Plasmodium falciparum transfected with ultra bright nanoluc luciferase offers high sensitivity detection for the screening of growth and cellular trafficking inhibitors

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Azevedo, Mauro F ^a   Nie, Catherine Q ^a   Elsworth, Brendan ^a,b   Charnaud, Sarah C ^a,b   Sanders, Paul R ^a   Crabb, Brendan S ^a,b,c   Gilson, Paul R ^a,b  

^a BURNET INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BREFELDIN A; FUROSEMIDE; LUCIFERASE; NANOLUC LUCIFERASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; LOOP DIURETIC AGENT; PROTEIN SYNTHESIS INHIBITOR; PROTOZOAL PROTEIN;

ARTICLE; BIOLUMINESCENCE; CELL FRACTIONATION; CELL TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; ERYTHROCYTE; GENETIC TRANSFECTION; MICROBIAL GROWTH; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SENSITIVITY ANALYSIS; ANIMAL; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; FIREFLY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SCREENING; HUMAN; METABOLISM; PARASITOLOGY; PENAEIDAE; PROTEIN ENGINEERING; REPORTER GENE; SENSITIVITY AND SPECIFICITY; TRANSPORT AT THE CELLULAR LEVEL; TROPHOZOITE;

PLASMODIUM FALCIPARUM;

ANIMALS; BIOLOGICAL TRANSPORT; BREFELDIN A; CARRIER PROTEINS; ERYTHROCYTES; FIREFLIES; FUROSEMIDE; GENES, REPORTER; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LUCIFERASES; PENAEIDAE; PLASMODIUM FALCIPARUM; PROTEIN ENGINEERING; PROTEIN SYNTHESIS INHIBITORS; PROTOZOAN PROTEINS; SENSITIVITY AND SPECIFICITY; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; TROPHOZOITES;

EID: 84911937900     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112571     Document Type: Article

References (56)

1. WHO (2013) World malaria report 2013.
2. Gamo FJ, Sanz LM, Vidal J, de Cozar C, Alvarez E, et al. (2010) Thousands of chemical starting points for antimalarial lead identification. Nature 465: 305-310.
3. Guiguemde WA, Shelat AA, Bouck D, Duffy S, Crowther GJ, et al. (2010) Chemical genetics of Plasmodium falciparum. Nature 465: 311-315.
4. Lucumi E, Darling C, Jo H, Napper AD, Chandramohanadas R, et al. (2010) Discovery of potent small-molecule inhibitors of multidrug-resistant Plasmodium falciparum using a novel miniaturized high-throughput luciferase-based assay. Antimicrob Agents Chemother 54: 3597-3604.
5. Spangenberg T, Burrows JN, Kowalczyk P, McDonald S, Wells TN, et al. (2013) The open access malaria box: A drug discovery catalyst for neglected diseases. PLoS One 8: E62906.
6. Boddey JA, Hodder AN, Gunther S, Gilson PR, Patsiouras H, et al. (2010) An aspartyl protease directs malaria effector proteins to the host cell. Nature 463: 627-631.
7. Marti M, Spielmann T (2013) Protein export in malaria parasites: Many membranes to cross. Curr Opin Microbiol 16: 445-451.
8. Pasini EM, Braks JA, Fonager J, Klop O, Aime E, et al. (2013) Proteomic and genetic analyses demonstrate that Plasmodium berghei blood stages export a large and diverse repertoire of proteins. Mol Cell Proteomics 12: 426-448.
9. Maier AG, Cooke BM, Cowman AF, Tilley L (2009) Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol 7: 341-354.
10. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, et al. (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparuminfected human erythrocytes. Cell 134: 48-61.
11. Nguitragool W, Bokhari AA, Pillai AD, Rayavara K, Sharma P, et al. (2011) Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell 145: 665-677.
12. de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ, et al. (2009) A newly discovered protein export machine in malaria parasites. Nature 459: 945-949.
13. Beck JR, Muralidharan V, Oksman A, Goldberg DE (2014) PTEX component HSP101 mediates export of diverse malaria effectors into host erythrocytes. Nature 511: 592-595.
14. Elsworth B, Matthews K, Nie CQ, Kalanon M, Charnaud SC, et al. (2014) PTEX is an essential nexus for protein export in malaria parasites. Nature 511: 587-591.
15. Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, et al. (2011) Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc Natl Acad Sci U S A 108: E1214-1223.
16. Lucantoni L, Duffy S, Adjalley SH, Fidock DA, Avery VM (2013) Identification of MMV malaria box inhibitors of plasmodium falciparum early-stage gametocytes using a luciferase-based high-throughput assay. Antimicrob Agents Chemother 57: 6050-6062.
17. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306: 1930-1933.
18. Goonewardene R, Daily J, Kaslow D, Sullivan TJ, Duffy P, et al. (1993) Transfection of the malaria parasite and expression of firefly luciferase. Proc Natl Acad Sci U S A 90: 5234-5236.
19. Militello KT, Wirth DF (2003) A new reporter gene for transient transfection of Plasmodium falciparum. Parasitol Res 89: 154-157.
20. Azevedo MF, del Portillo HA (2007) Promoter regions of Plasmodium vivax are poorly or not recognized by Plasmodium falciparum. Malar J 6: 20.
21. Frank M, Dzikowski R, Costantini D, Amulic B, Berdougo E, et al. (2006) Strict pairing of var promoters and introns is required for var gene silencing in the malaria parasite Plasmodium falciparum. J Biol Chem 281: 9942-9952.
22. Horrocks P, Lanzer M (1999) Mutational analysis identifies a five base pair cisacting sequence essential for GBP130 promoter activity in Plasmodium falciparum. Mol Biochem Parasitol 99: 77-87.
23. Che P, Cui L, Kutsch O, Cui L, Li Q (2012) Validating a firefly luciferase-based high-throughput screening assay for antimalarial drug discovery. Assay Drug Dev Technol 10: 61-68.
24. Cui L, Miao J, Wang J, Li Q, Cui L (2008) Plasmodium falciparum: Development of a transgenic line for screening antimalarials using firefly luciferase as the reporter. Exp Parasitol 120: 80-87.
25. Ekland EH, Schneider J, Fidock DA (2011) Identifying apicoplast-targeting antimalarials using high-throughput compatible approaches. FASEB J 25: 3583-3593.
26. Hasenkamp S, Sidaway A, Devine O, Roye R, Horrocks P (2013) Evaluation of bioluminescence-based assays of anti-malarial drug activity. Malar J 12: 58.
27. Khan T, van Brummelen AC, Parkinson CJ, Hoppe HC (2012) ATP and luciferase assays to determine the rate of drug action in in vitro cultures of Plasmodium falciparum. Malar J 11: 369.
28. Burghaus PA, Lingelbach K (2001) Luciferase, when fused to an N-terminal signal peptide, is secreted from transfected Plasmodium falciparum and transported to the cytosol of infected erythrocytes. J Biol Chem 276: 26838-26845.
29. Hall MP, Unch J, Binkowski BF, Valley MP, Butler BL, et al. (2012) Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate. ACS Chem Biol 7: 1848-1857.
30. de Azevedo MF, Gilson PR, Gabriel HB, Simoes RF, Angrisano F, et al. (2012) Systematic analysis of FKBP inducible degradation domain tagging strategies for the human malaria parasite Plasmodium falciparum. PLoS One 7: E40981.
31. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
32. Deitsch K, Driskill C, Wellems T (2001) Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res 29: 850-853.
33. Hasenkamp S, Russell KT, Horrocks P (2012) Comparison of the absolute and relative efficiencies of electroporation-based transfection protocols for Plasmodium falciparum. Malar J 11: 210.
34. Makler MT, Hinrichs DJ (1993) Measurement of the lactate dehydrogenase activity of Plasmodium falciparum as an assessment of parasitemia. Am J Trop Med Hyg 48: 205-210.
35. Zhang JH, Chung TD, Oldenburg KR (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4: 67-73.
36. Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, et al. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137: 13-21.
37. Bullen HE, Charnaud SC, Kalanon M, Riglar DT, Dekiwadia C, et al. (2012) Biosynthesis, localization, and macromolecular arrangement of the Plasmodium falciparum translocon of exported proteins (PTEX). J Biol Chem 287: 7871-7884.
38. Jackson KE, Spielmann T, Hanssen E, Adisa A, Separovic F, et al. (2007) Selective permeabilization of the host cell membrane of Plasmodium falciparuminfected red blood cells with streptolysin O and equinatoxin II. Biochem J 403: 167-175.
39. Boddey JA, Carvalho TG, Hodder AN, Sargeant TJ, Sleebs BE, et al. (2013) Role of plasmepsin V in export of diverse protein families from the Plasmodium falciparum exportome. Traffic 14: 532-550.
40. Heiber A, Kruse F, Pick C, Gruring C, Flemming S, et al. (2013) Identification of new PNEPs indicates a substantial non-PEXEL exportome and underpins common features in Plasmodium falciparum protein export. PLoS Pathog 9: E1003546.
41. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, et al. (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306: 1934-1937.
42. Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K, et al. (2006) Lineagespecific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 7: R12.
43. van Ooij C, Tamez P, Bhattacharjee S, Hiller NL, Harrison T, et al. (2008) The malaria secretome: From algorithms to essential function in blood stage infection. PLoS Pathog 4: E1000084.
44. Elsworth B, Crabb BS, Gilson PR (2014) Protein export in malaria parasites: An update. Cell Microbiol 16: 355-363.
45. Boddey JA, Moritz RL, Simpson RJ, Cowman AF (2009) Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10: 285-299.
46. Knuepfer E, Rug M, Klonis N, Tilley L, Cowman AF (2005) Trafficking of the major virulence factor to the surface of transfected P. falciparum-infected erythrocytes. Blood 105: 4078-4087.
47. Wickham ME, Rug M, Ralph SA, Klonis N, McFadden GI, et al. (2001) Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J 20: 5636-5649.
48. Gilson PR, O'Donnell RA, Nebl T, Sanders PR, Wickham ME, et al. (2008) MSP1(19) miniproteins can serve as targets for invasion inhibitory antibodies in Plasmodium falciparum provided they contain the correct domains for cell surface trafficking. Mol Microbiol 68: 124-138.
49. Bouyer G, Cueff A, Egee S, Kmiecik J, Maksimova Y, et al. (2011) Erythrocyte peripheral type benzodiazepine receptor/voltage-dependent anion channels are upregulated by Plasmodium falciparum. Blood 118: 2305-2312.
50. Duranton C, Huber SM, Tanneur V, Brand VB, Akkaya C, et al. (2004) Organic osmolyte permeabilities of the malaria-induced anion conductances in human erythrocytes. J Gen Physiol 123: 417-426.
51. Huber SM, Uhlemann AC, Gamper NL, Duranton C, Kremsner PG, et al. (2002) Plasmodium falciparum activates endogenous Cl(2) channels of human erythrocytes by membrane oxidation. EMBO J 21: 22-30.
52. Crabb BS, Cowman AF (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.
53. Fernandez-Becerra C, de Azevedo MF, Yamamoto MM, del Portillo HA (2003) Plasmodium falciparum: New vector with bi-directional promoter activity to stably express transgenes. Exp Parasitol 103: 88-91.
54. Ansorge I, Benting J, Bhakdi S, Lingelbach K (1996) Protein sorting in Plasmodium falciparum-infected red blood cells permeabilized with the poreforming protein streptolysin O. Biochem J 315 (Pt 1): 307-314.
55. Chang HH, Falick AM, Carlton PM, Sedat JW, DeRisi JL, et al. (2008) Nterminal processing of proteins exported by malaria parasites. Mol Biochem Parasitol 160: 107-115.
56. Collins CR, Hackett F, Strath M, Penzo M, Withers-Martinez C, et al. (2013) Malaria parasite cGMP-dependent protein kinase regulates blood stage merozoite secretory organelle discharge and egress. PLoS Pathog 9: E1003344.