The treatment of Plasmodium falciparum-infected erythrocytes with chloroquine leads to accumulation of ferriprotoporphyrin IX bound to particular parasite proteins and to the inhibition of the parasite's 6-phosphogluconate dehydrogenase

Parasite

Volumn 10, Issue 1, 2003, Pages 39-50

  Famin, O ^a   Ginsburg, H ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Chloroquine; Enzyme inhibition; Ferriprotoporphyrin IX; Malaria; Plasmodium falciparum; Protein binding

Indexed keywords

CHLOROQUINE; HEMATIN; ANTIMALARIAL AGENT; FERRIPROTOPORPHYRIN IX CHLOROQUINE COMPLEX; FERRIPROTOPORPHYRIN IX-CHLOROQUINE COMPLEX; HEMIN; PHOSPHOGLUCONATE DEHYDROGENASE; PROTOZOAL PROTEIN;

ARTICLE; BIOMINERALIZATION; CONTROLLED STUDY; CYTOSOL; DEGRADATION; DETOXIFICATION; DRUG RECEPTOR BINDING; ERYTHROCYTE; GLYCOLYSIS; NONHUMAN; PLASMODIUM FALCIPARUM; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; ERYTHROCYTE MEMBRANE; HUMAN; KINETICS; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PROTEIN BINDING;

PLASMODIUM FALCIPARUM;

ANIMALS; ANTIMALARIALS; CHLOROQUINE; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; GLYCOLYSIS; HEMIN; HUMANS; KINETICS; MALARIA, FALCIPARUM; PHOSPHOGLUCONATE DEHYDROGENASE; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTOZOAN PROTEINS;

EID: 0038312099     PISSN: 1252607X     EISSN: None     Source Type: Journal    
DOI: 10.1051/parasite/2003101p39     Document Type: Article

References (51)

1. ALANO P., PREMAWANSA S., BRUCE M.C. & CARTER R. A stage specific gene expressed at the onset of gametocytogenesis in Plasmodium falciparum. Molecular and Biochemical Parasitology, 1991, 46, 81-88.
2. ATAMNA H., PASCARMONA G. & GINSBURG H. Hexose-monophosphate shunt activity in intact Plasmodium falciparum infected erythrocytes and in free parasites. Molecular and Biochemical Parasitology, 1994, 67, 79-89.
3. ATAMNA H. & GINSBURG H. Heme degradation in the presence of glutathione - A proposed mechanism to account for the high levels of non-heme iron found in the membranes of hemoglobinopathic red blood cells. Journal of Biological Chemistry, 1995, 270, 24876-24883.
4. BEUTLER E. Red Cell Metabolism. A Manual of Biochemical Methods. Grune & Stratton. New York, 1984.
5. BONNEFOY S., ATTAL G., LANGSLEY G., TEKAIA F. & MERCEREAU-PUIJALON O. Molecular characterization of the heat shock protein 90 gene of the human malaria parasite Plasmodium falciparum. Molecular and Biochemical Parasitology, 1994, 67, 157-170.
6. BRAY P.G., JANNEH O., RAYNES K.J., MUNGTHIN M., GINSBURG H. & WARD S.A. Cellular uptake of chloroquine is dependent on binding to ferriprotoporphyrin IX and is independent of NHE activity in Plasmodium falciparum. Journal of Cell Biology, 1999, 145, 363-376.
7. BUCKLING A.G.J., TAYLOR L.H., CARLTON J.M.R. & READ A.F. Adaptive changes in Plasmodium transmission strategies following chloroquine chemotherapy. Proceedings of the Royal Society, London (Biology), 1997, 264, 553-559.
8. BUCKLING A., RANFORD-CARTWRIGHT L.C., MILES A. & READ A.F. Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology, 1999, 118, 339-346.
9. BUTCHER G.A. Antimalarial drugs and the mosquito transmission of Plasmodium. International Journal of Parasitology, 1997, 27, 975-987.
10. CARLTON J., MACKINNON M. & WALLIKER D. A chloroquine resistance locus in the rodent malaria parasite Plasmodium chabaudi. Molecular and Biochemical Parasitology, 1998, 93, 57-72.
11. DUTTAROY A., BOURBEAU D., WANG X.L. & WANG E. Apoptosis rate can be accelerated or decelerated by overexpression or reduction of the level of elongation factor-1α. Experimental Cell Research, 1998, 238, 168-176.
12. EGAN T.J., COMBRINCK J.M., EGAN J., HEARNE G.R., MARQUES H.M., NTENTENI S., SEWELL B.T., SMITH P.J., TAYLOR D., VAN SCHALKWYK D.A. & WALDEN J.C. The fate of haem iron in the malaria parasite Plasmodium falciparum. Biochemical Journal 2002, 365, 343-347.
13. FAMIN O., KRUGLIAK M. & GINSBURG H. Kinetics of inhibition of glutathione-mediated degradation of ferriprotoporphyrin IX by antimalarial drugs. Biochemical Pharmacology, 1999, 58, 59-68.
14. FAMIN O. & GINSBURG H. Differential effects of 4-aminoquinoline- containing antimalarial drugs on hemoglobin digestion in Plasmodium falciparum-infected erythrocytes. Biochemical Pharmacology, 2002, 63, 393-398.
15. FRANCIS R.T. Jr & BECKER R.R. Specific indication of homeoproteins in polacrylamide gels using a double-staining process. Analytical Biochemistry, 1984, 136, 509-514.
16. FRANCIS S.E., SULLIVAN D.J. Jr & GOLDBERG D.E. Hemoglobin metabolism in the malaria parasite Plasmodium falciparum. Annual Reviews in Microbiology, 1997, 57, 97-123.
17. GAUTRET P., LANDAU I., TAILHARDAT L., MILTGEN F., COQUELIN F., VOZA T., CHABAUD A.G. & JACQUEMIN J.L. The effects of subcurative doses of chloroquine on Plasmodium vinckei petteri gametocytes and on their infectivity to mosquitoes. International Journal of Parasitology, 2000, 30, 1193-1198.
18. GINSBURG H., FAMIN O., ZHANG J.M. & KRUGLIAK M. Inhibition of glutathione-dependent degradation of heme by chloroquine and amodiaquine as a possible basis for their antimalarial mode of action. Biochemical Pharmacology, 1998, 56, 1305-1313.
19. GINSBURG H. & KRUGLIAK M. Chloroquine - some open questions on its antimalarial mode of action and resistance. Drug Resistance Update, 1999, 2, 180-187.
20. GOLDBERG D.E. & SLATER A.F. Plasmodium and the infected erythrocyte - the pathway of hemoglobin degradation in malaria parasite. Parasitology Today, 1992, 8, 280-283.
21. KANAANI J. & GINSBURG H. Metabolic interconnection between the human malarial parasite Plasmodium falciparum and its host erythrocyte: Regulation of ATP levels by means of an adenylate translocator and adenylate kinase. Journal of Biological Chemistry, 1989, 264, 3194-3199.
22. KAPPES B., SUETTERLIN B.W., HOFER-WARBINEK R., HUMAR R. & FRANKLIN R.M. Two major phosphoproteins of Plasmodium falciparum are heat shock proteins. Molecular and Biochemical Parasitology, 1993, 59, 83-94.
23. KNOWLES G., DAVIDSON W.L., JOLLEY D. & ALPERS M.P. The relationship between the in vitro response of Plasmodium falciparum to chloroquine, quinine and mefloquine. Transactions of the Royal Socity of Tropical Medicine and Hygiene, 1984, 78, 146-150.
24. KRUGLIAK M. & GINSBURG H. Studies on the antimalarial mode of action of quinoline-containing drugs: time-dependence and irreversibility of drug action, and interactions with compounds that alter the function of the parasite's food vacuole. Life Sciences, 1991, 49, 1213-1219.
25. KUMAR N., NAGASAWA H., SACCI J.B. JR, SINA B.J., AIKAWA M., ATKINSON C., UPARANUKRAW P., KUBIAK L.B., AZAD A.F. & HOLLINGDALE M.R. Expression of members of the heat-shock protein-70 family in the exoerythrocytic stages of Plasmodium berghei and Plasmodium falciparum. Parasitology Research, 1993, 79, 109-113.
26. KUTNER S., BREUER W.V., GINSBURG H., ALEY S.B. & CABANTCHIK Z.I. Characterization of permeation pathways in the plasma membrane of human erythrocytes infected with early stages of Plasmodium falciparum: association with parasite development. Journal of Cell Physiology, 1985, 725, 521-527.
27. LAMBROS C.J. & VANDERBERG J.P. Synchronization of Plasmodium falciparum erythrocytic stages in culture. Journal of Parasitology, 1979, 65, 418-420.
28. LAMBROS C. & NOTSCH J.D. Plasmodium falciparum: mefloquine resistance produced in vitro. Bulletin of the World Health Organization, 1984, 62, 433-438.
29. LEE P., YE Z., VAN DYKE K. & KIRK R.G. X-ray microanalysis of Plasmodium falciparum and infected red blood cells: effect of qinghaosu and chloroquine on potassium, sodium, and phosphorus composition. American Journal of Tropical Medicine and Hygiene, 1988, 39, 157-165.
30. LOBO C.A., KONINGS R.N.H. & KUMAR N. Expression of early gametocyte-stage antigens Pfg27 and Pfs16 in synchronized gametocytes and non-gametocyte producing clones of Plasmodium falciparum. Molecular and Biochemical Parasitology, 1994, 68, 151-154.
31. LORIA P., MILLER S., FOLEY M. & TILLEY L. Inhibition of the peroxidative degradation of haem as the basis of action of chloroquine and other quinoline antimalarials. Biochemical Journal, 1999, 339, 363-370.
32. MALHOTRA K., SALMON D., LE B. & VILDE J.L. Potentiation of chloroquine activity against Plasmodium falciparum by the peroxidase-hydrogen peroxide system. Antimicrobial Agents and Chemotherapy, 1990, 34, 1981-1985.
33. MENTING J.G., TILLEY L., DEADY L.W., NG K., SIMPSON R.J., COWMAN A.F. & FOLEY M. The antimalarial drug, chloroquine, interacts with lactate dehydrogenase from Plasmodium falciparum. Molecular and Biochemical Parasitology, 1997, 88, 215-224.
34. MERKLI B. & RICHLE R.W. Studies on the resistance to single and combined antimalarials in the Plasmodium berghei mouse model. Acta Tropica, 1980, 37, 228-231.
35. MONTI D., BASILICO N., PARAPINI S., PASINI E., OLLIARO P. & TAKAMELLI D. Does chloroquine really act through oxidative stress? FEBS Letters, 2002, 522, 3-5.
36. READ J.A., WILKINSON K.W., TRANTER R., SESSIONS R.B. & BRADY R.L. Chloroquine binds in the cofactor binding site of Plasmodium falciparum lactate dehydrogenase. Journal of Biological Chemistry, 1999, 274, 10213-10218.
37. SCHEIBEL T. & BUCHNER J. The Hsp90 complex - a super-chaperone machine as a novel drug target. Biochemical Pharmacology, 1998, 56, 675-682.
38. SHERMAN I.W. Biochemistry of Plasmodium (Malarial Parasites). Microbiological Reviews, 1979, 43, 453-493.
39. SINDEN R.E., BUTCHER G.A., BILLKER O. & FLECK S.L. Regulation of infectivity of Plasmodium to the mosquito vector. Advances in Parasitology, 1996, 38, 53-117.
40. Su X.Z. & WELLEMS T.E. Sequence, transcript characterization and polymorphisms of a Plasmodium falciparum gene belonging to the heat-shock protein HSP 90 family. Gene. 1994, 151, 225-230.
41. SUROLIA N. & PADMANABAN G. Chloroquine inhibits heme-dependent protein synthesis in Plasmodium falciparum. Proceedings of the National Academy of the USA 1991, 88, 4786-4790.
42. TARDIEUX I., BAINES I., MOSSAKOWSKA M. & WARD G.E. Actin-binding proteins of invasive malaria parasites and the regulation of actin polymerization by a complex of 32/34-kDa proteins associated with heat shock protein 70 kDa. Molecular and Biochemical Parasitology, 1998, 93, 295-308.
43. VINKENOOG R., SPERANCA M.A., VAN BREEMEN O., RAMESAR J., WILLIAMSON D.H., ROSS-MACDONALD P.B., THOMAS A.W., JANSE C.J., DEL PORTILLO H.A. & WATERS A.P. Malaria parasites contain two identical copies of an elongation factor 1-α gene. Molecular and Biochemical Parasitology, 1998, 94, 1-12.
44. WARD S.A., BRAY P.G., MUNGTHIN M. & HAWLEY S.R. Current views on the mechanisms of resistance to quinoline-containing drugs in Plasmodium falciparum. Annals of Tropical Medicine and Parasitology, 1995, 89, 121-124.
45. WEBSTER H.K., BOUDREAU E.F., PAVANAND K., YONGVANITCHIT K. & PANG L.W. Antimalarial drug susceptibility testing of Plasmodium falciparum in Thailand using a microdilution method. American Journal of Tropical Medicine and Hygiene, 1985a, 34, 228-235.
46. WEBSTER H.K., THAITHONG S., PAVANAND K., YONGVANITCHIT K., PINSWASDI C. & BOUDREAU E.F. Cloning and characterization of mefloquine-resistant Plasmodium falciparum from Thailand. American Journal of Tropical Medicine and Hygiene, 1985b, 34, 1022-1027.
47. Yayon A., Vande Waa J.A., Yayon M., Geary T.G. & Jensen J.B. Stage-dependent effects of chloroquine on Plasmodium falciparum in vitro. Journal of Protozoology, 1983, 30, 642-647.
48. YAYON A., TIMBERG R., FRIEDMAN S. & GINSBURG H. Effects of chloroquine on the feeding mechanism of the intraerythrocytic human malarial parasite Plasmodium falciparum. Journal of Protozoology, 1984, 31, 367-372.
49. ZEREZ C.R. & TANAKA K.R. A continuous spectrophotometric assay for pyrimidine-5′-nucleotidase. Analytical Biochemistry, 1985, 151, 282-285.
50. ZEREZ C.R., HSEIH J.W. & TANAKA K.R. Inhibition of red blood cell enzymes by hemin: a mechanism for hemolysis in hemoglobinopathies. American Journal of Tropical Medicine and Hygiene, 1987, 100, 329-338.
51. ZHANG J.M., KRUGLIAK M. & GINSBURG H. The fate of ferriprotorphyrin IX in malaria infected erythrocytes in conjunction with the mode of action of antimalarial drugs. Molecular and Biochemical Parasitology, 1999, 99, 129-141.