Advancements in transfection technologies for Plasmodium

International Journal for Parasitology

Volumn 37, Issue 1, 2007, Pages 1-10

  Balu, Bharath ^a   Adams, John H ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Gene transfer; Malaria; Plasmodium; Transfection; Transformation

Indexed keywords

ENDOPARASITE; GENE TRANSFER; GENETIC ANALYSIS; MALARIA; PROTOZOAN;

DISEASE MARKER; GENE EXPRESSION; GENE TRANSFER; GENETIC ANALYSIS; GENETIC MANIPULATION; GENETIC TRANSFECTION; GENETIC TRANSFORMATION; MALARIA; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM CYNOMOLGI; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM YOELII; POLYMERASE CHAIN REACTION; REVIEW; TECHNOLOGY;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; DNA, PROTOZOAN; GENE EXPRESSION; GENES, PROTOZOAN; GENETIC MARKERS; HUMANS; MALARIA; MUTAGENESIS; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; TRANSFECTION; TRANSGENES;

EID: 33845626667     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.10.001     Document Type: Review

References (78)

1. Adisa A., Rug M., Klonis N., Foley M., Cowman A.F., and Tilley L. The signal sequence of exported protein-1 directs the green fluorescent protein to the parasitophorous vacuole of transfected malaria parasites. J. Biol. Chem. 278 (2003) 6532-6542
2. Balu B., Shoue D.A., Fraser Jr. M.J., and Adams J.H. High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proc. Natl. Acad. Sci. USA 102 (2005) 16391-16396
3. Ben Mamoun C., Gluzman I.Y., Hott C., MacMillan S.K., Amarakone A.S., Anderson D.L., Carlton J.M., Dame J.B., Chakrabarti D., Martin R.K., Brownstein B.H., and Goldberg D.E. Co-ordinated programme of gene expression during asexual intraerythrocytic development of the human malaria parasite Plasmodium falciparum revealed by microarray analysis. Mol. Microbiol. 39 (2001) 26-36
4. Bozdech Z., Zhu J., Joachimiak M.P., Cohen F.E., Pulliam B., and DeRisi J.L. Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome. Biol. 4 (2003) R9
5. Braks J.A., Franke-Fayard B., Kroeze H., Janse C.J., and Waters A.P. Development and application of a positive-negative selectable marker system for use in reverse genetics in Plasmodium. Nucleic Acids Res. 34 (2006) e39
6. Branda C.S., and Dymecki S.M. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 6 (2004) 7-28
7. Carlton J. The Plasmodium vivax genome sequencing project. Trends Parasitol. 19 (2003) 227-231
8. Carlton J.M., Angiuoli S.V., Suh B.B., Kooij T.W., Pertea M., Silva J.C., Ermolaeva M.D., Allen J.E., Selengut J.D., Koo H.L., Peterson J.D., Pop M., Kosack D.S., Shumway M.F., Bidwell S.L., Shallom S.J., van Aken S.E., Riedmuller S.B., Feldblyum T.V., Cho J.K., Quackenbush J., Sedegah M., Shoaibi A., Cummings L.M., Florens L., Yates J.R., Raine J.D., Sinden R.E., Harris M.A., Cunningham D.A., Preiser P.R., Bergman L.W., Vaidya A.B., van Lin L.H., Janse C.J., Waters A.P., Smith H.O., White O.R., Salzberg S.L., Venter J.C., Fraser C.M., Hoffman S.L., Gardner M.J., and Carucci D.J. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii. Nature 419 (2002) 512-519
9. Carvalho T.G., Thiberge S., Sakamoto H., and Menard R. Conditional mutagenesis using site-specific recombination in Plasmodium berghei. Proc. Natl. Acad. Sci. USA 101 (2004) 14931-14936
10. Cary L.C., Goebel M., Corsaro B.G., Wang H.G., Rosen E., and Fraser M.J. Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 172 (1989) 156-169
11. Cowman A.F. Functional analysis of drug resistance in Plasmodium falciparum in the post-genomic era. Int. J. Parasitol. 31 (2001) 871-878
12. Crabb B.S., Rug M., Gilberger T.W., Thompson J.K., Triglia T., Maier A.G., and Cowman A.F. Transfection of the human malaria parasite Plasmodium falciparum. Methods Mol. Biol. 270 (2004) 263-276
13. Date S.V., and Stoeckert Jr. C.J. Computational modeling of the Plasmodium falciparum interactome reveals protein function on a genome-wide scale. Genome Res. 16 (2006) 542-549
14. de Koning-Ward T.F., Janse C.J., and Waters A.P. The development of genetic tools for dissecting the biology of malaria parasites. Annu. Rev. Microbiol. 54 (2000) 157-185
15. de Koning-Ward T.F., Waters A.P., and Crabb B.S. Puromycin-N-acetyltransferase as a selectable marker for use in Plasmodium falciparum. Mol. Biochem. Parasitol. 117 (2001) 155-160
16. Deitsch K., Driskill C., and Wellems T. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res. 29 (2001) 850-853
17. Donald R.G., and Roos D.S. Stable molecular transformation of Toxoplasma gondii: a selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria. Proc. Natl. Acad. Sci. USA 90 (1993) 11703-11707
18. Duraisingh M.T., Triglia T., and Cowman A.F. Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int. J. Parasitol. 32 (2002) 81-89
19. Ecker A., Moon R., Sinden R.E., and Billker O. Generation of gene targeting constructs for Plasmodium berghei by a PCR-based method amenable to high throughput applications. Mol. Biochem. Parasitol. 145 (2006) 265-268
20. Fidock D.A., and Wellems T.E. 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 (1997) 10931-10936
21. Fidock D.A., Nomura T., and Wellems T.E. Cycloguanil and its parent compound proguanil demonstrate distinct activities against Plasmodium falciparum malaria parasites transformed with human dihydrofolate reductase. Mol. Pharmacol. 54 (1998) 1140-1147
22. Florens L., Washburn M.P., Raine J.D., Anthony R.M., Grainger M., Haynes J.D., Moch J.K., Muster N., Sacci J.B., Tabb D.L., Witney A.A., Wolters D., Wu Y., Gardner M.J., Holder A.A., Sinden R.E., Yates J.R., and Carucci D.J. A proteomic view of the Plasmodium falciparum life cycle. Nature 419 (2002) 520-526
23. Foth B.J., Ralph S.A., Tonkin C.J., Struck N.S., Fraunholz M., Roos D.S., Cowman A.F., and McFadden G.I. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299 (2003) 705-708
24. Fraser M.J., Brusca J.S., Smith G.E., and Summers M.D. Transposon-mediated mutagenesis of a baculovirus. Virology 145 (1985) 356-361
25. Gardiner D.L., Skinner-Adams T.S., Spielmann T., and Trenholme K.R. Malaria transfection and transfection vectors. Trends Parasitol. 19 (2003) 381-383
26. 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., and Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 (2002) 498-511
27. Gardner M.J., Shallom S.J., Carlton J.M., Salzberg S.L., Nene V., Shoaibi A., Ciecko A., Lynn J., Rizzo M., Weaver B., Jarrahi B., Brenner M., Parvizi B., Tallon L., Moazzez A., Granger D., Fujii C., Hansen C., Pederson J., Feldblyum T., Peterson J., Suh B., Angiuoli S., Pertea M., Allen J., Selengut J., White O., Cummings L.M., Smith H.O., Adams M.D., Venter J.C., Carucci D.J., Hoffman S.L., and Fraser C.M. Sequence of Plasmodium falciparum chromosomes 2, 10, 11 and 14. Nature 419 (2002) 531-534
28. Goonewardene R., Daily J., Kaslow D., Sullivan T.J., Duffy P., Carter R., Mendis K., and Wirth D. Transfection of the malaria parasite and expression of firefly luciferase. Proc. Natl. Acad. Sci. USA 90 (1993) 5234-5236
29. Groth A.C., and Calos M.P. Phage integrases: biology and applications. J. Mol. Biol. 335 (2004) 667-678
30. Hall N., Karras M., Raine J.D., Carlton J.M., Kooij T.W., Berriman M., Florens L., Janssen C.S., Pain A., Christophides G.K., James K., Rutherford K., Harris B., Harris D., Churcher C., Quail M.A., Ormond D., Doggett J., Trueman H.E., Mendoza J., Bidwell S.L., Rajandream M.A., Carucci D.J., Yates III J.R., Kafatos F.C., Janse C.J., Barrell B., Turner C.M., Waters A.P., and Sinden R.E. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307 (2005) 82-86
31. Hayward R.E., Derisi J.L., Alfadhli S., Kaslow D.C., Brown P.O., and Rathod P.K. Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Mol. Microbiol. 35 (2000) 6-14
32. Hiller N.L., Bhattacharjee S., van Ooij C., Liolios K., Harrison T., Lopez-Estrano C., and Haldar K. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306 (2004) 1934-1937
33. Janse C.J., Franke-Fayard B., Mair G.R., Ramesar J., Thiel C., Engelmann S., Matuschewski K., van Gemert G.J., Sauerwein R.W., and Waters A.P. High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol. Biochem. Parasitol. 145 (2006) 60-70
34. Johnson J.R., Florens L., Carucci D.J., and Yates III J.R. Proteomics in malaria. J. Proteome Res. 3 (2004) 296-306
35. Jongco A.M., Ting L.M., Thathy V., Mota M.M., and Kim K. Improved transfection and new selectable markers for the rodent malaria parasite Plasmodium yoelii. Mol. Biochem. Parasitol. 146 (2006) 242-250
36. Kadekoppala M., Cheresh P., Catron D., Ji D.D., Deitsch K., Wellems T.E., Seifert H.S., and Haldar K. Rapid recombination among transfected plasmids, chimeric episome formation and trans gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 112 (2001) 211-218
37. Kocken C.H., van der Wel A., and Thomas A.W. Plasmodium cynomolgi: transfection of blood-stage parasites using heterologous DNA constructs. Exp. Parasitol. 93 (1999) 58-60
38. Kocken C.H., Ozwara H., van der Wel A., Beetsma A.L., Mwenda J.M., and Thomas A.W. Plasmodium knowlesi provides a rapid in vitro and in vivo transfection system that enables double-crossover gene knockout studies. Infect Immun. 70 (2002) 655-660
39. LaCount D.J., Vignali M., Chettier R., Phansalkar A., Bell R., Hesselberth J.R., Schoenfeld L.W., Ota I., Sahasrabudhe S., Kurschner C., Fields S., and Hughes R.E. A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438 (2005) 103-107
40. Lasonder E., Ishihama Y., Andersen J.S., Vermunt A.M., Pain A., Sauerwein R.W., Eling W.M., Hall N., Waters A.P., Stunnenberg H.G., and Mann M. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419 (2002) 537-542
41. Le Roch K.G., Zhou Y., Batalov S., and Winzeler E.A. Monitoring the chromosome 2 intraerythrocytic transcriptome of Plasmodium falciparum using oligonucleotide arrays. Am. J. Trop. Med. Hyg. 67 (2002) 233-243
42. Le Roch K.G., Zhou Y., Blair P.L., Grainger M., Moch J.K., Haynes J.D., De La Vega P., Holder A.A., Batalov S., Carucci D.J., and Winzeler E.A. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301 (2003) 1503-1508
43. Lopez-Estrano C., Bhattacharjee S., Harrison T., and Haldar K. Cooperative domains define a unique host cell-targeting signal in Plasmodium falciparum-infected erythrocytes. Proc. Natl. Acad. Sci. USA 100 (2003) 12402-12407
44. Maier A.G., Braks J.A., Waters A.P., and Cowman A.F. Negative selection using yeast cytosine deaminase/uracil phosphoribosyl transferase in Plasmodium falciparum for targeted gene deletion by double crossover recombination. Mol. Biochem. Parasitol. 150 (2006) 118-121
45. Mamoun C.B., Gluzman I.Y., Goyard S., Beverley S.M., and Goldberg D.E. A set of independent selectable markers for transfection of the human malaria parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 96 (1999) 8716-8720
46. Mamoun C.B., Truong R., Gluzman I., Akopyants N.S., Oksman A., and Goldberg D.E. Transfer of genes into Plasmodium falciparum by polyamidoamine dendrimers. Mol. Biochem. Parasitol. 103 (1999) 117-121
47. Marti M., Good R.T., Rug M., Knuepfer E., and Cowman A.F. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306 (2004) 1930-1933
48. Meissner M., Brecht S., Bujard H., and Soldati D. Modulation of myosin A expression by a newly established tetracycline repressor-based inducible system in Toxoplasma gondii. Nucleic Acids Res. 29 (2001) E115
49. Meissner M., Schluter D., and Soldati D. Role of Toxoplasma gondii myosin A in powering parasite gliding and host cell invasion. Science 298 (2002) 837-840
50. Meissner M., Krejany E., Gilson P.R., de Koning-Ward T.F., Soldati D., and Crabb B.S. Tetracycline analogue-regulated transgene expression in Plasmodium falciparum blood stages using Toxoplasma gondii transactivators. Proc. Natl. Acad. Sci. USA 102 (2005) 2980-2985
51. Mendis K., Sina B.J., Marchesini P., and Carter R. The neglected burden of Plasmodium vivax malaria. Am. J. Trop. Med. Hyg. 64 (2001) 97-106
52. Mota M.M., Thathy V., Nussenzweig R.S., and Nussenzweig V. Gene targeting in the rodent malaria parasite Plasmodium yoelii. Mol. Biochem. Parasitol. 113 (2001) 271-278
53. Myrick A., Munasinghe A., Patankar S., and Wirth D.F. Mapping of the Plasmodium falciparum multidrug resistance gene 5′-upstream region, and evidence of induction of transcript levels by antimalarial drugs in chloroquine sensitive parasites. Mol. Microbiol. 49 (2003) 671-683
54. Nkrumah L.J., Muhle R.A., Moura P.A., Ghosh P., Hatfull G.F., Jacobs Jr. W.R., and Fidock D.A. Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat. Methods 3 (2006) 615-621
55. O'Donnell R., Preiser P.R., Williamson D.H., Moore P.W., Cowman A.F., and Crabb B.S. An alteration in concatameric structure is associated with efficient segregation of plasmids in transfected Plasmodium falciparum parasites. Nucleic Acids Res. 29 (2001) 716-724
56. O'Donnell R.A., Freitas-Junior L.H., Preiser P.R., Williamson D.H., Duraisingh M., McElwain T.F., Scherf A., Cowman A.F., and Crabb B.S. A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes. Embo J. 21 (2002) 1231-1239
57. Pfahler J.M., Galinski M.R., Barnwell J.W., and Lanzer M. Transient transfection of Plasmodium vivax blood stage parasites. Mol. Biochem. Parasitol. (2006)
58. Reed M.B., Saliba K.J., Caruana S.R., Kirk K., and Cowman A.F. Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature 403 (2000) 906-909
59. Sakamoto H., Thiberge S., Akerman S., Janse C.J., Carvalho T.G., and Menard R. Towards systematic identification of Plasmodium essential genes by transposon shuttle mutagenesis. Nucleic Acids Res. 33 (2005) e174
60. Sam-Yellowe T.Y., Florens L., Wang T., Raine J.D., Carucci D.J., Sinden R., and Yates III J.R. Proteome analysis of rhoptry-enriched fractions isolated from Plasmodium merozoites. J. Proteome Res. 3 (2004) 995-1001
61. Sanders P.R., Gilson P.R., Cantin G.T., Greenbaum D.C., Nebl T., Carucci D.J., McConville M.J., Schofield L., Hodder A.N., Yates III J.R., and Crabb B.S. Distinct protein classes including novel merozoite surface antigens in raft-like membranes of Plasmodium falciparum. J. Biol. Chem. 280 (2005) 40169-40176
62. Sato S., and Wilson R.J. The genome of Plasmodium falciparum encodes an active delta-aminolevulinic acid dehydratase. Curr. Genet. 40 (2002) 391-398
63. Sijwali P.S., and Rosenthal P.J. Gene disruption confirms a critical role for the cysteine protease falcipain-2 in hemoglobin hydrolysis by Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 101 (2004) 4384-4389
64. Snow R.W., Guerra C.A., Noor A.M., Myint H.Y., and Hay S.I. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434 (2005) 214-217
65. Sultan A.A., Thathy V., de Koning-Ward T.F., and Nussenzweig V. Complementation of Plasmodium berghei TRAP knockout parasites using human dihydrofolate reductase gene as a selectable marker. Mol. Biochem. Parasitol. 113 (2001) 151-156
66. Suthram S., Sittler T., and Ideker T. The Plasmodium protein network diverges from those of other eukaryotes. Nature 438 (2005) 108-112
67. Thathy V., and Menard R. Gene targeting in Plasmodium berghei. Methods Mol. Med. 72 (2002) 317-331
68. Trang D.T., Huy N.T., Kariu T., Tajima K., and Kamei K. One-step concentration of malarial parasite-infected red blood cells and removal of contaminating white blood cells. Malar J. 3 (2004) 7
69. van der Wel A.M., Tomas A.M., Kocken C.H., Malhotra P., Janse C.J., Waters A.P., and Thomas A.W. Transfection of the primate malaria parasite Plasmodium knowlesi using entirely heterologous constructs. J. Exp. Med. 185 (1997) 1499-1503
70. van Dijk M.R., McConkey G.A., Vinkenoog R., Waters A.P., and Janse C.J. Mechanisms of pyrimethamine resistance in two different strains of Plasmodium berghei. Mol. Biochem. Parasitol. 68 (1994) 167-171
71. van Dijk M.R., Waters A.P., and Janse C.J. Stable transfection of malaria parasite blood stages. Science 268 (1995) 1358-1362
72. van Dijk M.R., Janse C.J., and Waters A.P. Expression of a Plasmodium gene introduced into subtelomeric regions of Plasmodium berghei chromosomes. Science 271 (1996) 662-665
73. Voss T.S., Healer J., Marty A.J., Duffy M.F., Thompson J.K., Beeson J.G., Reeder J.C., Crabb B.S., and Cowman A.F. A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439 (2006) 1004-1008
74. Waller R.F., Reed M.B., Cowman A.F., and McFadden G.I. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. Embo J. 19 (2000) 1794-1802
75. Walliker D., Quakyi I.A., Wellems T.E., McCutchan T.F., Szarfman A., London W.T., Corcoran L.M., Burkot T.R., and Carter R. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236 (1987) 1661-1666
76. Wellems T.E., Panton L.J., Gluzman I.Y., do Rosario V.E., Gwadz R.W., Walker-Jonah A., and Krogstad D.J. Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature 345 (1990) 253-255
77. Wu Y., Sifri C.D., Lei H.H., Su X.Z., and Wellems T.E. Transfection of Plasmodium falciparum within human red blood cells. Proc. Natl. Acad. Sci. USA 92 (1995) 973-977
78. Wu Y., Kirkman L.A., and Wellems T.E. Transformation of Plasmodium falciparum malaria parasites by homologous integration of plasmids that confer resistance to pyrimethamine. Proc. Natl. Acad. Sci. 93 (1996) 1130-1134