Hemozoin and antimalarial drug discovery

Future Medicinal Chemistry

Volumn 5, Issue 12, 2013, Pages 1437-1450

  Fong, Kim Y ^a   Wright, David W ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; ARTEMISININ; CHLOROQUINE; HEME; HEME OXYGENASE; HEMOGLOBIN; HEMOZOIN;

ANOPHELES; ANTIMALARIAL ACTIVITY; ANTIMALARIAL DRUG SUSCEPTIBILITY; BIOMINERALIZATION; CATABOLISM; CONCENTRATION RESPONSE; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYTOTOXICITY; DETOXIFICATION; DRUG DESIGN; DRUG HALF LIFE; DRUG SCREENING; GAMETOCYTE; HIGH THROUGHPUT SCREENING; HYDROGEN BOND; IC 50; ISOTHERMAL TITRATION CALORIMETRY; LIPID MEMBRANE; MEROZOITE; MOLECULAR INTERACTION; NONHUMAN; PARASITE SURVIVAL; PHENOTYPE; PLASMODIUM; PLASMODIUM (LIFE CYCLE STAGE); PRIORITY JOURNAL; REVIEW; TROPHOZOITE;

EID: 84881516620     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.13.113     Document Type: Review

References (85)

1. World Malaria Report. WHO press, Geneva, Switzerland (2012).
2. Teklehaimanot A, Mejia P. Malaria and poverty. Ann. NY Acad. Sci. 1136, 32-37 (2008).
3. Sigma-Tau Group. ACT to combat malaria receives marketing authorization from EMA Venture. Geneva, Switzerland (2011).
4. Matuschewski K, Nunes AC, Nussenzweig V, Menard R. Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J. 21(7), 1597-1606 (2002).
5. Prudencio M, Rodriguez A, Mota MM. The silent path to thousands of merozoites: the Plasmodium liver stage. Nat. Rev. Microbiol. 4(11), 849-856 (2006).
6. Tilley L, Dixon MWA, Kirk K. The Plasmodium falciparum-infected red blood cell. Int. J. Biochem. Cell Biol. 43(6), 839-842 (2011).
7. Goldberg DE, Slater AFG, Cerami A, Henderson GB. Hemoglobin degradation in the malaria parasite plasmodium-falciparum - an ordered process in a unique organelle. Proc. Natl Acad. Sci. USA 87(8), 2931-2935 (1990).
8. Egan TJ. Haemozoin formation. Mol. Biochem. Parasitol. 157(2), 127-136 (2008).
9. Choi AMK, Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell Mol. Biol. 15(1), 9-19 (1996).
10. Sigala PA, Crowley JR, Hsieh S, Henderson JP, Goldberg DE. Direct tests of enzymatic heme degradation by the malaria parasite Plasmodium falciparum. J. Biol. Chem. 287(45) (2012).
11. Ponka P. Cell biology of heme. Am. J. Med. Sci. 318(4), 241-256 (1999).
12. Egan TJ, Chen JYJ, de Villiers KA et al. Haemozoin (beta-haematin) biomineralization occurs by self-assembly near the lipid/water interface. FEBS Lett. 580(21), 5105-5110 (2006).
13. Marom N, Tkatchenko A, Kapishnikov S, Kronik L, Leiserowitz L. Structure and formation of synthetic hemozoin: insights from first-principles calculations. Cryst. Growth Des. 11(8), 3332-3341 (2011).
14. Klonis N, Dilanian R, Hanssen E et al. Hematin-hematin self-association states involved in the formation and reactivity of the malaria parasite pigment, hemozoin. Biochemistry 49(31), 6804-6811 (2010).
15. Slater AFG, Cerami A. Inhibition by chloroquine of a novel heme polymerase enzyme-activity in malaria trophozoites. Nature 355(6356), 167-169 (1992).
16. Sullivan DJ, Gluzman IY, Goldberg DE. Plasmodium hemozoin formation mediated by histidine-rich proteins. Science 271(5246), 219-222 (1996).
17. Jani D, Nagarkatti R, Beatty W et al. HDP - a novel heme detoxification protein from the malaria parasite. PLoS Pathogens 4(4) (2008).
18. Fitch CD, Cai GZ, Chen YF, Shoemaker JD. Involvement of lipids in ferriprotoporphyrin IX polymerization in malaria. Biochim. Biophys. Acta. 1454(1), 31-37 (1999).
19. Pandey AV, Babbarwal VK, Okoyeh JN et al. Hemozoin formation in malaria: a two-step process involving histidine-rich proteins and lipids. Biochem. Biophys. Res. Commun. 308(4), 736-743 (2003).
20. Pisciotta JM, Coppens I, Tripathi AK et al. The role of neutral lipid nanospheres in Plasmodium falciparum haem crystallization. Biochem. J. 402, 197-204 (2007).
21. Hoang AN, Ncokazi KK, de Villiers KA, Wright DW, Egan TJ. Crystallization of synthetic haemozoin (beta-haematin) nucleated at the surface of lipid particles. Dalton Trans. 39(5), 1235-1244 (2010).
22. Hoang AN, Sandlin RD, Omar A, Egan TJ, Wright DW. The neutral lipid composition present in the digestive vacuole of Plasmodium falciparum concentrates heme and mediates beta-hematin formation with an unusually low activation energy. Biochemistry, 49(47), 10107-10116 (2010).
23. Hempelmann E, Motta C, Hughes R, Ward SA, Bray PG. Plasmodium falciparum: sacrificing membrane to grow crystals? Trends Parasitol. 19(1), 23-26 (2003).
24. Stiebler R, Correa Soares JBR, Timm BL et al. On the mechanisms involved in biological heme crystallization. J. Bioenerg. Biomemb. 43(1), 93-99 (2011).
25. Kapishnikov S, Weiner A, Shimoni E et al. Oriented nucleation of hemozoin at the digestive vacuole membrane in Plasmodium falciparum. Proc. Natl Acad. Sci. USA 109(28), 11188-11193 (2012).
26. Wongsrichanalai C, Pickard AL, Wernsdorfer WH, Meshnick SR. Epidemiology of drug-resistant malaria. Lancet Infect. Dis. 2(4), 209-218 (2002).
27. Martin RE, Marchetti RV, Cowan AI, Howitt SM, Broeer S, Kirk K. Chloroquine transport via the malaria parasite's chloroquine resistance transporter. Science, 325(5948), 1680-1682 (2009).
28. Raj DK, Mu J, Jiang H et al. Disruption of a Plasmodium falciparum multidrug resistance-associated protein (PfMRP) alters its fitness and transport of antimalarial drugs and glutathione. J. Biol. Chem. 284(12), 7687-7696 (2009).
29. Ecker A, Lehane AM, Clain J, Fidock DA. PfCRT and its role in antimalarial drug resistance. Trends Parasitol. 28(11), 504-514 (2012).
30. Sanchez CP, Rohrbach P, McLean JE, Fidock DA, Stein WD, Lanzer M. Differences in trans-stimulated chloroquine efflux kinetics are linked to PfCRT in Plasmodium falciparum. Mol. Microbiol. 64(2), 407-420 (2007).
31. Achan J, Talisuna AO, Erhart A et al. Quinine, an old anti-malarial drug in a modern world: role in the treatment of malaria. Malar. J. 10(144) (2011).
32. Sullivan DJ, Gluzman IY, Russell DG, Goldberg DE. On the molecular mechanism of chloroquine's antimalarial action. Proc. Natl Acad. Sci. USA 93(21), 11865-11870 (1996).
33. Egan TJ, Ncokazi KK. Quinoline antimalarials decrease the rate of beta-hematin formation. J. Inorg. Biochem. 99(7), 1532-1539 (2005).
34. de Dios AC, Casabianca LB, Kosar A, Roepe PD. Structure of the amodiaquine-FPIX mu oxo dimer solution complex at atomic resolution. Inorg. Chem. 43(25), 8078-8084 (2004).
35. Vippagunta SR, Dorn A, Matile H et al. Structural specificity of chloroquine-hematin binding related to inhibition of hematin polymerization and parasite growth. J. Med. Chem. 42(22), 4630-4639 (1999).
36. de Dios AC, Tycko R, Ursos LMB, Roepe PD. NMR studies of chloroquine-ferriprotoporphyrin IX complex. J. Phys. Chem. 107(30), 5821-5825 (2003).
37. de Villiers KA, Marques HM, Egan TJ. The crystal structure of halofantrine-ferriprotoporphyrin IX and the mechanism of action of arylmethanol antimalarials. J. Inorg. Biochem. 102(8), 1660-1667 (2008).
38. de Villiers KA, Gildenhuys J, le Roex T. Iron(III) protoporphyrin IX complexes of the antimalarial cinchona alkaloids quinine and quinidine. ACS Chem. Biol. 7(4), 666-671 (2012).
39. Fitch CD. Antimalarial schizontocides - ferriprotoporphyrin-IX interaction hypothesis. Parasitol. Today 2(12), 330-331 (1986).
40. Solomonov I, Osipova M, Feldman Y et al. Crystal nucleation, growth, and morphology of the synthetic malaria pigment beta-hematin and the effect thereon by quinoline additives: the malaria pigment as a target of various antimalarial drugs. J. Am. Chem. Soc. 129(9), 2615-2627 (2007).
41. Buller R, Peterson ML, Almarsson O, Leiserowitz L. Quinoline binding site on malaria pigment crystal: a rational pathway for antimalaria drug design. Cryst. Growth Des. 2(6), 553-562 (2002).
42. Riscoe M, Kelly JX, Winter R. Xanthones as antimalarial agents: discovery, mode of action, and optimization. Curr. Med. Chem. 12(21) (2005).
43. Kelly JX, Winter R, Peyton DH, Hinrichs DJ, Riscoe M. Optimization of xanthones for antimalarial activity: the 3,6-bis-omega- diethylaminoalkoxyxanthone series. Antimicrob. Agents Chemother. 46(1), 144-150 (2002).
44. Ignatushchenko MV, Winter RW, Bachinger HP, Hinrichs DJ, Riscoe MK. Xanthones as antimalarial agents; studies of a possible mode of action. FEBS Lett. 409(1) (1997).
45. Kelly JX, Winter R, Riscoe M, Peyton DH. A spectroscopic investigation of the binding interactions between 4,5-dihydroxyxanthone and heme. J. Inorg. Biochem. 86(2-3), 617-625 (2001).
46. Ignatushchenko MV, Winter RW, Riscoe M. Xanthones as antimalarial agents: stage specificity. Am. J. Trop Med Hyg. 62(1), 77-81 (2000).
47. Hsu E. Reflections on the 'discovery' of the antimalarial qinghao. Br. J. Clin.Pharmacol. 61(6), 666-670 (2006).
48. Meshnick SR, Thomas A, Ranz A, Xu CM, Pan HZ. Artemisinin (qinghaosu) - the role of intracellular hemin in its mechanism of antimalarial action. Mol. Biochem.Parasitol. 49(2), 181-190 (1991).
49. Cazelles J, Robert A, Meunier B. Alkylation of heme by artemisinin, an antimalarial drug. C. R. Acad. Sci. Paris, Chimie 4(2), 85-89 (2001).
50. Hong YL, Yang YZ, Meshnick SR. The interaction of artemisinin with malarial hemozoin. Mol. Biochem. Parasitol. 63(1), 121-128 (1994).
51. Klonis N, Crespo-Ortiz MP, Bottova I et al. Artemisinin activity against Plasmodium falciparum requires hemoglobin uptake and digestion. Proc. Natl Acad. Sci. USA 108(28), 11405-11410 (2011).
52. Hoppe HC, van Schalkwyk DA, Wiehart UIM, Meredith SA, Egan J, Weber BW. Antimalarial quinolines and artemisinin inhibit endocytosis in Plasmodium falciparum. Antimicrob. Agents Chemother. 48(7), 2370-2378 (2004).
53. Weissbuch I, Leiserowitz L. Interplay between malaria, crystalline hemozoin formation, and antimalarial drug action and design. Chem. Rev. 108(11), 4899-4914 (2008).
54. Hartwig CL, Lauterwasser EMW, Mahajan SS, Hoke JM, Cooper RA, Renslo AR. Investigating the antimalarial action of 1,2,4-trioxolanes with fluorescent chemical probes. J. Med. Chem. 54(23), 8207-8213 (2011).
55. Hartwig CL, Rosenthal AS, D'Angelo J, Griffin CE, Posner GH, Cooper RA. Accumulation of artemisinin trioxane derivatives within neutral lipids of Plasmodium falciparum malaria parasites is endoperoxide-dependent. Biochem. Pharmacol. 77(3), 322-336 (2009).
56. Haynes RK, Monti D, Taramelli D, Basilico N, Parapini S, Olliaro P. Artemisinin antimalarials do not inhibit hemozoin formation. Antimicrob. Agents Chemother. 47(3), 1175-1175 (2003).
57. Janzen WP. High throughput screening as a discovery tool in the pharmaceutical industry. Lab. Robotics Autom. 8(5), 261-265 (1996).
58. Dove A. High-throughput screening goes to school. Nat. Methods 4(6), 523-529 (2007).
59. Sams-Dodd F. Target-based drug discovery: is something wrong? Drug Discov. Today 10(2), 139-147 (2005).
60. Johnson JD, Dennull RA, Gerena L, Lopez-Sanchez M, Roncal NE, Waters NC. Assessment and continued validation of the malaria SYBR green I-based fluorescence assay for use in malaria drug screening. Antimicrob. Agents Chemother. 51(6), 1926-1933 (2007).
61. Orjuela-Sanchez P, Duggan E, Nolan J, Frangos JA, Carvalho LJM. A lactate dehydrogenase ELISA-based assay for the in vitro determination of Plasmodium berghei sensitivity to anti-malarial drugs. Malaria J. 11 (2012).
62. Vivas L, Easton A, Kendrick H et al. Plasmodium falciparum: stage specific effects of a selective inhibitor of lactate dehydrogenase. Exp. Parasitol. 111(2), 105-114 (2005).
63. Gamo FJ, Sanz LM, Vidal J et al. Thousands of chemical starting points for antimalarial lead identification. Nature 465, 305-310 (2010).
64. Plouffe D, Brinker A, McNamara C et al. In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc. Natl Acad. Sci. USA 105(26), 9059-9064 (2008).
65. Butler D. GlaxoSmithKline goes public with malaria data. Nature doi:10.1038/news.2010.20 (26 January 2010).
66. Cressey D. Data sharing aids the fight against malaria. Nature News (14 February 2012).
67. Garavito G, Monje MC, Maurel S, Valentin A, Nepveu F, Deharo E. A non-radiolabeled heme-GSH interaction test for the screening of antimalarial compounds. Exp. Parasitol. 116(3), 311-313 (2007).
68. Chong CR, Sullivan DJ. Inhibition of heme crystal growth by antimalarials and other compounds: implications for drug discovery. Biochem. Pharmacol. 66(11), 2201-2212 (2003).
69. Kurosawa Y, Dorn A, Kitsuji-Shirane M et al. Hematin polymerization assay as a high-throughput screen for identification of new antimalarial pharmacophores. Antimicrob. Agents Chemother. 44(10), 2638-2644 (2000).
70. Basilico N, Pagani E, Monti D, Olliaro P, Taramelli D. A microtitre-based method for measuring the haem polymerization inhibitory activity (HPIA) of antimalarial drugs. J. Antimicrob. Chemother. 42(1), 55-60 (1998).
71. Huy NT, Uyen DT, Maeda A et al. Simple colorimetric inhibition assay of heme crystallization for high-throughput screening of antimalarial compounds. Antimicrob. Agents Chemother. 51(1), 350-353 (2007).
72. Carter MD, Phelan VV, Sandlin RD, Bachmann BO, Wright DW. Lipophilic mediated assays for beta-hematin inhibitors. Comb. Chem. High Throughput Screen. 13(3), 285-292 (2010).
73. Rush MA, Baniecki ML, Mazitschek R et al. Colorimetric high-throughput screen for detection of heme crystallization inhibitors. Antimicrob. Agents Chemother. 53(6), 2564-2568 (2009).
74. Sandlin RD, Carter MD, Lee PJ et al. Use of the NP-40 detergent-mediated assay in discovery of inhibitors of beta-hematin crystallization. Antimicrob. Agents Chemother. 55(7), 3363-3369 (2011).
75. Combrinck JM, Mabotha TE, Ncokazi KK et al. Insights into the role of heme in the mechanism of action of antimalarials. ACS Chem. Bio. 8(1), 133-137 (2013).
76. High Content Screening: Science, Techniques and Applications. Haney SA (Ed.). John Wiley and Sons, Inc., Hoboken, NJ, USA (2008).
77. Cervantes S, Prudhomme J, Carter D et al. High-content live cell imaging with RNA probes: advancements in high-throughput antimalarial drug discovery. BMC Cell Biol. 10(45), 1-10 (2009).
78. Cervantes S, Stout PE, Prudhomme J et al. High content live cell imaging for the discovery of new antimalarial marine natural products. BMC Infect. Dis. 12(1), 1-9 (2012).
79. Bellemare MJ, Bohle DS, Brosseau CN et al. Autofluorescence of condensed heme aggregates in malaria pigment and its synthetic equivalent hematin anhydride (beta-hematin). J. Phys. Chem. B 113(24), 8391-8401 (2009).
80. Schwarzer E, Bellomo G, Giribaldi G, Ulliers D, Arese P. Phagocytosis of malarial pigment haemozoin by human monocytes: a confocal microscopy study. Parasitology 123, 125-131 (2001).
81. Carney CK, Schrimpe AC, Halfpenny K et al. The basis of the immunomodulatory activity of malaria pigment (hemozoin). J. Biol. Inorg. Chem. 11(7), 917-929 (2006).
82. Openhealth News. Medicines for Malaria Venture and EMBL-EBI establish one-stop shop for malaria drug data. European Molecular Biology Laboratory - European Bioinformatics Institute, Hinxton, UK (2012).
83. Olszewski KL, Morrisey JM, Wilinski D et al. Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe 5(2), 191-199 (2009).
84. Gebregiworgis T, Powers R. Application of NMR metabolomics to search for human disease biomarkers. Comb. Chem. High Throughput Screen. 15(8), 595-610 (2012).
85. Touze J, Fourcade L, Pradines B, Hovette P, Paule P, Heno P. Mechanism of action of antimalarials. Value combined atovaquone/proguanil. Med. Trop. (Mars) 62(3), 219-224 (2002).