An assessment of drug-haematin binding as a mechanism for inhibition of haematin polymerisation by quinoline antimalarials

Biochemical Pharmacology

Volumn 55, Issue 6, 1998, Pages 727-736

  Dorn, Arnulf ^a   Vippagunta, Sudha Rani ^b   Matile, Hugues ^a   Jaquet, Catherine ^a   Vennerstrom, Jonathan L ^b   Ridley, Robert G ^a,c  

^a F HOFFMANN LA ROCHE LTD   (Switzerland)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Oxo dimer; Drug haematin binding; Haematin polymerisation; Haemozoin; Malaria; Quinoline antimalarials

Indexed keywords

AMODIAQUINE; ANTIMALARIAL AGENT; CHLOROQUINE; HALOFANTRINE; HEMATIN; MEFLOQUINE; MEPACRINE; N1,N2 BIS(7 CHLORO QUINOLIN 4 YL)CYCLOHEXANE 1,2 DIAMINE; PRIMAQUINE; PYRONARIDINE; QUININE; QUINOLONE DERIVATIVE; RO 48 6910; UNCLASSIFIED DRUG;

ANTIMALARIAL ACTIVITY; ARTICLE; DRUG PROTEIN BINDING; MICROCALORIMETRY; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN POLYMERIZATION;

ANIMALS; ANTIMALARIALS; BIOPOLYMERS; ENTROPY; EVALUATION STUDIES; HEMIN; HYDROGEN-ION CONCENTRATION; PLASMODIUM FALCIPARUM; QUINOLINES; THERMODYNAMICS;

EID: 0032520664     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(97)00510-8     Document Type: Article

References (59)

1. Goldberg DE, Slater AFG. The pathway of hemoglobin degradation in malaria parasites. Parasitol Today. 8:1992;280-283.
2. Olliaro PL, Goldberg DE. The Plasmodium digestive vacuole metabolic headquarters and choice drug target . Parasitol Today. 11:1995;294-297.
3. Schacter BA. Heme catabolism by heme oxygenase physiology, regulation, and mechanism of action . Semin Hematol. 25:1988;349-369.
4. Fitch CD, Kanjananggulpan P. The state of ferriprotoporphyrin IX in malaria pigment. J Biol Chem. 262:1987;15552-15555.
5. Slater AFG, Swiggard WJ, Orton BR, Flitter WD, Goldberg DE, Cerami A, Henderson GB. An iron-carboxylate bond links the heme units of malaria pigment. Proc Natl Acad Sci USA. 88:1991;325-329.
6. Brémard C, Girerd JJ, Kowalewski P, Merlin JC, Moreau S. Spectroscopic investigations of malaria pigment. Appl Spectroscopy. 47:1993;1837-1842.
7. Bohle SD, Dinnebier RE, Madsen SK, Stephens PW. Characterization of the products of the heme detoxification pathway in malarial late trophozoites by X-ray diffraction. J Biol Chem. 272:1997;713-716.
8. Slater AFG, Cerami A. Inhibition by chloroquine of a novel haem polymerase enzyme activity in malaria trophozoites. Nature. 355:1992;167-169.
9. Egan TJ, Ross DC, Adams PA. Quinoline anti-malarial drugs inhibit spontaneous formation of β-hematin (malaria pigment). FEBS Lett. 352:1994;54-57.
10. Dorn A, Stoffel R, Matile H, Bubendorf A, Ridley RG. Malarial haemozoin/β-haematin supports haem polymerization in the absence of protein. Nature. 374:1995;269-271.
11. Sullivan DJ, Gluzman IY, Goldberg DE. Plasmodium hemozoin formation mediated by histidine-rich proteins. Science. 271:1996;219-222.
12. Ridley RG. Haemozoin formation in malaria parasites is there a haem polymerase? Trends Microbiol. 4:1996;253-254.
13. Dorn A, Vippagunta SR, Matile H, Bubendorf A, Vennerstrom JL, Ridley RG. A comparison and analysis of several ways to promote haematin (haem) polymerisation and an assessment of its initiation in vitro. Biochem Pharmacol. 55:1998;737-747.
14. Chou AC, Chevli R, Fitch CD. Ferriprotoporphyrin IX fulfills the criteria for identification as the chloroquine receptor of malaria parasites. Biochemistry. 19:1980;1543-1549.
15. Vennerstrom JL, Ellis WY, Ager AL, Andersen SL, Gerena L, Milhous WK. Bisquinolines. 1. N,N-bis(7-chloro-quinolin-4-yl)alkanediamines with potential against chloroquine-resistant malaria. J Med Chem. 35:1992;2129-2134.
16. 2-bis(7-chloro-quinolin-4-yl)cyclohexane-1,2-diamine. A comparison of two stereoisomers and a detailed evaluation of the (S,S)-enantiomer, Ro 47-7737. Antimicrob Agents Chemother. 41:1997;677-686.
17. Nodiff EA, Chatterjee S, Musallam HA. Antimalarial activity of the 8-aminoquinolines. Prog Med Chem. 28:1991;1-40.
18. Trager W, Jensen JB. Human malaria parasites in continous culture. Science. 193:1976;673-675.
19. Desjardins RE, Canfield CJ, Haynes JD, Chulay JD. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother. 16:1979;710-718.
20. Ridley RG, Hofheinz W, Matile H, Jaquet C, Dorn A, Masciadri R, Jolidon S, Richter WF, Guenzi A, Girometta M-A, Urwyler H, Huber W, Thaithong S, Peters W. 4-Aminoquinoline analogs of chloroquine with shortened side chains retain activity against chloroquine-resistant Plasmodium falciparum. Antimicrob Agents Chemother. 40:1996;1846-1854.
21. Ashong JO, Blench IP, Warhurst DC. The composition of haemozoin from Plasmodium falciparum. Trans Royal Soc Trop Med Hyg. 83:1989;167-172.
22. Freire E, Mayorga OL, Straume M. Isothermal titration calorimetry. Anal Chem. 62:1990;950A-959A.
23. Wiseman T, Williston S, Brandts JF, Lin L-N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem. 179:1989;131-137.
24. Yayon A, Cabantchik ZI, Ginsburg H. Identification of the acidic compartment of Plasmodium falciparum-infected erythrocytes as the target of the antimalarial drug chloroquine. EMBO J. 3:1984;2695-2700.
25. Krogstad DJ, Schlesinger PH, Gluzman IY. Antimalarials increase vesicle pH in Plasmodium falciparum. J Cell Biol. 101:1985;2302-2309.
26. Brown SB, Dean TC, Jones P. Aggregation of ferrihaems. Dimerization and protolytic equilibria of protoferrihaem and deuteroferrihaem in aqueous solution. Biochem J. 117:1970;733-739.
27. Silver J, Lukas B. Mössbauer studies on protoporphyrin IX iron (III) solutions. Inorg Chim Acta. 78:1983;219-224.
28. Inada Y, Shibata K. The soret band of monomeric hematin and its changes on polymerization. Biochem Biophys Res Comm. 9:1962;323-327.
29. Moreau S, Perly B, Biguet J. Interactions de la chloroquine avec la ferriprotoporphyrine IX. Étude par résonance magnétique nucléaire. Biochimie. 64:1982;1015-1025.
30. White WI. Aggregation of porphyrins and metalloporphyrins. Dolphin D. The Porphyrins Vol. V, Physical Chemistry, Part C. 1978;303-339 Academic Press, New York.
31. Gushimana Y, Doepner B, Martinez-Hackert E, Ilgenfritz G. Kinetics of quinine-deuterohemin binding. Biophys Chem. 47:1993;153-162.
32. Blokzijl W, Engberts JBFN. Hydrophobe Effekte - Ansichten und Tatsachen. Angew Chem. 105:1993;1610-1648.
33. Gilli P, Ferretti V, Gilli G, Borea PA. Enthalpy-entropy compensation in drug-receptor binding. J Phys Chem. 98:1994;1515-1518.
34. Hawley SR, Bray PG, Park BK, Ward SA. Amodiaquine accumulation in Plasmodium falciparum as a possible explanation for its superior antimalarial activity over chloroquine. Mol Biochem Parasitol. 80:1996;15-25.
35. Raynes K, Foley M, Tilley L, Deady LW. Novel bisquinoline antimalarials. Synthesis, antimalarial activity, and inhibition of haem polymerisation. Biochem Pharmacol. 52:1996;551-559.
36. Chavalitshewinkoon P, Wilairat P, Gamage S, Denny WA, Figgit D, Ralph R. Structure-activity relationships and mode of action of 9-anilinoacridines against chloroquine-resistant Plasmodium falciparum in vitro. Antimicrob Agents Chemother. 37:1993;403-406.
37. Basco LK, LeBras J. In vitro activity of pyronaridine against African strains of Plasmodium falciparum. Ann Trop Med Parasitol. 86:1992;447-454.
38. 3H-chloroquine. Am J Pathol. 67:1972;277-284.
39. Sullivan DJ Jr, Gluzman IY, Russell DG, Goldberg DE. On the molecular mechanism of chloroquine's antimalarial action. Proc Natl Acad Sci USA. 93:1996;11865-11870.
40. 3H]chloroquine by chloroquine-sensitive and chloroquine-resistant strains of Plasmodium falciparum lack of correlation of uptake and sensitivity . Biochem Pharmacol. 35:1986;3805-3812.
41. Adovelande J, Boulard Y, Berry J-P, Galle P, Slodzian G, Schrével J. Detection and cartography of the fluorinated antimalarial drug mefloquine in normal and Plasmodium falciparum infected red blood cells by scanning ion microscopy and mass spectrometry. Biol Cell. 80:1994;185-192.
42. Moreau S, Charet P, Prensier G. Affinity of antimalarial drugs for stacked haematin linked on sepharose. Ann Trop Med Parasitol. 80:1986;169-176.
43. Jearnpipatkul A, Panijpan B. Molecular complexes of quinoline antimalarials with iron-porphyrin components of protease-digested methemoglobin. Chem Biol Interactions. 33:1980;83-90.
44. Warhurst DC. The quinoline-haemin interactions and its relationship to antimalarial activity. Biochem Pharmacol. 30:1981;3323-3327.
45. Constantinidis I, Satterlee JD. UV-visible and carbon NMR studies of quinine binding to urohemin I chloride and uroporphyrin I in aqueous solution. J Am Chem Soc. 110:1988;927-932.
46. Constantinidis I, Satterlee JD. UV-visible and carbon NMR studies of chloroquine binding to urohemin I chloride and uroporphyrin I in aqueous solution. J Am Chem Soc. 110:1988;4391-4395.
47. Behere DV, Goff HM. High affinity binding of quinine to iron (III) porphyrins novel formation of alkoxide complexes from alcohols and amines . J Am Chem Soc. 106:1984;4945-4950.
48. Moreau S, Perly B, Chachaty C, Deleuze C. A nuclear magnetic resonace study of the interactions of antimalarial drugs with porphyrins. Biochim Biophys Acta. 840:1985;107-116.
49. Blauer G, Akkawi M, Bauminger ER. Further evidence for the interaction of the antimalarial drug amodiaquine with ferriprotoporphyrin IX. Biochem Pharm. 46:1993;1573-1576.
50. Adams PA, Berman PAM, Egan TJ, Marsh PJ, Silver J. The iron environment in heme and heme-antimalarial complexes of pharmacological interest. J Inorg Biochem. 63:1996;69-77.
51. Caughey WS, Barlow CH, O'Keeffe DH, O'Toole MC. Spectroscopic studies of cis and trans effects in hemes and hemins. Ann New York Acad Sci. 206:1973;296-309.
52. Macomber PB, Sprinz H, Tousimis AJ. Morphological effects of chloroquine on Plasmodium berghei in mice. Nature. 214:1967;937-939.
53. Slater AFG. Chloroquine mechanism of drug action and resistance in Plasmodium falciparum . Pharmacol Ther. 57:1993;203-235.
54. Chou AC, Fitch CD. Control of heme polymerase by chloroquine and other quinoline derivatives. Biochem Biophys Res Comm. 195:1993;422-427.
55. Asawamahasakda W, Ittarat I, Chang C-C, McElroy P, Meshnick SR. Effects of antimalarials and protease inhibitors on plasmodial hemozoin production. Mol Biochem Parasitol. 67:1994;183-191.
56. Gabay T, Krugliak M, Shalmiev G, Ginsburg H. Inhibition by anti-malarial drugs of haemoglobin denaturation and iron release in acidified red blood cell lysates - a possible mechanism of their antimalarial effect? Parasitology. 108:1994;371-381.
57. Orjih AU, Banyal HS, Chevli R, Fitch CD. Hemin lyses malaria parasites. Science. 214:1981;667-669.
58. Ginsburg H, Demel RA. The effect of ferriprotoporphyrin IX and chloroquine on phospholipid monolayers and the possible implications to antimalarial activity. Biochim Biophys Acta. 732:1983;316-319.
59. Hebbel RP, Eaton JW. Pathobiology of heme interaction with the erythrocyte membrane. Semin Hematol. 26:1989;136-149.