A novel way to grow hemozoin-like crystals in vitro and its use to screen for hemozoin inhibiting antimalarial compounds

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Thomas, Vincent ^a   Góis, Ana ^b   Ritts, Bruce ^c   Burke, Peter ^d   Hänscheid, Thomas ^b   McDonnell, Gerald ^e  

^a STERIS SA R and D   (France)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^c STERIS Corporation   (United States)

^d STERIS Corporation   (United States)

^e STERIS Limited   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMODIAQUINE; AMPICILLIN; ANTI PRION COMPOUND; ANTIMALARIAL AGENT; ANTIVIRUS AGENT; ARTEMISININ; CHEMICAL COMPOUND; CHLOROQUINE; CLINDAMYCIN; CR 36; DEXTRAN SULFATE; DOXYCYCLINE; GENTAMICIN; HALOFANTRINE; HEMATIN; HEMOZOIN; HEMOZOIN LIKE CRYSTAL; MEFLOQUINE; MEPACRINE; PENTOSAN POLYSULFATE; POLYMYXIN B; QUININE; QUINOLINE; ROLITETRACYCLINE; TETRACYCLINE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTALLIZATION; DRUG ACTIVITY; DRUG DETERMINATION; DRUG SCREENING; ELECTRON MICROSCOPY; HEMOZOIN INHIBITING ACTIVITY; ILEAL FLUID DEPENDENT ORGANISM; IN VITRO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROORGANISM; PLASMODIUM FALCIPARUM; X RAY DIFFRACTION;

ANIMALS; ANTIMALARIALS; CHEMISTRY, PHARMACEUTICAL; CRYSTALLIZATION; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; HEME; HEMEPROTEINS; HEMIN; HEMOGLOBINS; MICROSCOPY, ELECTRON; PLASMODIUM FALCIPARUM; PRIONS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; X-RAY DIFFRACTION;

PLASMODIUM FALCIPARUM; PLASMODIUM PARASITES;

EID: 84864004293     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041006     Document Type: Article

References (40)

1. Dondorp AM, Fairhurst RM, Slutsker L, Macarthur JR, Breman JG, et al. (2011) The threat of artemisinin-resistant malaria. New England Journal of Medicine 365: 1073-1075.
2. Weissbuch I, Leiserowitz L, (2008) Interplay between malaria, crystalline hemozoin formation, and antimalarial drug action and design. Chemical Reviews 108: 4899-4914.
3. Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK, (2000) The structure of malaria pigment beta-haematin. Nature 404: 307-310.
4. Jaramillo M, Bellemare M-J, Martel C, Shio MT, Contreras AP, et al. (2009) Synthetic Plasmodium-like hemozoin activates the immune response: a morphology- function study. PloS one 4: e6957-e6957.
5. Huy NT, Uyen DT, Maeda A, Trang DT, Oida T, et al. (2007) Simple colorimetric inhibition assay of heme crystallization for high-throughput screening of antimalarial compounds. Antimicrobial Agents and Chemotherapy 51: 350-353.
6. Ncokazi KK, Egan TJ, (2005) A colorimetric high-throughput beta-hematin inhibition screening assay for use in the search for antimalarial compounds. Analytical Biochemistry 338: 306-319.
7. Basilico N, Pagani E, Monti D, Olliaro P, Taramelli D, (1998) A microtitre-based method for measuring the haem polymerization inhibitory activity (HPIA) of antimalarial drugs. Journal of Antimicrobial Chemotherapy 42: 55-60.
8. Parapini S, Basilico N, Pasini E, Egan TJ, Olliaro P, et al. (2000) Standardization of the physicochemical parameters to assess in vitro the beta-hematin inhibitory activity of antimalarial drugs. Exp Parasitol 96: 249-256.
9. Haynes RK, Monti D, Taramelli D, Basilico N, Parapini S, et al. (2003) Artemisinin antimalarials do not inhibit hemozoin formation. Antimicrobial Agents and Chemotherapy 47: 1175.
10. Sandlin RD, Carter MD, Lee PJ, Auschwitz JM, Leed SE, et al. (2011) Use of the NP-40 detergent-mediated assay in discovery of inhibitors of beta-hematin crystallization. Antimicrobial Agents and Chemotherapy 55: 3363-3369.
11. Vennerstrom JL, Nuzum EO, Miller RE, Dorn A, Gerena L, et al. (1999) 8-Aminoquinolines active against blood stage Plasmodium falciparum in vitro inhibit hematin polymerization. Antimicrobial Agents and Chemotherapy 43: 598-602.
12. Korth C, May BC, Cohen FE, Prusiner SB, (2001) Acridine and phenothiazine derivatives as pharmacotherapeutics for prion disease. Proc Natl Acad Sci U S A 98: 9836-9841.
13. Kocisko DA, Baron GS, Rubenstein R, Chen J, Kuizon S, et al. (2003) New inhibitors of scrapie-associated prion protein formation in a library of 2000 drugs and natural products. J Virol 77: 10288-10294.
14. Thompson MJ, Louth JC, Little SM, Jackson MP, Boursereau Y, et al. (2012) Synthesis and Evaluation of 1-Amino-6-halo-beta-carbolines as Antimalarial and Antiprion Agents. Chem Med Chem 7: 578-586.
15. Klingenstein R, Melnyk P, Leliveld SR, Ryckebusch A, Korth C, (2006) Similar structure-activity relationships of quinoline derivatives for antiprion and antimalarial effects. J Med Chem 49: 5300-5308.
16. Burdon DW, (1989) A novel replicating agent isolated from the human intestinal tract having characteristics shared with Creutzfeldt-Jakob and related agents. J Med Microbiol 29: 145-157.
17. Burdon DW, Wakeman JG, Nayyar P, (1996) Replication of IFDO on a chemically defined medium. J Med Microbiol 45: 10-15.
18. Dyas AC, Burdon DW, (1990) Studies of a novel agent possessing resistance to moist heat and disinfectants: parallels with Creutzfeldt-Jakob agent. J Hosp Infect 15: 265-272.
19. Burdon DW, (1999) Does variant Creutzfeldt-Jakob disease have an Achilles heel? Lancet 353: 1271.
20. Frita R, Rebelo M, Pamplona A, Vigario AM, Mota MM, et al. (2011) Simple flow cytometric detection of haemozoin containing leukocytes and erythrocytes for research on diagnosis, immunology and drug sensitivity testing. Malaria journal 10: 74.
21. Demirev PA, Feldman AB, Kongkasuriyachai D, Scholl P, Sullivan D Jr, et al. (2002) Detection of malaria parasites in blood by laser desorption mass spectrometry. Anal Chem 74: 3262-3266.
22. Fichet G, Comoy E, Duval C, Antloga K, Dehen C, et al. (2004) Novel methods for disinfection of prion-contaminated medical devices. Lancet 364: 521-526.
23. Solomonov I, Osipova M, Feldman Y, Baehtz C, Kjaer K, et al. (2007) 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. Journal of the American Chemical Society 129: 2615-2627.
24. Pisciotta JM, Coppens I, Tripathi AK, Scholl PF, Shuman J, et al. (2007) The role of neutral lipid nanospheres in Plasmodium falciparum haem crystallization. Biochemical Journal 402: 197-204.
25. Omodeo-Sale F, Cortelezzi L, Basilico N, Casagrande M, Sparatore A, et al. (2009) Novel antimalarial aminoquinolines: heme binding and effects on normal or Plasmodium falciparum-parasitized human erythrocytes. Antimicrobial Agents and Chemotherapy 53: 4339-4344.
26. Niles JC, Derisi JL, Marletta MA, (2009) Inhibiting Plasmodium falciparum growth and heme detoxification pathway using heme-binding DNA aptamers. Proceedings of the National Academy of Sciences of the United States of America 106: 13266-13271.
27. Rodrigues JR, Gamboa de Dominguez N, (2007) Plasmodium berghei: in vitro and in vivo activity of dequalinium. Exp Parasitol 115: 19-24.
28. Mullie C, Jonet A, Desgrouas C, Taudon N, Sonnet P, (2012) Differences in anti-malarial activity of 4-aminoalcohol quinoline enantiomers and investigation of the presumed underlying mechanism of action. Malaria journal 11: 65.
29. Trang DT, Huy NT, Uyen DT, Sasai M, Shiono T, et al. (2006) Inhibition assay of beta-hematin formation initiated by lecithin for screening new antimalarial drugs. Analytical Biochemistry 349: 292-296.
30. Chen MM, Shi L, Sullivan DJ Jr, (2001) Haemoproteus and Schistosoma synthesize heme polymers similar to Plasmodium hemozoin and beta-hematin. Molecular & Biochemical Parasitology 113: 1-8.
31. Munoz-Durango K, Maciuk A, Harfouche A, Torijano-Gutierrez S, Jullian JC, et al. (2012) Detection, characterization, and screening of heme-binding molecules by mass spectrometry for malaria drug discovery. Analytical Chemistry 84: 3324-3329.
32. Krishna S, Pulcini S, Fatih F, Staines H, (2010) Artemisinins and the biological basis for the PfATP6/SERCA hypothesis. Trends in Parasitology 26: 517-523.
33. Dahl EL, Shock JL, Shenai BR, Gut J, DeRisi JL, et al. (2006) Tetracyclines specifically target the apicoplast of the malaria parasite Plasmodium falciparum. Antimicrobial Agents and Chemotherapy 50: 3124-3131.
34. Ramya TN, Mishra S, Karmodiya K, Surolia N, Surolia A, (2007) Inhibitors of nonhousekeeping functions of the apicoplast defy delayed death in Plasmodium falciparum. Antimicrobial Agents and Chemotherapy 51: 307-316.
35. Anonymous (2008) Regulation (EC) No 1272/2008. Regulation on classification, labelling and packaging of substances and mixtures, amending and repealing Directives 67/548/EEC and 1999/45/EC, and amending Regulation (EC) No 1907/2006. Official Journal of the European Union L353: 1-1355.
36. Murakami-Kubo I, Doh-Ura K, Ishikawa K, Kawatake S, Sasaki K, et al. (2004) Quinoline derivatives are therapeutic candidates for transmissible spongiform encephalopathies. J Virol 78: 1281-1288.
37. Dolphin GT, Chierici S, Ouberai M, Dumy P, Garcia J, (2008) A multimeric quinacrine conjugate as a potential inhibitor of Alzheimer's beta-amyloid fibril formation. Chembiochem 9: 952-963.
38. Larramendy-Gozalo C, Barret A, Daudigeos E, Mathieu E, Antonangeli L, et al. (2007) Comparison of CR36, a new heparan mimetic, and pentosan polysulfate in the treatment of prion diseases. Journal of General Virology 88: 1062-1067.
39. Slater AF, Swiggard WJ, Orton BR, Flitter WD, Goldberg DE, et al. (1991) An iron-carboxylate bond links the heme units of malaria pigment. Proceedings of the National Academy of Sciences of the United States of America 88: 325-329.
40. Coban C, Ishii KJ, Sullivan DJ, Kumar N, (2002) Purified malaria pigment (hemozoin) enhances dendritic cell maturation and modulates the isotype of antibodies induced by a DNA vaccine. Infection and Immunity 70: 3939-3943.