Structural specificity of chloroquine-hematin binding related to inhibition of hematin polymerization and parasite growth

Journal of Medicinal Chemistry

Volumn 42, Issue 22, 1999, Pages 4630-4639

  Vippagunta, Sudha Rani ^a   Dorn, Arnulf ^b   Matile, Hugues ^b   Bhattacharjee, Apurba K ^c   Karle, Jean M ^c   Ellis, William Y ^c   Ridley, Robert G ^b   Vennerstrom, Jonathan L ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; HEMATIN;

ANTIMALARIAL ACTIVITY; ARTICLE; BINDING AFFINITY; DRUG PROTEIN BINDING; DRUG SCREENING; DRUG SPECIFICITY; DRUG STRUCTURE; ENTHALPY; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN POLYMERIZATION; STOICHIOMETRY;

EID: 0033523894     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm9902180     Document Type: Article

References (94)

1. Bray, P. G.; Ward, S. A. A Comparison of the Phenomenology and Genetics of Multidrug Resistance in Cancer Cells and Quinoline Resistance in Plasmodium falciparum. Pharmacol. Ther. 1998, 77, 1-28.
2. (a) Ridley, R. G. Haemoglobin Degradation and Haem Polymerization as Antimalarial Drug Targets. J. Pharm. Pharmacol. 1997, 49S, 43-48.
3. (b) Ridley, R. G.; Dorn, A.; Vippagunta, S. R.; Vennerstrom, J. L. Haematin (haem) Polymerization and its Inhibition by Quinoline Antimalarials. Ann. Trop. Med. Parasitol. 1987, 91, 559-566.
4. (a) Chou, A. C.; Chevli, R.; Fitch, C. D. Ferriprotoporphyrin IX Fulfills the Criteria for Identification as the Chloroquine Receptor of Malaria Parasites. Biochemistry 1980,19, 1543-1549.
5. (b) Egan, T. J.; Mavuso, W. W.; Ross, D. C.; Marques, H. M. Thermodynamic Factors Controlling the Interaction of Quinoline Antimalarial Drugs With Ferriprotoporphyrin IX. J. Inorg. Biochem. 1997, 68, 137-145.
6. (c) Sullivan, D. J., Jr.; Gluzman, I. Y.; Russell, D. G.; Goldberg, D. E. On the Molecular Mechanism of Chloroquine's Antimalarial Action. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 11865-11870.
7. (d) Sullivan, D. J., Jr.; Matile, H.; Ridley, R. G.; Goldberg, D. E. A Common Mechanism for Blockade of Heme Polymerization by Antimalarial Quinolines. J. Biol. Chem. 1998, 273, 31103-31107.
8. (e) Bray, P. G.; Mungthin, M.; Ridley, R. G.; Ward, S. A. Access to Hematin: The Basis of Chloroquine Resistance. Mol. Pharmacol. 1998, 54, 170-179.
9. (f) Dorn, A.; Vippagunta, S. R.; Matile, H.; Jaquet, C.; Vennerstrom, J. L.; Ridley, R. G. An Assessment of Drug-Hematin Binding as a Mechanism for Inhibition of Hematin Polymerisation by Quinoline Antimalarials. Biochem. Pharmacol. 1998, 55, 727-736.
10. (a) Slater, A. F. G.; Cerami, A. Inhibition By Chloroquine of a Novel Haem Polymerase Enzyme Activity in Malaria Trophozoites. Nature 1992, 355, 167-169.
11. (b) Orjih, A. U.; Fitch, C. D. Hemozoin Production by Plasmodium falciparum: Variation With Strain and Exposure to Chloroquine. Biochim. Biophys. Acta 1993, 1157, 270-274.
12. (c) Egan, T. J.; Ross, D. C.; Adams, P. A. Quinoline Anti-Malarial Drugs Inhibit Spontaneous Formation of β-Hematin (Malaria Pigment). FEES Lett. 1994, 352, 54-57.
13. (d) Dorn, A.; Stoffel, R.; Matile, H.; Bubendorf, A.; Ridley, R. G. Malarial Haemozoin/β-Hematin Supports Haem Polymerization in the Absence of Protein. Nature 1995, 374, 269-271.
14. (a) Chou, A. C.; Fitch, C. D. Hemolysis of Mouse Erythrocytes by Ferriprotoporphyrin IX and Chloroquine. J. Clin. Invest. 1980, 66, 856-858.
15. (b) Orjih, A. U.; Banyal, H. S.; Chevli, R.; Fitch, C. D. Hemin Lyses Malaria Parasites. Science 1881, 214, 667-669.
16. (c) Ginsburg, H.; Demel, R. A. The Effect of Ferriprotoporphyrin IX and Chloroquine on Phospholipid Monolayers and the Possible Implications to Antimalarial Activity. Biochim. Biophys. Acta 1983, 732, 316-319.
17. (d) Hebbel, R. P.; Eaton, J. W. Pathobiology of Heme Interaction with the Erythrocyte Membrane. Semin. Hematol. 1989, 26, 136-149.
18. (e) 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. 1998, 56, 1305-1313.
19. (f) Sugioka, Y.; Suzuki, M. The Chemical Basis for the Ferriprotoporphyrin IX-Chloroquine Complex Induced Lipid Peroxidation. Biochim. Biophys. Acta 1991, 1074, 19-24.
20. (a) Fiteh, C. D.; Kanjananggulpan, P. The State of Ferriprotoporphyrin IX in Malaria Pigment. J. Biol. Chem. 1987, 262, 15552-15555.
21. (b) Slater, A. F. G.; Swiggard, W. J.; Orton, B. R.; Flitter, W. D.; Goldberg, D. E.; Cerami, A.; Henderson, G. B. An Iron-Carboxylate Bond Links the Heme Units of Malaria Pigment. Proc. Natl Acad. Sci. U.S.A. 1991, 88, 325-329.
22. (c) Bohle, S. D.; Dinnebier, R. E.; Madsen, S.; Stephens, P. W. Characterization of the Products of the Heme Detoxification Pathway in Malarial Late Trophozoites by X-ray Diffraction. J. Biol. Chem. 1997, 272, 713-716.
23. Moreau, S.; Perly, B.; Biguet, J. Interactions de la Chloroquine Avec la Ferriprotoporphyrine DC. Étude par Résonance Magné tique Nucléaire. Biochimie 1982, 64, 1015-1025.
24. Adams, P. A.; Berman, P. A. M.; Egan, T. J.; Marsh, P. J.; Silver, J. The Iron Environment in Heme and Heme-Antimalarial Complexes of Pharmacological Interest. J. Inorg. Biochem. 1996, 63, 69-77.
25. (a) Cohen, S. N.; Phifer, K. O.; Yielding, K. L. Complex Formation Between Chloroquine and Ferrihaemic Acid In Vitro, and its Effect on the Antimalarial Action of Chloroquine. Nature 1964, 202, 805-806.
26. (b) Blauer, G.; Ginsburg, H. Complexes of Antimalarial Drugs with Ferriprotoporphyrin IX, Biochem. Int. 1982, 5, 519-523.
27. (c) Jearnpipatkul, A.; Govitrapong, P.; Yuthavong, Y.; Wilairat, P.; Panijpan, B. Binding of Antimalarial Drugs to Hemozoin from Plasmodium berghei. Experientia 1980, 36, 1063-1064.
28. (d) Jearnpipatkul, A.; Panijpan, B. Molecular complexes of quinoline antimalarials with iron-porphyrin components of protease-digested methemoglobin. Chem. Biol. Interact. 1980, 33, 83-90.
29. de Almeida Ribeiro, M. C.; Augusto, O.; da Costa Ferreira, A. M. Inhibitory Effect of Chloroquine on the Peroxidase Activity of Ferriprotoporphyrin DC. J. Chem. Soc., Dalton Trans. 1995, 3759-3766.
30. O'Neill, P. M.; Bray, P. G.; Hawley, S. R.; Ward, S. A.; Park, B. K. 4-Aminoquinolines-Past, Present, and Future: A Chemical Perspective. Pharmacol. Ther. 1998, 77, 29-58.
31. Price, C. C.; Roberts, R. M. The Synthesis of 4-Hydroxyquinolines. I. Through Ethoxymethylenemalonic Ester. J. Am. Chem. Soc. 1946, 68, 1204-1208.
32. De, D.; Krogstad, F. M.; Cogswell, F. B.; Krogstad, D. J. Aminoquinolines that Circumvent Resistance in Plasmodium falciparum In Vitro. Am. J. Trop. Med. Hyg. 1996, 55, 579-583.
33. Surrey, A. R.; Hammer, H. F. Some 7-Substituted 4-Aminoquinoline Derivatives. J. Am. Chem. Soc. 1946, 68, 113-116.
34. (a) Yayon, A.; Cabantchik, Z. I.; Ginsburg, H. Identification of the Acidic Compartment of Plasmodium falciparum-Infected Erythrocytes as the Target of the Antimalarial Drug Chloroquine. EMBO J. 1984, 3, 2695-2700.
35. (b) Krogstad, D. J.; Schlesinger, P. H.; Gluzman, I. Y. Antimalarials Increase Vesicle pH in Plasmodium falciparum. J. Cell. Biol. 1985, 101, 2302-2309.
36. (a) Brown, S. B.; Dean, T. C.; Jones, P. Aggregation of Ferrihaems. Dimerization and Protolytic Equilibria of Protoferrihaem and Deuterioferrihaem in Aqueous Solution. Biochem. J. 1970, 117, 733-739.
37. (b) Silver, J.; Lukas, B. Mössbauer Studies on Protoporphyrin IX Iron(III) Solutions. Inorg. Chim. Acta 1983, 78, 219-224.
38. (c) Bednarski, T. M.; Jordan, J. Electron-Transfer Characteristics of the Prosthetic Group of Hemoproteins. J. Am. Chem. Soc. 1967, 89, 1552-1558,
39. -1 at pH 4.8 (ref 16a) still strongly favors the μ-oxo dimer.
40. White, W. I. Aggregation of Porphyrins and Metalloporphyrins. In The Porphyrins, Vol. V; Dolphin, D., Ed.; Physical Chemistry, Part C; Academic Press: New York, 1978; pp 303-339.
41. Diederich, F.; Smithrud, D. B.; Sanford, E. M.; Wyman, T. B.; Ferguson, S. B.; Carcanague, D. R.; Chao, I.; Houk, K. N. Solvent Effects in Molecular Recognition. Acta Chem. Scand. 1992, 46, 205-215.
42. Lemieux, R. U. How Water Provides the Impetus for Molecular Recognition in Aqueous Solution. Ace. Chem. Res. 1990, 29, 373-380.
43. Lumry, R.; Rajender, S. Enthalpy-Entropy Compensation Phenomena in Water Solutions of Proteins and Small Molecules: A Ubiquitous Property of Water. Biopolyners 1970, 9, 1125-1227.
44. Blokzijl, W.; Engberts, J. B. F. N. Hydrophobe Effekte -Ansichten und Tatsachen. Angew. Chem. 1993, 105, 1610-1648.
45. Muller, N. Search for a Realistic View of Hydrophobic Effects. Ace. Chem. Res. 1990, 23, 24-28.
46. Gilli, P.; Ferretti, V.; Gilli, G.; Borea, P. A. Enthalpy-Entropy Compensation in Drug-Receptor Binding. J. Phys. Chem. 1994, 98, 1515-1518.
47. (a) Hunter, C. A.; Sanders, J. K. M. The Nature of π-π Interactions. J. Am. Chem. Soc. 1990, 112, 5525-5534.
48. (b) Hunter, C. A. Arene-Arene Interactions: Electrostatic or Charge Transfer? Angew. Chem., Int. Ed. Engl. 1993, 32, 1584-1586.
49. (a) Ridley, R. G.; Hofheinz, W.; Matile, H.; Jaquet, C.; Dorn, A.; Masciadri, R.; Jolidon, S.; Richter, W. F.; Guenzi, A.; Girometta, M. A.; Urwyler, H.; Huber, W.; Thaithong, C.; Peters, W. 4-Aminoquinoline Analogues of Chloroquine With Shortened Side Chains Retain Acitivity Against Chioroquine-Resistant Plasmodium falciparum. Antimicrob. Agents Chemother. 1996, 40, 1846-1854.
50. (b) De, D.; Krogstad, F. M.; Byers, L. D.; Krogstad, D. J. Structure-Activity Relationships for Antiplasmodial Activity among 7-Substituted 4-AminoquinolineB. J. Med. Chem. 1998, 41, 4918-4926.
51. (a) Geary, T. G.; Divo, A. A.; Jensen, J. B. Activity of Quinoline Containing Antimalarials Against Chloroquine-Sensitive and Resistant Strains of Plasmodium falciparum In Vitro. Trans. R. Soc. Trop. Med. Hyg. 1987, 81, 499-503.
52. (b) Aderounmu, A. F. In Vitro Assessment of the Antimalarial Activity of Chloroquine and Its Major Metabolites. Ann. Trop. Med. Parasitol. 1984, 78, 581-585.
53. Veignei, E.; Moreau, S. The Mode of Action of Chloroquine. Non-Weak Base Properties of 4-Aminoquinolines and Antimalarial Effects on Strains of Plasmodium. Ann. Trop. Med. Parasitol. 1991, 85, 229-237.
54. Bray, P. G.; Hawley, S. R.; Mungthin, M.; Ward, S. A. Physico-chemical Properties Correlated with Drug Resistance and the Reversal of Drug Resistance in Plasmodium falciparum. Mol. Pharmacol. 1996, 50, 1559-1566.
55. Hawley, S. R.; Bray, P. G.; Mungthin, M.; Atkinson, J. D.; O'Neill, P. M.; Ward, S. A. Relationship Between Antimalarial Drug Activity, Accumulation, and Inhibition of Heme Polymerization in Plasmodium falciparum In Vitro. Antimicrob. Agents Chemother. 1998, 42, 682-686.
56. O'Neill, P. M.; Willock, D. J.; Hawley, S. R.; Bray, P. G.; Storr, R. C.; Ward, S. A.; Park, B. K. Synthesis, Antimalarial Activity, and Molecular Modeling of Tebuquine Analogues. J. Med. Chem. 1997, 40, 437-448.
57. Vippagunta, S. R.; Dorn, A.; Ridley, R. G.; Vennerstrom, J. L. Unpublished results.
58. Koh, H. L.; Go, M. L.; Ngiam, T. L.; Mark, J. W. Conformational and Structural Features Determining In Vitro Antimalarial Activity in Some Indolo[3,2-c]Quinolines, Anilinoquinolines and Tetrahydroindolo[3,2-d]Benzazepines. Eur. J. Med. Chem. 1994, 29, 107-113.
59. diethyl distances are 8.615 Å (3-21G*) and 8.508 Å from X-ray data (Karle, J. M.; Karle, I. L. Redetermination of the Molecular Structure of the Antimalarial Chloroquine Bis-(dihydrogenphosphate) Dihydrate. Acta Crystallogr. 1988, C44, 1605-1608).
60. Constantinides, I.; Satterlee, J. D. UV-Visible and Carbon NMR Studies of Chloroquine Binding to Urohemin I Chloride and Uroporphyrin I in Aqueous Solutions. J. Am. Chem. Soc. 1988, 110, 4391-4395.
61. Caughey, W S.; Barlow, C. H.; O'Keeffe, D. H.; O'Toole, M. C. Spectroscopic Studies of Cis and Trans Effects in Hemes and Hemins. Ann. N.Y. Acad. Sci. 1973, 206, 296-309.
62. Heaton, N. J.; Bello, P.; Herradón, B.; del Campo, A.; Jiménez-Barbero, J. NMR Study of Intramolecular Interactions between Aromatic Groups: van der Waals, Charge-Transfer, or Quadrupolar Interactions? J. Am. Chem. Soc. 1988, 120, 12371-12384.
63. Schneider, H.; Wang, M. Ligand-Porphyrin Complexes: Quantitative Evaluation of Stacking and Ionic Contributions. J. Org. Chem. 1994, 59, 7464-7472.
64. Ferrari, V.; Cutler, D. J. Temperature Dependence of the Acid Dissociation Constants of Chloroquine. J. Pharm. Sci. 1987, 76, 554-556.
65. Macomber, D. B.; Sprinz, H.; Tousimis, A. J. Morphological Effects of Chloroquine on Plasmodium berghei in Mice. Nature 1967, 214, 937.
66. Fitch, C. D.; Chevli, R.; Gonzalez, Y. Chloroquine-Resistant Plasmodium falciparum: Effect of Substrate on Chloroquine and Amodiaquine Accumulation. Antimicrob. Agents Chemother. 1974, 6, 757-762.
67. Hawley, S. R.; Bray, P. G.; O'Neill, P. M.; Kevin Park, B.; Ward, S. A. The Role of Drug Accumulation in 4-Aminoquinoline Antimalarial Potency. Biochem. Pharmacol. 1996, 52, 723-733.
68. (a) Vippagunta, S. R.; Dorn, A.; Bubendorf, A.; Ridley, R. G.; Vennerstrom, J. L. Deferoxamine: Stimulation of Hematin Polymerization and Antagonism of its Inhibition by Chloroquine. Biochem. Pharmacol. 1998, 58, 817-824.
69. (b) Blauer, G.; Ginsburg, H. Complexes of Antimalarial Drugs With Ferriprotoporphyrin IX. Biochem. Int. 1982, 5, 519-523.
70. (c) Grinberg, L. N.; Soprunov, F. F. Metabolism of Erythrocyte Infected with Malaria Parasite and the Action of Antimalarial Drugs Biomed. Biochim. Acta 1983, 11/12, S317-S321.
71. Saliba, K. J.; FoIb, P. I.; Smith, P. J. Role for the Plasmodium falciparum Digestive Vacuole in Chloroquine Resistance. Biochem. Pharmacol. 1998, 56, 313-320.
72. Bass, G. E.; Hudson, D. R.; Parker, J. E.; Purcell, W. P. Mechanism of Antimalarial Activity of Chloroquine Analogues From Quantitative Structure Activity Studies. Free Energy Related Model. J. Med. Chem. 1971, 14, 275-282.
73. Thompson, P. E.; Werbel, L. M. 4-Aminoquinolines. Antimalarial Agents: Chemistry and Pharmacology; Academic Press: New York, 1972; pp 150-193.
74. Coatney, G. R.; Cooper, W. C.; Eddy, N. B.; Greenberg, J. Survey of Antimalarial Agents; Public Health Monograph No. 9; U.S. Government Printing Office: Washington, DC, 1953.
75. Su, X.; Kirkman, L A.; Fujioka, H.; Wellems, T. E. Complex Polymorphisms in an ∼330 Kda Protein are Linked to Chloroquine-Resistant P. falciparum in Southeast Asia and Africa. Cell 1997, 91, 593-603.
76. Wünsch, S.; Sanchez, C. P.; Gekle, M.; Grobe-Wortmann, L.; Wiesner, J. Differential Stimulation of the Na±/H± Exchanger Determines Chloroquine Uptake in Plasmodium falciparum. J. Cell. Biol. 1998, 140, 335-345.
77. Ridley, R. G.; Hudson, A. T. Quinoline Antimalarials. Exp. Opin. Ther. Patents 1998, 8, 121-135.
78. Carmack, M.; Bullitt, Jr., O. H.; Handrick, G. R.; Kissinger, L. W.; Von, I. The Synthesis of 4-(4-Amino-1-methylbutylamino)-7-chloroquinoline and Some 4-(4-Monoalkylamino-1-methylbutylamino)-7-chloroquinolines. J. Am. Chem. Soc. 1946, 68, 1220-1225.
79. Drake, N. L.; Creech, H. J.; Garman, J. A.; Haywood, S. T.; Peck, R. M.; VanHook, J. O.; Walton, E. Synthetic Antimalarials. The Preparation of Certain 4-Aminoquinolines. J. Am. Chem. Soc. 1946, 68, 1208-1213.
80. Price, C. C.; Leonard, N. J.; Reitsema, R. H. Synthesis of 4-Hydroxyquinolines. V. A Direct Synthesis from β-Anilinoacrylates. J. Am. Chem. Soc. 1946, 68, 1256-1259.
81. Steck, E. A.; Hallock, L. L.; Holland, A. J.; Fletcher, L. T. Quinolines. V. Some Polysubstituted 4-(4′-Diethylamino-1′-methylbutylamino)quinolines. J. Am. Chem. Soc. 1948, 70, 1012-1015.
82. Steck, E. A.; Hallock, L. L.; Holland, A. J. Quinolines. III. The Synthesis of 5- and 7-Chloro and Bromo-3-methyl-4-dialkyl-aminoalkylaminoquinolines. J. Am. Chem. Soc. 1946, 68, 380-383.
83. Hofheinz, W.; Jaquet, C.; Jolidon, S. Aminochinolin-Derivate mit einer Wirksamkeit gegen Malariaerreger. European Patent Application 94116281.0, June 1995.
84. Baker, R. H.; Dodson, R. M.; Riegel, B. The Dealkylation of 4-(4-Diethylamino-1-methylbutylamino)-7-chloroquinoline, SN 7618. J. Am. Chem. Soc. 1947, 69, 704.
85. Ellis, J.; Gellert, E.; Robson, J. Synthesis of Some New Iodoquinolines. Aust. J. Chem. 1973, 26, 907-911.
86. Baker, R. H.; Lappin, G. R.; Albisetti, C. J., Jr.; Riegel, B. The Decarboxylation of Nitro Substituted 3-Carboxy-4-quinolinols by Pyrolysis of Their Silver Salts. J Am. Chem. Soc. 1946, 68, 1267.
87. Bevington, P. R. Data Reduction and Error Analysis in the Physical Sciences; McGraw-Hill: New York, 1969; p 236.
88. Ashong, J. O.; Blench, I. P.; Warhurst, D. C. The Composition of Haemozoin from Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 1989, 83, 167-172.
89. Trager, W.; Jensen, J. B. Human Malaria Parasites in Continuous Culture. Science 1976, 193, 673-675.
90. Desjardins, R. E.; Canfield, C. J.; Haynes, J. D.; Chulay, J. D. Quantitative Assessment of Antimalarial Activity In Vitro by a Semiautomated Microdilution Technique. Antimicrob, Agents Chemother. 1979, 16, 710-718.
91. Fleischer, E. B.; Srivastava, T. S. The structure and properties of μ-Oxo bis(tetraphenylporphineiron (III)). J. Am. Chem. Soc. 1969, 91, 2403-2405.
92. Halgren, T. A. Merck Molecular Force Field. 1. Basis, Form, Scope, Parametrization, and Performance of MMFF94. J. Comput. Chem. 1996, 17, 490-641.
93. Politzer, P.; Truhlar, D. G. Chemical Applications of Atomic and Molecular Electrostatic Potentials; Plenum: New York, 1981.
94. Naray-Szabo, G.; Ferenczy, G. G. Molecular Electrostatics. Chem. Rev. 1995, 95, 829-847.