Cytostatic versus cytocidal profiling of quinoline drug combinations via modified fixed-ratio isobologram analysis

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Gorka, Alexander P ^a,b   Jacobs, Lauren M ^a   Roepe, Paul D ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Combination therapy; Cytocidal; Isobologram; P. falciparum; Quinoline

Indexed keywords

4 AMINOQUINOLINE; AMODIAQUINE; CHLOROQUINE; CYTOSTATIC AGENT; HEME; METHYLENE BLUE; MULTIDRUG RESISTANCE PROTEIN 1; PRIMAQUINE; TAFENOQUINE;

ARTICLE; CYTOSTASIS; CYTOTOXICITY; DRUG ACTIVITY; DRUG ANTAGONISM; DRUG EFFICACY; DRUG POTENTIATION; DRUG RESISTANCE; GROWTH INHIBITION; LD 50; NONHUMAN; PLASMODIUM FALCIPARUM;

ANIMALS; ANTIMALARIALS; CELL DIVISION; CELL SURVIVAL; DRUG COMBINATIONS; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; HUMANS; INHIBITORY CONCENTRATION 50; MALARIA; PLASMODIUM FALCIPARUM; QUINOLINES;

EID: 84884172337     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-332     Document Type: Article

References (68)

1. World Health Organization, World malaria report Geneva,Switzerland: World Health Organization 2010 http://www.who.int/malaria/publications/atoz/ 9789241564106/en/index.html
2. Molecular and physiologic basis of quinoline drug resistance in Plasmodium falciparum malaria. Roepe PD, Future Microbiol 2009 4 441 455 10.2217/fmb.09.15 19416013
3. A major genome region underlying artemisinin resistance in malaria. Cheeseman IH, Miller BA, Nair S, Nkhoma S, Tan A, Tan JC, Al Saai S, Phyo AP, Moo CL, Lwin KM, McGready R, Ashley E, Imwong M, Stepniewska K, Yi P, Dondorp AM, Mayxay M, Newton PN, White NJ, Nosten F, Ferdig MT, Anderson TJ, Science 2012 336 79 82 10.1126/science.1215966 22491853
4. New medicines to improve control and contribute to the eradication of malaria. Wells TN, Alonso PL, Gutteridge WE, Nat Rev Drug Discov 2009 8 879 891 10.1038/nrd2972 19834482
5. WHO, Guidelines for the treatment of malaria Geneva, Switzerland: World Health Organization 2 2010 http://www.who.int/malaria/publications/atoz/ 9789241547925/en/index.html
6. Primaquine to prevent transmission of falciparum malaria. White NJ, Lancet Infect Dis 2009 13 175 181
7. Effects of antimalarial molecules on the gametocyte stage of Plasmodium falciparum: the debate. Dechy-Cabaret O, Benoit-Vical F, J Med Chem 2012 55 10328 10344 10.1021/jm3005898 23075290
8. Blood stage antimalarial efficacy of primaquine in Plasmodium vivax malaria. Pukrittayakamee S, Vanijanonta S, Chantra A, Clemens R, White NJ, J Infect Dis 1994 169 932 935 10.1093/infdis/169.4.932 8133114 (Pubitemid 24102139)
9. Observations on early and late post-sporozoite tissue stages in primate malaria. IV. Pre-erythrocytic schizonts and/or hypnozoites of Chesson and North Korean strains of Plasmodium vivax in the chimpanzee. Krotoski WA, Garnham PC, Cogswell FB, Collins WE, Bray RS, Gwasz RW, Killick-Kendrick R, Wolf RH, Sinden R, Hollingdale M, Am J Trop Med Hyg 1986 35 263 274 3513645 (Pubitemid 16055390)
10. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Wells TNC, Burrows JN, Baird JK, Trends Parasitol 2010 26 145 151 10.1016/j.pt.2009.12.005 20133198
11. The antimalarial action of primaquine against the blood and tissue stages of falciparum malaria (Panama, P-F-6 strain). Arnold J, Alving AS, Hockwald RS, Clayman CB, Dern RJ, Beutler E, Flanagan CL, Jeffery GM, J Lab Clin Med 1955 46 391 397 13252317
12. Effect of antimalarial drugs on Plasmodium falciparum gametocytes. Peatey CL, Skinner-Adams TS, Dixon MWA, McCarthy JS, Gardiner DL, Trenholme KR, J Infect Dis 2009 200 1518 1521 10.1086/644645 19848586
13. A high-throughput assay for the identification of drugs against late-stage Plasmodium falciparum gametocytes. Peatey CL, Spicer TP, Hodder PS, Trenholme KR, Gardiner DL, Mol Biochem Parasitol 2011 180 127 131 10.1016/j.molbiopara.2011.09.002 21939693
14. Gametocytocidal and sporontocidal effects of primaquine and of sulfadiazine with pyrimethamine in a chloroquine-resistant strain of Plasmodium falciparum. Rieckmann KH, McNamara JV, Frischer H, Stockert TA, Carason PE, Powell RD, Bull World Health Organ 1968 38 625 632 4876731
15. Transmission-blocking activities of quinine, primaquine, and artesunate. Chotivanich K, Sattabongkot J, Udomsangpetch R, Looareesuwan S, Day NPJ, Coleman RE, White NJ, Antimicrob Agents Chemother 2006 60 1927 1930 (Pubitemid 43807507)
16. Rationale for short course primaquine in Africa to interrupt malaria transmission. Eziefula AC, Gosling R, Hwang J, Hsiang MS, Bousema T, Seidlein L, Drakely C, Malar J 2011 11 360
17. In-vitro activity of primaquine against the asexual blood stages of Plasmodium falciparum. Basco LK, Bickii J, Ringwald P, Ann Trop Med Parasitol 1999 93 179 182 10.1080/00034989958663 10474643 (Pubitemid 29358540)
18. Synthesis, antiprotozoal, antimicrobial, β-hematin inhibition, cytotoxicity and methemoglobin (metHb) formation activities of bis(8-aminoquinolines). Kaur K, Jain M, Khan SI, Jacob MR, Tekwani BL, Singh S, Singh PP, Jain R, Bioorg Med Chem 2011 19 197 210 10.1016/j.bmc.2010.11.036 21172735
19. Cytostatic versus cytocidal activities of chloroquine analogues and inhibition of hemozoin crystal growth. Gorka AP, Alumasa JN, Sherlach KS, Jacobs LM, Nickley KB, Brower JP, de Dios AC, Roepe PD, Antimicrob Agents Chemother 2013 57 356 364 10.1128/AAC.01709-12 23114783
20. Relative to quinine and quinidine, their 9-epimers exhibit decreased cytostatic activity and altered heme binding but similar cytocidal activity versus Plasmodium falciparum. Gorka AP, Sherlach KS, de Dios AC, Roepe PD, Antimicrob Agents Chemother 2013 57 365 374 10.1128/AAC.01234-12 23114754
21. An assessment of drug-haematin binding as a mechanism for inhibition of haematin polymerisation by quinoline antimalarials. Dorn A, Vippagunta SR, Matile H, Jaquet C, Vennerstrom JL, Ridley RG, Biochem Pharmacol 1998 55 727 736 10.1016/S0006-2952(97)00510-8 9586944 (Pubitemid 28319636)
22. Quinoline antimalarial drugs inhibit spontaneous formation of β-hematin (malaria pigment). Egan TJ, Ross DC, Adams PA, FEBS Lett 1994 352 54 57 10.1016/0014-5793(94)00921-X 7925942 (Pubitemid 24291758)
23. Standardization of the physicochemical parameters to assess in vitro the β-hematin inhibitory activity of antimalarial drugs. Parapini S, Basilico N, Pasini E, Egan TJ, Olliaro P, Taramelli D, Monti D, Exp Parasitol 2000 96 249 256 10.1006/expr.2000.4583 11162378 (Pubitemid 32195402)
24. Glucose-6-phosphate dehydrogenase deficiency. Cappellini MD, Fiorelli G, Lancet 2008 371 64 67 10.1016/S0140-6736(08)60073-2 18177777
25. Rationale for recommending a lower dose of primaquine as a Plasmodium falciparum gametocytocide in populations where G6PD deficiency is common. White NJ, Qiao LG, Qi G, Luzzatto L, Malar J 2012 11 418 10.1186/1475-2875-11-418 23237606
26. Rationale for short course primaquine in Africa to interrupt malaria transmission. Ezifula AC, Gosling R, Hwang J, Hsiang MS, Bousema T, Seidlein L, Drakeley C, Malar J 2012 11 360 10.1186/1475-2875-11-360 23130957
27. Pharmacokinetics of primaquine in man. I. Studies of the absolute bioavailability and effects of dose size. Mihaly GW, Ward SA, Edwards G, Nicholl DD, L'E Orme M, Breckenridge AM, Br J Clin Pharmac 1985 19 745 750 10.1111/j.1365-2125.1985.tb02709.x (Pubitemid 15232141)
28. A new primaquine analogue, tafenoquine (WR 238605), for prophylaxis against Plasmodium falciparum malaria. Shanks GD, Oloo AJ, Aleman GM, Ohrt C, Klotz FW, Braitman D, Horton J, Brueckner R, Clin Infect Dis 2001 33 1968 1974 10.1086/324081 11700577 (Pubitemid 33152389)
29. In vitro activity of tafenoquine against the asexual blood stages of Plasmodium falciparum isolates from Gabon, Senegal, and Djibouti. Pradines B, Mamfoumbi MM, Tall A, Sokhna C, Koeck JL, Fusai T, Mosnier J, Czarnecki E, Spiegel A, Trape JF, Kombila M, Rogier C, Antimicrob Agents Chemother 2006 50 3225 3226 10.1128/AAC.00777-06 16940138 (Pubitemid 44396447)
30. First-time-in-humans safety and pharmacokinetics of WR 238605, a new antimalarial. Brueckner RP, Lasseter KC, Lin ET, Schuster BG, Am J Trop Med Hyg 1998 58 645 649 9598455 (Pubitemid 28237265)
31. Plasma concentrations of tafenoquine, a new long-acting antimalarial agent, in Thai soldiers receiving monthly prophylaxis. Edstein MD, Kocisko DA, Walsh DS, Eamsila C, Charles BG, Rieckmann KH, Clin Infect Dis 2003 37 1654 1658 10.1086/379718 14689348 (Pubitemid 37549953)
32. Improving the therapeutic index of 8-aminoquinolines by the use of drug combinations: review of the literature and proposal for future investigations. Myint HY, Berman J, Walker L, Pybus B, Melendez V, Baird JK, Ohrt C, Am J Trop Med Hyg 2011 85 1010 1014 10.4269/ajtmh.2011.11-0498 22144436
33. Primaquine synergizes the activity of chloroquine against chloroquine-resistant P. falciparum. Bray PG, Deed S, Fox E, Kalkanidis M, Mungthin M, Deady LW, Tilley L, Biochem Pharmacol 2005 70 1158 1166 10.1016/j.bcp.2005.07.021 16139253 (Pubitemid 41317510)
34. Therapeutic efficacy of chloroquine combined with primaquine against Plasmodium falciparum in Northeastern Papua, Indonesia. Baird JK, Wiady I, Sutanihardja A, Suradi D, Suradi P, Basri H, Sekartuti, Ayomi E, Fryauff DJ, Hoffman SL, Am J Trop Med Hyg 2002 66 659 660 12224570 (Pubitemid 35001035)
35. Efficacy of chloroquine plus primaquine treatment and pfcrt mutation in uncomplicated falciparum malaria patients in Rangamati, Bangladesh. Kawai A, Arita N, Matsumoto Y, Kawabata M, Chowdhury MS, Saito-Ito A, Parasitol Int 2011 60 341 346 10.1016/j.parint.2011.05.007 21645634
36. Treatment of chloroquine-resistant Plasmodium vivax with chloroquine and primaquine or halofantrine. Baird JK, Basri H, Subianto B, Fryauff DJ, McElroy PD, Leksana B, Richie TL, Masbar S, Wignall FS, Hoffman SL, J Infect Dis 1995 171 1678 1682 10.1093/infdis/171.6.1678 7769318
37. Ueber die Wirkung des Methylenblau bei Malaria. Ehrlich P, Guttmann P, Berliner klinische Wochhenschrift 1891 28 953 956
38. Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, Eappen AG, Richman A, Sim B, KL L, MCS H, SL F, DA, Proc Natl Acad Sci U S A 2011 108 1214 E1223 10.1073/pnas. 1112037108 22042867
39. In vitro assessment of methylene blue on chloroquine-sensitive and -resistant Plasmodium falciparum strains reveals synergistic action with artemisinins. Akoachere M, Buchholz K, Fischer E, Burhenne J, Haefeli WE, Schirmer RH, Becker K, Antimicrob Agents Chemother 2005 49 4592 4597 10.1128/AAC.49.11.4592-4597.2005 16251300 (Pubitemid 41552588)
40. Blood schizontocidal activity of methylene blue in combination with antimalarials against Plasmodium falciparum. Garavito G, Bertani S, Rincon J, Maurel S, Monje MC, Landau I, Valentin A, Deharo E, Parasite 2007 14 135 140 10.1051/parasite/2007142135 17645185 (Pubitemid 46996359)
41. Methylene blue as an antimalarial agent. Schirmer RH, Coulibaly B, Stich A, Scheiwein M, Merkle H, Eubel J, Becker K, Becher H, Muller O, Zich T, Schiek W, Kouyate B, Redox Rep 2003 8 272 275 10.1179/135100003225002899 14962363 (Pubitemid 38035586)
42. Mode of antimalarial effect of methylene blue and some of its analogues on Plasmodium falciparum in culture and their inhibition of P. vinckei petteri and P. yoelii nigeriensis in vivo. Atamna H, Krugliak M, Shalmiev G, Deharo E, Pescarmona G, Ginsburg H, Biochem Pharmacol 1996 51 693 700 10.1016/S0006- 2952(95)02258-9 8615907 (Pubitemid 26080142)
43. Antimalarial dyes revisited: xanthenes, azines, oxazines, and thiazines. Vennerstrom JL, Makler MT, Angerhofer CK, Williams JA, Antimicrob Agents Chemother 1995 39 2671 2677 10.1128/AAC.39.12.2671 8593000
44. Glutathione reductase-Null malaria parasites have normal blood stage growth but arrest during development in the mosquito. Pastrana-Mena R, Dinglasan RR, Franke-Fayard B, Vega-Rodríguez J, Fuentes-Caraballo M, Baerga-Ortiz A, Coppens I, Jacobs-Lorena M, Janse CJ, Serrano AE, J Biol Chem 2010 285 27045 27056 10.1074/jbc.M110.122275 20573956
45. Elevated levels of methaemoglobin in Tanzanian children with severe and uncomplicated malaria. Antsey NM, Hassanali MY, Mlalasi J, Manyenga D, Mwaikambo ED, Trans R Soc Trop Med Hyg 1996 90 147 151 10.1016/S0035-9203(96)90118-2 8761575 (Pubitemid 26141084)
46. Recombinant Plasmodium falciparum glutathione reductase is inhibited by the antimalarial dye methylene blue. Farber PM, Arscott LD Jr, Williams CH, Becker K, Schirmer RH, FEBS Lett 1998 422 311 314 10.1016/S0014-5793(98)00031-3 9498806 (Pubitemid 28075485)
47. Interactions of methylene blue with human disulfide reductases and their orthologues from Plasmodium falciparum. Buchholz K, Schirmer RH, Eubell JK, Akoachere MB, Dandekar T, Becker K, Gromer S, Antimicrob Agents Chemother 2008 52 183 191 10.1128/AAC.00773-07 17967916
48. Prodrug form of a Plasmodium falciparum glutathione reductase inhibitor conjugated with a 4-anilinoquinoline. Davioud-Charvet E, Delarue S, Biot C, Schwöbel B, Boehme CC, Müssigbrodt A, Maes L, Sergheraert C, Grellier P, Schirmer RH, Becker KA, J Med Chem 2001 44 4268 4276 10.1021/jm010268g 11708927 (Pubitemid 33095332)
49. Methylene blue for malaria in Africa: results from a dose-finding study in combination with chloroquine. Meissner PE, Mandi G, Coulibaly B, Witte S, Tapsoba T, Mansmann U, Rengelhausen J, Schiek W, Jahn A, Walter-Sack I, Mikus G, Burhenne J, Reidel K-D, Schirmer RH, Kouyate B, Muller O, Malar J 2006 5 84 10.1186/1475-2875-5-84 17026773 (Pubitemid 44607525)
50. Strong gametocytocidal effect of methylene blue-based combination therapy against falciparum malaria: a randomised controlled trial. Coulibaly B, Zoungrana A, Mockenhaupt FP, Schirmer RH, Klose C, Mansmann U, Meissner PE, Muller O, PLoS One 2009 4 5318 10.1371/journal.pone.0005318 19415120
51. Safety and efficacy of methylene blue combined with artesunate or amodiaquine for uncomplicated falciparum malaria: a randomized controlled trial from Burkina Faso. Zoungrana A, Coulibaly B, Sié A, Walter-Sack I, Mockenhaupt FP, Kouyaté B, Schirmer RH, Klose C, Mansmann U, Meissner P, Müller O, PLoS One 2008 3 1630 10.1371/journal.pone.0001630 18286187 (Pubitemid 351850988)
52. Plasmodium falciparum resistance to cytocidal versus cytostatic effects of chloroquine. Paguio MF, Bogle KL, Roepe PD, Mol Biochem Parasitol 2011 178 1 6 10.1016/j.molbiopara.2011.03.003 21470564
53. Human malarial parasites in continuous culture. Trager W, Jensen WB, Science 1976 193 673 675 10.1126/science.781840 781840
54. Novel, rapid, and inexpensive cell-based quantification of antimalarial drug efficacy. Bennett TN, Paguio M, Gligorijevic B, Seudieu C, Kosar AD, Davidson E, Roepe PD, Antimicrob Agents Chemother 2004 48 1807 1810 10.1128/AAC.48.5.1807-1810.2004 15105139 (Pubitemid 38544393)
55. Modified fixed-ratio isobologram method for studying in vitro interactions between atovaquone and proguanil or dihydroartemisinin against drug-resistant strains of Plasmodium falciparum. Fivelman QL, Adagu IS, Warhurst DC, Antimicrob Agents Chemother 2004 48 4097 4102 10.1128/AAC.48.11.4097-4102. 2004 15504827 (Pubitemid 39434861)
56. Design, synthesis, and evaluation of 10-N-substituted acridones as novel chemosensitizers in Plasmodium falciparum. Kelly JX, Smilkstein MJ, Cooper RA, Lane KD, Johnson RA, Janowsky A, Dodean RA, Hinrichs DJ, Winter R, Riscoe M, Antimicrob Agents Chemother 2007 51 4133 4140 10.1128/AAC.00669-07 17846138 (Pubitemid 350057815)
57. Discovery of dual function acridones as a new antimalarial chemotype. Kelly JX, Smilkstein MJ, Brun R, Wittlin S, Cooper RA, Lane KD, Janowsky A, Johnson RA, Dodean RA, Winter R, Hinrichs DJ, Riscoe MK, Nature 2009 459 270 273 10.1038/nature07937 19357645
58. A method for testing for synergy with any number of agents. Berenbaum MC, J Infec Dis 1978 137 122 130 10.1093/infdis/137.2.122 (Pubitemid 8289152)
59. Synergy between two calcium channel blockers, verapamil and fantofarone (SR33557), in reversing chloroquine resistance in Plasmodium falciparum. Adovelande J, Deleze J, Schrevel J, Biochem Pharmacol 1998 55 433 440 10.1016/S0006-2952(97)00482-6 9514077 (Pubitemid 28070147)
60. Isobologram analysis in MATLAB for combined effects of two agents in dose-response experiments. Wagenpfeil S, Trieber U, Lehmer A, Medical Data Analysis: 4th International Symposium, ISMDA 2003, Berlin, Germany, LNCS 2868 Berlin: Springer-Verlag Berlin Heidelberg, Perner P, Brause R, Holzhutter H-G, 2003 4 47 54
61. An overview of drug combination analysis with isobolograms. Tallarida RJ, J Pharmacol Exp Ther 2006 319 1 7 10.1124/jpet.106.104117 16670349 (Pubitemid 44455105)
62. Reduced digestive vacuolar accumulation of chloroquine is not linked to resistance to chloroquine toxicity. Cabrera M, Paguio MF, Xie C, Roepe PD, Biochemistry 2009 48 11152 11154 10.1021/bi901765v 19883122
63. Mutations in the P. Falciparum digestive vacuole transmembrane protein PFCRT and evidence for their role in chloroquine resistance. Fidock DA, Nomura T, Talley AK, Cooper RA, Dzekunov SM, Ferdig MT, Ursos LM, Sidhu AB, Naudé B, Deitsch KW, Su XZ, Wootton JC, Roepe PD, Wellems TE, Mol Cell 2000 6 861 871 10.1016/S1097-2765(05)00077-8 11090624
64. Several alleles of the multidrug-resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Foote SJ, Kyle DE, Martin RK, Oduola AM, Forsyth K, Kemp DJ, Cowman AF, Nature 1990 345 255 258 10.1038/345255a0 2185424 (Pubitemid 20163056)
65. In vivo selection of Plasmodium falciparum parasites carrying the chloroquine-susceptible pfcrt K76 allele after treatment with artemether-lumefantrine in Africa. Sisowath C, Petersen I, Veiga MI, Mårtensson A, Premji Z, Björkman A, Fidock DA, Gil JP, J Infect Dis 2009 199 750 757 10.1086/596738 19210165
66. Regulation of intracellular glutathione levels in erythrocytes infected with chloroquine-sensitive and chloroquine-resistant Plasmodium falciparum. Meirjohann S, Walter RD, Muller S, Biochem J 2002 368 761 768 10.1042/BJ20020962 12225291 (Pubitemid 36042677)
67. Glutathione is involved in the antimalarial action of chloroquine and its modulation affects drug sensitivity of human and murine species of Plasmodium. Ginsburg H, Golenser J, Redox Rep 2003 8 276 279 10.1179/135100003225002907 14962364 (Pubitemid 38035587)
68. Quinoline drug-heme interactions and implications for antimalarial cytostatic versus cytocidal activities. Gorka AP, de Dios A, Roepe PD, J Med Chem 2013 April 29 [Epub ahead of print] PMID 23586757