Investigations into the role of the Plasmodium falciparum SERCA (PfATP6) L263E mutation in artemisinin action and resistance

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 9, 2010, Pages 3842-3852

  Valderramos, Stephanie Gaw ^a,b   Scanfeld, Daniel ^a   Uhlemann, Anne Catrin ^a,c   Fidock, David A ^a   Krishna, Sanjeev ^c  

^a NewYork Presbyterian Hospital   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISININ; ARTESUNATE; DIHYDROARTEMISININ;

ALLELE; ANTIBIOTIC SENSITIVITY; ANTIMALARIAL DRUG RESISTANCE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENETIC SCREENING; GENETIC TRANSFECTION; GENETIC VARIABILITY; IC 50; MOLECULAR CLONING; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIMALARIALS; ARTEMISININS; INHIBITORY CONCENTRATION 50; MALARIA, FALCIPARUM; MUTATION; PLASMODIUM FALCIPARUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 77956108989     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00121-10     Document Type: Article

References (59)

1. Akompong, T., J. VanWye, N. Ghori, and K. Haldar. 1999. Artemisinin and its derivatives are transported by a vacuolar-network of Plasmodium falciparum and their anti-malarial activities are additive with toxic sphingolipid analogues that block the network. Mol. Biochem. Parasitol. 101:71-79.
2. Asawamahasakda, W., I. Ittarat, Y. M. Pu, H. Ziffer, and S. R. Meshnick. 1994. Reaction of antimalarial endoperoxides with specific parasite proteins. Antimicrob. Agents Chemother. 38:1854-1858.
3. Bertaux, L., H. Quang Le, V. Sinou, N. X. Thanh, and D. Parzy. 2009. New PfATP6 mutations found in Plasmodium falciparum isolates from Vietnam. Antimicrob. Agents Chemother. 53:4570-4571.
4. Bhisutthibhan, J., and S. R. Meshnick. 2001. Immunoprecipitation of [(3)H]dihydroartemisinin translationally controlled tumor protein (TCTP) adducts from Plasmodium falciparum-infected erythrocytes by using anti-TCTP antibodies. Antimicrob. Agents Chemother. 45:2397-2399.
5. Bozdech, Z., M. Llinas, B. L. Pulliam, E. D. Wong, J. Zhu, and J. L. DeRisi. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1:E5.
6. Bray, P. G., S. A. Ward, and P. M. O'Neill. 2005. Quinolines and artemisinin: chemistry, biology and history, p. 444. In D. Sullivan and S. Krishna (ed.), Malaria: drugs, disease and post-genomic biology, 1st. ed., vol. 295. Springer-Verlag, Berlin, Germany.
7. Cardi, D. 2009. Ph.D. thesis. Université Paris XI, Paris, France.
8. Chavchich, M., L. Gerena, J. Peters, N. Chen, Q. Cheng, and D. E. Kyle. 2010. Role of pfmdr1 amplification and expression in induction of resistance to artemisinin derivatives in Plasmodium falciparum. Antimicrob. Agents Chemother. 54:2455-2464.
9. Coghi, P., N. Basilico, D. Taramelli, W. C. Chan, R. K. Haynes, and D. Monti. 2009. Interaction of artemisinins with oxyhemoglobin Hb-Fe(II), Hb-Fe(II), carboxyHb-Fe(II), heme-Fe(II), and carboxyheme Fe(II): significance for mode of action and implications for therapy of cerebral malaria. ChemMedChem. 4:2045-2053.
10. Combe, A., D. Giovannini, T. G. Carvalho, S. Spath, B. Boisson, C. Loussert, S. Thiberge, C. Lacroix, P. Gueirard, and R. Menard. 2009. Clonal conditional mutagenesis in malaria parasites. Cell Host Microbe 5:386-396.
11. Crabb, B. S., and A. F. Cowman. 1996. Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 93:7289-7294.
12. 2+-ATPase orthologue of Plasmodium falciparum (PfATP6). Infect. Genet. Evol. 8:340-345.
13. del Pilar Crespo, M., T. D. Avery, E. Hanssen, E. Fox, T. V. Robinson, P. Valente, D. K. Taylor, and L. Tilley. 2008. Artemisinin and a series of novel endoperoxide antimalarials exert early effects on digestive vacuole morphology. Antimicrob. Agents Chemother. 52:98-109.
14. Dondorp, A. M., F. Nosten, P. Yi, D. Das, A. P. Phyo, J. Tarning, K. M. Lwin, F. Ariey, W. Hanpithakpong, S. J. Lee, P. Ringwald, K. Silamut, M. Imwong, K. Chotivanich, P. Lim, T. Herdman, S. S. An, S. Yeung, P. Singhasivanon, N. P. Day, N. Lindegardh, D. Socheat, and N. J. White. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 361:455-467.
15. Eastman, R. T., and D. A. Fidock. 2009. Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria. Nat. Rev. Microbiol. 7:864-874.
16. Eckstein-Ludwig, U., R. J. Webb, I. D. Van Goethem, J. M. East, A. G. Lee, M. Kimura, P. M. O'Neill, P. G. Bray, S. A. Ward, and S. Krishna. 2003. Artemisinins target the SERCA of Plasmodium falciparum. Nature 424:957-961.
17. Fidock, D. A., R. T. Eastman, S. A. Ward, and S. R. Meshnick. 2008. Recent highlights in antimalarial drug resistance and chemotherapy research. Trends Parasitol. 24:537-544.
18. Fidock, D. A., T. Nomura, and T. E. Wellems. 1998. Cycloguanil and its parent compound proguanil demonstrate distinct activities against Plasmodium falciparum malaria parasites transformed with human dihydrofolate reductase. Mol. Pharmacol. 54:1140-1147.
19. Gelb, M. H. 2007. Drug discovery for malaria: a very challenging and timely endeavor. Curr. Opin. Chem. Biol. 11:440-445.
20. Golenser, J., J. H. Waknine, M. Krugliak, N. H. Hunt, and G. E. Grau. 2006. Current perspectives on the mechanism of action of artemisinins. Int. J. Parasitol. 36:1427-1441.
21. Goodyer, I. D., and T. F. Taraschi. 1997. Plasmodium falciparum: a simple, rapid method for detecting parasite clones in microtiter plates. Exp. Parasitol. 86:158-160.
22. Haynes, R. K., W. C. Chan, C. M. Lung, A. C. Uhlemann, U. Eckstein, D. Taramelli, S. Parapini, D. Monti, and S. Krishna. 2007. The Fe(2+)-mediated decomposition, PfATP6 binding, and antimalarial activities of artemisone and other artemisinins: the unlikelihood of C-centered radicals as bioactive intermediates. ChemMedChem. 2:1480-1497.
23. Haynes, R. K., B. Fugmann, J. Stetter, K. H. Rieckmann, H.-D. Heilmann, H.-W. Chan, M.-K. Cheung, W.-L. Lam, H.-N. Wong, S. L. Croft, L. Vivas, L. Rattray, L. Stewart, W. Peters, B. L. Robinson, M. D. Edstein, B. M. Kotecka, D. E. Kyle, B. Beckermann, M. Gerisch, M. Radtke, G. Schmuck, W. Steinke, U. Wollborn, K. Schmeer, and A. Romer. 2006. Artemisone - a new, highly active antimalarial drug of the artemisinin class. Angew. Chem. Int. Ed. Engl. 45:1-8.
24. Haynes, R. K., and S. Krishna. 2004. Artemisinins: activities and actions. Microbes Infect. 6:1339-1346.
25. Hoppe, H. C., D. A. van Schalkwyk, U. I. Wiehart, S. A. Meredith, J. Egan, and B. W. Weber. 2004. Antimalarial quinolines and artemisinin inhibit endocytosis in Plasmodium falciparum. Antimicrob. Agents Chemother. 48:2370-2378.
26. Ibrahim, M. L., N. Khim, H. H. Adam, F. Ariey, and J. B. Duchemin. 2009. Polymorphism of PfATPase in Niger: detection of three new point mutations. Malar; J. 8:28.
27. Jambou, R., E. Legrand, M. Niang, N. Khim, P. Lim, B. Volney, M. T. Ekala, C. Bouchier, P. Esterre, T. Fandeur, and O. Mercereau-Puijalon. 2005. Resistance of Plasmodium falciparum field isolates to in-vitro artemether and point mutations of the SERCA-type PfATPase6. Lancet 366:1960-1963.
28. 2+-ATPase(PfATP6) and docking of artemisinin derivatives to PfATP6. Bioorg. Med. Chem. Lett. 15:2994-2997.
29. Kremsner, P. G., and S. Krishna. 2004. Antimalarial combinations. Lancet 364:285-294.
30. Krishna, S., L. Bustamante, R. K. Haynes, and H. M. Staines. 2008. Artemisinins: their growing importance in medicine. Trends Pharmacol. Sci. 29:520-527.
31. Le Roch, K. G., Y. Zhou, P. L. Blair, M. Grainger, J. K. Moch, J. D. Haynes, P. De La Vega, A. A. Holder, S. Batalov, D. J. Carucci, and E. A. Winzeler. 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301:1503-1508.
32. Li, W., W. Mo, D. Shen, L. Sun, J. Wang, S. Lu, J. M. Gitschier, and B. Zhou. 2005. Yeast model uncovers dual roles of mitochondria in the action of artemisinin. PLoS Genet. 1:e36.
33. Mamoun, C. B., I. Y. Gluzman, S. Goyard, S. M. Beverley, and D. E. Goldberg. 1999. A set of independent selectable markers for transfection of the human malaria parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. U. S. A. 96:8716-8720.
34. Menegon, M., A. R. Sannella, G. Majori, and C. Severini. 2008. Detection of novel point mutations in the Plasmodium falciparum ATPase6 candidate gene for resistance to artemisinins. Parasitol. Int. 57:233-235.
35. Nagamune, K., W. L. Beatty, and L. D. Sibley. 2007. Artemisinin induces calcium-dependent protein secretion in the protozoan parasite Toxoplasma gondii. Eukaryot. Cell 6:2147-2156.
36. 2+-ATPase (PfATP6). J. Mol. Model. [Epub ahead of print.] doi:10.1007/s00894-010-0726-4.
37. Noedl, H., S. Krudsood, W. Leowattana, N. Tangpukdee, W. Thanachartwet, S. Looareesuwan, R. S. Miller, M. Fukuda, K. Jongsakul, K. Yingyuen, S. Sriwichai, C. Ohrt, and C. Knirsch. 2007. In vitro antimalarial activity of azithromycin, artesunate, and quinine in combination and correlation with clinical outcome. Antimicrob. Agents Chemother. 51:651-656.
38. Noedl, H., Y. Se, K. Schaecher, B. L. Smith, D. Socheat, and M. M. Fukuda. 2008. Evidence of artemisinin-resistant malaria in western Cambodia. N. Engl. J. Med. 359:2619-2620.
39. O'Neill, P. M., and G. H. Posner. 2004. A medicinal chemistry perspective on artemisinin and related endoperoxides. J. Med. Chem. 47:2945-2964.
40. Omara-Opyene, A. L., P. A. Moura, C. R. Sulsona, J. A. Bonilla, C. A. Yowell, H. Fujioka, D. A. Fidock, and J. B. Dame. 2004. Genetic disruption of the Plasmodium falciparum digestive vacuole plasmepsins demonstrates their functional redundancy. J. Biol. Chem. 279:54088-54096.
41. Pandey, A. V., B. L. Tekwani, R. L. Singh, and V. S. Chauhan. 1999. Artemisinin, an endoperoxide antimalarial, disrupts the hemoglobin catabolism and heme detoxification systems in malarial parasite. J. Biol. Chem. 274:19383-19388.
42. Reed, M. B., K. J. Saliba, S. R. Caruana, K. Kirk, and A. F. Cowman. 2000. PgH1 modulates sensitivity and resistance of multiple antimalarials in Plasmodium falciparum. Nature 403:906-909.
43. Riganti, C., S. Doublier, D. Viarisio, E. Miraglia, G. Pescarmona, D. Ghigo, and A. Bosia. 2009. Artemisinin induces doxorubicin resistance in human colon cancer cells via calcium-dependent activation of HIF-1alpha and P-glycoprotein overexpression. Br. J. Pharmacol. 156:1054-1066.
44. Robert, A., F. Benoit-Vical, C. Claparols, and B. Meunier. 2005. The antimalarial drug artemisinin alkylates heme in infected mice. Proc. Natl. Acad. Sci. U. S. A. 102:13676-13680.
45. Sidhu, A. B., A. C. Uhlemann, S. G. Valderramos, J. C. Valderramos, S. Krishna, and D. A. Fidock. 2006. Decreasing pfmdr1 copy number in Plasmodium falciparum malaria heightens susceptibility to mefloquine, lumefantrine, halofantrine, quinine, and artemisinin. J. Infect. Dis. 194:528-535.
46. Sidhu, A. B., S. G. Valderramos, and D. A. Fidock. 2005. pfmdr1 mutations contribute to quinine resistance and enhance mefloquine and artemisinin sensitivity in Plasmodium falciparum. Mol. Microbiol. 57:913-926.
47. Sidhu, A. B., D. Verdier-Pinard, and D. A. Fidock. 2002. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298:210-213.
48. Stockwin, L. H., B. Han, S. X. Yu, M. G. Hollingshead, M. A. ElSohly, W. Gul, D. Slade, A. M. Galal, and D. L. Newton. 2009. Artemisinin dimer anticancer activity correlates with heme-catalyzed reactive oxygen species generation and endoplasmic reticulum stress induction. Int. J. Cancer 125:1266-1275.
49. Tahar, R., P. Ringwald, and L. K. Basco. 2009. Molecular epidemiology of malaria in Cameroon. XXVIII. In vitro activity of dihydroartemisinin against clinical isolates of Plasmodium falciparum and sequence analysis of the P. falciparum ATPase 6 gene. Am. J. Trop. Med. Hyg. 81:13-18.
50. ter Kuile, F., N. J. White, P. Holloway, G. Pasvol, and S. Krishna. 1993. Plasmodium falciparum: in vitro studies of the pharmacodynamic properties of drugs used for the treatment of severe malaria. Exp. Parasitol. 76:85-95.
51. Toovey, S., L. Y. Bustamante, A. C. Uhlemann, J. M. East, and S. Krishna. 2008. Effect of artemisinins and amino alcohol partner antimalarials on mammalian sarcoendoplasmic reticulum calcium adenosine triphosphatase activity. Basic Clin. Pharmacol. Toxicol. 103:209-213.
52. Toyoshima, C., and T. Mizutani. 2004. Crystal structure of the calcium pump with a bound ATP analogue. Nature 29:529-535. (Pubitemid 38998620)
53. Toyoshima, C., M. Nakasako, H. Nomura, and H. Ogawa. 2000. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature 405:647-655. (Pubitemid 30428644)
54. Uhlemann, A. C., A. Cameron, U. Eckstein-Ludwig, J. Fischbarg, P. Iserovich, F. A. Zuniga, M. East, A. Lee, L. Brady, R. K. Haynes, and S. Krishna. 2005. A single amino acid residue can determine the sensitivity of SERCAs to artemisinins. Nat. Struct. Mol. Biol. 12:628-629.
55. Valderramos, S. G., J. C. Valderramos, L. Musset, L. A. Purcell, O. Mercereau-Puijalon, E. Legrand, and D. A. Fidock. 2010. Identification of a mutant PfCRT-mediated chloroquine tolerance phenotype in Plasmodium falciparum. PLoS Pathog. 6:e1000887.
56. White, N. J. 2008. Qinghaosu (artemisinin): the price of success. Science 320:330-334.
57. Witkowski, B., J. Lelievre, M. J. Barragan, V. Laurent, X. Z. Su, A. Berry, and F. Benoit-Vical. 2010. Increased tolerance to artemisinin in Plasmodium falciparum is mediated by a quiescence mechanism. Antimicrob. Agents Chemother. 54:1872-1877.
58. Woodrow, C. J., R. K. Haynes, and S. Krishna. 2005. Artemisinins. Postgrad Med. J. 81:71-78.
59. 2+-ATPase isoform transcripts. Am. J. Physiol. 269:C775-784.