The Next Opportunity in Anti-Malaria Drug Discovery: The Liver Stage

1. CarterRMendisKN 2002 Evolutionary and historical aspects of the burden of malaria. Clin Microbiol Rev 15 564 594

2. SachsJMalaneyP 2002 The economic and social burden of malaria. Nature 415 680 685

3. SnowRWGuerraCANoorAMMyintHYHaySI 2005 The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434 214 217

4. Wolrd Health Organization. 2010 World Malaria Report 2010

5. PrudencioMRodriguezAMotaMM 2006 The silent path to thousands of merozoites: the Plasmodium liver stage. Nat Rev Microbiol 4 849 856

6. MendisKSinaBJMarchesiniPCarterR 2001 The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 64 97 106

7. BassatQAlonsoPL 2011 Defying malaria: fathoming severe Plasmodium vivax disease. Nat Med 17 48 49

8. PriceRNTjitraEGuerraCAYeungSWhiteNJ 2007 Vivax malaria: neglected and not benign. Am J Trop Med Hyg 77 79 87

9. WellsTNBurrowsJNBairdJK 2010 Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol 26 145 151

10. BairdJK 2005 Effectiveness of antimalarial drugs. N Engl J Med 352 1565 1577

11. DondorpAMYeungSWhiteLNguonCDayNP 2010 Artemisinin resistance: current status and scenarios for containment. Nat Rev Microbiol 8 272 280

12. MazierDReniaLSnounouG 2009 A pre-emptive strike against malaria's stealthy hepatic forms. Nat Rev Drug Discov 8 854 864

13. WhiteNJ 2004 Antimalarial drug resistance. J Clin Invest 113 1084 1092

14. GardnerMJHallNFungEWhiteOBerrimanM 2002 Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 498 511

15. PatelVMazitschekRColemanBNguyenCUrgaonkarS 2009 Identification and characterization of small molecule inhibitors of a class I histone deacetylase from Plasmodium falciparum. J Med Chem 52 2185 2187

16. SriwilaijaroenNBoonmaSAttasartPPothikasikornJPanyimS 2009 Inhibition of Plasmodium falciparum proliferation in vitro by double-stranded RNA directed against malaria histone deacetylase. Biochem Biophys Res Commun 381 144 147

17. BaldwinJMichnoffCHMalmquistNAWhiteJRothMG 2005 High-throughput screening for potent and selective inhibitors of Plasmodium falciparum dihydroorotate dehydrogenase. J Biol Chem 280 21847 21853

18. BookerMLBastosCMKramerMLBarkerRHJrSkerljR 2010 Novel inhibitors of plasmodium falciparum dihydroorotate dehydrogenase with anti-malarial activity in the mouse model. J Biol Chem 285 33054 33064

19. BrobeyRKSanoGItohFAsoKKimuraM 1996 Recombinant Plasmodium falciparum dihydrofolate reductase-based in vitro screen for antifolate antimalarials. Mol Biochem Parasitol 81 225 237

20. LeePJBhonsleJBGaonaHWHuddlerDPHeadyTN 2009 Targeting the fatty acid biosynthesis enzyme, beta-ketoacyl-acyl carrier protein synthase III (PfKASIII), in the identification of novel antimalarial agents. J Med Chem 52 952 963

21. SharmaSSharmaSKModakRKarmodiyaKSuroliaN 2007 Mass spectrometry-based systems approach for identification of inhibitors of Plasmodium falciparum fatty acid synthase. Antimicrob Agents Chemother 51 2552 2558

22. BanieckiMLWirthDFClardyJ 2007 High-throughput Plasmodium falciparum growth assay for malaria drug discovery. Antimicrob Agents Chemother 51 716 723

23. GamoFJSanzLMVidalJde CozarCAlvarezE 2010 Thousands of chemical starting points for antimalarial lead identification. Nature 465 305 310

24. GoonewardeneRDailyJKaslowDSullivanTJDuffyP 1993 Transfection of the malaria parasite and expression of firefly luciferase. Proc Natl Acad Sci U S A 90 5234 5236

25. CervantesSPrudhommeJCarterDGopiKGLiQ 2009 High-content live cell imaging with RNA probes: advancements in high-throughput antimalarial drug discovery. BMC Cell Biol 10 45

26. EckerAMoonRSindenREBillkerO 2006 Generation of gene targeting constructs for Plasmodium berghei by a PCR-based method amenable to high throughput applications. Mol Biochem Parasitol 145 265 268

27. GuiguemdeWAShelatAABouckDDuffySCrowtherGJ 2010 Chemical genetics of Plasmodium falciparum. Nature 465 311 315

28. RottmannMMcNamaraCYeungBKLeeMCZouB 2010 Spiroindolones, a potent compound class for the treatment of malaria. Science 329 1175 1180

29. BascoLKBickiiJRingwaldP 1999 In-vitro activity of primaquine against the asexual blood stages of Plasmodium falciparum. Ann Trop Med Parasitol 93 179 182

30. BrayPGDeedSFoxEKalkanidisMMungthinM 2005 Primaquine synergises the activity of chloroquine against chloroquine-resistant P. falciparum. Biochem Pharmacol 70 1158 1166

31. BairdJKHoffmanSL 2004 Primaquine therapy for malaria. Clin Infect Dis 39 1336 1345

32. CappelliniMDFiorelliG 2008 Glucose-6-phosphate dehydrogenase deficiency. Lancet 371 64 74

33. Le RochKGZhouYBlairPLGraingerMMochJK 2003 Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301 1503 1508

34. WestenbergerSJMcCleanCMChattopadhyayRDhariaNVCarltonJM 2010 A systems-based analysis of Plasmodium vivax lifecycle transcription from human to mosquito. PLoS Negl Trop Dis 4 e653 doi:10.1371/journal.pntd.0000653

35. WilliamsCTAzadAF 2010 Transcriptional analysis of the pre-erythrocytic stages of the rodent malaria parasite, Plasmodium yoelii. PLoS ONE 5 e10267 doi:10.1371/journal.pone.0010267

36. KappeSHDuffyPE 2006 Malaria liver stage culture: in vitro veritas? Am J Trop Med Hyg 74 706 707

37. Calvo-CalleJMMorenoAElingWMNardinEH 1994 In vitro development of infectious liver stages of P. yoelii and P. berghei malaria in human cell lines. Exp Parasitol 79 362 373

38. HollingdaleMRLeefJLMcCulloughMBeaudoinRL 1981 In vitro cultivation of the exoerythrocytic stage of Plasmodium berghei from sporozoites. Science 213 1021 1022

39. MazierDBeaudoinRLMelloukSDruilhePTexierB 1985 Complete development of hepatic stages of Plasmodium falciparum in vitro. Science 227 440 442

40. Bruna-RomeroOHafallaJCGonzalez-AseguinolazaGSanoGTsujiM 2001 Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR. Int J Parasitol 31 1499 1502

41. WitneyAADoolanDLAnthonyRMWeissWRHoffmanSL 2001 Determining liver stage parasite burden by real time quantitative PCR as a method for evaluating pre-erythrocytic malaria vaccine efficacy. Mol Biochem Parasitol 118 233 245

42. NatarajanRThathyVMotaMMHafallaJCMenardR 2001 Fluorescent Plasmodium berghei sporozoites and pre-erythrocytic stages: a new tool to study mosquito and mammalian host interactions with malaria parasites. Cell Microbiol 3 371 379

43. TarunASBaerKDumpitRFGraySLejarceguiN 2006 Quantitative isolation and in vivo imaging of malaria parasite liver stages. Int J Parasitol 36 1283 1293

44. PrudencioMRodriguesCDAtaideRMotaMM 2008 Dissecting in vitro host cell infection by Plasmodium sporozoites using flow cytometry. Cell Microbiol 10 218 224

45. GegoASilvieOFranetichJFFarhatiKHannounL 2006 New approach for high-throughput screening of drug activity on Plasmodium liver stages. Antimicrob Agents Chemother 50 1586 1589

46. PrudencioMRodriguesCDHannusMMartinCRealE 2008 Kinome-wide RNAi screen implicates at least 5 host hepatocyte kinases in Plasmodium sporozoite infection. PLoS Pathog 4 e1000201 doi:10.1371/journal.ppat.1000201

47. RodriguesCDHannusMPrudencioMMartinCGoncalvesLA 2008 Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host Microbe 4 271 282

48. MwakingweATingLMHochmanSChenJSinnisP 2009 Noninvasive real-time monitoring of liver-stage development of bioluminescent Plasmodium parasites. J Infect Dis 200 1470 1478

49. PloemenIHPrudencioMDouradinhaBGRamesarJFonagerJ 2009 Visualisation and quantitative analysis of the rodent malaria liver stage by real time imaging. PLoS ONE 4 e7881 doi:10.1371/journal.pone.0007881

50. ChattopadhyayRVelmuruganSChakiathCAndrews DonkorLMilhousW 2010 Establishment of an in vitro assay for assessing the effects of drugs on the liver stages of Plasmodium vivax malaria. PLoS ONE 5 e14275 doi:10.1371/journal.pone.0014275

51. DembeleLGegoAZeemanAMFranetichJFSilvieO 2011 Towards an in vitro model of Plasmodium hypnozoites suitable for drug discovery. PLoS ONE 6 e18162 doi:10.1371/journal.pone.0018162

52. TarunASPengXDumpitRFOgataYSilva-RiveraH 2008 A combined transcriptome and proteome survey of malaria parasite liver stages. Proc Natl Acad Sci U S A 105 305 310

53. HallNKarrasMRaineJDCarltonJMKooijTW 2005 A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307 82 86