Nuclear gene targeting in Chlamydomonas using engineered zinc-finger nucleases

Plant Journal

Volumn 73, Issue 5, 2013, Pages 873-882

  Sizova, Irina ^a,c   Greiner, Andre ^a   Awasthi, Mayanka ^b   Kateriya, Suneel ^b   Hegemann, Peter ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF DELHI   (India)

^c RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

Author keywords

channelrhodopsin 1; Chlamydomonas reinhardtii; homologous recombination; light sensing; non homologous end joining; photoreceptors; technical advance

Indexed keywords

CHANNELRHODOPSIN-1; CHLAMYDOMONAS REINHARDTII; HOMOLOGOUS RECOMBINATION; LIGHT SENSING; NONHOMOLOGOUS END JOINING; PHOTORECEPTORS; TECHNICAL ADVANCES;

CLONING; GALLIUM ALLOYS; ZINC;

GENES;

ALGAL PROTEIN; ANTIBODY; ENDONUCLEASE; KANAMYCIN KINASE; PAROMOMYCIN; RECOMBINANT PROTEIN; ZINC FINGER PROTEIN;

ANIMAL; ARTICLE; CELL NUCLEUS; CHLAMYDOMONAS REINHARDTII; DRUG EFFECT; GENE TARGETING; GENETIC ENGINEERING; GENETIC TRANSFORMATION; GENETICS; HOMOLOGOUS RECOMBINATION; IMMUNOLOGY; METHODOLOGY; MUTAGENESIS; RABBIT; TRANSGENIC ORGANISM;

ALGAL PROTEINS; ANIMALS; ANTIBODIES; CELL NUCLEUS; CHLAMYDOMONAS REINHARDTII; ENDONUCLEASES; GENE TARGETING; GENETIC ENGINEERING; HOMOLOGOUS RECOMBINATION; KANAMYCIN KINASE; MUTAGENESIS; ORGANISMS, GENETICALLY MODIFIED; PAROMOMYCIN; RABBITS; RECOMBINANT PROTEINS; TRANSFORMATION, GENETIC; ZINC FINGERS;

ALGAE; CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

EID: 84874478059     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12066     Document Type: Article

References (43)

1. Bartsch, S., Kang, L.E., and, Symington, L.S., (2000) RAD51 is required for the repair of plasmid double-stranded DNA gaps from either plasmid or chromosomal templates. Mol. Cell. Biol. 20, 1194-1205. (Pubitemid 30069240)
2. Berthold, P., Tsunoda, S.P., Ernst, O.P., Mages, W., Gradmann, D., and, Hegemann, P., (2008) Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization. Plant Cell, 20, 1665-1677. (Pubitemid 352844170)
3. Bibikova, M., Golic, M., Golic, K.G., and, Carroll, D., (2002) Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics, 161, 1169-1175. (Pubitemid 34831440)
4. Cao, M., Fu, Y., Guo, Y., and, Pan, J., (2009) Chlamydomonas (Chlorophyceae) colony PCR. Protoplasma, 235, 107-110.
5. Carroll, D., (2011) Zinc-finger nucleases: a panoramic view. Curr. Gene Ther. 11, 2-10.
6. Cerutti, H., Ma, X., Msanne, J., and, Repas, T., (2011) RNA-mediated silencing in algae: biological roles and tools for analysis of gene function. Eukaryot. Cell, 10, 1164-1172.
7. Ebnet, E., Fischer, M., Deininger, W., and, Hegemann, P., (1999) Volvoxrhodopsin, a light-regulated sensory photoreceptor of the spheroidal green alga Volvox carteri. Plant Cell, 11, 1473-1484.
8. Einhauer, A., and, Jungbauer, A., (2001) The FLAG peptide, a versatile fusion tag for the purification of recombinant proteins. J. Biochem. Biophys. Methods 49, 455-465. (Pubitemid 33022564)
9. Gonzalez-Ballester, D., Pootakham, W., Mus, F., et al,. (2011) Reverse genetics in Chlamydomonas: a platform for isolating insertional mutants. Plant Methods, 7, 24.
10. Guo, J., Gaj, T., and, Barbas, C.F. 3rd., (2010) Directed evolution of an enhanced and highly efficient FokI cleavage domain for zinc finger nucleases. J. Mol. Biol. 400, 96-107.
11. Halford, S.E., Catto, L.E., Pernstich, C., Rusling, D.A., and, Sanders, K.L., (2011) The reaction mechanism of FokI excludes the possibility of targeting zinc finger nucleases to unique DNA sites. Biochem. Soc. Trans. 39, 584-588.
12. Handel, E.M., and, Cathomen, T., (2011) Zinc-finger nuclease based genome surgery: it's all about specificity. Curr. Gene Ther. 11, 28-37.
13. Huang, K., and, Beck, C.F., (2003) Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 100, 6269-6274. (Pubitemid 36576965)
14. Kim, Y.G., Cha, J., and, Chandrasegaran, S., (1996) Hybrid restriction enzymes: zinc finger fusions to FokI cleavage domain. Proc. Natl Acad. Sci. USA, 93, 1156-1160. (Pubitemid 26052857)
15. Kim, M.S., Stybayeva, G., Lee, J.Y., Revzin, A., and, Segal, D.J., (2011) A zinc finger protein array for the visual detection of specific DNA sequences for diagnostic applications. Nucleic Acids Res. 39, e29.
16. Kindle, K.L., (1990) High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 87, 1228-1232.
17. Kurowska, M., Daszkowska-Golec, A., Gruszka, D., Marzec, M., Szurman, M., Szarejko, I., and, Maluszynski, M., (2011) TILLING: a shortcut in functional genomics. J. Appl. Genet. 52, 371-390.
18. Lam, K.N., van Bakel, H., Cote, A.G., van der Ven, A., and, Hughes, T.R., (2011) Sequence specificity is obtained from the majority of modular C2H2 zinc-finger arrays. Nucleic Acids Res. 39, 4680-4690.
19. Maeder, M.L., Thibodeau-Beganny, S., Osiak, A., et al,. (2008) Rapid 'open-source' engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol. Cell 31, 294-301. (Pubitemid 352001401)
20. Maeder, M.L., Thibodeau-Beganny, S., Sander, J.D., Voytas, D.F., and, Joung, J.K., (2009) Oligomerized pool engineering (OPEN): an 'open-source' protocol for making customized zinc-finger arrays. Nat. Protoc. 4, 1471-1501.
21. Miller, J.C., Holmes, M.C., Wang, J., et al,. (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 25, 778-785. (Pubitemid 47052191)
22. Nagel, G., Ollig, D., Fuhrmann, M., Kateriya, S., Musti, A.M., Bamberg, E., and, Hegemann, P., (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science, 296, 2395-2398. (Pubitemid 34734214)
23. Perez-Pinera, P., Ousterout, D.G., Brown, M.T., and, Gersbach, C.A., (2012) Gene targeting to the ROSA26 locus directed by engineered zinc finger nucleases. Nucleic Acids Res. 40, 3741-3752.
24. Ramirez, C.L., Foley, J.E., Wright, D.A., et al,. (2008) Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods 5, 374-375. (Pubitemid 351619087)
25. Ramirez, C.L., Certo, M.T., Mussolino, C., Goodwin, M.J., Cradick, T.J., McCaffrey, A.P., Cathomen, T., Scharenberg, A.M., and, Joung, J.K., (2012) Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effects. Nucleic Acids Res. 40, 5560-5568.
26. Richardson, C., and, Jasin, M., (2000) Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol. 20, 9068-9075. (Pubitemid 32245935)
27. Richardson, C., Moynahan, M.E., and, Jasin, M., (1998) Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12, 3831-3842. (Pubitemid 29024846)
28. Sander, J.D., Zaback, P., Joung, J.K., Voytas, D.F., and, Dobbs, D., (2007) Zinc Finger Targeter (ZiFiT): an engineered zinc finger/target site design tool. Nucleic Acids Res. 35, W599-W605.
29. Sander, J.D., Zaback, P., Joung, J.K., Voytas, D.F., and, Dobbs, D., (2009) An affinity-based scoring scheme for predicting DNA-binding activities of modularly assembled zinc-finger proteins. Nucleic Acids Res. 37, 506-515.
30. Schroda, M., (2006) RNA silencing in Chlamydomonas: mechanisms and tools. Curr. Genet. 49, 69-84. (Pubitemid 43150117)
31. Schroda, M., Blöcker, D., and, Beck, C.F., (2000) The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J. 21, 121-131. (Pubitemid 30121306)
32. Sizova, I., Fuhrmann, M., and, Hegemann, P., (2001) A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene, 277, 221-229. (Pubitemid 32972123)
33. Snell, W.J., Pan, J., and, Wang, Q., (2004) Cilia and flagella revealed: from flagellar assembly in Chlamydomonas to human obesity disorders. Cell, 117, 693-697. (Pubitemid 38748886)
34. Symington, L.S., and, Gautier, J., (2011) Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271.
35. Takashima, Y., Sakuraba, M., Koizumi, T., Sakamoto, H., Hayashi, M., and, Honma, M., (2009) Dependence of DNA double strand break repair pathways on cell cycle phase in human lymphoblastoid cells. Environ. Mol. Mutagen. 50, 815-822.
36. Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S., and, Gregory, P.D., (2010) Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636-646.
37. Wah, D.A., Hirsch, J.A., Dorner, L.F., Schildkraut, I., and, Aggarwal, A.K., (1997) Structure of the multimodular endonuclease FokI bound to DNA. Nature, 388, 97-100. (Pubitemid 27283896)
38. Wolfe, S.A., Nekludova, L., and, Pabo, C.O., (2000) DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29, 183-212. (Pubitemid 30599592)
39. Wright, D.A., Townsend, J.A., Winfrey, R.J., Irwin, P.A., Rajagopal, J., Lonosky, P.M., Hall, B.D., Jondle, M.D., and, Voytas, D.F., (2005) High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J. 44, 693-705.
40. Zhang, F., Vierock, J., Yizhar, O., et al. (2011) The microbial opsin family of optogenetic tools. Cell, 147, 1446-1457.
41. Zorin, B., Hegemann, P., and, Sizova, I., (2005) Nuclear-gene targeting by using single-stranded DNA avoids illegitimate DNA integration in Chlamydomonas reinhardtii. Eukaryot. Cell 4, 1264-1272. (Pubitemid 41004139)
42. Zorin, B., Lu, Y., Sizova, I., and, Hegemann, P., (2009) Nuclear gene targeting in Chlamydomonas as exemplified by disruption of the PHOT gene. Gene, 432, 91-96.
43. Zou, J., Maeder, M.L., Mali, P., et al. (2009) Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell, 5, 97-110.