Plasmodium cell biology should inform strategies used in the development of antimalarial transmission-blocking drugs

Future Medicinal Chemistry

Volumn 4, Issue 18, 2012, Pages 2251-2263

  Delves, Michael J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOQUINOLINE; 8 AMINOQUINOLINE DERIVATIVE; ADENOSINE TRIPHOSPHATE; AMINOALCOHOL; ANTIMALARIAL AGENT; ARTEMETHER PLUS BENFLUMETOL; ARTEMISININ; ATOVAQUONE; AZITHROMYCIN; DOXYCYCLINE; ENDOPEROXIDE; FOLIC ACID ANTAGONIST; METHYLENE BLUE; NITD 609; PHOSPHOTRANSFERASE; PRIMAQUINE; PYRIMETHAMINE; SCHIZONTICIDE; SPIROINDOLONE; SULFADOXINE; TAFENOQUINE; UNCLASSIFIED DRUG;

APICOPLAST; ASSAY; CYTOLOGY; DISEASE TRANSMISSION; ENERGY METABOLISM; FERTILIZATION; GAMETOCYTE; GENE REPRESSION; GENETIC TRANSCRIPTION; HUMAN; MALARIA; NONHUMAN; OOCYST; PLASMODIUM; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RNA TRANSLATION; SINGLE DRUG DOSE; SPOROZOITE;

ANIMALS; ANTIMALARIALS; DRUG DISCOVERY; HUMANS; MALARIA; PLASMODIUM;

EID: 84871068874     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.12.182     Document Type: Review

References (98)

1. Alonso PL, Brown G, Arevalo-Herrera M et al. A research agenda to underpin malaria eradication. PLoS Med. 8(1), e1000406 (2011).
2. Delves M, Plouffe D, Scheurer C et al. The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. PLoS Med. 9(2), e1001169 (2012).
3. Gamo F-J, Sanz LM, Vidal J et al. Thousands of chemical starting points for antimalarial lead identification. Nature 465(7296), 305-310 (2010).
4. Guiguemde WA, Shelat AA, Bouck D et al. Chemical genetics of Plasmodium falciparum. Nature 465(7296), 311-315 (2010).
5. Plouffe D, Brinker A, McNamara C et al. In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc. Natl Acad. Sci. USA 105(26), 9059-9064 (2008).
6. Lelièvre J, Almela MJ, Lozano S et al. Activity of clinically relevant antimalarial drugs on Plasmodium falciparum mature gametocytes in an atp bioluminescence 'transmission blocking' assay. PLoS ONE 7(4), e35019 (2012).
7. Adjalley SH, Johnston GL, Li T et al. Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc. Natl Acad. Sci. USA 108(47), E1214-E1223 (2011).
8. Tanaka TQ, Williamson KC. A malaria gametocytocidal assay using oxidoreduction indicator, alamarBlue. Mol. Biochem. Parasitol. 177(2), 160-163 (2011).
9. Delves MJ, Ramakrishnan C, Blagborough AM, Leroy D, Wells TNC, Sinden RE. A high-throughput assay for the identification of malarial transmission- blocking drugs and vaccines. Int. J. Parasitol. 42(11), 999-1006 (2012).
10. Sinden RE. Sexual development of malarial parasites. Adv. Parasitol. 22, 153-216 (1983).
11. Smalley ME. Plasmodium falciparum gametocytes: the effect of chloroquine on their development. Trans. R. Soc. Trop. Med. Hyg. 71(6), 526-529 (1977).
12. Chutmongkonkul M, Maier WA, Seitz HM. A new model for testing gametocytocidal effects of some antimalarial drugs on Plasmodium falciparum in vitro. Ann. Trop. Med. Parasitol. 86(3), 207-215 (1992).
13. Kumar N, Zheng H. Stage-specific gametocytocidal effect in vitro of the antimalaria drug qinghaosu on Plasmodium falciparum. Parasitol. Res. 76(3), 214-218 (1990). (Pubitemid 20116097)
14. Sinden RE, Smalley ME. Gametocytogenesis of Plasmodium falciparum in vitro: the cell-cycle. Parasitology 79(2), 277-296 (1979). (Pubitemid 10242529)
15. Bousema T, Okell L, Shekalaghe S et al. Revisiting the circulation time of Plasmodium falciparum gametocytes: molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malar. J. 9, 136 (2010).
16. Butcher GA. Antimalarial drugs and the mosquito transmission of Plasmodium. Int. J. Parasitol. 27(9), 975-987 (1997). (Pubitemid 27423685)
17. Chotivanich K, Sattabongkot J, Udomsangpetch R et al. Transmission-blocking activities of quinine, primaquine, and artesunate. Antimicrob. Agents Chemother. 50(6), 1927-1930 (2006). (Pubitemid 43807507)
18. Hawking F, Worms MJ, Gammage K. 24-and 48-hour cycles of malaria parasites in the blood; their purpose, production and control. Trans. R. Soc. Trop. Med. Hyg. 62(6), 731-760 (1968).
19. Khan SM, Franke-Fayard B, Mair GR et al. Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121(5), 675-687 (2005). (Pubitemid 40797591)
20. Robert V, Sokhna CS, Rogier C, Ariey F, Trape JF. Sex ratio of Plasmodium falciparum gametocytes in inhabitants of Dielmo, Senegal. Parasitology. 127(Pt 1), 1-8 (2003). (Pubitemid 36836572)
21. Gbotosho GO, Sowunmi A, Happi CT, Okuboyejo TM. Plasmodium falciparum gametocyte carriage, sex ratios and asexual parasite rates in Nigerian children before and after a treatment protocol policy change instituting the use of artemisinin-based combination therapies. Mem. Inst. Oswaldo Cruz. 106(6), 685-690 (2011).
22. Billker O, Lindo V, Panico M et al. Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito. Nature 392(6673), 289-292 (1998). (Pubitemid 28155102)
23. Toyé PJ, Sinden RE, Canning EU. The action of metabolic inhibitors on microgametogenesis in Plasmodium yoelii nigeriensis. Z Parasitenkd. 53(2), 133-141 (1977). (Pubitemid 8212320)
24. Raabe AC, Billker O, Vial HJ, Wengelnik K. Quantitative assessment of DNA replication to monitor microgametogenesis in Plasmodium berghei. Mol. Biochem. Parasitol. 168(2), 172-176 (2009).
25. Baker DA. Malaria gametocytogenesis. Mol. Biochem. Parasitol. 172(2), 57-65 (2010).
26. Mair GR, Braks JAM, Garver LS et al. Regulation of sexual development of Plasmodium by translational repression. Science 313(5787), 667-669 (2006). (Pubitemid 44201144)
27. Ecker A, Bushell ESC, Tewari R, Sinden RE. Reverse genetics screen identifies six proteins important for malaria development in the mosquito. Mol. Microbiol. 70(1), 209-220 (2008).
28. Raine JD, Ecker A, Mendoza J, Tewari R, Stanway RR, Sinden RE. Female inheritance of malarial lap genes is essential for mosquito transmission. PLoS Pathog. 3(3), e30 (2007).
29. van Dijk MR, Janse CJ, Thompson J et al. A central role for P48/45 in malaria parasite male gamete fertility. Cell 104(1), 153-164 (2001). (Pubitemid 32144980)
30. Pringle GA. Count of the sporozoites in an oocyst of Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 59, 289-290 (1965).
31. Sinden RE, Blagborough AM, Ramakrishnan C, Biswas S, Delves MJ. The design and interpretation of laboratory assays measuring mosquito transmission of Plasmodium. Trends Parasitol. 28(11), 457-465 (2012).
32. Giao PT, Vries PJ, Binh TQ, Nam NV, Kager PA. Early diagnosis and treatment of uncomplicated malaria and patterns of health seeking in Vietnam. Trop. Med. Int. Health. 10(9), 919-925 (2005). (Pubitemid 41291233)
33. Tangpukdee N, Krudsood S, Srivilairit S et al. Gametocyte clearance in uncomplicated and severe Plasmodium falciparum malaria after artesunate-mefloquine treatment in Thailand. Korean J. Parasitol. 46(2), 65-70 (2008).
34. Sinden RE. Gametocytogenesis of Plasmodium falciparum in vitro: ultrastructural observations on the lethal action of chloroquine. Ann. Trop. Med. Parasitol. 76(1), 15-23 (1982). (Pubitemid 12150842)
35. Peatey CL, Spicer T, Hodder P, Trenholme KR, Gardiner DL. A high-throughput assay for the identification of drugs against late-stage Plasmodium falciparum gametocytes. Mol. Biochem. Parasitol. 180(2), 127-131 (2011).
36. Sáenz FE, Mutka T, Udenze K, Oduola AMJ, Kyle DE. Novel 4-aminoquinoline analogs highly active against the blood and sexual stages of Plasmodium in vivo and in vitro. Antimicrob. Agents Chemother. 56(9), 4685-4692 (2012).
37. Buchholz K, Burke TA, Williamson KC, Wiegand RC, Wirth DF, Marti M. A high-throughput screen targeting malaria transmission stages opens new avenues for drug development. J. Infect. Dis. 203(10), 1445-1453 (2011).
38. Sinden RE. A biologist's perspective on malaria vaccine development. Hum. Vaccin. 6(1), 3-11 (2010).
39. Hartwig CL, Rosenthal AS, D'Angelo J, Griffin CE, Posner GH, Cooper RA. Accumulation of artemisinin trioxane derivatives within neutral lipids of Plasmodium falciparum malaria parasites is endoperoxide-dependent. Biochem. Pharmacol. 77(3), 322-336 (2009).
40. Klonis N, Crespo-Ortiz MP, Bottova I et al. Artemisinin activity against Plasmodium falciparum requires hemoglobin uptake and digestion. Proc. Natl Acad. Sci. USA 108(28), 11405-11410 (2011).
41. Krishna S, Pulcini S, Fatih F, Staines H. Artemisinins and the biological basis for the PfATP6/SERCA hypothesis. Trends Parasitol. 26(11), 517-523 (2010).
42. Arnou B, Montigny C, Morth JP et al. The Plasmodium falciparum Ca(2+)-ATPase PfATP6: insensitive to artemisinin, but a potential drug target. Biochem. Soc. Trans. 39(3), 823-831 (2011).
43. Chen PQ, Li GQ, Guo XB et al. The infectivity of gametocytes of Plasmodium falciparum from patients treated with artemisinin. Chin. Med. J. 107(9), 709-711 (1994).
44. Bousema JT, Schneider P, Gouagna LC et al. Moderate effect of artemisinin-based combination therapy on transmission of Plasmodium falciparum. J. Infect. Dis. 193(8), 1151-1159 (2006).
45. Price RN, Nosten F, Luxemburger C et al. Effects of artemisinin derivatives on malaria transmissibility. Lancet 347(9016), 1654-1658 (1996). (Pubitemid 26177386)
46. Okell L, Drakeley C, Ghani A, Bousema T, Sutherland C. Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials. Malar. J. 7(1), 125 (2008).
47. Kurosawa Y, Dorn A, Kitsuji-Shirane M et al. Hematin polymerization assay as a high-throughput screen for identification of new antimalarial pharmacophores. Antimicrob. Agents Chemother. 44(10), 2638-2644 (2000).
48. Mungthin M, Bray PG, Ridley RG, Ward SA. Central Role of Hemoglobin Degradation in Mechanisms of Action of 4-Aminoquinolines, Quinoline Methanols, and Phenanthrene Methanols. Antimicrob Agents Chemother. 42(11), 2973-2977 (1998). (Pubitemid 28501235)
49. Hogh B, Gamage-Mendis A, Butcher GA et al. The differing impact of chloroquine and pyrimethamine/sulfadoxine upon the infectivity of malaria species to the mosquito vector. Am. J. Trop. Med. Hyg. 58(2), 176-182 (1998). (Pubitemid 28096223)
50. Coleman RE, Clavin AM, Milhous WK. Gametocytocidal and sporontocidal activity of antimalarials against Plasmodium berghei ANKA in ICR Mice and Anopheles stephensi mosquitoes. Am. J. Trop. Med. Hyg. 46(2), 169-182 (1992).
51. Burgess RW, Bray RS. The effect of a single dose of primaquine on the gametocytes, gametogony and sporogony of Laverania falciparum. Bull. World Health Organ. 24(4-5), 451-456 (1961).
52. Wilairatana P, Krudsood S, Tangpukdee N. Appropriate time for primaquine treatment to reduce Plasmodium falciparum transmission in hypoendemic areas. Korean J. Parasitol. 48(2), 179-182 (2010).
53. Vale N, Moreira R, Gomes P. Primaquine revisited six decades after its discovery. Eur. J. Med. Chem. 44(3), 937-953 (2009).
54. Salcedo-Sora JE, Ochong E, Beveridge S, et al. The molecular basis of folate salvage in Plasmodium falciparum characterization of two folate transporters. J. Biol. Chem. 286(52), 44659-44668 (2011).
55. Shute PG, Maryon M. The effect of pyrimethamine (daraprim) on the gametocytes and oocysts of Plasmodium falciparum and Plasmodium vivax. Trans. R. Soc. Trop. Med. Hyg. 48(1), 50-52 (1954).
56. Kone A, van de Vegte-Bolmer M, Siebelink-Stoter R, et al. Sulfadoxine-pyrimethamine impairs Plasmodium falciparum gametocyte infectivity and Anopheles mosquito survival. Int. J. Parasitol. 40(10), 1221-1228 (2010).
57. Teklehaimanot A, Nguyen-Dinh P, Collins WE, Barber AM, Campbell CC. Evaluation of sporontocidal compounds using Plasmodium falciparum gametocytes produced in vitro. Am. J. Trop. Med. Hyg. 34(3), 429-434 (1985). (Pubitemid 15041362)
58. Saito-Nakano Y, Tanabe K, Mita T. Identification of pyrimethamine-and chloroquine-resistant Plasmodium falciparum in Africa between 1984 and 1998: genotyping of archive blood samples. Malar. J. 10(1), 388 (2011).
59. Delves MJ, Sinden RE. A semi-automated method for counting fluorescent malaria oocysts increases the throughput of transmission blocking studies. Malar. J. 9(1), 35 (2010).
60. Ezzet F, van Vugt M, Nosten F, Looareesuwan S, White NJ. Pharmacokinetics and pharmacodynamics of lumefantrine (benflumetol) in acute falciparum malaria. Antimicrob. Agents Chemother. 44(3), 697-704 (2000). (Pubitemid 30117964)
61. V Pelt-Koops JC, Pett HE, Graumans W et al. The spiroindolone drug candidate NITD609 potently inhibits gametocytogenesis and blocks Plasmodium falciparum transmission to Anopheles mosquito vector. Antimicrob Agents Chemother. 56(7), 3544-3548 (2012).
62. Mens PF, Sawa P, van Amsterdam SM, et al. A randomized trial to monitor the efficacy and effectiveness by QT-NASBA of artemether-lumefantrine versus dihydroartemisinin-piperaquine for treatment and transmission control of uncomplicated Plasmodium falciparum malaria in western Kenya. Malar. J. 7, 237 (2008).
63. Okafor HU, Shu EN, Oguonu T. Therapeutic efficacy and effect on gametocyte carriage of an artemisinin and a non-based combination treatment in children with uncomplicated P. falciparum malaria, living in an area with high-level chloroquine resistance. J. Trop. Pediatr. 56(6), 398-406 (2010).
64. Buchholz K, Schirmer RH, Eubel JK et al. Interactions of methylene blue with human disulfide reductases and their orthologues from Plasmodium falciparum. Antimicrob Agents Chemother. 52(1), 183-191 (2008).
65. Coulibaly B, Zoungrana A, Mockenhaupt FP, et al. Strong gametocytocidal effect of methylene blue-based combination therapy against falciparum malaria: a randomised controlled trial. PLoS ONE 4(5), e5318 (2009).
66. Barton V, Fisher N, Biagini GA, Ward SA, O'Neill PM. Inhibiting Plasmodium cytochrome bc1: a complex issue. Curr. Op. Chem. Biol. 14(4), 440-446 (2010).
67. Painter HJ, Morrisey JM, Vaidya AB. Mitochondrial electron transport inhibition and viability of intraerythrocytic Plasmodium falciparum. Antimicrob Agents Chemother. 54(12), 5281-5287 (2010).
68. Fleck SL, Pudney M, Sinden RE. The effect of atovaquone (566C80) on the maturation and viability of Plasmodium falciparum gametocytes in vitro. Trans. R. Soc. Trop. Med. Hyg. 90(3), 309-312 (1996). (Pubitemid 26188885)
69. Fowler RE, Billingsley PF, Pudney M, Sinden RE. Inhibitory action of the anti-malarial compound atovaquone (566C80) against Plasmodium berghei ANKA in the mosquito, Anopheles stephensi. Parasitol. 108(4), 383-388 (1994). (Pubitemid 24159560)
70. Fowler RE, Sinden RE, Pudney M. Inhibitory activity of the anti-malarial atovaquone (566C80) against ookinetes, oocysts, and sporozoites of Plasmodium berghei. J. Parasitol. 81(3), 452-458 (1995).
71. Na-Bangchang K, Manyando C, Ruengweerayut R et al. The pharmacokinetics and pharmacodynamics of atovaquone and proguanil for the treatment of uncomplicated Falciparum malaria in third-trimester pregnant women. Eur. J. Clin. Pharmacol. 61(8), 573-582 (2005). (Pubitemid 41414241)
72. Butcher GA, Sinden RE. Persistence of Atovaquone in Human Sera Following Treatment: inhibition of P. Falciparum Development in vivo and in vitro. Am. J. Trop. Med. Hyg. 68(1), 111-114 (2003). (Pubitemid 38234858)
73. Rottmann M, McNamara C, Yeung BKS et al. Spiroindolones, a potent compound class for the treatment of malaria. Science 329(5996), 1175-1180 (2010).
74. Yeung BKS, Zou B, Rottmann M et al. Spirotetrahydro beta-carbolines (spiroindolones): a new class of potent and orally efficacious compounds for the treatment of malaria. J. Med. Chem. 53(14), 5155-5164 (2010
75. Mather MW, Vaidya AB. Mitochondria in malaria and related parasites: ancient, diverse and streamlined. J. Bioenerg. Biomembr. 40(5), 425-433 (2008).
76. Painter HJ, Morrisey JM, Mather MW, Vaidya AB. Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum. Nature 446(7131), 88-91 (2007). (Pubitemid 46348043)
77. Baldwin J, Michnoff CH, Malmquist NA et al. High-throughput screening for potent and selective inhibitors of Plasmodium falciparum dihydroorotate dehydrogenase. J. Biol. Chem. 280(23), 21847-21853 (2005). (Pubitemid 40827835)
78. Olszewski KL, Mather MW, Morrisey JM et al. Branched tricarboxylic acid metabolism in Plasmodium falciparum. Nature 466(7307), 774-778 (2010).
79. Bulusu V, Jayaraman V, Balaram H. Metabolic fate of fumarate, a side product of purine salvage pathway in the intraerythrocytic stages of Plasmodium falciparum. J. Biol. Chem. 286(11), 9236-9245 (2011).
80. Mogi T, Kita K. Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium. Parasitol. Int. 59(3), 305-312 (2010).
81. Krungkrai J, Prapunwattana P, Krungkrai SR. Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite 7(1), 19-26 (2000).
82. Krungkrai J. The multiple roles of the mitochondrion of the malarial parasite. Parasitol. 129(Pt 5), 511-524 (2004). (Pubitemid 39473002)
83. Hall N, Karras M, Raine JD et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307(5706), 82-86 (2005). (Pubitemid 40093481)
84. Boysen KE, Matuschewski K. Arrested oocyst maturation in Plasmodium parasites lacking type II NADH:ubiquinone dehydrogenase. J. Biol. Chem. 286(37), 32661-32671 (2011).
85. Hino A, Hirai M, Tanaka TQ, Watanabe Y-I, Matsuoka H, Kita K. Critical roles of the mitochondrial complex II in oocyst formation of rodent malaria parasite Plasmodium berghei. J. Biochem. (2012) (In Press).
86. Dahl EL, Rosenthal PJ. Multiple antibiotics exert delayed effects against the Plasmodium falciparum apicoplast. Antimicrob. Agents Chemother. 51(10), 3485-3490 (2007). (Pubitemid 47519333)
87. Yeh E, Derisi JL. Chemical Rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol. 9(8), e1001138 (2011).
88. Shimizu S, Osada Y, Kanazawa T, Tanaka Y, Arai M. Suppressive effect of azithromycin on Plasmodium berghei mosquito-stage development and apicoplast replication. Malar. J. 9(1), 73 (2010).
89. Stanway RR, Witt T, Zobiak B, Aepfelbacher M, Heussler VT. GFP-targeting allows visualization of the apicoplast throughout the life cycle of live malaria parasites. Biol. Cell 101(7), 415-430, (2009).
90. Tewari R, Straschil U, Bateman A et al. The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission. Cell Host Microbe 8(4), 377-387 (2010).
91. Ojo KK, Pfander C, Mueller NR et al. Transmission of malaria to mosquitoes blocked by bumped kinase inhibitors. J. Clin. Invest. 122(6), 2301-2305 (2012).
92. Taylor HM, McRobert L, Grainger M et al. The malaria parasite cyclic GMP-dependent protein kinase plays a central role in blood-stage schizogony. Eukaryotic Cell 9(1), 37-45 (2010).
93. McRobert L, Taylor CJ, Deng W et al. Gametogenesis in malaria parasites is mediated by the cGMP-dependent protein kinase. PLoS Biol. 6(6), e139 (2008).
94. Sebastian S, Brochet M, Collins MO et al. A Plasmodium calcium-dependent protein kinase controls zygote development and transmission by translationally activating repressed mRNAs. Cell Host Microbe 12(1), 9-19 (2012).
95. Mair GR, Lasonder E, Garver LS et al. Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog. 6(2), e1000767 (2010).
96. Billker O, Shaw MK, Margos G, Sinden RE. The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 115(1), 1-7 (1997). (Pubitemid 27337220)
97. Talman AM, Lacroix C, Marques SR et al. PbGEST mediates malaria transmission to both mosquito and vertebrate host. Mol. Microbiol. 82(2), 462-474 (2011).
98. Billker O, Dechamps S, Tewari R, Wenig G, Franke-Fayard B, Brinkmann V. Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite. Cell 117(4), 503-514 (2004). (Pubitemid 38610235)