References
Atamna H, Krugliak M, Shalmiev G, Deharo E, Pescarmona G, Ginsburg H (1996) Mode of antimalarial effect of methylene blue and some of its analoques on Plasmodium falciparum in culture and their inhibition of P. vinckei petteri and P. yoelli nigeriensis in vivo. Biochem Pharmacol 51:693–700
Ball EG, McKee RW, Anfinsen CB, Cruz WO, Geiman QM (1948) Studies on malarial parasites. IX. Chemical and metabolic changes during growth and multiplication in vivo and in vitro. J Biol Chem 175:547–571
Bäuerlein E (ed) (2004) Biomineralization. Wiley-VCH Verlag GmbH, Weinheim
Bray PG, Mungthin M, Ridley RG, Ward SA (1998) Access to hematin: the basis of chloroquine resistance. Mol Pharmacol 54:170–179
Bray PG, Ward SA, O’Neill PM (2005) Quinolines and artemisinin: chemistry, biology and history. Curr Top Microbiol Immunol 295:3–38
Brown WH (1911) Malarial pigment (so-called melanin): its nature and mode of production. J Exp Med 13:290–300
Carbone T (1891) Sulla natura chimica del pigmento malarico. G R Accad Med Torino 39:901–906
Chong CR, Sullivan DJ (2003) Inhibition of heme crystal growth by antimalarials and other compounds: implication for drug discovery. Biochem Pharmacol 66:2201–2212
Coatney GR (1963) Pitfalls in a discovery: the chronicle of chloroquine. Am J Trop Med Hyg 12:121–128
Dascombe MJ, Drew MG, Morris H, Wilairat P, Auparakkitanon S, Moule WA, Alizadeh-Shekalgourabi S, Evans PG, Lloyd M, Dyas AM, Carr P, Ismail FM (2005) Mapping antimalarial pharmacophores as a useful tool for the rapid discovery of drugs effective in vivo: design, construction, characterization, and pharmacology of metaquine. J Med Chem 48:5423–5436
Deegan T, Maegraith BG (1956) Studies on the nature of malarial pigment (hemozoin). Ann Trop Med Parasitol 50:194–211
Deharo E, Garcia RN, Oporto P, Gimenez A, Sauvain M, Jullian V, Ginsburg H (2002) A non-radiolabelled ferriprotoporphyrin IX biomineralisation inhibition test for the high throughput screening of antimalarial compounds. Exp Parasitol 100:252–2566
Dünschede H-B (1971) Tropenmedizinische Forschung bei Bayer. Michael Triltsch Verlag, Düsseldorf
Egan TJ (2002) Physico-chemical aspects of hemozoin (malaria pigment) structure and formation. J Inorg Biochem 91:19–26
Egan TJ (2006) Interactions of quinoline antimalarials with hematin in solution. J Inorg Biochem 100:916–926
Egan TJ, Hempelmann E, Mavuso WW (1999) Characterisation of synthetic beta-haematin and effects of the antimalarial drugs quinidine, halofantrine, desbutylhalofantrine and mefloquine on its formation. J Inorg Biochem 73:101–107
Egan TJ, Mavuso WW, Ncokazi KK (2001) The mechanism of beta-hematin formation in acetate solution. Parallels between hemozoin formation and biomineralization processes. Biochemistry 40:204–213
Ezzet F, van Vugt M, Nosten F, Looareesuwan S, White NJ (2000) Pharmacokinetics and pharmacodynamics of lumefantrine (benflumetol) in acute falciparum malaria. Antimicrob Agents Chemother 44:697–704
Fitch CD (2004) Ferriprotoporphyrin IX, phospholipids, and the antimalarial actions of quinoline drugs. Life Sci 74:1957–1972
Fitch CD, Kanjananggulpan P (1987) The state of ferriprotoporphyrin IX in malaria pigment. J Biol Chem 262:15552–15555
Frerichs FT (1858) Pathologisch-anatomischer Atlas zur Klinik der Leberkrankheiten Band I: Klinik der Leberkrankheiten, Kapitel VIII Die Pigmentleber. Melanämische Leber. Veränderungen der Leber bei Intermittens. 325–368, F. Vieweg und Sohn, Braunschweig
Guttmann P, Ehrlich P (1891) Ueber die Wirkung desMethylenblau bei Malaria. Berliner Klinische Wochenschrift 39:953–956
Hamsik A (1925) Zur Darstellung des Oxyhämins. Hoppe-Seyler Z Physiol Chem 148:99–110
Harinasuta T, Migasen S, Bunnag D (1962) Chloroquine resistance in Plasmodium falciparum in Thailand. In: UNESCO First Regional Symposium on Scientific Knowledge of Tropical Parasites pp. 148–153, University of Singapore, Singapore
Hempelmann E, Egan TJ (2002) Pigment biocrystallization in Plasmodium falciparum. Trends Parasitol 18:11
Hempelmann E, Marques HM (1994) Analysis of malaria pigment from Plasmodium falciparum. J Pharmacol Toxicol Methods 32:25–30
Hempelmann E, Motta C, Hughes R, Ward SA, Bray PG (2003) Plasmodium falciparum: sacrificing membrane to grow crystals? Trends Parasitol 19:23–26
Homewood CA, Moore GA, Warhurst DC, Atkinson EM (1975) Purification and some properties of malarial pigment. Ann Trop Med Parasitol 69:283–287
Kaufman TS, Ruveda EA (2005) The quest for quinine: those who won the battles and those who won the war. Angew Chem Int Ed 44:854–885
Laveran CLA (1880) A newly discovered parasite in the blood of patients suffering from malaria. Parasitic etiology of attacks of malaria. Translated from the French and reprinted. In: Kean BH, Mott KE, Russell AJ (eds) Tropical Medicine and Parasitology. Classic Investigations. Vol. 1, 1978: Cornell University Press, Ithaca, New York
Leed A, DuBay K, Ursos LM, Sears D, De Dios AC, Roepe PD (2002) Solution structures of antimalarial drug–heme complexes. Biochemistry 41:10245–10255
Lemberg R, Legge JW (1949) Hematin compounds and bile pigments. Interscience, New York
Lew VL, Tiffert T, Ginsburg H (2003) Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum infected red blood cells. Blood 101:4189–4194
Lowenstam HA, Weiner S (1989) On biomineralization. Oxford University Press, New York
Macomber PB, Sprinz H, Tousimis AJ (1967) Morphological effects of chloroquine on Plasmodium berghei in mice. Nature 214:937–939
Mann S (2002) Biomineralization. Oxford University Press, New York
Meckel H (1847) Ueber schwarzes Pigment in der Milz und dem Blute einer Geisteskranken. Zeitschr f Psychiatrie IV:198–226
Moore DV, Lanier JE (1961) Observations on two Plasmodium falciparum infections with an abnormal response to chloroquine. Am J Trop Med Hyg 10:5–9
Omodeo-Sale F, Motti A, Dondorp A, White NJ, Taramelli D (2005) Destabilisation and subsequent lysis of human erythrocytes induced by Plasmodium falciparum haem products. Eur J Haematol 74:324–332
Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK (2000) The structure of malaria pigment beta-haematin. Nature 404:307–310
Peters W (1964) Pigment formation and nuclear division in chloroquine-resistant malaria parasites (Plasmodium berghei, Vincke and Lips, 1948). Nature 203:1290–1291
Scholl PF, Tripathi AK, Sullivan DJ (2005) Bioavailable iron and heme metabolism in Plasmodium falciparum. Curr Top Microbiol Immunol 295:293–324
Schulemann W (1932) Synthetic anti-malarial preparations. Proc R Soc Med 25:897–905
Sharma V (2005) Therapeutic drugs for targeting chloroquine resistance in malaria. Mini-Reviews in Medical Chemistry 5:337–351
Slater AFG, Cerami A (1992) Inhibition by chloroquine of a novel haem polymerase enzyme activity in malaria trophozoites. Nature 355:167–169
Slater AFG, Swiggard WJ, Orton BR, Flitter WD, Goldberg DE, Cerami A, Henderson GB (1991) An iron-carboxylate bond links the heme units of malaria pigment. PNAS 88:325–329
Smith DC, Sanford LB (1985) Laveran’s germ: the reception and use of a medical discovery. Am J Trop Med Hyg 34:2–20
Sullivan DJ (2002) Hemozoin, a biocrystal synthesized during the degradation of hemoglobin. In: Matsumura S, Steinbüchel A (eds) Biopolymers, vol. 9, Wiley-VCH Verlag GmbH, Weinheim pp 129–163
Tekwani BL, Walker LA (2005) Targeting the hemozoin synthesis pathway for new antimalarial drug discovery: technologies for in vitro β-hematin formation assay. Comb Chem High Throughput Screen 8:61–67
Vennerstrom JL, Makler MT, Angerhofer CK, William JA (1995) Antimalarial dyes revisited: xanthenes, azines, oxazines and thiazines. Antimicrob Agents Chemother 39:2671–2677
Virchow R (1849) Zur pathologischen Physiologie des Blutes. Arch Pathol Anatomie 2:587–598
Wainwright M, Amaral L (2005) The phenothiazinium chromophore and the evolution of antimalarial drugs. Trop Med Int Health 10:501–511
Warhurst DC, Hockley DJ (1967) Mode of action of chloroquine on Plasmodium berghei and P. cynomolgi. Nature 214:935–936
Warhurst DC, Craig JC, Adagu IS, Meyer DJ, Lee SY (2003) The relationship of physico-chemical properties and structure of the differential antiplasmodial activity of the cinchona alkaloids. Malar J 2:26
Wellems TE, Plowe CV (2001) Chloroquine-resistant malaria. J Infect Dis 184:770–776
Woodward RB, Doering WE (1945) The total synthesis of quinine. J Am Chem Soc 67:860–874
Ziegler J, Linck R, Wright DW (2001) Heme aggregation inhibitors: antimalarial drugs targeting an essential biomineralization process. Curr Med Chem 8:171–189
Acknowledgements
Electron micrographs (Figs. 3 and 4) were imaged by Lawrence Bannister and John Hopkins, Department of Anatomy and Human Science, Guy’s, King’s and St Thomas’ Medical School, London. The freeze fracture replica was prepared by Anthony Brain, Centre for Ultrastructural Imaging, King’s College London. The advice and support of Graham H. Mitchell, Guy’s Hospital London, is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hempelmann, E. Hemozoin Biocrystallization in Plasmodium falciparum and the antimalarial activity of crystallization inhibitors. Parasitol Res 100, 671–676 (2007). https://doi.org/10.1007/s00436-006-0313-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-006-0313-x