Site-specific genome editing in Plasmodium falciparum using engineered zinc-finger nucleases

Nature Methods

Volumn 9, Issue 10, 2012, Pages 993-998

  Straimer, Judith ^a   Lee, Marcus C S ^a   Lee, Andrew H ^a   Zeitler, Bryan ^b   Williams, April E ^c   Pearl, Jocelynn R ^b   Zhang, Lei ^b   Rebar, Edward J ^b   Gregory, Philip D ^b   Llinás, Manuel ^c   Urnov, Fyodor D ^b   Fidock, David A ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

^b SANGAMO BIOSCIENCES INC   (United States)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; ZINC FINGER NUCLEASE;

ALLELE; ARTICLE; DOUBLE STRANDED DNA BREAK; EGFP GENE; GENE; GENE DELETION; GENE LOCUS; GENE TARGETING; GENETIC ENGINEERING; GENOME; NONHUMAN; PFCRT GENE; PLASMODIUM FALCIPARUM; POINT MUTATION; PRIORITY JOURNAL; PROTOZOAL GENETICS;

ALLELES; BASE SEQUENCE; CHLOROQUINE; DRUG RESISTANCE; ENDONUCLEASES; GENOME, PROTOZOAN; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTEIN ENGINEERING; ZINC FINGERS;

PLASMODIUM FALCIPARUM;

EID: 84867085052     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.2143     Document Type: Article

References (39)

1. Dondorp, A.M. et al. The threat of artemisinin-resistant malaria. N. Engl. J. Med. 365, 1073-1075 (2011).
2. Meissner, M., Breinich, M.S., Gilson, P.R. & Crabb, B.S. Molecular genetic tools in Toxoplasma and Plasmodium: achievements and future needs. Curr. Opin. Microbiol. 10, 349-356 (2007).
3. Anderson, T., Nkhoma, S., Ecker, A. & Fidock, D. How can we identify parasite genes that underlie antimalarial drug resistance? Pharmacogenomics 12, 59-85 (2011).
4. Bibikova, M., Golic, M., Golic, K.G. & Carroll, D. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161, 1169-1175 (2002).
5. Carroll, D. Genome engineering with zinc-finger nucleases. Genetics 188, 773-782 (2011).
6. Miller, J.C. et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 25, 778-785 (2007).
7. Doyon, Y. et al. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat. Methods 8, 74-79 (2011).
8. Urnov, F.D. et al. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646 (2010).
9. Gardner, M.J. et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511 (2002).
10. Mimitou, E.P. & Symington, L.S. DNA end resection: many nucleases make light work. DNA Repair (Amst.) 8, 983-995 (2009).
11. Szymczak, A.L. et al. Correction of multi-gene deficiency in vivo using a single ′self-cleaving′ 2A peptide-based retroviral vector. Nat. Biotechnol. 22, 589-594 (2004).
12. Adjalley, S.H. et al. Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc. Natl. Acad. Sci. USA 108, E1214-E1223 (2011).
13. Fidock, D.A., Nomura, T. & 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, 1140-1147 (1998).
14. Deitsch, K., Driskill, C. & Wellems, T. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res. 29, 850-853 (2001).
15. Fidock, D.A. et al. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol. Cell 6, 861-871 (2000).
16. Bray, P.G. et al. Defining the role of PfCRT in Plasmodium falciparum chloroquine resistance. Mol. Microbiol. 56, 323-333 (2005).
17. Summers, R.L., Nash, M.N. & Martin, R.E. Know your enemy: understanding the role of PfCRT in drug resistance could lead to new antimalarial tactics. Cell. Mol. Life Sci. 69, 1967-1995 (2012).
18. Sidhu, A.B.S., Verdier-Pinard, D. & Fidock, D.A. Chloroquine resistance in Plasmodium falciparum malaria parasites conferred by pfcrt mutations. Science 298, 210-213 (2002).
19. Valderramos, S.G. et al. Identification of a mutant PfCRT-mediated chloroquine tolerance phenotype in Plasmodium falciparum. PLoS Pathog. 6, e1000887 (2010).
20. Doyon, J.B. et al. Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat. Cell Biol. 13, 331-337 (2011).
21. Doyon, Y. et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat. Biotechnol. 26, 702-708 (2008).
22. Cooper, R.A. et al. 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 (2002).
23. Martin, R.E. et al. Chloroquine transport via the malaria parasite′s chloroquine resistance transporter. Science 325, 1680-1682 (2009).
24. Sá, J.M. et al. Geographic patterns of Plasmodium falciparum drug resistance distinguished by differential responses to amodiaquine and chloroquine. Proc. Natl. Acad. Sci. USA 106, 18883-18889 (2009).
25. Elliott, B. et al. Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell. Biol. 18, 93-101 (1998).
26. Carvalho, T.G. & Menard, R. Manipulating the Plasmodium genome. Curr. Issues Mol. Biol. 7, 39-55 (2005).
27. Sidhu, A.B.S., Valderramos, S.G. & Fidock, D.A. pfmdr1 mutations contribute to quinine resistance and enhance mefloquine and artemisinin sensitivity in Plasmodium falciparum. Mol. Microbiol. 57, 913-926 (2005).
28. Urnov, F.D. et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651 (2005).
29. Geurts, A.M. et al. Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325, 433 (2009).
30. Lee, M.C., Moura, P.A., Miller, E.A. & Fidock, D.A. Plasmodium falciparum Sec24 marks transitional ER that exports a model cargo via a diacidic motif. Mol. Microbiol. 68, 1535-1546 (2008).
31. Ecker, A. et al. Evidence that mutant PfCRT facilitates the transmission to mosquitoes of chloroquine-treated Plasmodium gametocytes. J. Infect. Dis. 203, 228-236 (2011).
32. Nkrumah, L.J. et al. Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat. Methods 3, 615-621 (2006).
33. Oyola, S.O. et al. Optimizing Illumina next-generation sequencing library preparation for extremely AT-biased genomes. BMC Genomics 13, 1 (2012).
34. Goecks, J., Nekrutenko, A. & Taylor, J. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 11, R86 (2010).
35. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
36. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
37. DePristo, M.A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
38. Robinson, J.T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26 (2011).
39. Ekland, E.H., Schneider, J. & Fidock, D.A. Identifying apicoplast-targeting antimalarials using high-throughput compatible approaches. FASEB J. 25, 3583-3593 (2011).