Commun. 306:250-255.
2. Araújo-Santos, J. M., A. Parodi-Talice, S. Castanys, and F. Gamarro. 2005. The overexpression of an intracellular ABCA-like transporter alters phospholipid trafficking in Leishmania. Biochem. Biophys. Res. Commun. 330:349-355.
3. Barraud de Lagerie, S., E. Comets, C. Gautrand, C. Fernandez, D. Auchere, E. Singlas, F. Mentre, and F. Gimenez. 2004. Cerebral uptake of mefloquine enantiomers with and without the P-gp inhibitor elacridar (GF1210918) in mice. Br. J. Pharmacol. 141:1214-1222.
4. Bird, D., F. Beisson, A. Brigham, J. Shin, S. Greer, R. Jetter, L. Kunst, X. Wu, A. Yephremov, and L. Samuels. 2007. Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J. 52:485-498.
5. BoseDasgupta, S., A. Ganguly, A. Roy, T. Mukherjee, and H. K. Majumder. 2008. A novel ATP-binding cassette transporter, ABCG6 is involved in chemoresistance of Leishmania. Mol. Biochem. Parasitol. 158:176-188.
6. Castanys-Muñoz, E., N. Alder-Baerens, T. Pomorski, F. Gamarro, and S. Castanys. 2007. A novel ATP-binding cassette transporter from Leishmania is involved in transport of phosphatidylcholine analogues and resistance to alkyl-phospholipids. Mol. Microbiol. 64:1141-1153.
7. Chappuis, F., S. Sundar, A. Hailu, H. Ghalib, S. Rijal, R. W. Peeling, J. Alvar, and M. Boelaert. 2007. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat. Rev. Microbiol. 5:873-882.
8. Chiquero, M. J., J. M. Perez-Victoria, F. O'Valle, J. M. Gonzalez-Ros, R. G. del Moral, J. A. Ferragut, S. Castanys, and F. Gamarro. 1998. Altered drug membrane permeability in a multidrug-resistant Leishmania tropica line. Biochem. Pharmacol. 55:131-139.
9. Croft, S. L., S. Sundar, and A. H. Fairlamb. 2006. Drug resistance in leishmaniasis. Clin. Microbiol. Rev. 19:111-126.
10. Cserepes, J., Z. Szentpetery, L. Seres, C. Ozvegy-Laczka, T. Langmann, G. Schmitz, H. Glavinas, I. Klein, L. Homolya, A. Varadi, B. Sarkadi, and N. B. Elkind. 2004. Functional expression and characterization of the human ABCG1 and ABCG4 proteins: indications for heterodimerization. Biochem. Biophys. Res. Commun. 320:860-867.
11. Graf, G. A., L. Yu, W. P. Li, R. Gerard, P. L. Tuma, J. C. Cohen, and H. H. Hobbs. 2003. ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion. J. Biol. Chem. 278:48275-48282.
12. Ha, D. S., J. K. Schwarz, S. J. Turco, and S. M. Beverley. 1996. Use of the green fluorescent protein as a marker in transfected Leishmania. Mol. Biochem. Parasitol. 77:57-64.
13. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113.
14. Ivens, A. C., C. S. Peacock, E. A. Worthey, L. Murphy, G. Aggarwal, M. Berriman, E. Sisk, M. A. Rajandream, E. Adlem, R. Aert, A. Anupama, Z. Apostolou, P. Attipoe, N. Bason, C. Bauser, A. Beck, S. M. Beverley, G. Bianchettin, K. Borzym, G. Bothe, C. V. Bruschi, M. Collins, E. Cadag, L. Ciarloni, C. Clayton, R. M. Coulson, A. Cronin, A. K. Cruz, R. M. Davies, J. De Gaudenzi, D. E. Dobson, A. Duesterhoeft, G. Fazelina, N. Fosker, A. C. Frasch, A. Fraser, M. Fuchs, C. Gabel, A. Goble, A. Goffeau, D. Harris, C. Hertz-Fowler, H. Hilbert, D. Horn, Y. Huang, S. Klages, A. Knights, M. Kube, N. Larke, L. Litvin, A. Lord, T. Louie, M. Marra, D. Masuy, K. Matthews, S. Michaeli, J. C. Mottram, S. Muller-Auer, H. Munden, S. Nelson, H. Norbertczak, K. Oliver, S. O'Neil, M. Pentony, T. M. Pohl, C. Price, B. Purnelle, M. A. Quail, E. Rabbinowitsch, R. Reinhardt, M. Rieger, J. Rinta, J. Robben, L. Robertson, J. C. Ruiz, S. Rutter, D. Saunders, M. Schafer, J. Schein, D. C. Schwartz, K. Seeger, A. Seyler, S. Sharp, H. Shin, D. Sivam, R. Squares, S. Squares, V. Tosato, C. Vogt, G. Volckaert, R. Wambutt, T. Warren, H. Wedler, J. Woodward, S. Zhou, W. Zimmermann, D. F. Smith, J. M. Blackwell, K. D. Stuart, B. Barrell, et al. 2005. The genome of the kinetoplastid parasite, Leishmania major. Science 309:436-442.
15. Kennedy, M. L., F. Cortes-Selva, J. M. Pérez-Victoria, I. A. Jimenez, A. G. Gonzalez, O. M. Muñoz, F. Gamarro, S. Castanys, and A. G. Ravelo. 2001. Chemosensitization of a multidrug-resistant Leishmania tropica line by new sesquiterpenes from Maytenus magellanica and Maytenus chubutensis. J. Med. Chem. 44:4668-4676.
16. Kirk, K., and K. J. Saliba. 2001. Chloroquine resistance and the pH of the malaria parasite's digestive vacuole. Drug Resist. Updat. 4:335-337.
17. Kobayashi, A., Y. Takanezawa, T. Hirata, Y. Shimizu, K. Misasa, N. Kioka, H. Arai, K. Ueda, and M. Matsuo. 2006. Efflux of sphingomyelin, cholesterol and phosphatidylcholine by ABCG1. J. Lipid Res. 47:1791-1802.
18. Kusuhara, H., and Y. Sugiyama. 2007. ATP-binding cassette, subfamily G (ABCG family). Pflugers Arch. 453:735-744.
19. Lario, A., A. Gonzalez, and G. Dorado. 1997. Automated laser-induced fluorescence DNA sequencing: equalizing signal-to-noise ratios significantly enhances overall performance. Anal. Biochem. 247:30-33.
20. Leprohon, P., D. Legare, I. Girard, B. Papadopoulou, and M. Ouellette. 2006. Modulation of Leishmania ABC protein gene expression through life stages and among drug-resistant parasites. Eukaryot. Cell 5:1713-1725.
21. 2+. Biochem. J. 322:251-257.
22. Mullin, K. A., B. J. Foth, S. C. Ilgoutz, J. M. Callaghan, J. L. Zawadzki, G. I. McFadden, and M. J. McConville. 2001. Regulated degradation of an endoplasmic reticulum membrane protein in a tubular lysosome in Leishmania mexicana. Mol. Biol. Cell 12:2364-2377.
23. Oerlemans, R., J. van der Heijden, J. Vink, B. A. Dijkmans, G. J. Kaspers, W. F. Lems, G. L. Scheffer, I. Ifergan, R. J. Scheper, J. Cloos, Y. G. Assaraf, and G. Jansen. 2006. Acquired resistance to chloroquine in human CEM T cells is mediated by multidrug resistance-associated protein 1 and provokes high levels of cross-resistance to glucocorticoids. Arthritis Rheum. 54:557-568.
24. Parodi-Talice, A., J. M. Araújo, C. Torres, J. M. Pérez-Victoria, F. Gamarro, and S. Castanys. 2003. The overexpression of a new ABC transporter in Leishmania is related to phospholipid trafficking and reduced infectivity. Biochim. Biophys. Acta 1612:195-207.
25. Pérez-Victoria, F. J., S. Castanys, and F. Gamarro. 2003. Leishmania donovani resistance to miltefosine involves a defective inward translocation of the drug. Antimicrob. Agents Chemother. 47:2397-2403.
26. Pérez-Victoria, F. J., F. Gamarro, M. Ouellette, and S. Castanys. 2003. Functional cloning of the miltefosine transporter. A novel P-type phospholipid translocase from Leishmania involved in drug resistance. J. Biol. Chem. 278:49965-49971.
27. Pérez-Victoria, F. J., M. P. Sanchez-Canete, K. Seifert, S. L. Croft, S. Sundar, S. Castanys, and F. Gamarro. 2006. Mechanisms of experimental resistance of Leishmania to miltefosine: implications for clinical use. Drug Resist. Updat. 9:26-39.
28. Pérez-Victoria, J. M., F. Cortes-Selva, A. Parodi-Talice, B. I. Bavchvarov, F. J. Pérez-Victoria, F. Munoz-Martinez, M. Maitrejean, M. P. Costi, D. Barron, A. Di Pietro, S. Castanys, and F. Gamarro. 2006. Combination of suboptimal doses of inhibitors targeting different domains of LtrMDR1 efficiently overcomes resistance of Leishmania spp. to miltefosine by inhibiting drug efflux. Antimicrob. Agents Chemother. 50:3102-3110.
29. Pérez-Victoria, J. M., A. Parodi-Talice, C. Torres, F. Gamarro, and S. Castanys. 2001. ABC transporters in the protozoan parasite Leishmania. Int. Microbiol. 4:159-166.
30. Pérez-Victoria, J. M., F. J. Pérez-Victoria, A. Parodi-Talice, I. A. Jimenez, A. G. Ravelo, S. Castanys, and F. Gamarro. 2001. Alkyl-lysophospholipid resistance in multidrug-resistant Leishmania tropica and chemosensitization by a novel P-glycoprotein-like transporter modulator. Antimicrob. Agents Chemother. 45:2468-2474.
31. Pohl, A., P. F. Devaux, and A. Herrmann. 2005. Function of prokaryotic and eukaryotic ABC proteins in lipid transport. Biochim. Biophys. Acta 1733:29-52.
32. Pomorski, T., and A. K. Menon. 2006. Lipid flippases and their biological functions. Cell. Mol. Life Sci. 63:2908-2921.
33. Sano, O., A. Kobayashi, K. Nagao, K. Kumagai, N. Kioka, K. Hanada, K. Ueda, and M. Matsuo. 2007. Sphingomyelin-dependence of cholesterol efflux mediated by ABCG1. J. Lipid Res. 48:2377-2384.
34. Valderramos, S. G., and D. A. Fidock. 2006. Transporters involved in resistance to antimalarial drugs. Trends Pharmacol. Sci. 27:594-601.
35. van Meer, G., D. Halter, H. Sprong, P. Somerharju, and M. R. Egmond. 2006. ABC lipid transporters: extruders, flippases, or flopless activators? FEBS Lett. 580:1171-1177.
36. Velamakanni, S., S. L. Wei, T. Janvilisri, and H. W. van Veen. 2007. ABCG transporters: structure, substrate specificities and physiological roles: a brief overview. J. Bioenerg. Biomembr. 39:465-471.
37. Wang, R. B., C. L. Kuo, L. L. Lien, and E. J. Lien. 2003. Structure-activity relationship: analyses of P-glycoprotein substrates and inhibitors. J. Clin. Pharm. Ther. 28:203-228.
38. Wu, C. P., A. Klokouzas, S. B. Hladky, S. V. Ambudkar, and M. A. Barrand. 2005. Interactions of mefloquine with ABC proteins, MRP1 (ABCC1) and MRP4 (ABCC4) that are present in human red cell membranes. Biochem. Pharmacol. 70:500-510.