From the genome to the phenome: Tools to understand the basic biology of plasmodium falciparum

Journal of Eukaryotic Microbiology

Volumn 61, Issue 6, 2014, Pages 655-671

  Webster, Wesley A J ^a,b   McFadden, Geoffrey I ^b  

^a DEAKIN UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Apicoplast; Drug target; Genetic manipulation; Knockout; Malaria. metabolism; Phenotype

Indexed keywords

BIOLOGY; DRUG DEVELOPMENT; GENE EXPRESSION; GENETIC ENGINEERING; GENOME; LIFE CYCLE; MALARIA; METABOLISM; MUTATION; PHENOTYPE; PROTOZOAN;

PLASMODIUM FALCIPARUM;

ANIMAL; ERYTHROCYTE; GENE; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; METABOLISM; MUTATION; PARASITOLOGY; PATHOGENICITY; PHENOTYPE; PLASMODIUM FALCIPARUM;

ANIMALS; ERYTHROCYTES; GENES, PROTOZOAN; GENOME, PROTOZOAN; LIFE CYCLE STAGES; MUTATION; PHENOTYPE; PLASMODIUM FALCIPARUM;

EID: 84923583445     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/jeu.12176     Document Type: Article

References (138)

1. Agop-Nersesian, C., Pfahler, J., Lanzer, M. & Meissner, M. 2008. Functional expression of ribozymes in Apicomplexa: towards exogenous control of gene expression by inducible RNA-cleavage. Int. J. Parasitol., 38:673-681.
2. Ahmed, A. & Sharma, Y. D. 2008. Ribozyme cleavage of Plasmodium falciparum gyrase A gene transcript affects the parasite growth. Parasitol. Res., 103:751-763.
3. Allary, M., Lu, J. Z., Zhu, L. & Prigge, S. T. 2007. Scavenging of the cofactor lipoate is essential for the survival of the malaria parasite Plasmodium falciparum. Mol. Microbiol., 63:1331-1344.
4. Andenmatten, N., Egarter, S., Jackson, A. J., Jullien, N., Herman, J. P. & Meissner, M. 2013. Conditional genome engineering in Toxoplasma gondii uncovers alternative invasion mechanisms. Nat. Methods, 10:125-127.
5. Ariey, F., Witkowski, B., Amaratunga, C., Beghain, J., Langlois, A. C., Khim, N., Kim, S., Duru, V., Bouchier, C., Ma, L., Lim, P., Leang, R., Duong, S., Sreng, S., Suon, S., Chuor, C. M., Bout, D. M., Menard, S., Rogers, W. O., Genton, B., Fandeur, T., Miotto, O., Ringwald, P., Le Bras, J., Berry, A., Barale, J. C., Fairhurst, R. M., Benoit-Vical, F., Mercereau-Puijalon, O. & Menard, D. 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature, 505:50-55.
6. Armstrong, C. M. & Goldberg, D. E. 2007. An FKBP destabilization domain modulates protein levels in Plasmodium falciparum. Nat. Methods, 4:1007-1009.
7. Balabaskaran Nina, P., Morrisey, J. M., Ganesan, S. M., Ke, H., Pershing, A. M., Mather, M. W. & Vaidya, A. B. 2011. ATP synthase complex of Plasmodium falciparum: dimeric assembly in mitochondrial membranes and resistance to genetic disruption. J. Biol. Chem., 286:41312-41322.
8. Balu, B., Singh, N., Maher, S. P. & Adams, J. H. 2010. A genetic screen for attenuated growth identifies genes crucial for intraerythrocytic development of Plasmodium falciparum. PLoS ONE, 5:e13282.
9. Balu, B., Shoue, D. A., Fraser, M. J. Jr & Adams, J. H. 2005. High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proc. Natl Acad. Sci. USA, 102:16391-16396.
10. Balu, B., Chauhan, C., Maher, S. P., Shoue, D. A., Kissinger, J. C., Fraser, M. J. Jr & Adams, J. H. 2009. piggyBac is an effective tool for functional analysis of the Plasmodium falciparum genome. BMC Microbiol., 9:83.
11. Balu, B., Maher, S. P., Pance, A., Chauhan, C., Naumov, A. V., Andrews, R. M., Ellis, P. D., Khan, S. M., Lin, J. W., Janse, C. J., Rayner, J. C. & Adams, J. H. 2011. CCR4-associated factor 1 coordinates the expression of Plasmodium falciparum egress and invasion proteins. Eukaryot. Cell, 10:1257-1263.
12. Banaszynski, L. A., Chen, L. C., Maynard-Smith, L. A., Ooi, A. G. & Wandless, T. J. 2006. A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell, 126:995-1004.
13. Barfod, A., Persson, T. & Lindh, J. 2009. In vitro selection of RNA aptamers against a conserved region of the Plasmodium falciparum erythrocyte membrane protein 1. Parasitol. Res., 105:1557-1566.
14. Baum, J., Papenfuss, A. T., Mair, G. R., Janse, C. J., Vlachou, D., Waters, A. P., Cowman, A. F., Crabb, B. S. & de Koning-Ward, T. F. 2009. Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res., 37:3788-3798.
15. Beck, J. R., Muralidharan, V., Oksman, A. & Goldberg, D. E. 2014. PTEX component HSP101 mediates export of diverse malaria effectors into host erythrocytes. Nature, 511:592-595.
16. Belmont, B. J. & Niles, J. C. 2010. Engineering a direct and inducible protein-RNA interaction to regulate RNA biology. ACS Chem. Biol., 5:851-861.
17. Berois, M., Romero-Severson, J. & Severson, D. W. 2012. RNAi knock-downs support roles for the mucin-like (AeIMUC1) gene and short-chain dehydrogenase/reductase (SDR) gene in Aedes aegypti susceptibility to Plasmodium gallinaceum. Med. Vet. Entomol., 26:112-115.
18. Bethke, L., Thomas, S., Walker, K., Lakhia, R., Rangarajan, R. & Wirth, D. 2007. The role of DNA mismatch repair in generating genetic diversity and drug resistance in malaria parasites. Mol. Biochem. Parasitol., 155:18-25.
19. Bozdech, Z., Llinas, M., Pulliam, B. L., Wong, E. D., Zhu, J. & De-Risi, J. L. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol., 1: E5.
20. Brecht, S., Erdhart, H., Soete, M. & Soldati, D. 1999. Genome engineering of Toxoplasma gondii using the site-specific recombinase Cre. Gene, 234:239-247.
21. Buchholz, F., Angrand, P. O. & Stewart, A. F. 1998. Improved properties of FLP recombinase evolved by cycling mutagenesis. Nat. Biotechnol., 16:657-662.
22. Buchholz, F., Ringrose, L., Angrand, P. O., Rossi, F. & Stewart, A. F. 1996. Different thermostabilities of FLP and Cre recombinases: implications for applied site-specific recombination. Nucleic Acids Res., 24:4256-4262.
23. Bullen, H. E., Charnaud, S. C., Kalanon, M., Riglar, D. T., Dekiwadia, C., Kangwanrangsan, N., Torii, M., Tsuboi, T., Baum, J., Ralph, S. A., Cowman, A. F., de Koning-Ward, T. F., Crabb, B. S. & Gilson, P. R. 2012. Biosynthesis, localization, and macromolecular arrangement of the Plasmodium falciparum translocon of exported proteins (PTEX). J. Biol. Chem., 287:7871-7884.
24. Caro, F., Miller, M. G. & DeRisi, J. L. 2012. Plate-based transfection and culturing technique for genetic manipulation of Plasmodium falciparum. Malar. J., 11:22.
25. Carvalho, T. G., Thiberge, S., Sakamoto, H. & Menard, R. 2004. Conditional mutagenesis using site-specific recombination in Plasmodium berghei. Proc. Natl Acad. Sci. USA, 101:14931-14936.
26. Castellini, M. A., Buguliskis, J. S., Casta, L. J., Butz, C. E., Clark, A. B., Kunkel, T. A. & Taraschi, T. F. 2011. Malaria drug resistance is associated with defective DNA mismatch repair. Mol. Biochem. Parasitol., 177:143-147.
27. Chu, B. W., Banaszynski, L. A., Chen, L. C. & Wandless, T. J. 2008. Recent progress with FKBP-derived destabilizing domains. Bioorg. Med. Chem. Lett., 18:5941-5944.
28. Chulay, J. D., Haynes, J. D. & Diggs, C. L. 1983. Plasmodium falciparum: assessment of in vitro growth by [3H]hypoxanthine incorporation. Exp. Parasitol., 55:138-146.
29. Clark, D. L., Chrisey, L. A., Campbell, J. R. & Davidson, E. A. 1994. Non-sequence-specific antimalarial activity of oligodeoxynucleotides. Mol. Biochem. Parasitol., 63:129-134.
30. Collart, M. A. 2003. Global control of gene expression in yeast by the Ccr4-Not complex. Gene, 313:1-16.
31. Collins, C. R., Das, S., Wong, E. H., Andenmatten, N., Stallmach, R., Hackett, F., Herman, J. P., Muller, S., Meissner, M. & Blackman, M. J. 2013. Robust inducible Cre recombinase activity in the human malaria parasite Plasmodium falciparum enables efficient gene deletion within a single asexual erythrocytic growth cycle. Mol. Microbiol., 88:687-701.
32. Combe, A., Giovannini, D., Carvalho, T. G., Spath, S., Boisson, B., Loussert, C., Thiberge, S., Lacroix, C., Gueirard, P. & Menard, R. 2009. Clonal conditional mutagenesis in malaria parasites. Cell Host Microbe, 5:386-396.
33. Cooper, R. A., Ferdig, M. T., Su, X. Z., Ursos, L. M., Mu, J., Nomura, T., Fujioka, H., Fidock, D. A., Roepe, P. D. & Wellems, T. E. 2002. Alternative mutations at position 76 of the vacuolar transmembrane protein PfCRT are associated with chloroquine resistance and unique stereospecific quinine and quinidine responses in Plasmodium falciparum. Mol. Pharmacol., 61:35-42.
34. Crabb, B. S., Triglia, T., Waterkeyn, J. G. & Cowman, A. F. 1997. Stable transgene expression in Plasmodium falciparum. Mol. Biochem. Parasitol., 90:131-144.
35. Crane, C. M., Kaiser, J., Ramsden, N. L., Lauw, S., Rohdich, F., Eisenreich, W., Hunter, W. N., Bacher, A. & Diederich, F. 2006. Fluorescent inhibitors for IspF, an enzyme in the non-mevalonate pathway for isoprenoid biosynthesis and a potential target for antimalarial therapy. Angew. Chem. Int. Ed. Engl., 45:1069-1074.
36. Date, S. V. & Stoeckert, C. J. Jr 2006. Computational modeling of the Plasmodium falciparum interactome reveals protein function on a genome-wide scale. Genome Res., 16:542-549.
37. de Azevedo, M. F., Gilson, P. R., Gabriel, H. B., Simoes, R. F., Angrisano, F., Baum, J., Crabb, B. S. & Wunderlich, G. 2012. Systematic analysis of FKBP inducible degradation domain tagging strategies for the human malaria parasite Plasmodium falciparum. PLoS ONE, 7:e40981.
38. de Koning-Ward, T. F., Waters, A. P. & Crabb, B. S. 2001. Puromycin-N-acetyltransferase as a selectable marker for use in Plasmodium falciparum. Mol. Biochem. Parasitol., 117:155-160.
39. de Koning-Ward, T. F., Gilson, P. R., Boddey, J. A., Rug, M., Smith, B. J., Papenfuss, A. T., Sanders, P. R., Lundie, R. J., Maier, A. G., Cowman, A. F. & Crabb, B. S. 2009. A newly discovered protein export machine in malaria parasites. Nature, 459:945-949.
40. 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.
41. Deponte, M., Hoppe, H. C., Lee, M. C., Maier, A. G., Richard, D., Rug, M., Spielmann, T. & Przyborski, J. M. 2012. Wherever I may roam: protein and membrane trafficking in P. falciparum-infected red blood cells. Mol. Biochem. Parasitol., 186:95-116.
42. Deshmukh, A. S., Srivastava, S., Herrmann, S., Gupta, A., Mitra, P., Gilberger, T. W. & Dhar, S. K. 2012. The role of N-terminus of Plasmodium falciparum ORC1 in telomeric localization and var gene silencing. Nucleic Acids Res., 40:5313-5331.
43. Duraisingh, M. T., Triglia, T. & Cowman, A. F. 2002. Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int. J. Parasitol., 32:81-89.
44. Dvorin, J. D., Martyn, D. C., Patel, S. D., Grimley, J. S., Collins, C. R., Hopp, C. S., Bright, A. T., Westenberger, S., Winzeler, E., Blackman, M. J., Baker, D. A., Wandless, T. J. & Duraisingh, M. T. 2010. A plant-like kinase in Plasmodium falciparum regulates parasite egress from erythrocytes. Science, 328:910-912.
45. Ecker, A., Lehane, A. M., Clain, J. & Fidock, D. A. 2012. PfCRT and its role in antimalarial drug resistance. Trends Parasitol., 28:504-514.
46. Ehlgen, F., Pham, J. S., de Koning-Ward, T., Cowman, A. F. & Ralph, S. A. 2012. Investigation of the Plasmodium falciparum food vacuole through inducible expression of the chloroquine resistance transporter (PfCRT). PLoS ONE, 7:e38781.
47. El Bissati, K., Downie, M. J., Kim, S. K., Horowitz, M., Carter, N., Ullman, B. & Ben Mamoun, C. 2008. Genetic evidence for the essential role of PfNT1 in the transport and utilization of xanthine, guanine, guanosine and adenine by Plasmodium falciparum. Mol. Biochem. Parasitol., 161:130-139.
48. Elsworth, B., Matthews, K., Nie, C. Q., Kalanon, M., Charnaud, S. C., Sanders, P. R., Chisholm, S. A., Counihan, N. A., Shaw, P. J., Pino, P., Chan, J. A., Azevedo, M. F., Rogerson, S. J., Beeson, J. G., Crabb, B. S., Gilson, P. R. & de Koning-Ward, T. F. 2014. PTEX is an essential nexus for protein export in malaria parasites. Nature, 511:587-591.
49. Epp, C., Raskolnikov, D. & Deitsch, K. W. 2008. A regulatable transgene expression system for cultured Plasmodium falciparum parasites. Malar. J., 7:86.
50. Fidock, D. A. & Wellems, T. E. 1997. Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc. Natl Acad. Sci. USA, 94:10931-10936.
51. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. & Mello, C. C. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391:806-811.
52. Flores, M. V., Atkins, D., Wade, D., O’Sullivan, W. J. & Stewart, T. S. 1997. Inhibition of Plasmodium falciparum proliferation in vitro by ribozymes. J. Biol. Chem., 272:16940-16945.
53. Foth, B. J., Ralph, S. A., Tonkin, C. J., Struck, N. S., Fraunholz, M., Roos, D. S., Cowman, A. F. & McFadden, G. I. 2003. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science, 299:705-708.
54. Ganesan, S. M., Morrisey, J. M., Ke, H., Painter, H. J., Laroiya, K., Phillips, M. A., Rathod, P. K., Mather, M. W. & Vaidya, A. B. 2011. Yeast dihydroorotate dehydrogenase as a new selectable marker for Plasmodium falciparum transfection. Mol. Biochem. Parasitol., 177:29-34.
55. Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, J. C., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. & Barrell, B. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, 419:498-511.
56. Gavigan, C. S., Kiely, S. P., Hirtzlin, J. & Bell, A. 2003. Cyclosporin-binding proteins of Plasmodium falciparum. Int. J. Parasitol., 33:987-996.
57. Ghorbal, M., Gorman, M., Macpherson, C. R., Martins, R. M., Scherf, A. & Lopez-Rubio, J. J. 2014. Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nat. Biotechnol., 32:819-821.
58. Ginsburg, H. 2006. Progress in in silico functional genomics: the malaria Metabolic Pathways database. Trends Parasitol., 22:238-240.
59. Gissot, M., Briquet, S., Refour, P., Boschet, C. & Vaquero, C. 2005. PfMyb1, a Plasmodium falciparum transcription factor, is required for intra-erythrocytic growth and controls key genes for cell cycle regulation. J. Mol. Biol., 346:29-42.
60. Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J. D., Jacq, C., Johnston, M., Louis, E. J., Mewes, H. W., Murakami, Y., Philippsen, P., Tettelin, H. & Oliver, S. G. 1996. Life with 6000 genes. Science, 274(546):563-567.
61. Gopalakrishnan, A. M., Kundu, A. K., Mandal, T. K. & Kumar, N. 2013. Novel nanosomes for gene delivery to Plasmodium falciparum-infected red blood cells. Sci. Rep., 3:1534.
62. Gossen, M. & Bujard, H. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl Acad. Sci. USA, 89:5547-5551.
63. Hasenkamp, S., Russell, K. T. & Horrocks, P. 2012. Comparison of the absolute and relative efficiencies of electroporation-based transfection protocols for Plasmodium falciparum. Malar. J., 11:210.
64. Herm-Gotz, A., Agop-Nersesian, C., Munter, S., Grimley, J. S., Wandless, T. J., Frischknecht, F. & Meissner, M. 2007. Rapid control of protein level in the apicomplexan Toxoplasma gondii. Nat. Methods, 4:1003-1005.
65. Hunsicker, A., Steber, M., Mayer, G., Meitert, J., Klotzsche, M., Blind, M., Hillen, W., Berens, C. & Suess, B. 2009. An RNA aptamer that induces transcription. Chem. Biol., 16:173-180.
66. Ikadai, H., Shaw Saliba, K., Kanzok, S. M., McLean, K. J., Tanaka, T. Q., Cao, J., Williamson, K. C. & Jacobs-Lorena, M. 2013. Transposon mutagenesis identifies genes essential for Plasmodium falciparum gametocytogenesis. Proc. Natl Acad. Sci. USA, 110:E1676-E1684.
67. Jomaa, H., Wiesner, J., Sanderbrand, S., Altincicek, B., Weidemeyer, C., Hintz, M., Turbachova, I., Eberl, M., Zeidler, J., Lichtenthaler, H. K., Soldati, D. & Beck, E. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science, 285:1573-1576.
68. Jones, M. L., Collins, M. O., Goulding, D., Choudhary, J. S. & Rayner, J. C. 2012. Analysis of protein palmitoylation reveals a pervasive role in Plasmodium development and pathogenesis. Cell Host Microbe, 12:246-258.
69. Kadekoppala, M., Cheresh, P., Catron, D., Ji, D. D., Deitsch, K., Wellems, T. E., Seifert, H. S. & Haldar, K. 2001. Rapid recombination among transfected plasmids, chimeric episome formation and trans gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol., 112:211-218.
70. Khan, T., van Brummelen, A. C., Parkinson, C. J. & Hoppe, H. C. 2012. ATP and luciferase assays to determine the rate of drug action in in vitro cultures of Plasmodium falciparum. Malar. J., 11:369.
71. Kirkman, L. A., Lawrence, E. A. & Deitsch, K. W. 2014. Malaria parasites utilize both homologous recombination and alternative end joining pathways to maintain genome integrity. Nucleic Acids Res., 42:370-379.
72. Koshy, A. A., Fouts, A. E., Lodoen, M. B., Alkan, O., Blau, H. M. & Boothroyd, J. C. 2010. Toxoplasma secreting Cre recombinase for analysis of host-parasite interactions. Nat. Methods, 7:307-309.
73. Kreidenweiss, A., Hopkins, A. V. & Mordmuller, B. 2013. 2A and the auxin-based degron system facilitate control of protein levels in Plasmodium falciparum. PLoS ONE, 8:e78661.
74. Kumar, R., Adams, B., Oldenburg, A., Musiyenko, A. & Barik, S. 2002. Characterisation and expression of a PP1 serine/threonine protein phosphatase (PfPP1) from the malaria parasite, Plasmodium falciparum: demonstration of its essential role using RNA interference. Malar. J., 1:5.
75. LeRoux, M., Lakshmanan, V. & Daily, J. P. 2009. Plasmodium falciparum biology: analysis of in vitro versus in vivo growth conditions. Trends Parasitol., 25:474-481.
76. Lindner, S. E., Mikolajczak, S. A., Vaughan, A. M., Moon, W., Joyce, B. R., Sullivan, W. J.Jr & Kappe, S. H. 2013. Perturbations of Plasmodium Puf2 expression and RNA-seq of Puf2-deficient sporozoites reveal a critical role in maintaining RNA homeostasis and parasite transmissibility. Cell. Microbiol., 15:1266-1283.
77. Lyko, B., Hammershaimb, E. A., Nguitragool, W., Wellems, T. E. & Desai, S. A. 2012. A high-throughput method to detect Plasmodium falciparum clones in limiting dilution microplates. Malar. J., 11:124.
78. Maier, A. G., Braks, J. A., Waters, A. P. & Cowman, A. F. 2006. Negative selection using yeast cytosine deaminase/uracil phosphoribosyl transferase in Plasmodium falciparum for targeted gene deletion by double crossover recombination. Mol. Biochem. Parasitol., 150:118-121.
79. Malhotra, P., Dasaradhi, P. V., Kumar, A., Mohmmed, A., Agrawal, N., Bhatnagar, R. K. & Chauhan, V. S. 2002. Doublestranded RNA-mediated gene silencing of cysteine proteases (falcipain-1 and-2) of Plasmodium falciparum. Mol. Microbiol., 45:1245-1254.
80. Mamoun, C. B., Gluzman, I. Y., Beverley, S. M. & Goldberg, D. E. 2000. Transposition of the Drosophila element mariner within the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol., 110:405-407.
81. Mamoun, C. B., Gluzman, I. Y., Goyard, S., Beverley, S. M. & Goldberg, D. E. 1999a. A set of independent selectable markers for transfection of the human malaria parasite Plasmodium falciparum. Proc. Natl Acad. Sci. USA, 96:8716-8720.
82. Mamoun, C. B., Truong, R., Gluzman, I., Akopyants, N. S., Oksman, A. & Goldberg, D. E. 1999b. Transfer of genes into Plasmodium falciparum by polyamidoamine dendrimers. Mol. Biochem. Parasitol., 103:117-121.
83. Matuschewski, K., Ross, J., Brown, S. M., Kaiser, K., Nussenzweig, V. & Kappe, S. H. 2002. Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J. Biol. Chem., 277:41948-41953.
84. McMillan, P. J., Millet, C., Batinovic, S., Maiorca, M., Hanssen, E., Kenny, S., Muhle, R. A., Melcher, M., Fidock, D. A., Smith, J. D., Dixon, M. W. & Tilley, L. 2013. Spatial and temporal mapping of the PfEMP1 export pathway in Plasmodium falciparum. Cell. Microbiol., 15:1401-1418.
85. McNamara, C. W., Lee, M. C., Lim, C. S., Lim, S. H., Roland, J., Nagle, A., Simon, O., Yeung, B. K., Chatterjee, A. K., Mc-Cormack, S. L., Manary, M. J., Zeeman, A. M., Dechering, K. J., Kumar, T. R., Henrich, P. P., Gagaring, K., Ibanez, M., Kato, N., Kuhen, K. L., Fischli, C., Rottmann, M., Plouffe, D. M., Bursulaya, B., Meister, S., Rameh, L., Trappe, J., Haasen, D., Timmerman, M., Sauerwein, R. W., Suwanarusk, R., Russell, B., Renia, L., Nosten, F., Tully, D. C., Kocken, C. H., Glynne, R. J., Bodenreider, C., Fidock, D. A., Diagana, T. T. & Winzeler, E. A. 2013. Targeting Plasmodium PI(4)K to eliminate malaria. Nature, 504:248-253.
86. McRobert, L. & McConkey, G. A. 2002. RNA interference (RNAi) inhibits growth of Plasmodium falciparum. Mol. Biochem. Parasitol., 119:273-278.
87. Meissner, M., Schluter, D. & Soldati, D. 2002. Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science, 298:837-840.
88. Meissner, M., Brecht, S., Bujard, H. & Soldati, D. 2001. Modulation of myosin A expression by a newly established tetracycline repressor-based inducible system in Toxoplasma gondii. Nucleic Acids Res., 29:E115.
89. Meissner, M., Krejany, E., Gilson, P. R., de Koning-Ward, T. F., Soldati, D. & Crabb, B. S. 2005. Tetracycline analogue-regulated transgene expression in Plasmodium falciparum blood stages using Toxoplasma gondii transactivators. Proc. Natl Acad. Sci. USA, 102:2980-2985.
90. Miao, J., Li, X. & Cui, L. 2010. Cloning of Plasmodium falciparum by single-cell sorting. Exp. Parasitol., 126:198-202.
91. Mikolajczak, S. A., Lakshmanan, V., Fishbaugher, M., Camargo, N., Harupa, A., Kaushansky, A., Douglass, A. N., Baldwin, M., Healer, J., O’Neill, M., Phuong, T., Cowman, A. & Kappe, S. H. 2014. A next-generation genetically attenuated Plasmodium falciparum parasite created by triple gene deletion. Mol. Ther., 22:1707-1715.
92. Muralidharan, V., Oksman, A., Pal, P., Lindquist, S. & Goldberg, D. E. 2012. Plasmodium falciparum heat shock protein 110 stabilizes the asparagine repeat-rich parasite proteome during malarial fevers. Nat. Commun., 3:1310.
93. Muralidharan, V., Oksman, A., Iwamoto, M., Wandless, T. J. & Goldberg, D. E. 2011. Asparagine repeat function in a Plasmodium falciparum protein assessed via a regulatable fluorescent affinity tag. Proc. Natl Acad. Sci. USA, 108:4411-4416.
94. Niles, J. C., Derisi, J. L. & Marletta, M. A. 2009. Inhibiting Plasmodium falciparum growth and heme detoxification pathway using heme-binding DNA aptamers. Proc. Natl Acad. Sci. USA, 106:13266-13271.
95. Nkrumah, L. J., Muhle, R. A., Moura, P. A., Ghosh, P., Hatfull, G. F., Jacobs, W. R. Jr & Fidock, D. A. 2006. Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat. Methods, 3:615-621.
96. O’Donnell, R. A., Freitas-Junior, L. H., Preiser, P. R., Williamson, D. H., Duraisingh, M., McElwain, T. F., Scherf, A., Cowman, A. F. & Crabb, B. S. 2002. A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes. EMBO J., 21:1231-1239.
97. O’Neill, M. T., Phuong, T., Healer, J., Richard, D. & Cowman, A. F. 2010. Gene deletion from Plasmodium falciparum using FLP and Cre recombinases: implications for applied site-specific recombination. Int. J. Parasitol., 41:117-123.
98. Painter, H. J., Altenhofen, L. M., Kafsack, B. F. & Llinas, M. 2013. Whole-genome analysis of Plasmodium spp. utilizing a new agilent technologies DNA microarray platform. Methods Mol. Biol., 923:213-219.
99. Panikashvili, D., Savaldi-Goldstein, S., Mandel, T., Yifhar, T., Franke, R. B., Hofer, R., Schreiber, L., Chory, J. & Aharoni, A. 2007. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol., 145:1345-1360.
100. Pei, Y., Tarun, A. S., Vaughan, A. M., Herman, R. W., Soliman, J. M., Erickson-Wayman, A. & Kappe, S. H. 2010. Plasmodium pyruvate dehydrogenase activity is only essential for the parasite’s progression from liver infection to blood infection. Mol. Microbiol., 75:957-971.
101. Pillai, A. D., Addo, R., Sharma, P., Nguitragool, W., Srinivasan, P. & Desai, S. A. 2013. Malaria parasites tolerate a broad range of ionic environments and do not require host cation remodelling. Mol. Microbiol., 88:20-34.
102. Pino, P., Sebastian, S., Kim, E. A., Bush, E., Brochet, M., Volkmann, K., Kozlowski, E., Llinas, M., Billker, O. & Soldati-Favre, D. 2012. A tetracycline-repressible transactivator system to study essential genes in malaria parasites. Cell Host Microbe, 12:824-834.
103. Plouffe, D., Brinker, A., McNamara, C., Henson, K., Kato, N., Kuhen, K., Nagle, A., Adrian, F., Matzen, J. T., Anderson, P., Nam, T. G., Gray, N. S., Chatterjee, A., Janes, J., Yan, S. F., Trager, R., Caldwell, J. S., Schultz, P. G., Zhou, Y. & Winzeler, E. A. 2008. In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc. Natl Acad. Sci. USA, 105:9059-9064.
104. Prommana, P., Uthaipibull, C., Wongsombat, C., Kamchonwongpaisan, S., Yuthavong, Y., Knuepfer, E., Holder, A. A. & Shaw, P. J. 2013. Inducible knockdown of Plasmodium gene expression using the glmS ribozyme. PLoS ONE, 8:e73783.
105. Prudencio, M., Rodrigues, C. D., Hannus, M., Martin, C., Real, E., Goncalves, L. A., Carret, C., Dorkin, R., Rohl, I., Jahn-Hoffmann, K., Luty, A. J., Sauerwein, R., Echeverri, C. J. & Mota, M. M. 2008. Kinome-wide RNAi screen implicates at least 5 host hepatocyte kinases in Plasmodium sporozoite infection. PLoS Pathog., 4:e1000201.
106. Ralph, S. A., van Dooren, G. G., Waller, R. F., Crawford, M. J., Fraunholz, M. J., Foth, B. J., Tonkin, C. J., Roos, D. S. & McFadden, G. I. 2004. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol., 2:203-216.
107. Reininger, L., Garcia, M., Tomlins, A., Muller, S. & Doerig, C. 2012. The Plasmodium falciparum, nima-related kinase Pfnek-4: a marker for asexual parasites committed to sexual differentiation. Malar. J., 11:250.
108. Riglar, D. T., Rogers, K. L., Hanssen, E., Turnbull, L., Bullen, H. E., Charnaud, S. C., Przyborski, J., Gilson, P. R., Whitchurch, C. B., Crabb, B. S., Baum, J. & Cowman, A. F. 2013. Spatial association with PTEX complexes defines regions for effector export into Plasmodium falciparum-infected erythrocytes. Nat. Commun., 4:1415.
109. Rosinski-Chupin, I., Chertemps, T., Boisson, B., Perrot, S., Bischoff, E., Briolay, J., Couble, P., Menard, R., Brey, P. & Baldacci, P. 2007. Serial analysis of gene expression in Plasmodium berghei salivary gland sporozoites. BMC Genomics, 8:466.
110. Rug, M. & Maier, A. G. 2013. Transfection of Plasmodium falciparum. Methods Mol. Biol., 923:75-98.
111. Russo, I., Oksman, A., Vaupel, B. & Goldberg, D. E. 2009. A calpain unique to alveolates is essential in Plasmodium falciparum and its knockdown reveals an involvement in pre-S-phase development. Proc. Natl Acad. Sci. USA, 106:1554-1559.
112. Sanchez, B. A., Varotti, F. P., Rodrigues, F. G. & Carvalho, L. H. 2007. Validation of a Plasmodium falciparum parasite transformed with green fluorescent protein for antimalarial drug screening. J. Microbiol. Methods, 69:518-522.
113. Sidhu, A. B., Verdier-Pinard, D. & Fidock, D. A. 2002. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science, 298:210-213.
114. Sijwali, P. S. & Rosenthal, P. J. 2004. Gene disruption confirms a critical role for the cysteine protease falcipain-2 in hemoglobin hydrolysis by Plasmodium falciparum. Proc. Natl Acad. Sci. USA, 101:4384-4389.
115. Skinner-Adams, T. S., Hawthorne, P. L., Trenholme, K. R. & Gardiner, D. L. 2003. GATEWAY vectors for Plasmodium falciparum transfection. Trends Parasitol., 19:17-18.
116. Solyakov, L., Halbert, J., Alam, M. M., Semblat, J. P., Dorin-Semblat, D., Reininger, L., Bottrill, A. R., Mistry, S., Abdi, A., Fennell, C., Holland, Z., Demarta, C., Bouza, Y., Sicard, A., Nivez, M. P., Eschenlauer, S., Lama, T., Thomas, D. C., Sharma, P., Agarwal, S., Kern, S., Pradel, G., Graciotti, M., Tobin, A. B. & Doerig, C. 2011. Global kinomic and phospho-proteomic analyses of the human malaria parasite Plasmodium falciparum. Nat. Commun., 2:565.
117. Spalding, M. D., Allary, M., Gallagher, J. R. & Prigge, S. T. 2010. Validation of a modified method for Bxb1 mycobacteriophage integrase-mediated recombination in Plasmodium falciparum by localization of the H-protein of the glycine cleavage complex to the mitochondrion. Mol. Biochem. Parasitol., 172:156-160.
118. Spillman, N. J., Allen, R. J., McNamara, C. W., Yeung, B. K., Winzeler, E. A., Diagana, T. T. & Kirk, K. 2013. Na(+) regulation in the malaria parasite Plasmodium falciparum involves the cation ATPase PfATP4 and is a target of the spiroindolone antimalarials. Cell Host Microbe, 13:227-237.
119. Straimer, J., Lee, M. C., Lee, A. H., Zeitler, B., Williams, A. E., Pearl, J. R., Zhang, L., Rebar, E. J., Gregory, P. D., Llinas, M., Urnov, F. D. & Fidock, D. A. 2012. Site-specific genome editing in Plasmodium falciparum using engineered zinc-finger nucleases. Nat. Methods, 9:993-998.
120. Sullivan, D. J. 2013. Plasmodium drug targets outside the genetic control of the parasite. Curr. Pharm. Des., 19:282-289.
121. Tonkin, C. J., Foth, B. J., Ralph, S. A., Struck, N., Cowman, A. F. & McFadden, G. I. 2008. Evolution of malaria parasite plastid targeting sequences. Proc. Natl Acad. Sci. USA, 105:4781-4785.
122. Tonkin, C. J., van Dooren, G. G., Spurck, T. P., Struck, N. S., Good, R. T., Handman, E., Cowman, A. F. & McFadden, G. I. 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.
123. Tuteja, R., Pradhan, A. & Sharma, S. 2008. Plasmodium falciparum signal peptidase is regulated by phosphorylation and required for intra-erythrocytic growth. Mol. Biochem. Parasitol., 157:137-147.
124. Van Dooren, G. G., Stimmler, L. M. & McFadden, G. I. 2006. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol. Rev., 30:596-630.
125. Van Schaijk, B. C., Vos, M. W., Janse, C. J., Sauerwein, R. W. & Khan, S. M. 2010. Removal of heterologous sequences from Plasmodium falciparum mutants using FLPe-recombinase. PLoS ONE, 5:e15121.
126. Van Schaijk, B. C., Kumar, T. R., Vos, M. W., Richman, A., van Gemert, G. J., Li, T., Eappen, A. G., Williamson, K. C., Morahan, B. J., Fishbaugher, M., Kennedy, M., Camargo, N., Khan, S. M., Janse, C. J., Sim, K. L., Hoffman, S. L., Kappe, S. H., Sauerwein, R. W., Fidock, D. A. & Vaughan, A. M. 2014. Type II fatty acid biosynthesis is essential for Plasmodium falciparum sporozoite development in the midgut of Anopheles mosquitoes. Eukaryot. Cell, 13:550-559.
127. Van Tyne, D., Park, D. J., Schaffner, S. F., Neafsey, D. E., Angelino, E., Cortese, J. F., Barnes, K. G., Rosen, D. M., Lukens, A. K., Daniels, R. F., Milner, D. A. Jr, Johnson, C. A., Shlyakhter, I., Grossman, S. R., Becker, J. S., Yamins, D., Karlsson, E. K., Ndiaye, D., Sarr, O., Mboup, S., Happi, C., Furlotte, N. A., Eskin, E., Kang, H. M., Hartl, D. L., Birren, B. W., Wiegand, R. C., Lander, E. S., Wirth, D. F., Volkman, S. K. & Sabeti, P. C. 2011. Identification and functional validation of the novel antimalarial resistance locus PF10_0355 in Plasmodium falciparum. PLoS Genet., 7:e1001383.
128. VanWye, J. D. & Haldar, K. 1997. Expression of green fluorescent protein in Plasmodium falciparum. Mol. Biochem. Parasitol., 87:225-229.
129. Vaughan, A. M., O’Neill, M. T., Tarun, A. S., Camargo, N., Phuong, T. M., Aly, A. S., Cowman, A. F. & Kappe, S. H. 2009. Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell. Microbiol., 11:506-520.
130. Wagner, J. C., Platt, R. J., Goldfless, S. J., Zhang, F. & Niles, J. C. 2014. Efficient CRISPR-Cas9-mediated genome editing in Plasmodium falciparum. Nat. Methods, 11:915-918.
131. Webster, W. A. J. 2013. Establishing and elucidating conditional genetic manipulation of the malaria parasite, Plasmodium falciparum. Master of Philosophy. School of Botany, The University of Melbourne. 116 p.
132. Wilson, D. W., Crabb, B. S. & Beeson, J. G. 2010. Development of fluorescent Plasmodium falciparum for in vitro growth inhibition assays. Malar. J., 9:152.
133. Wong, E. H., Hasenkamp, S. & Horrocks, P. 2011. Analysis of the molecular mechanisms governing the stage-specific expression of a prototypical housekeeping gene during intraerythrocytic development of P. falciparum. J. Mol. Biol., 408:205-221.
134. Woodcroft, B. J., McMillan, P. J., Dekiwadia, C., Tilley, L. & Ralph, S. A. 2012. Determination of protein subcellular localization in apicomplexan parasites. Trends Parasitol., 28:546-554.
135. Wu, Y., Kirkman, L. A. & Wellems, T. E. 1996. Transformation of Plasmodium falciparum malaria parasites by homologous integration of plasmids that confer resistance to pyrimethamine. Proc. Natl Acad. Sci. USA, 93:1130-1134.
136. Wu, Y., Sifri, C. D., Lei, H. H., Su, X. Z. & Wellems, T. E. 1995. Transfection of Plasmodium falciparum within human red blood cells. Proc. Natl Acad. Sci. USA, 92:973-977.
137. Yeh, E. & DeRisi, J. L. 2011. Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol., 9:e1001138.
138. Yeh, I., Hanekamp, T., Tsoka, S., Karp, P. D. & Altman, R. B. 2004. Computational analysis of Plasmodium falciparum metabolism: organizing genomic information to facilitate drug discovery. Genome Res., 14:917-924.