Sitamaquine overcomes ABC-mediated resistance to miltefosine and antimony in Leishmania

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 8, 2011, Pages 3838-3844

  Pérez Victoria, José M ^a   Bavchvarov, Boris I ^a   Torrecillas, Iván R ^b   Martínez García, Marta ^a   López Martín, Carmen ^a   Campillo, Mercedes ^b   Castanys, Santiago ^a   Gamarro, Francisco ^a  

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

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ANTIMONY TARTRATE; KETOCONAZOLE; MILTEFOSINE; PROTEIN LABCC3; PROTEIN LMDR1; PROTEIN MRPA; SITAMAQUINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; DRUG ACCUMULATION; DRUG SENSITIVITY; DRUG STRUCTURE; LEISHMANIA TROPICA; MOLECULAR DOCKING; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL;

AMINOQUINOLINES; ANTIMONY; ANTIPROTOZOAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, BACTERIAL; KETOCONAZOLE; LEISHMANIA TROPICA; LEISHMANIASIS; PHOSPHORYLCHOLINE; PROTEIN BINDING;

EID: 79960312292     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00065-11     Document Type: Article

References (47)

1. 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.
2. Bray, P. G., S. Deed, E. Fox, M. Kalkanidis, M. Mungthin, L. W. Deady, and L. Tilley. 2005. Primaquine synergises the activity of chloroquine against chloroquine-resistant P. falciparum. Biochem. Pharmacol. 70:1158-1166.
3. Castanys-Munoz, 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.
4. Castanys-Munoz, E., J. M. Perez-Victoria, F. Gamarro, and S. Castanys. 2008. Characterization of an ABCG-like transporter from the protozoan parasite Leishmania with a role in drug resistance and transbilayer lipid movement. Antimicrob. Agents Chemother. 52:3573-3579.
5. Cheng, T., et al. 2007. Computation of octanol-water partition coefficients by guiding an additive model with knowledge. J. Chem. Infect. Model. 47:2140-2148.
6. Chiquero, M. J., et al. 1998. Altered drug membrane permeability in a multidrug-resistant Leishmania tropica line. Biochem. Pharmacol. 55:131-139.
7. Coelho, A. C., S. M. Beverley, and P. C. Cotrim. 2003. Functional genetic identification of PRP1, an ABC transporter superfamily member conferring pentamidine resistance in Leishmania major. Mol. Biochem. Parasitol. 130: 83-90.
8. Cortes-Selva, F., et al. 2004. SAR studies of dihydro-beta-agarofuran sesquiterpenes as inhibitors of the multidrug-resistance phenotype in a Leishmania tropica line overexpressing a P-glycoprotein-like transporter. J. Med. Chem. 47:576-587.
9. Crowley, E., and R. Callaghan. 2010. Multidrug efflux pumps: drug binding - gates or cavity? FEBS J. 277:530-539.
10. Dawson, R. J., and K. P. Locher. 2006. Structure of a bacterial multidrug ABC transporter. Nature 443:180-185.
11. Di Pietro, A., et al. 2002. Modulation by flavonoids of cell multidrug resistance mediated by P-glycoprotein and related ABC transporters. Cell. Mol. Life Sci. 59:307-322.
12. Egan, T. J. 2006. Chloroquine and primaquine: combining old drugs as a new weapon against falciparum malaria? Trends Parasitol. 22:235-237.
13. Ford, J. M., and W. N. Hait. 1990. Pharmacology of drugs that alter multi-drug resistance in cancer. Pharmacol. Rev. 42:155-199.
14. Grondin, K., A. Haimeur, R. Mukhopadhyay, B. P. Rosen, and M. Ouellette. 1997. Co-amplification of the gamma-glutamylcysteine synthetase gene gsh1 and of the ABC transporter gene pgpA in arsenite-resistant Leishmania tarentolae. EMBO J. 16:3057-3065. (Pubitemid 27234945)
15. Hayeshi, R., C. Masimirembwa, S. Mukanganyama, and A. L. Ungell. 2006. The potential inhibitory effect of antiparasitic drugs and natural products on P-glycoprotein mediated efflux. Eur. J. Pharm. Sci. 29:70-81.
16. Kedzierski, L., et al. 2009. Leishmaniasis: current treatment and prospects for new drugs and vaccines. Curr. Med. Chem. 16:599-614.
17. Legare, D., et al. 2001. ABC proteins of Leishmania. J. Bioenerg. Biomembr. 33:469-474.
18. 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. (Pubitemid 44641711)
19. Loo, T. W., M. C. Bartlett, and D. M. Clarke. 2008. Arginines in the first transmembrane segment promote maturation of a P-glycoprotein processing mutant by hydrogen bond interactions with tyrosines in transmembrane segment 11. J. Biol. Chem. 283:24860-24870.
20. Loo, T. W., M. C. Bartlett, and D. M. Clarke. 2010. Human P-glycoprotein is active when the two halves are clamped together in the closed conformation. Biochem. Biophys. Res. Commun. 395:436-440.
21. Loo, T. W., M. C. Bartlett, and D. M. Clarke. 2009. Identification of residues in the drug translocation pathway of the human multidrug resistance P-glycoprotein by arginine mutagenesis. J. Biol. Chem. 284:24074-24087.
22. Loo, T. W., and D. M. Clarke. 2008. Mutational analysis of ABC proteins. Arch. Biochem. Biophys. 476:51-64.
23. Lopez-Martin, C., J. M. Perez-Victoria, L. Carvalho, S. Castanys, and F. Gamarro. 2008. Sitamaquine sensitivity in Leishmania species is not mediated by drug accumulation in acidocalcisomes. Antimicrob. Agents Chemother. 52:4030-4036.
24. Martin, C., et al. 2000. Communication between multiple drug binding sites on P-glycoprotein. Mol. Pharmacol. 58:624-632.
25. Mukherjee, A., et al. 2007. Role of ABC transporter MRPA, gamma-glutamylcysteine synthetase and ornithine decarboxylase in natural antimonyresistant isolates of Leishmania donovani. J. Antimicrob. Chemother. 59: 204-211.
26. Perez-Victoria, F. J., et al. 2006. Mechanisms of experimental resistance of Leishmania to miltefosine: implications for clinical use. Drug Resist. Updat. 9:26-39.
27. Perez-Victoria, J. M., et al. 1999. Correlation between the affinity of flavonoids binding to the cytosolic site of Leishmania tropica multidrug transporter and their efficiency to revert parasite resistance to daunomycin. Biochemistry 38:1736-1743.
28. Perez-Victoria, J. M., et al. 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. Perez-Victoria, J. M., et al. 2002. Multidrug resistance phenotype mediated by the P-glycoprotein-like transporter in Leishmania: a search for reversal agents. Curr. Drug Targets 3:311-333. (Pubitemid 34705094)
30. Perez-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.
31. Perez-Victoria, J. M., et al. 2001. High-affinity binding of silybin derivatives to the nucleotide-binding domain of a Leishmania tropica P-glycoproteinlike transporter and chemosensitization of a multidrug-resistant parasite to daunomycin. Antimicrob. Agents Chemother. 45:439-446.
32. Perez-Victoria, J. M., et al. 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.
33. Perez-Victoria, J. M., et al. 1999. New natural sesquiterpenes as modulators of daunomycin resistance in a multidrug-resistant Leishmania tropica line. J. Med. Chem. 42:4388-4393.
34. Pham, Y. T., et al. 2000. Interactions of racemic mefloquine and its enantiomers with P-glycoprotein in an immortalised rat brain capillary endothelial cell line, GPNT. Biochim. Biophys. Acta 1524:212-219.
35. Reed, M. B., K. J. Saliba, S. R. Caruana, K. Kirk, and A. F. Cowman. 2000. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 403:906-909.
36. Riffkin, C. D., et al. 1996. Modulation of the function of human MDR1 P-glycoprotein by the antimalarial drug mefloquine. Biochem. Pharmacol. 52:1545-1552.
37. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
38. Sanchez, C. P., A. Dave, W. D. Stein, and M. Lanzer. 2010. Transporters as mediators of drug resistance in Plasmodium falciparum. Int. J. Parasitol. 40:1109-1118.
39. Sangraula, H., K. K. Sharma, S. Rijal, S. Dwivedi, and S. Koirala. 2003. Orally effective drugs for kala-azar (visceral leishmaniasis): focus on miltefosine and sitamaquine. J. Assoc. Physicians India 51:686-690. (Pubitemid 41279895)
40. Sanner, M. F. 1999. Python: a programming language for software integration and development. J. Mol. Graph. Model. 17:57-61.
41. Seeliger, D., and B. L. de Groot. 2010. Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J. Comput. Aided Mol. Des. 24:417-422.
42. Sharom, F. J. 2008. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 9:105-127. (Pubitemid 351560534)
43. Trott, O., and A. J. Olson. 2010. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31:455-461.
44. Vanden Bossche, H., et al. 1998. Antifungal drug resistance in pathogenic fungi. Med. Mycol. 36:119-128.
45. Vezmar, M., and E. Georges. 2000. Reversal of MRP-mediated doxorubicin resistance with quinoline-based drugs. Biochem. Pharmacol. 59:1245-1252.
46. Ward, A., C. L. Reyes, J. Yu, C. B. Roth, and G. Chang. 2007. Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc. Natl. Acad. Sci. U. S. A. 104:19005-19010.
47. 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.