An integrated strategy for efficient vector construction and multi-gene expression in Plasmodium falciparum

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Wagner, Jeffrey C ^a   Goldfless, Stephen J ^a   Ganesan, Suresh M ^a   Lee, Marcus C S ^b   Fidock, David A ^b   Niles, Jacquin C ^a  

^a Massachusetts Institute of Technology   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2A LIKE PEPTIDE; PEPTIDE; PLASMID VECTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MIGRATION; EXPRESSION VECTOR; GENE CASSETTE; GENE EXPRESSION; GENE SEGREGATION; GENETIC PROCEDURES; GIBSON ASSEMBLY METHOD; HOMOLOGOUS RECOMBINATION; MOLECULAR CLONING; MULTIGENE FAMILY; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RELIABILITY; SACCHAROMYCES CEREVISIAE;

GENE EXPRESSION; GENETIC VECTORS; GENETICS, MICROBIAL; MOLECULAR BIOLOGY; PLASMIDS; PLASMODIUM FALCIPARUM; TRANSGENES;

EID: 84886175099     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-373     Document Type: Article

References (43)

1. WHO, World Malaria Report: 2012 Geneva: World Health Organization 2012
2. Drug-resistant malaria. Hyde JE, Trends Parasitol 2005 21 494 498 10.1016/j.pt.2005.08.020 16140578 (Pubitemid 41447018)
3. Genome sequence of the human malaria parasite Plasmodium falciparum. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan M-S, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DMA, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B, Nature 2002 419 498 511 10.1038/nature01097 12368864
4. The complete nucleotide sequence of chromosome 3 of Plasmodium falciparum. Bowman S, Lawson D, Basham D, Brown D, Chillingworth T, Churcher CM, Craig A, Davies RM, Devlin K, Feltwell T, Gentles S, Gwilliam R, Hamlin N, Harris D, Holroyd S, Hornsby T, Horrocks P, Jagels K, Jassal B, Kyes S, McLean J, Moule S, Mungall K, Murphy L, Oliver K, Quail MA, Rajandream MA, Rutter S, Skelton J, Squares R, Squares S, Sulston JE, Whitehead S, Woodward JR, Newbold C, Barrell BG, Nature 1999 400 532 538 10.1038/22964 10448855 (Pubitemid 29381795)
5. Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. Gardner MJ, Tettelin H, Carucci DJ, Cummings LM, Aravind L, Koonin EV, Shallom S, Mason T, Yu K, Fujii C, Pederson J, Shen K, Jing J, Aston C, Lai Z, Schwartz DC, Pertea M, Salzberg S, Zhou L, Sutton GG, Clayton R, White O, Smith HO, Fraser CM, Adams MD, Venter JC, Hoffman SL, Science 1998 282 1126 1132 9804551 (Pubitemid 28516242)
6. Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Crabb BS, Cowman AF, Proc Natl Acad Sci USA 1996 93 7289 7294 10.1073/pnas.93.14.7289 8692985 (Pubitemid 26243542)
7. A set of independent selectable markers for transfection of the human malaria parasite Plasmodium falciparum. Mamoun CB, Gluzman IY, Goyard S, Beverley SM, Goldberg DE, Proc Natl Acad Sci USA 1999 96 8716 8720 10.1073/pnas.96.15.8716 10411941 (Pubitemid 29354857)
8. Chloroquine resistance modulated in vitro by expression levels of the Plasmodium falciparum chloroquine resistance transporter. Waller KL, Muhle RA, Ursos LM, Horrocks P, Verdier-Pinard D, Sidhu ABS, Fujioka H, Roepe PD, Fidock DA, J Biol Chem 2003 278 33593 33601 10.1074/jbc.M302215200 12813054 (Pubitemid 37055813)
9. Analysis of the molecular mechanisms governing the stage-specific expression of a prototypical housekeeping gene during intraerythrocytic development of P. falciparum. Wong EH, Hasenkamp S, Horrocks P, J Mol Biol 2011 408 205 221 10.1016/j.jmb.2011.02.043 21354176
10. Has the time come for us to complement our malaria parasites? Goldberg DE, Janse CJ, Cowman AF, Waters AP, Trends Parasitol 2010 27 1 1 2 20667784
11. piggyBac is an effective tool for functional analysis of the Plasmodium falciparum genome. Balu B, Chauhan C, Maher S, Shoue D, Kissinger J, Fraser M, Adams J, BMC Microbiol 2009 9 83 10.1186/1471-2180-9-83 19422698
12. High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Balu B, Shoue DA, Fraser MJ, Adams JH, Proc Natl Acad Sci USA 2005 102 16391 16396 10.1073/pnas.0504679102 16260745 (Pubitemid 41688924)
13. Transfection of the human malaria parasite Plasmodium falciparum. Crabb BS, Rug M, Gilberger T-W, Thompson JK, Triglia T, Maier AG, Cowman AF, Methods Mol Biol 2004 270 263 276 15153633
14. E unum pluribus: multiple proteins from a self-processing polyprotein. De Felipe P, Luke GA, Hughes LE, Gani D, Halpin C, Ryan MD, Trends Biotechnol 2006 24 68 75 10.1016/j.tibtech.2005.12.006 16380176 (Pubitemid 43151978)
15. Site-specific genome editing in Plasmodium falciparum using engineered zinc-finger nucleases. Straimer J, Lee MCS, Lee AH, Zeitler B, Williams AE, Pearl JR, Zhang L, Rebar EJ, Gregory PD, Llinás M, Urnov FD, Fidock DA, Nat Methods 2012 9 993 998 10.1038/nmeth.2143 22922501
16. Recombination-mediated PCR-directed plasmid construction in vivo in yeast. Oldenburg KR, Vo KT, Michaelis S, Paddon C, Nucleic Acids Res 1997 25 451 452 10.1093/nar/25.2.451 9016579 (Pubitemid 27303343)
17. Enzymatic assembly of DNA molecules up to several hundred kilobases. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO, Nat Methods 2009 6 343 345 10.1038/nmeth.1318 19363495
18. Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nkrumah LJ, Muhle RA, Moura PA, Ghosh P, Hatfull GF, Jacobs WR, Fidock DA, Nat Methods 2006 3 615 621 10.1038/nmeth904 16862136 (Pubitemid 44123428)
19. A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes. O'Donnell RA, Freitas-Junior LH, Preiser PR, Williamson DH, Duraisingh M, McElwain TF, Scherf A, Cowman AF, Crabb BS, EMBO J 2002 21 1231 1239 10.1093/emboj/21.5.1231 11867551 (Pubitemid 34206196)
20. Centromere plasmid: a new genetic tool for the study of Plasmodium falciparum. Iwanaga S, Kato T, Kaneko I, Yuda M, PLoS ONE 2012 7 33326 10.1371/journal.pone.0033326 22479383
21. Malaria Research and Reference Reagent Resource Center (MR4). http://www.mr4.org
22. New yeast recombineering tools for bacteria. Shanks RMQ, Kadouri DE, MacEachran DP, O'Toole GA, Plasmid 2009 62 88 97 10.1016/j.plasmid.2009.05.002 19477196
23. Frozen competent yeast cells that can be transformed with high efficiency using the LiAc/SS carrier DNA/PEG method. Gietz RD, Schiestl RH, Nat Protoc 2007 2 1 4 17401330 (Pubitemid 47040061)
24. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Deitsch K, Driskill C, Wellems T, Nucleic Acids Res 2001 29 850 853 10.1093/nar/29.3.850 11160909 (Pubitemid 32124398)
25. Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Fidock DA, Wellems TE, Proc Natl Acad Sci USA 1997 94 10931 10936 10.1073/pnas.94.20.10931 9380737 (Pubitemid 27430838)
26. NIH Image to ImageJ: 25 years of image analysis. Schneider CA, Rasband WS, Eliceiri KW, Nat Methods 2012 9 671 675 10.1038/nmeth.2089 22930834
27. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, Handman E, Cowman AF, McFadden GI, Mol Biochem Parasitol 2004 137 13 21 10.1016/j.molbiopara.2004.05. 009 15279947 (Pubitemid 38987938)
28. Stable transgene expression in Plasmodium falciparum. Crabb BS, Triglia T, Waterkeyn JG, Cowman AF, Mol Biochem Parasitol 1997 90 131 144 10.1016/S0166-6851(97)00143-6 9497038 (Pubitemid 28044383)
29. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, Thompson JK, Freitas-Junior LH, Scherf A, Crabb BS, Cowman AF, Cell 2005 121 13 24 10.1016/j.cell.2005.01.036 15820675
30. Comparison of the absolute and relative efficiencies of electroporation-based transfection protocols for Plasmodium falciparum. Hasenkamp S, Russell KT, Horrocks P, Malar J 2012 11 210 10.1186/1475-2875-11- 210 22720754
31. Comparison of Plasmodium falciparum transfection methods. Skinner-Adams TS, Lawrie PM, Hawthorne PL, Gardiner DL, Trenholme KR, Malar J 2003 2 19 10.1186/1475-2875-2-19 12869208
32. Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, Vanin EF, Vignali DAA, Nat Biotechnol 2004 22 589 594 10.1038/nbt957 15064769 (Pubitemid 38585911)
33. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. Waller RF, Reed MB, Cowman AF, McFadden GI, EMBO J 2000 19 1794 1802 10.1093/emboj/19.8.1794 10775264 (Pubitemid 30204391)
34. Targeting GFP to the malarial mitochondrion. Sato S, Rangachari K, Wilson RJM, Mol Biochem Parasitol 2003 130 155 158 10.1016/S0166-6851(03)00166-X 12946854 (Pubitemid 37289135)
35. Function of the plasmodium export element can be blocked by green fluorescent protein. Knuepfer E, Rug M, Cowman AF, Mol Biochem Parasitol 2005 142 258 262 10.1016/j.molbiopara.2005.04.005 15951034 (Pubitemid 40835918)
36. Inhibition of 2A-mediated 'cleavage' of certain artificial polyproteins bearing N-terminal signal sequences. de Felipe P, Luke GA, Brown JD, Ryan MD, Biotechnol J 2010 5 213 223 10.1002/biot.200900134 19946875
37. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. Fernandez V, Hommel M, Chen Q, Hagblom P, Wahlgren M, J Exp Med 1999 190 1393 1404 10.1084/jem.190.10.1393 10562315
38. The Plasmodium falciparum STEVOR multigene family mediates antigenic variation of the infected erythrocyte. Niang M, Yan Yam X, Preiser PR, PLoS Pathog 2009 5 1000307 10.1371/journal.ppat.1000307 19229319
39. A post-genomic view of the mitochondrion in malaria parasites. Vaidya AB, Mather MW, Curr Top Microbiol Immunol 2005 295 233 250 10.1007/3-540-29088-5-9 16265893 (Pubitemid 41236517)
40. Metabolic maps and functions of the Plasmodium mitochondrion. van Dooren GG, Stimmler LM, McFadden GI, FEMS Microbiol Rev 2006 30 596 630 10.1111/j.1574-6976.2006.00027.x 16774588 (Pubitemid 43855768)
41. Plasmodium falciparum apicoplast drugs: targets or off-targets? Botté CY, Dubar F, McFadden GI, Maréchal E, Biot C, Chem Rev 2012 112 1269 1283 10.1021/cr200258w 22026508
42. An alternative model for heme biosynthesis in the malarial parasite. Padmanaban G, Nagaraj VA, Rangarajan PN, Trends Biochem Sci 2007 32 443 449 10.1016/j.tibs.2007.09.005 17928230 (Pubitemid 47588947)
43. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, Szestak T, Chesson J, Wu Y, Hughes K, Coppel RL, Newbold C, Beeson JG, Craig A, Crabb BS, Cowman AF, Cell 2008 134 48 61 10.1016/j.cell.2008.04.051 18614010 (Pubitemid 351905737)