Novel approaches in antimalarial drug discovery

Expert Opinion on Drug Discovery

Volumn 8, Issue 11, 2013, Pages 1325-1337

  Held, Jana ^a,b   Kreidenweiss, Andrea ^a,b   Mordmüller, Benjamin ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b German Centre for Diabetes Research   (Germany)

Author keywords

CHMI; Gametocyte; Hypnozoite; Nanoparticle; Plasmodium

Indexed keywords

ANTIMALARIAL AGENT; ARTEMETHER; ARTEMISININ; ARTEROLANE; ARTESUNATE; BULAQUINE; CHLOROQUINE; DSM 265; FERROQUINE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; KAE 609; KAF 156; LIPOSOME; NANOCARRIER; NANOPARTICLE; NITD 609; NPC 1161B; PRIMAQUINE; QUININE; TAFENOQUINE; UNCLASSIFIED DRUG;

DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG EFFICACY; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HUMAN; LIFE CYCLE STAGE; MALARIA; MALARIA CONTROL; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM OVALE; PLASMODIUM VIVAX; PRIORITY JOURNAL; RECOMMENDED DRUG DOSE; REVIEW; SINGLE DRUG DOSE;

ANIMALS; ANTIMALARIALS; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; HUMANS; PLASMODIUM;

EID: 84886638407     PISSN: 17460441     EISSN: 1746045X     Source Type: Journal    
DOI: 10.1517/17460441.2013.843522     Document Type: Review

References (138)

1. World Health Organization (WHO). World Malaria Report 2012. Geneva, Switzerland: World Health Organization (WHO); 2012
2. Murray CJ, Rosenfeld LC, Lim SS, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012;379(9814): 413-31
3. Andriopoulos P, Economopoulou A, Spanakos G, Assimakopoulos G. A local outbreak of autochthonous Plasmodium vivax malaria in Laconia, Greece-a re-emerging infection in the southern borders of Europe? Int J Infect Dis 2013;17(2):e125-8
4. World Health Organisation (WHO) ROfEI. Centralized information system for infectious diseases (CISID) database. Malaria. World Health Organization; Copenhagen: 2012. Available from: http://data.euro.who.int/cisid/[[Last accessed 24 May 2013] .. Data base of WHO showing all registered malaria cases in Europe stratified by country and by year.
5. WHO Malaria Policy Advisory Committee and Secretariat. Malaria Policy Advisory Committee to the WHO: conclusions and recommendations of September 2012 meeting. Malar J 2012;11: 424
6. Alonso PL, Brown G, Arevalo-Herrera M, et al. A research agenda to underpin malaria eradication. PLoS Med 2011;8(1):e1000406. Requirements for antimalarial drug development in the era of malaria eradication.
7. Feachem R, Sabot O. A new global malaria eradication strategy. Lancet 2008;371(9624): 1633-5
8. RTS,S Clinical Trials Partnership. Agnandji ST, Lell B, Fernandes JF, et al. A Phase 3 trial of RTS,S/AS01 malaria vaccine in african infants. New Engl J Med 2012;367(24): 2284-95. Efficacy data of the first antimalarial vaccine in a Phase III clinical trial in African infants.
9. Riley EM, Stewart VA. Immune mechanisms in malaria: new insights in vaccine development. Nat Med 2013;19(2): 168-78
10. D'Alessandro U, Buttiens H. History and importance of antimalarial drug resistance. Trop Med Int Health 2001;6(11): 845-8
11. Petersen I, Eastman R, Lanzer M. Drug-resistant malaria: molecular mechanisms and implications for public health. FEBS Lett 2011;585(11): 1551-62
12. Kremsner PG, Taylor T, Issifou S, et al. A simplified intravenous artesunate regimen for severe malaria. J Infect Dis 2012;205(2): 312-19
13. Kremsner PG, Krishna S. Antimalarial combinations. Lancet 2004;364(9430): 285-94
14. Dondorp AM, Nosten F, Yi P, et al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 2009;361(5): 455-67
15. Noedl H, Socheat D, Satimai W. Artemisinin-resistant malaria in Asia. N Engl J Med 2009;361(5): 540-1
16. Noedl H, Se Y, Schaecher K, et al. Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 2008;359(24): 2619-20
17. Cheeseman IH, Miller BA, Nair S, et al. A major genome region underlying artemisinin resistance in malaria. Science 2012;336(6077): 79-82
18. Anthony MP, Burrows JN, Duparc S, et al. The global pipeline of new medicines for the control and elimination of malaria. Malar J 2012;11: 316
19. Tschan S, Kremsner PG, Mordmuller B. Emerging drugs for malaria. Expert Opin Emerg Drugs 2012;17(3): 319-33
20. Burrows JN. Antimalarial drug discovery: where next? Fut Med Chem 2012;4(18): 2233-5
21. Mordmuller B, Kremsner PG. Malarial parasites vs. antimalarials: never-ending rumble in the jungle. Curr Mol Med 2006;6(2): 247-51
22. Burrows JN, Hooft van Huijsduijnen R, Mohrle JJ, et al. Designing the next generation of medicines for malaria control and eradication. Malar J 2013;12: 187
23. MMV. Global malaria portfolio. 2013.Available from: http://www.mmv. org/research-development/rd-portfolio [Cited 28 May2013] .. Webpage showing the current antimalarial portfolio in the different phases of clinical development.
24. Olliaro P, Wells TN. The global portfolio of new antimalarial medicines under development. Clin Pharmacol Ther 2009;85(6): 584-95
25. Rosenthal PJ. Antimalarial drug discovery: old and new approaches. J Exp Biol 2003;206(Pt 21): 3735-44
26. Aguiar AC, Rocha EM, Souza NB, et al. New approaches in antimalarial drug discovery and development: a review. Mem Inst Oswaldo Cruz 2012;107(7): 831-45
27. Calderon F, Wilson DM, Gamo FJ. Antimalarial drug discovery: recent progress and future directions. Prog Med Chem 2013;52: 97-151
28. Wells TN, Alonso PL, Gutteridge WE. New medicines to improve control and contribute to the eradication of malaria. Nat Rev Drug Discov 2009;8(11): 879-91
29. Dubar F, Egan TJ, Pradines B, et al. The antimalarial ferroquine: role of the metal and intramolecular hydrogen bond in activity and resistance. ACS Chem Biol 2011;6(3): 275-87
30. Kreidenweiss A, Kremsner PG, Dietz K, Mordmuller B. In vitro activity of ferroquine (SAR97193) is independent of chloroquine resistance in Plasmodium falciparum. Am J Trop Med Hyg 2006;75(6): 1178-81
31. Talisuna AO, Karema C, Ogutu B, et al. Mitigating the threat of artemisinin resistance in Africa: improvement of drug-resistance surveillance and response systems. Lancet Infect Dis 2012;12(11): 888-96
32. Mandal S, Moudgil M, Mandal SK. Rational drug design. Eur J Pharmacol 2009;625(1-3): 90-100
33. Wells TN. Microbiology. Is the tide turning for new malaria medicines? Science 2010;329(5996): 1153-4
34. Swinney DC, Anthony J. How were new medicines discovered? Nat Rev Drug Discov 2011;10(7): 507-19
35. Sams-Dodd F. Target-based drug discovery: is something wrong? Drug Discov Today 2005;10(2): 139-47
36. Jomaa H, Wiesner J, Sanderbrand S, et al. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 1999;285(5433): 1573-6
37. Brucher K, Illarionov B, Held J, et al. alpha-Substituted beta-oxa isosteres of fosmidomycin: synthesis and biological evaluation. J Med Chem 2012;55(14): 6566-75
38. Baldwin J, Michnoff CH, Malmquist NA, et al. High-throughput screening for potent and selective inhibitors of Plasmodium falciparum dihydroorotate dehydrogenase. J Biol Chem 2005;280(23): 21847-53
39. Coteron JM, Marco M, Esquivias J, et al. Structure-guided lead optimization of triazolopyrimidine-ring substituents identifies potent Plasmodium falciparum dihydroorotate dehydrogenase inhibitors with clinical candidate potential. J Med Chem 2011;54(15): 5540-61
40. Yuthavong Y, Tarnchompoo B, Vilaivan T, et al. Malarial dihydrofolate reductase as a paradigm for drug development against a resistance-compromised target. Proc Natl Acad Sci USA 2012;109(42): 16823-8
41. Gamo FJ, Sanz LM, Vidal J, et al. Thousands of chemical starting points for antimalarial lead identification. Nature 2010;465(7296): 305-10. One of the studies identifying new compounds against P. falciparum blood stages in a high throughput screen.
42. Guiguemde WA, Shelat AA, Bouck D, et al. Chemical genetics of Plasmodium falciparum. Nature 2010;465(7296): 311-15. One of the studies identifying new compounds against P. falciparum blood stages in a high throughput screen.
43. Rottmann M, McNamara C, Yeung BK, et al. Spiroindolones, a potent compound class for the treatment of malaria. Science 2010;329(5996): 1175-80. One of the studies identifying new compounds against P. falciparum blood stages in a high throughput screen and further description of the compound which is now in Phase II clinical trials.
44. ChEMBL-NTD-Neglected Tropical Disease archive. 2013. Available from: https://www.ebi.ac.uk/chemblntd [Last accessed 24 May 2013]
45. Meister S, Plouffe DM, Kuhen KL, et al. Imaging of Plasmodium liver stages to drive next-generation antimalarial drug discovery. Science 2011;334(6061): 1372-7. One of the studies identifying new compounds against P. falciparum blood stages in a high throughput screen.
46. Derbyshire ER, Prudencio M, Mota MM, Clardy J. Liver-stage malaria parasites vulnerable to diverse chemical scaffolds. Proc Natl Acad Sci USA 2012;109(22): 8511-16. One of the studies identifying new compounds against P. yoelii liver stages in a high throughput screen.
47. van 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 2012;56(7): 3544-8. One of the studies identifying new compounds against P. berghei liver stages in a high throughput screen.
48. Lang-Unnasch N, Murphy AD. Metabolic changes of the malaria parasite during the transition from the human to the mosquito host. Annu Rev Microbiol 1998;52: 561-90
49. Peatey CL, Skinner-Adams TS, Dixon MW, et al. Effect of antimalarial drugs on Plasmodium falciparum gametocytes. J Infect Dis 2009;200(10): 1518-21
50. Dechy-Cabaret O, Benoit-Vical F. Effects of antimalarial molecules on the gametocyte stage of Plasmodium falciparum: the debate. J Med Chem 2012;55(23): 10328-44
51. Robert V, Awono-Ambene HP, Le Hesran JY, Trape JF. Gametocytemia and infectivity to mosquitoes of patients with uncomplicated Plasmodium falciparum malaria attacks treated with chloroquine or sulfadoxine plus pyrimethamine. Am J Trop Med Hyg 2000;62(2): 210-16
52. Dunyo S, Milligan P, Edwards T, et al. Gametocytaemia after drug treatment of asymptomatic Plasmodium falciparum. PLoS Clin Trials 2006;1(4):e20
53. Schneider P, Bousema T, Omar S, et al. (Sub)microscopic Plasmodium falciparum gametocytaemia in Kenyan children after treatment with sulphadoxine-pyrimethamine monotherapy or in combination with artesunate. Int J Parasitol 2006;36(4): 403-8
54. 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 2010;40(10): 1221-8
55. Shinondo CJ, Lanners HN, Lowrie RC Jr, Wiser MF. Effect of pyrimethamine resistance on sporogony in a Plasmodium berghei/Anopheles stephensi model. Exp Parasitol 1994;78(2): 194-202
56. Targett G, Drakeley C, Jawara M, et al. Artesunate reduces but does not prevent posttreatment transmission of Plasmodium falciparum to Anopheles gambiae. J Infect Dis 2001;183(8): 1254-9
57. Shekalaghe S, Drakeley C, Gosling R, et al. Primaquine clears submicroscopic Plasmodium falciparum gametocytes that persist after treatment with sulphadoxine-pyrimethamine and artesunate. PLoS One 2007;2(10):e1023
58. Graves PM, Gelband H, Garner P. Primaquine for reducing Plasmodium falciparum transmission. Cochrane Database Syst Rev 2012;9:CD008152
59. John GK, Douglas NM, von Seidlein L, et al. Primaquine radical cure of Plasmodium vivax: a critical review of the literature. Malar J 2012;11: 280
60. Vale N, Moreira R, Gomes P. Primaquine revisited six decades after its discovery. Eur J Med Chem 2009;44(3): 937-53
61. von Seidlein L, Auburn S, Espino F, et al. Review of key knowledge gaps in glucose-6-phosphate dehydrogenase deficiency detection with regard to the safe clinical deployment of 8-aminoquinoline treatment regimens: a workshop report. Malar J 2013;12: 112
62. Howes RE, Battle KE, Satyagraha AW, et al. G6PD deficiency: global distribution, genetic variants and primaquine therapy. Adv Parasitol 2013;81: 133-201
63. WHO Working Group. Glucose-6-phosphate dehydrogenase deficiency. Bull World Health Organ 1989;67(6): 601-11
64. Cappellini MD, Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet 2008;371(9606): 64-74
65. Mordmuller B, Turrini F, Long H, et al. Neutrophils and monocytes from subjects with the Mediterranean G6PD variant: effect of Plasmodium falciparum hemozoin on G6PD activity, oxidative burst and cytokine production. Eur Cytokine Netw 1998;9(3): 239-45
66. Manganelli G, Fico A, Martini G, Filosa S. Discussion on pharmacogenetic interaction in G6PD deficiency and methods to identify potential hemolytic drugs. Cardiovasc Hematol Disord Drug Targets 2010;10(2): 143-50
67. Manganelli G, Masullo U, Passarelli S, Filosa S. Glucose-6-phosphate dehydrogenase deficiency: disadvantages and possible benefits. Cardiovasc Hematol Disord Drug Targets 2013;13(1): 73-82
68. Shah NK, Schapira A, Juliano JJ, et al. A non-randomized controlled trial of artesunate plus sulfadoxine-pyrimethamine with or without primaquine for preventing the post-treatment circulation of Plasmodium falciparum gametocytes. Antimicrob Agents Chemother 2013;
69. Krudsood S, Wilairatana P, Tangpukdee N, et al. Safety and tolerability of elubaquine (bulaquine, CDRI 80/53) for treatment of Plasmidium vivax malaria in Thailand. Korean J Parasitol 2006;44(3): 221-8
70. Gogtay NJ, Kamtekar KD, Dalvi SS, et al. A randomized, parallel study of the safety and efficacy of 45 mg primaquine versus 75 mg bulaquine as gametocytocidal agents in adults with blood schizonticide-responsive uncomplicated falciparum malaria [ISCRTN50134587]. BMC Infect Dis 2006;6: 16
71. Peatey CL, Spicer TP, Hodder PS, et al. A high-throughput assay for the identification of drugs against late-stage Plasmodium falciparum gametocytes. Mol Biochem Parasitol 2011;180(2): 127-31
72. Lelievre 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 2012;7(4):e35019
73. Chevalley S, Coste A, Lopez A, et al. Flow cytometry for the evaluation of anti-plasmodial activity of drugs on Plasmodium falciparum gametocytes. Malar J 2010;9: 49
74. Tanaka TQ, Williamson KC. A malaria gametocytocidal assay using oxidoreduction indicator, alamarBlue. Mol Biochem Parasitol 2011;177(2): 160-3
75. Gething PW, Elyazar IR, Moyes CL, et al. A long neglected world malaria map: plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis 2012;6(9):e1814
76. Price RN, Tjitra E, Guerra CA, et al. Vivax malaria: neglected and not benign. Am J Trop Med Hyg 2007;77(6 Suppl): 79-87
77. Yohannes AM, Teklehaimanot A, Bergqvist Y, Ringwald P. Confirmed vivax resistance to chloroquine and effectiveness of artemether-lumefantrine for the treatment of vivax malaria in Ethiopia. Am J Trop Med Hyg 2011;84(1): 137-40
78. Mombo-Ngoma G, Kleine C, Basra A, et al. Prospective evaluation of artemether-lumefantrine for the treatment of non-falciparum and mixed-species malaria in Gabon. Malar J 2012;11: 120
79. White NJ. Determinants of relapse periodicity in Plasmodium vivax malaria. Malar J 2011;10: 297
80. Baird JK, Hoffman SL. Primaquine therapy for malaria. Clin Infect Dis 2004;39(9): 1336-45
81. Galappaththy GN, Omari AA, Tharyan P. Primaquine for preventing relapses in people with Plasmodium vivax malaria. Cochrane Database Syst Rev 2007(1):CD004389
82. Adak T, Valecha N, Sharma VP. Plasmodium vivax polymorphism in a clinical drug trial. Clin Diagn Lab Immunol 2001;8(5): 891-4
83. Dutta GP, Puri SK, Bhaduri AP, Seth M. Radical curative activity of a new 8-aminoquinoline derivative (CDRI 80/53) against Plasmodium cynomolgi B in monkeys. Am J Trop Med Hyg 1989;41(6): 635-7
84. Lell B, Faucher JF, Missinou MA, et al. Malaria chemoprophylaxis with tafenoquine: a randomised study. Lancet 2000;355(9220): 2041-5
85. Brueckner RP, Coster T, Wesche DL, et al. Prophylaxis of Plasmodium falciparum infection in a human challenge model with WR 238605, a new 8-aminoquinoline antimalarial. Antimicrob Agents Chemother 1998;42(5): 1293-4
86. Crockett M, Kain KC. Tafenoquine: a promising new antimalarial agent. Expert Opin Investig Drugs 2007;16(5): 705-15
87. Nanayakkara NP, Ager AL Jr, Bartlett MS, et al. Antiparasitic activities and toxicities of individual enantiomers of the 8-aminoquinoline 8-[(4-amino-1- methylbutyl)amino]-6-methoxy-4-methyl- 5-[3,4-dichlorophenoxy]quinol ine succinate. Antimicrob Agents Chemother 2008;52(6): 2130-7
88. Hollingdale MR, Collins WE, Campbell CC. In vitro culture of exoerythrocytic parasites of the North Korean strain of Plasmodium vivax in hepatoma cells. Am J Trop Med Hyg 1986;35(2): 275-6
89. Chattopadhyay R, Velmurugan S, Chakiath C, et al. Establishment of an in vitro assay for assessing the effects of drugs on the liver stages of Plasmodium vivax malaria. PLoS One 2010;5(12):e14275
90. Sattabongkot J, Yimamnuaychoke N, Leelaudomlipi S, et al. Establishment of a human hepatocyte line that supports in vitro development of the exo-erythrocytic stages of the malaria parasites Plasmodium falciparum and P. vivax. Am J Trop Med Hyg 2006;74(5): 708-15
91. Mazier D, Landau I, Druilhe P, et al. Cultivation of the liver forms of Plasmodium vivax in human hepatocytes. Nature 1984;307(5949): 367-9
92. Dembele L, Gego A, Zeeman AM, et al. Towards an in vitro model of Plasmodium hypnozoites suitable for drug discovery. PLoS One 2011;6(3):e18162
93. Voorberg-van der Wel A, Zeeman AM, van Amsterdam SM, et al. Transgenic fluorescent Plasmodium cynomolgi liver stages enable live imaging and purification of Malaria hypnozoite-forms. PLoS One 2013;8(1):e54888
94. Rodrigues T, Prudencio M, Moreira R, et al. Targeting the liver stage of malaria parasites: a yet unmet goal. J Med Chem 2012;55(3): 995-1012
95. Wells TN, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol 2010;26(3): 145-51
96. Noulin F, Borlon C, Van Den Abbeele J, et al. 1912-2012: a century of research on Plasmodium vivax in vitro culture. Trends Parasitol 2013;
97. Panichakul T, Sattabongkot J, Chotivanich K, et al. Production of erythropoietic cells in vitro for continuous culture of Plasmodium vivax. Int J Parasitol 2007;37(14): 1551-7
98. Noulin F, Borlon C, van den Eede P, et al. Cryopreserved reticulocytes derived from hematopoietic stem cells can be invaded by cryopreserved Plasmodium vivax isolates. PLoS One 2012;7(7):e40798
99. Lee KS, Divis PC, Zakaria SK, et al. Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathog 2011;7(4):e1002015
100. Singh B, Daneshvar C. Human infections and detection of plasmodium knowlesi. Clin Microbiol Rev 2013;26(2): 165-84
101. Moon RW, Hall J, Rangkuti F, et al. Adaptation of the genetically tractable malaria pathogen Plasmodium knowlesi to continuous culture in human erythrocytes. Proc Natl Acad Sci USA 2013;110(2): 531-6
102. Achan J, Talisuna AO, Erhart A, et al. Quinine, an old anti-malarial drug in a modern world: role in the treatment of malaria. Malar J 2011;10: 144
103. Baird JK, Surjadjaja C. Consideration of ethics in primaquine therapy against malaria transmission. Trends Parasitol 2011;27(1): 11-16
104. Kreidenweiss A, Kremsner PG, Mordmuller B. Comprehensive study of proteasome inhibitors against Plasmodium falciparum laboratory strains and field isolates from Gabon. Malar J 2008;7: 187
105. Tschan S, Kreidenweiss A, Stierhof YD, et al. Mitochondrial localization of the threonine peptidase PfHslV, a ClpQ ortholog in Plasmodium falciparum. Int J Parasitol 2010;40(13): 1517-23
106. Tschan S, Mordmuller B, Kun JF. Threonine peptidases as drug targets against malaria. Expert Opin Ther Targets 2011;15(4): 365-78
107. Davis ME, Chen ZG, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 2008;7(9): 771-82
108. Bao G, Mitragotri S, Tong S. Multifunctional Nanoparticles for Drug Delivery and Molecular Imaging. Annu Rev Biomed Eng 2013;
109. Kim BY, Rutka JT, Chan WC. Nanomedicine. N Engl J Med 2010;363(25): 2434-43
110. Tyagi RK, Garg NK, Sahu T. Vaccination Strategies against Malaria: novel carrier(s) more than a tour de force. J Control Release 2012;162(1): 242-54
111. Santos-Magalhaes NS, Mosqueira VC. Nanotechnology applied to the treatment of malaria. Adv Drug Deliv Rev 2010;62(4-5): 560-75
112. Murambiwa P, Masola B, Govender T, et al. Anti-malarial drug formulations and novel delivery systems: a review. Acta Trop 2011;118(2): 71-9
113. Green MD, D'Souza MJ, Holbrook JM, Wirtz RA. In vitro and in vivo evaluation of albumin-encapsulated primaquine diphosphate prepared by nebulization into heated oil. J Microencapsul 2004;21(4): 433-44
114. Singh KK, Vingkar SK. Formulation, antimalarial activity and biodistribution of oral lipid nanoemulsion of primaquine. Int J Pharm 2008;347(1-2): 136-43
115. Urban P, Estelrich J, Cortes A, Fernandez-Busquets X. A nanovector with complete discrimination for targeted delivery to Plasmodium falciparuminfected versus non-infected red blood cells in vitro. J Control Release 2011;151(2): 202-11. First report showing that nanoparticles can discriminate between infected and uninfected erythrocytes.
116. Fidock DA, Rosenthal PJ, Croft SL, et al. Antimalarial drug discovery: efficacy models for compound screening. Nat Rev Drug Discov 2004;3(6): 509-20
117. Jimenez-Diaz MB, Mulet T, Viera S, et al. Improved murine model of malaria using Plasmodium falciparum competent strains and non-myelodepleted NODscid IL2Rgammanull mice engrafted with human erythrocytes. Antimicrob Agents Chemother 2009;53(10): 4533-6
118. Moreno A, Badell E, Van Rooijen N, Druilhe P. Human malaria in immunocompromised mice: new in vivo model for chemotherapy studies. Antimicrob Agents Chemother 2001;45(6): 1847-53
119. Collins WE, Sullivan JS,Williams A, et al. The Santa Lucia strain of Plasmodium falciparum in Aotus monkeys. Am J Trop Med Hyg 2009;80(4): 536-40
120. Herrera S, Perlaza BL, Bonelo A, Arevalo-Herrera M. Aotus monkeys: their great value for anti-malaria vaccines and drug testing. Int J Parasitol 2002;32(13): 1625-35
121. Deye GA, Gettayacamin M, Hansukjariya P, et al. Use of a rhesus Plasmodium cynomolgi model to screen for anti-hypnozoite activity of pharmaceutical substances. Am J Trop Med Hyg 2012;86(6): 931-5
122. Dow GS, Gettayacamin M, Hansukjariya P, et al. Radical curative efficacy of tafenoquine combination regimens in Plasmodium cynomolgi-infected Rhesus monkeys (Macaca mulatta). Malar J 2011;10: 212
123. Langhorne J, Buffet P, Galinski M, et al. The relevance of non-human primate and rodent malaria models for humans. Malar J 2011;10(1): 23
124. Teixeira C, Gomes R. Experimental models in vaccine research: malaria and leishmaniasis. Braz J Med Biol Res 2013;46(2): 109-16
125. Jefferson T. Microbial challenge studies - a challenge worth accepting. Lancet 2005;366(9485): 531-3
126. Sauerwein RW, Roestenberg M, Moorthy VS. Experimental human challenge infections can accelerate clinical malaria vaccine development. Nat Rev Immunol 2011;11(1): 57-64 .. Review on utility of CHMI studies for antimalarial interventions.
127. Shapiro TA, Ranasinha CD, Kumar N, Barditch-Crovo P. Prophylactic activity of atovaquone against Plasmodium falciparum in humans. Am J Trop Med Hyg 1999;60(5): 831-6
128. Hoffman SL, Billingsley PF, James E, et al. Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum Vaccin 2010;6(1): 97-106
129. Epstein JE, Tewari K, Lyke KE, et al. Live attenuated malaria vaccine designed to protect through hepatic CD8(+) T cell immunity. Science 2011;334(6055): 475-80
130. Roestenberg M, Bijker EM, Sim BK, et al. Controlled human malaria infections by intradermal injection of cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg 2013;88(1): 5-13 .. First study showing that injection of cryopreserved sporozoites leads to a malaria infection.
131. McCarthy JS, Sekuloski S, Griffin PM, et al. A pilot randomised trial of induced blood-stage Plasmodium falciparum infections in healthy volunteers for testing efficacy of new antimalarial drugs. PLoS One 2011;6(8):e21914
132. Engwerda CR, Minigo G, Amante FH, McCarthy JS. Experimentally induced blood stage malaria infection as a tool for clinical research. Trends Parasitol 2012;28(11): 515-21
133. Duncan CJ, Draper SJ. Controlled human blood stage malaria infection: current status and potential applications. Am J Trop Med Hyg 2012;86(4): 561-5. Review on CHMI performed by blood stage parasites.
134. Pombo DJ, Lawrence G, Hirunpetcharat C, et al. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet 2002;360(9333): 610-17
135. Cheng Q, Lawrence G, Reed C, et al. Measurement of Plasmodium falciparum growth rates in vivo: a test of malaria vaccines. Am J Trop Med Hyg 1997;57(4): 495-500. First study evaluating in depth in vivo parasite growth after infection.
136. Hermsen CC, Telgt DS, Linders EH, et al. Detection of Plasmodium falciparum malaria parasites in vivo by real-time quantitative PCR. Mol Biochem Parasitol 2001;118(2): 247-51
137. Herrera S, Solarte Y, Jordan-Villegas A, et al. Consistent safety and infectivity in sporozoite challenge model of Plasmodium vivax in malaria-naive human volunteers. Am J Trop Med Hyg 2011;84(2 Suppl): 4-11
138. Herrera S, Fernandez O, Manzano MR, et al. Successful sporozoite challenge model in human volunteers with Plasmodium vivax strain derived from human donors. Am J Trop Med Hyg 2009;81(5): 740-6