A verapamil-sensitive chloroquine-associated H+ leak from the digestive vacuole in chloroquine-resistant malaria parasites

Journal of Cell Science

Volumn 121, Issue 10, 2008, Pages 1624-1632

  Lehane, Adele M ^a   Hayward, Rhys ^a   Saliba, Kevin J ^a,b   Kirk, Kiaran ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b Canberra Hospital   (Australia)

Author keywords

Chloroquine; Chloroquine resistance; Lysosome; Malaria

Indexed keywords

CHLOROQUINE; CONCANAMYCIN A; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; VERAPAMIL;

ALKALINIZATION; ANTIBIOTIC SENSITIVITY; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL SECRETION; CELL VACUOLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME INHIBITION; IC 50; MALARIA; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTON TRANSPORT; SENSITIVITY ANALYSIS; STRAIN DIFFERENCE;

ANIMALS; ANTIMALARIALS; CALCIUM CHANNEL BLOCKERS; CHLOROQUINE; DRUG RESISTANCE; ENZYME INHIBITORS; HYDROGEN; HYDROGEN-ION CONCENTRATION; MACROLIDES; PERMEABILITY; PLASMODIUM FALCIPARUM; PROTON PUMPS; VACUOLES; VERAPAMIL;

PLASMODIUM FALCIPARUM;

EID: 46249086673     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.016758     Document Type: Article

References (62)

1. Allen, R. J. W. and Kirk, K. (2004). The membrane potential of the intraerythrocytic malaria parasite Plasmodium falciparum. J. Biol. Chem. 279, 11264-11272.
2. Alleva, L. M. and Kirk, K. (2001). Calcium regulation in the intraerythrocytic malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 117, 121-128.
3. Bennett, T. N., Kosar, A. D., Ursos, L. M. B., Dzekunov, S., Sidhu, A. B. S., Fidock, D. A. and Roepe, P. D. (2004). Drug resistance-associated PfCRT mutations confer decreased Plasmodium falciparum digestive vacuolar pH. Mol. Biochem. Parasitol. 133, 99-114.
4. Bray, P. G., Mungthin, M., Ridley, R. G. and Ward, S. A. (1998). Access to hematin: the basis of chloroquine resistance. Mol. Pharmacol. 54, 170-179.
5. Bray, P. G., Janneh, O., Raynes, K. J., Mungthin, M., Ginsburg, H. and Ward, S. A. (1999). Cellular uptake of chloroquine is dependent on binding to ferriprotoporphyrin IX and is independent of NHE activity in Plasmodium falciparum. J. Cell Biol. 145, 363-376.
6. Bray, P. G., Martin, R. E., Tilley, L., Ward, S. A., Kirk, K. and Fidock, D. A. (2005). Defining the role of PfCRT in Plasmodium falciparum chloroquine resistance. Mol. Microbiol. 56, 323-333.
7. Bray, P. G., Mungthin, M., Hastings, I. M., Biagini, G. A., Saidu, D. K., Lakshmanan, V., Johnson, D. J., Hughes, R. H., Stocks, P. A., O'Neill, P. M. et al. (2006). PfCRT and the trans-vacuolar proton electrochemical gradient: regulating the access of chloroquine to ferriprotoporphyrin IX. Mol. Microbiol. 62, 239-251.
8. Chen, N., Russell, B., Fowler, E., Peters, J. and Cheng, Q. (2002). Levels of chloroquine resistance in Plasmodium falciparum are determined by loci other than pfcrt and pfmdr1. J. Infect. Dis. 185, 405-407.
9. Cooper, R. A., Ferdig, M. T., Su, X. Z., Ursos, L. M. B., Mu, J., Nomura, T., Fujioka, H., Fidock, D. A., Roepe, P. D. and Wellems, T. E. (2002). Alternative mutations at position 76 of the vacuolar transmembrane protein PfCRT are associated with chloroquine resistance and unique stereospecific quinine and quinidine responses in Plasmodium falciparum. Mol. Pharmacol. 61, 35-42.
10. Demaurex, N. (2002). pH homeostasis of cellular organelles. News Physiol. Sci. 17, 1-5.
11. Demaurex, N., Furuya, W., D'Souza, S., Bonifacino, J. S. and Grinstein, S. (1998). Mechanism of acidification of the trans-Golgi network (TGN). In situ measurements of pH using retrieval of TGN38 and furin from the cell surface. J. Biol. Chem. 273, 2044-2051.
12. Desjardins, R. E., Canfield, C. J., Haynes, J. D. and Chulay, J. D. (1979). Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob. Agents Chemother. 16, 710-718.
13. Duraisingh, M. T. and Cowman, A. F. (2005). Contribution of the pfmdr1 gene to antimalarial drug-resistance. Acta Trop. 94, 181-190.
14. Dzekunov, S. M., Ursos, L. M. B. and Roepe, P. D. (2000). Digestive vacuolar pH of intact intraerythrocytic P. falciparum either sensitive or resistant to chloroquine. Mol. Biochem. Parasitol. 110, 107-124.
15. Ferrari, V. and Cutler, D. J. (1991). Simulation of kinetic data on the influx and efflux of chloroquine by erythrocytes infected with Plasmodium falciparum. Evidence for a drug-importer in cbloroquine-sensitive strains. Biochem. Pharmacol. 42, S167-S179.
16. Fidock, D. A., Nomura, T., Talley, A. K., Cooper, R. A., Dzekunov, S. M., Ferdig, M. T., Ursos, L. M. B., Sidhu, A. B., Naude, B., Deitsch, K. W. et al. (2000). Mutations in the P.falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol. Cell 6, 861-871.
17. Fitch, C. D. (1970). Plasmodium falciparum in owl monkeys: drug resistance and chloroquine binding capacity. Science 169, 289-290.
18. Fitch, C. D. (2004). Ferriprotoporphyrin IX, phospholipids, and the antimalarial actions of quinoline drugs. Life Sci. 74, 1957-1972.
19. Francis, S. E., Sullivan, D. J., Jr and Goldberg, D. E. (1997). Hemoglobin metabolism in the malaria parasite Plasmodium falciparum. Amin. Rev. Microbiol. 51, 97-123.
20. Gligorijevic, B., Bennett, T., McAllister, R., Urbach, J. S. and Roepe, P. D. (2006). Spinning disk confocal microscopy of live, intraerythrocytic malarial parasites. 2. Altered vacuolar volume regulation in drug resistant malaria. Biochemistry 45, 12411-12423.
21. Grabe, M. and Oster, G. (2001). Regulation of organelle acidity. J. Gen. Physiol. 117, 329-344.
22. Hayward, R., Saliba, K. J. and Kirk, K. (2006). The pH of the digestive vacuole of Plasmodium falciparum is not associated with chloroquine resistance. J. Cell Sci. 119, 1016-1025.
23. Homewood, C. A., Warhurst, D. C., Peters, W. and Baggaley, V. C. (1972). Lysosomes, pH and the anti-malarial action of chloroquine. Nature 235, 50-52.
24. Kirk, K. and Saliba, K. J. (2001). Chloroquine resistance and the pH of the malaria parasite's digestive vacuole. Drug Resist. Updat. 4, 335-337.
25. Klonis, N., Tan, O., Jackson, K., Goldberg, P., Klemba, M. and Tilley, L. (2007). Evaluation of pH during cytostomal endocytosis and vacuolar catabolism of haemoglobin in Plasmodium falciparum. Biochem. J. 407, 343-354.
26. Krogstad, D. J., Schlesinger, P. H. and Gluzman, I. Y. (1985). Antimalarials increase vesicle pH in Plasmodium falciparum. J. Cell Biol. 101, 2302-2309.
27. Krogstad, D. J., Gluzman, I. Y., Kyle, D. E., Oduola, A. M., Martin, S. K., Milhous, W. K. and Schlesinger, P. H. (1987). Efflux of chloroquine from Plasmodium falciparum: mechanism of chloroquine resistance. Science 238, 1283-1285.
28. Kahn, Y., Rohrbach, P. and Lanzer, M. (2007). Quantitative pH measurements in Plasmodium falciparum-infected erythrocytes using pHluorin. Cell. Microbiol. 9, 1004-1013.
29. Llopis, J., McCaffery, J. M., Miyawaki, A., Farquhar, M. G. and Tsien, R. Y. (1998). Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. USA 95, 6803-6808.
30. + "leak". J. Biol. Chem. 266, 24540-24548.
31. Martin, R. E. and Kirk, K. (2004). The malaria parasite's chloroquine resistance transporter is a member of the drug/metabolite transporter superfamily. Mol. Biol. Evol. 21, 1938-1949.
32. Martin, R. E. and Kirk, K. (2007). Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood 109, 2217-2224.
33. Martin, S. K., Oduola, A. M. and Mithous, W. K. (1987). Reversal of chloroquine resistance in Plasmodium falciparum by verapamil. Science 235, 899-901.
34. Martinoia, E., Massonneau, A. and Frangne, N. (2000). Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol. 41, 1175-1186.
35. Meredith, D. (2004). Site-directed mutation of arginine 282 to glutamate uncouples the movement of peptides and protons by the rabbit proton-peptide cotransporter PepT1. J. Biol. Chem. 279, 15795-15798.
36. Mu, J., Ferdig, M. T., Feng, X., Joy, D. A., Duan, J., Furuya, T., Subramanian, G., Aravind, L., Cooper, R. A., Wootton, J. C. et al. (2003). Multiple transporters associated with malaria parasite responses to chloroquine and quinine. Mol. Microbiol. 49, 977-989.
37. Naude, B., Brzostowski, J. A., Kimmel, A. R. and Wellems, T. E. (2005). Dictyostelium discoideum expresses a malaria chloroquine resistance mechanism upon transfection with mutant, but not wild-type, Plasmodium falciparum transporter PfCRT. J. Biol. Chem. 280, 25596-25603.
38. Orjih, A. U., Ryerse, J. S. and Fitch, C. D. (1994). Hemoglobin catabolism and the killing of intraerythrocytic Plasmodium falciparum by chloroquine. Experientia 50, 34-39.
39. Paul, F., Roath, S., Melville, D., Warhurst, D. C. and Osisanya, J. O. (1981). Separation of malaria-infected erythrocytes from whole blood: use of a selective high-gradient magnetic separation technique. Lancet 2, 70-71.
40. Reeves, D. C., Liebelt, D. A., Lakshmanan, V., Roepe, P. D., Fidock, D. A. and Alkabas, M. H. (2006). Chloroquine-resistant isoforms of the Plasmodium falciparum chloroquine resistance transporter acidify lysosomal pH in HEK293 cells more than chloroquine-sensitive isoforms. Mol. Biochem. Parasitol. 150, 288-299.
41. +-ATPase. J. Biol. Chem. 274, 33213-33219.
42. Saliba, K. J., Folb, P. I. and Smith, P. J. (1998a). Role for the Plasmodium falciparum digestive vacuole in chloroquine resistance. Biochem. Pharmacol. 56, 313-320.
43. Saliba, K. J., Horner, H. A. and Kirk, K. (1998b). Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum. J. Biol. Chem. 273, 10190-10195.
44. +-pyrophosphatase. J. Biol. Chem. 278, 5605-5612.
45. Sanchez, C. P., Stein, W. and Lanzer, M. (2003). Trans stimulation provides evidence for a drug efflux carrier as the mechanism of chloroquine resistance in Plasmodium falciparum. Biochemistry 42, 9383-9394.
46. Sanchez, C. P., McLean, J. E., Stein, W. and Lanzer, M. (2004). Evidence for a substrate specific and inhibitable drug efflux system in chloroquine resistant Plasmodium falciparum strains. Biochemistry 43, 16365-16373.
47. Sanchez, C. P., McLean, J. E., Rohrbach, P., Fidock, D. A., Stein, W. D. and Lanzer, M. (2005). Evidence for a pfcrt-associated chloroquine efflux system in the human malarial parasite Plasmodium falciparum. Biochemistry 44, 9862-9870.
48. Sanchez, C. P., Stein, W. D. and Lanzer, M. (2007a). Is PfCRT a channel or a carrier? Two competing models explaining chloroquine resistance in Plasmodium falciparum. Trends Parasitol. 23, 332-339.
49. Sanchez, C. P., Rohrbach, P., McLean, J. E., Fidock, D. A., Stein, W. D. and Lanzer, M. (2007b). Differences in trans-stimulated chloroquine efflux kinetics are linked to PfCRT in Plasmodium falciparum. Mol. Microbiol. 64, 407-420.
50. Schapiro, F. B. and Grinstein, S. (2000). Determinants of the pH of the Golgi complex. J. Biol. Chem. 275, 21025-21032.
51. Schuldiner, S., Shirvan, A. and Linial, M. (1995). Vesicular neurotransmitter transporters: from bacteria to humans. Physiol. Rev. 75, 369-392.
52. Sidhu, A. B., Verdier-Pinard, D. and Fidock, D. A. (2002). Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298, 210-213.
53. Staalsoe, T., Giha, H. A., Dodoo, D., Theander, T. G. and Hviid, L. (1999). Detection of antibodies to variant antigens on Plasmodium falciparum-infected erythrocytes by flow cytometry. Cytometry 35, 329-336.
54. Tan, W., Gou, D. M., Tai, E., Zhao, Y. Z. and Chow, L. M. (2006). Functional reconstitution of purified chloroquine resistance membrane transporter expressed in yeast. Arch. Biochem. Biophys. 452, 119-128.
55. Tran, C. V. and Saier, M. H., Jr (2004). The principal chloroquine resistance protein of Plasmodium falciparum is a member of the drug/metabolite transporter superfamily. Microbiology 150, 1-3.
56. Trape, J. F. (2001). The public health impact of chloroquine resistance in Africa. Am. J. Trop. Med. Hyg. 64, 12-17.
57. Ursos, L. M. B., Dzekunov, S. M. and Roepe, P. D. (2000). The effects of chloroquine and verapamil on digestive vacuolar pH of P. falciparum either sensitive or resistant to chloroquine. Mol. Biochem. Parasitol. 110, 125-134.
58. van Schalkwyk, D. A. and Egan, T. J. (2006). Quinoline-resistance reversing agents for the malaria parasite Plasmodium falciparum. Drug Resist. Updat. 9, 211-226.
59. Warhurst, D. C., Craig, J. C. and Adagu, I. S. (2002). Lysosomes and drug resistance in malaria. Lancet 360, 1527-1529.
60. Wu, M. M., Grabe, M., Adams, S., Tsien, R. Y., Moore, H. P. and Machen, T. E. (2001). Mechanisms of pH regulation in the regulated secretory pathway. J. Biol. Chem. 276, 33027-33035.
61. Yayon, A., Cabantchik, Z. I. and Ginsburg, H. (1984). Identification of the acidic compartment of Plasmodium falciparum-infected human erythrocytes as the target of the antimalarial drug chloroquine. EMBO J. 3, 2695-2700.
62. Yayon, A., Cabantchik, Z. I. and Ginsburg, H. (1985). Susceptibility of human malaria parasites to chloroquine is pH dependent. Proc. Natl. Acad. Sci. USA 82, 2784-2788.