Potentiation of the antimalarial action of chloroquine in rodent malaria by drugs known to reduce cellular glutathione levels

Biochemical Pharmacology

Volumn 66, Issue 5, 2003, Pages 809-817

  Deharo, Eric ^a   Barkan, Daniel ^b   Krugliak, Miriam ^c   Golenser, Jacob ^b   Ginsburg, Hagai ^c  

^a Centre IRD de Guyane   (France)

^b HEBREW UNIVERSITY   (Israel)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Acetaminophen; Chloroquine; Drug potentiation; Indomethacin; Malaria; Plasmodium berghei; Plasmodium vinckei petteri

Indexed keywords

4 AMINOQUINOLINE DERIVATIVE; ACETYLCYSTEINE; AMODIAQUINE; ANTIMALARIAL AGENT; CHLOROQUINE; DISULFIRAM; GLUTATHIONE; HEMATIN; INDOMETACIN; MEFLOQUINE; PARACETAMOL; QUININE;

ACUTE TOXICITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL ACTIVITY; ARTICLE; BIOACCUMULATION; CELL LEVEL; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENCY; DRUG POTENTIATION; GLUTATHIONE METABOLISM; MALARIA; MICROBIAL DEGRADATION; MOUSE; MOUSE STRAIN; NONHUMAN; PARASITE CONTROL; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM VINCKEI; PRIORITY JOURNAL; RODENT; TOXICITY TESTING;

EID: 0041929642     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(03)00396-4     Document Type: Article

References (58)

1. Ginsburg H., Famin O., Zhang J., Krugliak M. Inhibition of glutathione-dependent degradation of heme by chloroquine and amodiaquine as a possible basis for their antimalarial mode of action. Biochem. Pharmacol. 56:1998;1305-1313.
2. Egan T.J. Structure-function relationships in chloroquine and related 4-aminoquinoline antimalarials. Mini Rev. Med. Chem. 1:2001;113-123.
3. Famin O., Krugliak M., Ginsburg H. Kinetics of inhibition of glutathione-mediated degradation of ferriprotoporphyrin IX by antimalarial drugs. Biochem. Pharmacol. 58:1999;59-68.
4. Zhang J., Krugliak M., Ginsburg H. The fate of ferriprotorphyrin IX in malaria-infected erythrocytes in conjunction with the mode of action of antimalarial drugs. Mol. Biochem. Parasitol. 99:1999;129-141.
5. Famin O., Ginsburg H. 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. 10:2003;39-50.
6. Dubois V.L., Platel D.F., Pauly G., Tribouley-Duret J. Plasmodium berghei: implication of intracellular glutathione and its related enzyme in chloroquine resistance in vivo. Exp. Parasitol. 81:1995;117-124.
7. Platel D.F.N., Mangou F., Tribouley D.J. Role of glutathione in the detoxification of ferriprotoporphyrin IX in chloroquine-resistant Plasmodium berghei. Mol. Biochem. Parasitol. 98:1999;215-223.
8. Perez-Rosado J., Gervais G.W., Ferrer R., Guez I., Peters W., Serrano A.E. Plasmodium berghei: analysis of the gamma-glutamylcysteine synthetase gene in drug-resistant lines. Exp. Parasitol. 101:2002;175-182.
9. Reed M.B., Saliba K.J., Caruana S.R., Kirk K., Cowman A.F. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature. 403:2000;906-909.
10. Sidhu A.B., Verdier-Pinard D., Fidock D.A. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science. 298:2002;210-213.
11. Borst P., Evers R., Kool M., Wijnholds J. A family of drug transporters: the multidrug resistance-associated proteins. J. Natl. Cancer Inst. 92:2000;1295-1302.
12. Bahl A., Brunk B., Crabtree J., Fraunholz M.J., Gajria B., Grant G.R., Ginsburg H., Gupta D., Kissinger J.C., Labo P., Li L., Mailman M.D., Milgram A.J., Pearson D.S., Roos D.S., Schug J., Stoeckert C.J. Jr., Whetzel P. Plasmo DB: the Plasmodium genome resource. An integrated database providing tools for accessing analyzing and mapping expression and sequence data (both finished and unfinished). Nucleic Acids Res. 30:2002;87-90.
13. Srivastava P., Puri S.K., Kamboj K.K., Pandey V.C. Glutathione-S-transferase activity in malarial parasites. Trop. Med. Int. Health. 4:1999;251-254.
14. Atamna H., Ginsburg H. The malaria parasite supplies glutathione to its host cell-investigation of glutathione transport and metabolism in human erythrocytes infected with Plasmodium falciparum. Eur. J. Biochem. 250:1997;670-679.
15. Cappellini M.D., Tavazzi D., Duca L., Graziadei G., Mannu F., Turrini F., Arese P., Fiorelli G. Metabolic indicators of oxidative stress correlate with haemichrome attachment to membrane, band 3 aggregation and erythrophagocytosis in beta-thalassaemia intermedia. Br. J. Haematol. 104:1999;504-512.
16. Tavazzi D., Comino A., Turrini F., Fiorelli G., Cappellini M.D. Indices of membrane alterations in beta-thalassemic erythrocytes. Hemoglobin. 22:1998;483-492.
17. Black M. Acetaminophen hepatotoxicity. Annu. Rev. Med. 35:1984;577-593.
18. Hinson J.A., Pike S.L., Pumford N.R., Mayeux P.R. Nitrotyrosine-protein adducts in hepatic centrilobular areas following toxic doses of acetaminophen in mice. Chem. Res. Toxicol. 11:1998;604-607.
19. Prescott L.F., Roscoe P., Wright N., Brown S.S. Plasma-paracetamol half-life and hepatic necrosis in patients with paracetamol overdosage. Lancet. 1:1971;519-522.
20. 2+. J. Biol. Chem. 260:1985;13035-13040.
21. Mitchell J.R., Jollow D.J., Potter W.Z., Gillette J.R., Brodie B.B. Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione. J. Pharmacol. Exp. Ther. 187:1973;211-217.
22. Uhlig S., Wendel A. Glutathione enhancement in various mouse organs and protection by glutathione isopropyl ester against liver injury. Biochem. Pharmacol. 39:1990;1877-1881.
23. Shao R., Ring S.C., Tarloff J.B. Coincubation of rat renal proximal tubules with hepatic subcellular fractions potentiates the effects of para-aminophenol. Fundam. Appl. Toxicol. 39:1997;101-108.
24. Hoffmann K.J., Axworthy D.B., Baillie T.A. Mechanistic studies on the metabolic activation of acetaminophen in vivo. Chem. Res. Toxicol. 3:1990;204-211.
25. Vane J.R. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat. New Biol. 231:1971;232-235.
26. Kulmacz R.J., Lands W.E. Stoichiometry and kinetics of the interaction of prostaglandin H synthase with anti-inflammatory agents. J. Biol. Chem. 260:1985;12572-12578.
27. Tanaka J., Yuda Y. Lipid peroxidation in gastric mucosal lesions induced by indomethacin in rat. Biol. Pharm. Bull. 19:1996;716-720.
28. Golenser J., Kamyl M., Tsafack A., Marva E., Cohen A., Kitrossky N., Chevion M. Correlation between destruction of malarial parasites by polymorphonuclear leucocytes and oxidative stress. Free Radic. Res. Commun. 17:1992;249-262.
29. Nnalue N.A., Friedman M.J. Evidence for a neutrophil-mediated protective response in malaria. Parasite Immunol. 10:1988;47-58.
30. Urban T., Jarstrand C., Wahlgren M., Berzins K. Detection and semiquantitative determination of antibodies against Plasmodium falciparum in human blood serum: NBT-reduction by polymorphonuclear leukocytes. J. Clin. Lab. Immunol. 25:1988;143-147.
31. Kumaratilake L.M., Rathjen D.A., Mack P., Widmer F., Prasertsiriroj V., Ferrante A. A synthetic tumor necrosis factor-alpha agonist peptide enhances human polymorphonuclear leukocyte-mediated killing of Plasmodium falciparum in vitro and suppresses Plasmodium chabaudi infection in mice. J. Clin. Invest. 95:1995;2315-2323.
32. Johansson B. A review of the pharmacokinetics and pharmacodynamics of disulfiram and its metabolites. Acta Psychiatr. Scand. Suppl. 369:1992;15-26.
33. Nagendra S.N., Shetty K.T., Subhash M.N., Guru S.C. Role of glutathione reductase system in disulfiram conversion to diethyldithiocarbamate. Life Sci. 49:1991;23-28.
34. Kelner M.J., Alexander N.M. Inhibition of erythrocyte superoxide dismutase by diethyldithiocarbamate also results in oxyhemoglobin-catalyzed glutathione depletion and methemoglobin production. J. Biol. Chem. 261:1986;1636-1641.
35. Burkitt M.J., Bishop H.S., Milne L., Tsang S.Y., Provan G.J., Nobel C.S., Orrenius S., Slater A.F. Dithiocarbamate toxicity toward thymocytes involves their copper-catalyzed conversion to thiuram disulfides which oxidize glutathione in a redox cycle without the release of reactive oxygen species. Arch. Biochem. Biophys. 353:1998;73-84.
36. Cen D., Gonzalez R.I., Buckmeier J.A., Kahlon R.S., Tohidian N.B., Meyskens F.L. Jr. Disulfiram induces apoptosis in human melanoma cells: a redox-related process. Mol. Cancer Ther. 1:2002;197-204.
37. Meshnick S.R., Scott M.D., Lubin B., Ranz A., Eaton J.W. Antimalarial activity of diethyldithiocarbamate. Potentiation by copper. Biochem. Pharmacol. 40:1990;213-216.
38. Peters W., Robinson B.L. The chemotherapy of rodent malaria. 47. Studies on pyronaridine and other mannich base antimalarials. Ann. Trop. Med. Parasitol. 86:1992;455-465.
39. Kucukardali Y., Cinan U., Acar H.V., Ozkan S., Top C., Nalbant S., Cermik H., Cankir Z., Danaci M. Comparison of the therapeutic efficacy of 4-methylpyrazole and N-acetylcysteine on acetaminophen (paracetamol) hepatotoxicity in rats. Curr. Med. Res. Opin. 18:2002;78-81.
40. +ATPase activity is related to disulfide bridge formation in subunit E as well as subunit A. Plant J. 28:2001;51-59.
41. Deneke S.M. Thiol-based antioxidants. Curr. Top. Cell Regul. 36:2000;151-180.
42. Clark I.A., Rockett K.A. Nitric oxide and parasitic disease. Adv. Parasitol. 37:1996;37-56.
43. Krishna S., Pukrittayakamee S., Supanaranond W., ter Kuile F., Ruprah M., Sura T., White N.J. Fever in uncomplicated Plasmodium falciparum malaria: randomized double-blind comparison of ibuprofen and paracetamol treatment. Trans. R. Soc. Trop. Med. Hyg. 89:1995;507-509.
44. Brandts C.H., Ndjave M., Graninger W., Kremsner P.G. Effect of paracetamol on parasite clearance time in Plasmodium falciparum malaria. Lancet. 350:1997;704-709.
45. Fasan P.O., Mabadeje A.F. A controlled trial of a combination of chloroquine with paracetamol in the treatment of acute malaria in a semi-immune population. J. Trop. Med. Hyg. 83:1980;191-193.
46. Mansor S.M., Edwards G., Roberts P.J., Ward S.A. The effect of malaria infection on paracetamol disposition in the rat. Biochem. Pharmacol. 41:1991;1707-1711.
47. Ismail S., Kokwaro G.O., Back D.J., Edwards G. Effect of malaria infection on the pharmacokinetics of paracetamol in rat. Xenobiotica. 24:1994;527-533.
48. Kokwaro G.O., Glazier A.P., Ward S.A., Breckenridge A.M., Edwards G. Effect of malaria infection and endotoxin-induced fever on phenacetin O-deethylation by rat liver microsomes. Biochem. Pharmacol. 45:1993;1235-1241.
49. Glazier A.P., Kokwaro G.O., Ismail S., Edwards G. Effect of an experimental malaria infection on the metabolism of phenacetin in the rat isolated perfused liver. Xenobiotica. 24:1994;785-793.
50. Ismail S., Na B.K., Karbwang J., Back D.J., Edwards G. Paracetamol disposition in Thai patients during and after treatment of falciparum malaria. Eur. J. Clin. Pharmacol. 48:1995;65-69.
51. Wilairatana P., Looareesuwan S., Kaojarern S., Vanijanonta S., Charoenlarp P. Gastric emptying in acute uncomplicated falciparum malaria. J. Trop. Med. Hyg. 98:1995;22-24.
52. Metz S.A. Anti-inflammatory agents as inhibitors of prostaglandin synthesis in man. Med. Clin. North Am. 65:1981;713-757.
53. Dunn M.J., Grone H.J. The relevance of prostaglandins in human hypertension. Adv. Prostaglandin Thromboxane Leukot. Res. 13:1985;179-187.
54. Sharma S., Sharma S.C. An update on eicosanoids and inhibitors of cyclooxygenase enzyme systems. Indian J. Exp. Biol. 35:1997;1025-1031.
55. Yang C.F., Xiao L.H., Tongren J.E., Sullivan J., Lal A.A., Collins W.E. Cytokine production in rhesus monkeys infected with Plasmodium coatneyi. Am. J. Trop. Med. Hyg. 61:1999;226-229.
56. Riley E.M., MacLennan C., Kwiatkowski D.K., Greenwood B.M. Suppression of in vitro lymphoproliferative responses in acute malaria patients can be partially reversed by indomethacin. Parasite Immunol. 11:1989;509-517.
57. Perkins D.J., Kremsner P.G., Weinberg J.B. Inverse relationship of plasma prostaglandin E2 and blood mononuclear cell cyclooxygenase-2 with disease severity in children with Plasmodium falciparum malaria. J. Infect. Dis. 183:2001;113-118.
58. Wolchok J.D., Williams L., Pinto J.T., Fleisher M., Krown S.E., Hwu W.J., Livingston P.O., Chang C., Chapman P.B. Phase I trial of high dose paracetamol and carmustine in patients with metastatic melanoma. Melanoma Res. 13:2003;189-196.