Stage independent chloroquine resistance and chloroquine toxicity revealed via spinning disk confocal microscopy

Molecular and Biochemical Parasitology

Volumn 159, Issue 1, 2008, Pages 7-23

  Gligorijevic, Bojana ^a,b   Purdy, Kyle ^a,b   Elliott, David A ^c   Cooper, Roland A ^d   Roepe, Paul D ^a,b  

^a GEORGETOWN UNIVERSITY   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d OLD DOMINION UNIVERSITY   (United States)

Author keywords

Delayed death; Hemozoin; Merozoite production

Indexed keywords

CHLOROQUINE;

ANTIBIOTIC RESISTANCE; ARTICLE; CELL CULTURE; CELL CYCLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE MUTATION; GENETIC TRANSFECTION; MEROZOITE; NONHUMAN; NUCLEAR DIVISION; PARASITE; PARASITEMIA; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCHIZONT; TOXICITY;

ANIMALS; ANTIMALARIALS; CHLOROQUINE; DRUG RESISTANCE; ERYTHROCYTES; INHIBITORY CONCENTRATION 50; LIFE CYCLE STAGES; MICROSCOPY, CONFOCAL; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; SCHIZONTS;

EID: 41549115882     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2007.12.014     Document Type: Article

References (55)

1. Gligorijevic B., McAllister R., Urbach J.S., and Roepe P.D. Spinning disk confocal microscopy of live, intraerythrocytic malarial parasites. 1. Quantification of hemozoin development for drug sensitive versus resistant malaria. Biochemistry 45 (2006) 12400-12410
2. Irvin J.L., Irvin E.M., and Parker F.S. The interaction of antimalarials with nucleic acids. Science 110 (1949) 3
3. Parker F.S., and Irvin J.L. The interaction of chloroquine with nucleic acids and nucleoproteins. J Biol Chem 199 (1952) 897-909
4. Cohen S.N., and Yielding K.L. Inhibition of DNA and RNA polymerase reactions by chloroquine. Proc Natl Acad Sci USA 54 (1965) 521-527
5. Ciak J., and Hahn F.E. Chloroquine: mode of action. Science 151 (1966) 347-349
6. O'Brien R.L., Olenick J.G., and Hahn F.E. Reactions of quinine, chloroquine, and quinacrine with DNA and their effects on the DNA and RNA polymerase reactions. Proc Natl Acad Sci USA 55 (1966) 1511-1517
7. Kwakye-Berko F., and Meshnick S. Sequence preference of chloroquine binding to DNA and prevention of Z-DNA formation. Mol Biochem Parasitol 39 (1990) 275-278
8. Meshnick S.R. Chloroquine as intercalator: a hypothesis revived. Parasitol Today 6 (1990) 77-79
9. Allison J.L., O'Brien R.L., and Hahn F.E. DNA: reaction with chloroquine. Science 149 (1965) 1111-1113
10. Fitch C.D. Chloroquine resistance in malaria: a deficiency of chloroquine binding. Proc Natl Acad Sci USA 64 (1969) 1181-1187
11. Aikawa M. High-resolution autoradiography of malarial parasites treated with 3 H-chloroquine. Am J Pathol 67 (1972) 277-284
12. Yayon A., Cabantchik Z.I., and Ginsburg H. Identification of the acidic compartment of Plasmodium falciparum-infected human erythrocytes as the target of the antimalarial drug chloroquine. EMBO J 3 (1984) 2695-2700
13. Orjih A.U., and Fitch C.D. Hemozoin production by Plasmodium falciparum: variation with strain and exposure to chloroquine. Biochim Biophys Acta 1157 (1993) 270-274
14. Fidock D.A., Nomura T., Talley A.K., Cooper R.A., Dzekunov S.M., Ferdig M.T., et al. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell 4 (2000) 861-871
15. Leed A., DuBay K., Ursos L.M., Sears D., De Dios A.C., and Roepe P.D. Solution structures of antimalarial drug-heme complexes. Biochemistry 41 32 (2002) 10245-10255
16. de Dios A.C., Casabianca L.B., Kosar A., and Roepe P.D. Structure of the amodiaquine-FPIX mu oxo dimer solution complex at atomic resolution. Inorg Chem 43 25 (2004) 8078-8084
17. Sullivan Jr. D.J., Gluzman I.Y., Russell D.G., and Goldberg D.E. On the molecular mechanism of chloroquine's antimalarial action. Proc Natl Acad Sci USA 93 (1996) 11865-11870
18. Goldberg D.E. Hemoglobin degradation. Curr Top Microbiol Immunol 295 (2005) 275-291
19. Zhang H., Paguio M., and Roepe P.D. The antimalarial drug resistance protein Plasmodium falciparum chloroquine resistance transporter binds chloroquine. Biochemistry 43 (2004) 8290-8296
20. Bray P.G., Mungthin M., Hastings I.M., Biagini G.A., Saidu D.K., Lakshmanan V., et al. PfCRT and the trans-vacuolar proton electrochemical gradient: regulating the access of chloroquine to ferriprotoporphyrin IX. Mol Microbiol 62 1 (2006) 238-251
21. Peters W. The chemotherapy of rodent malaria. X. Dynamics of drug resistance. II. Acquisition and loss of chloroquine resistance in Plasmodium berghei observed by continuous bioassay. Ann Trop Med Parasitol 64 (1970) 25-40
22. Smalley M.E. Plasmodium falciparum gametocytes: the effect of chloroquine on their development. Trans R Soc Trop Med Hyg 71 (1977) 526-529
23. Slater A.F. Chloroquine: mechanism of drug action and resistance in Plasmodium falciparum. Pharmacol Ther 57 (1993) 203-235
24. Zhang Y., Asante K.S., and Jung A. Stage-dependent inhibition of chloroquine on Plasmodium falciparum in vitro. J Parasitol 72 (1986) 830-836
25. Orjih A.U. Heme polymerase activity and the stage specificity of antimalarial action of chloroquine. J Pharmacol Exp Ther 282 (1997) 108-112
26. Yayon A., Vande Waa J.A., Yayon M., Geary T.G., and Jensen J.B. Stage-dependent effects of chloroquine on Plasmodium falciparum in vitro. J Protozool 30 (1983) 642-647
27. ter Kuile F., White N.J., Holloway P., Pasvol G., and Krishna S. Plasmodium falciparum: in vitro studies of the pharmacodynamic properties of drugs used for the treatment of severe malaria. Exp Parasitol 76 1 (1993) 85-95
28. Gligorijevic B., Bennett T., McAllister R., Urbach J.S., and Roepe P.D. Spinning disk confocal microscopy of live, intraerythrocytic malarial parasites. 2. Altered vacuolar volume regulation in drug resistant malaria. Biochemistry 45 (2006) 12411-12423
29. Bennett T.N., Paguio M., Gligorijevic B., Seudieu C., Kosar A.D., Davidson E., et al. Novel, rapid, and inexpensive cell-based quantification of antimalarial drug efficacy. Antimicrob Agents Chemother 48 (2004) 1807-1810
30. Trager W., and Jensen J.B. Human malaria parasites in continuous culture. Science 193 (1976) 673-675
31. Lambros C., and Vanderberg J.P. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65 (1979) 418-420
32. Elliott D.A. Serial sectioning via microtomy (or, How To Get Over 100 Consecutive Serial Sections On One TEM Gird). Microsc Today 15 (2007) 30-33
33. Langreth S.G., Jensen J.B., Reese R.T., and Trager W. Fine structure of human malaria in vitro. J Protozool 25 (1978) 443-452
34. Wellems T.E., Walker-Jonah A., and Panton L.J. Genetic mapping of the chloroquine-resistance locus on Plasmodium falciparum chromosome 7. Proc Natl Acad Sci USA 88 8 (1991) 3382-3386
35. Sidhu A.B., Verdier-Pinard D., and Fidock D.A. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298 5591 (2002) 210-213
36. Cooper R.A., Ferdig M.T., Su X.Z., Ursos L.M., Mu J., Nomura T., et al. Alternative mutations at position 76 of the vacuolar transmembrane protein PfCRT are associated with chloroquine resistance and unique stereospecific quinine and quinidine responses in Plasmodium falciparum. Mol Pharmacol 61 1 (2002) 35-42
37. van Dooren G.G., Marti M., Tonkin C.J., Stimmler L.M., Cowman A.F., and McFadden G.I. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol 57 (2005) 405-419
38. Gustafsson L.L., Walker O., Alvan G., Beermann B., Estevez F., Gleisner L., et al. Disposition of chloroquine in man after single intravenous and oral doses. Br J Clin Pharmacol 15 (1983) 471-479
39. De Vries P.J., Oosterhuis B., and Van Boxtel C.J. Single-dose pharmacokinetics of chloroquine and its main metabolite in healthy volunteers. Drug Invest 8 (1994) 143-149
40. Sanchez C.P., McLean J.E., Rohrbach P., Fidock D.A., Stein W.D., and Lanzer M. Evidence for a pfcrt-associated chloroquine efflux system in the human malarial parasite Plasmodium falciparum. Biochemistry 44 29 (2005) 9862-9870
41. Bennett T.N., Kosar A.D., Ursos L.M., Dzekunov S., Singh Sidhu A.B., Fidock D.A., et al. Drug resistance-associated pfCRT mutations confer decreased Plasmodium falciparum digestive vacuolar pH. Mol Biochem Parasitol 133 1 (2004) 99-114
42. Meierjohann S., Walter R.D., and Muller S. Regulation of intracellular glutathione levels in erythrocytes infected with chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Biochem J 368 Pt. 3 (2002) 761-768
43. Atkinson C.T., and Aikawa M. Ultrastructure of malaria-infected erythrocytes. Blood Cells 16 2-3 (1990) 351-368
44. Bannister L.H., Hopkins J.M., Margo G., Dluzewski A.R., and Mitchell G.H. Three dimensional ultrastructure of the ring stage of Plasmodium falciparum: evidence for export pathways. Microsc Microanal 10 (2004) 551-562
45. Barnwell J.W. Malaria. A new escape and evasion tactic. Nature 398 (1999) 562-563
46. Silvestrini F., Bozdech Z., Lanfrancotti A., Di Giulio E., Bultrini E., Picci L., et al. Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol Biochem Parasitol 143 (2005) 100-110
47. Willis R.C. Bloodsucker rising. Modern Drug Discov 4 (2001) 40-42
48. Ferreira M.U., da Silva Nunes M., and Wunderlich G. Antigenic diversity and immune evasion by malaria parasites. Clin Diagn Lab Immunol 11 (2004) 987-995
49. Alano P., and Carter R. Sexual differentiation in malaria parasites. Ann Rev Microbiol 44 (1990) 429-449
50. Janse C.J., van der Klooster P.F., van der Kaay H.J., van der Ploeg M., and Overdulve J.P. DNA synthesis in Plasmodium berghei during asexual and sexual development. Mol Biochem Parasitol 20 (1986) 173-182
51. Kudo, R. Protozoology. IL: Springfield; 1971.
52. Read M., Sherwin T., Holloway S.P., Gull K., and Hyde J.E. Microtubular organization visualized by immunofluorescence microscopy during erythrocytic schizogony in Plasmodium falciparum and investigation of post-translational modifications of parasite tubulin. Parasitology 106 Pt. 3 (1993) 223-232
53. Fritsch F.M., Mehlhorn H., Schein E., and Hauser M. The effects of drugs on the formation of Theileria annulata merozoites in vitro. Parasitol Res 74 (1988) 340-343
54. Maerki S., Brun R., Charman S.A., Dorn A., Matile H., and Wittlin S. In vitro assessment of the pharmacodynamic properties and the partitioning of OZ277/RBx-11160 in cultures of Plasmodium falciparum. J Antimicrob Chemother 58 1 (2006) 52-58
55. Ralph S.A., van Dooren G.G., Waller R.F., Crawford M.J., Fraunholz M.J., Foth B.J., et al. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev 2 (2004) 203-216