TALEN and CRISPR/Cas Genome Editing Systems: Tools of Discovery
- Authors: Nemudryi A.A.1,2,3, Valetdinova K.R.1,2,3,4, Medvedev S.P.1,2,3,4, Zakian S.M.1,2,3,4
-
Affiliations:
- Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences
- Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences
- Meshalkin Novosibirsk State Research Institute of Circulation Pathology, Ministry of Health of the Russian Federation
- Novosibirsk State University
- Issue: Vol 6, No 3 (2014)
- Pages: 19-40
- Section: Reviews
- Submitted: 17.01.2020
- Published: 15.09.2014
- URL: https://actanaturae.ru/2075-8251/article/view/10529
- DOI: https://doi.org/10.32607/20758251-2014-6-3-19-40
- ID: 10529
Cite item
Abstract
Precise studies of plant, animal and human genomes enable remarkable opportunities of obtained data application in biotechnology and medicine. However, knowing nucleotide sequences isn’t enough for understanding of particular genomic elements functional relationship and their role in phenotype formation and disease pathogenesis. In post-genomic era methods allowing genomic DNA sequences manipulation, visualization and regulation of gene expression are rapidly evolving. Though, there are few methods, that meet high standards of efficiency, safety and accessibility for a wide range of researchers. In 2011 and 2013 novel methods of genome editing appeared - this are TALEN (Transcription Activator-Like Effector Nucleases) and CRISPR (Clustered Regulatory Interspaced Short Palindromic Repeats)/Cas9 systems. Although TALEN and CRISPR/Cas9 appeared recently, these systems have proved to be effective and reliable tools for genome engineering. Here we generally review application of these systems for genome editing in conventional model objects of current biology, functional genome screening, cell-based human hereditary disease modeling, epigenome studies and visualization of cellular processes. Additionally, we review general strategies for designing TALEN and CRISPR/Cas9 and analyzing their activity. We also discuss some obstacles researcher can face using these genome editing tools.
Keywords
About the authors
A. A. Nemudryi
Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences; Meshalkin Novosibirsk State Research Institute of Circulation Pathology, Ministry of Health of the Russian Federation
Author for correspondence.
Email: zakian@bionet.nsc.ru
Россия
K. R. Valetdinova
Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences; Meshalkin Novosibirsk State Research Institute of Circulation Pathology, Ministry of Health of the Russian Federation; Novosibirsk State University
Email: zakian@bionet.nsc.ru
Россия
S. P. Medvedev
Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences; Meshalkin Novosibirsk State Research Institute of Circulation Pathology, Ministry of Health of the Russian Federation; Novosibirsk State University
Email: zakian@bionet.nsc.ru
Россия
S. M. Zakian
Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences; Meshalkin Novosibirsk State Research Institute of Circulation Pathology, Ministry of Health of the Russian Federation; Novosibirsk State University
Email: zakian@bionet.nsc.ru
Россия
References
- Capecchi M.R. // Nat. Rev. Genet. 2005, V.6, №6, P.507-512
- Kim Y.G., Cha J., Chandrasegaran S. // Proc. Natl. Acad. Sci. USA. 1996, V.93, №3, P.1156-1160
- Bibikova M., Golic M., Golic K.G., Carroll D. // Genetics. 2002, V.161, №3, P.1169-1175
- Townsend J.A., Wright D.A., Winfrei R.J., Fu F., Maeder M.L., Joung J.K., Voytas D.F. // Nature 2009, V.459, №7245, P.442-445
- Zhang F., Maeder M.L., Unger-Wallace E., Hoshaw J.P., Reyon D., Christian M., Li X., Pierick C.J., Dobbs D., Peterson T. // Proc. Natl. Acad. Sci. USA. 2010, V.107, №26, P.12028-12033
- Torikai H., Reik A., Liu P.Q., Zhou Y., Zhang L., Maiti S., Huls H., Miller J.C., Kebriaei P., Rabinovitch B. // Blood. 2012, V.119, №24, P.5697-5705
- Provasi E., Genovese P., Lombardo A., Magnani Z., Liu P.Q., Reik A., Chu V., Paschon D.E., Zhang L., Kuball J. // Nat. Med. 2012, V.18, №5, P.807-815
- Lombardo A., Cesana D., Genovese P., Di Stefano B., Provasi E., Colombo D.F., Neri M., Magnani Z., Cantore A., Lo Riso P. // Nat. Methods. 2011, V.8, №10, P.861-869
- Becker M. // Nat. Methods. 2012, V.9, №1, P.1
- Schornack S., Meyer A., Römer P., Jordan T., Lahaye T. // J. Plant Physiol. 2006, V.163, №3, P.256-272
- Romer P., Hahn S., Jordan T., Strauss T., Bonas U., Lahaye T. // Science. 2007, V.318, №5850, P.645-648
- Boch J., Scholze H., Schornack S., Landgraf A., Hahn S., Kay S., Lahaye T., Nickstandt A., Bonas U. // Science. 2009, V.326, №5959, P.1509-1512
- Moscou M.J., Bogdanove A.J. // Science. 2009, V.326, №5959, P.1501
- Lamb B.M., Mercer A.C., Barbas C.F. // Nucleic Acids Res. 2013, V.41, №21, P.9779-9785
- Christian M., Cermak T., Doyle E.L., Schmidt C., Zhang F., Hummel A., Bogdanove A.J., Voytas D.F. // Genetics. 2010, V.186, №2, P.757-761
- Cong L., Zhou R., Kuo Y.C., Cunniff M.M., Zhang F. // Nat. Commun. 2012, V.3, P.968
- Christian M.L., Demorest Z.L., Starker C.G., Osborn M.J., Nyquist M.D., Zhang Y., Carlson D.F., Bradley P., Bogdanove A.J., Voytas D.F. // PLoS One. 2012, V.7, №9, P.e45383
- Streubel J., Blucher C., Landgraf A., Boch J. // Nat. Biotechnol. 2012, V.30, №7, P.593-595
- Mak A.N., Bradley P., Cernadas R.A., Bogdanove A.J., Stoddard B.L. // Science. 2012, V.335, №6069, P.716-719
- Ishino Y., Shinagawa H., Makino K., Amemura M., Nakata A. // Journal of Bacteriology 1987, V.169, №2, P.5429-5433
- Haft D.H., Selengut J., Mongodin E.F., Nelson K.E. // PLoS Comput. Biol. 2005, V.1, №6, P.e60
- Bolotin A., Quinguis B., Sorokin A., Ehrlich S.D. // Microbiology. 2005, V.151, P.2551-2561
- Mojica F.J., Diez-Villasenor C., Garcia-Martinez J., Soria E. // J. Mol. Evol. 2005, V.60, №2, P.174-182
- Pourcel C., Salvignol G., Vergnaud G. // Microbiology. 2005, V.151, P.653-663
- Barrangou R., Flemaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P. // Science. 2007, V.315, №5819, P.1709-1712
- Grissa I., Vergnaud G., Pourcel C. // BMC Bioinformatics. 2007, V.8, P.172
- Makarova K.S., Haft D.H., Barrangou R., Brouns S.J., Charpentier E., Horvath P., Moineau S., Mojica F.J., Wolf Y.I., Yakunin A.F. // Nat. Rev. Microbiol. 2011, V.9, №6, P.467-477
- Mojica F.J., Diez-Villasenor C., Garcia-Martinez J., Almendros C. // Microbiology. 2009, V.155, P.733-740
- Swarts D.C., Mosterd C., van Passel M.W., Brouns S.J. // PLoS One. 2012. V. 7. № 4. 2012, V.7, №4, P.e35888
- Hale C.R., Majumdar S., Elmore J., Pfister N., Compton M., Olson S., Resch A.M., Glover C.V., Graveley B.R., Tern R.M. // Molecular Cell 2012, V.45, №3, P.292-302
- Lillestol R.K., Shah S.A., Brugger K., Redder P., Phan H., Christiansen J., Garrett R.A. // Mol. Microbiol. 2009, V.72, №1, P.259-272
- Carte J., Wang R., Li H., Terns R.M., Terns M.P. // Genes. Dev. 2008, V.22, №24, P.3489-3496
- Haurwitz R.E., Jinek M., Wiedenheft B., Zhou K., Doudna J.A. // Science. 2010, V.329, №5997, P.1355-1358
- Gesner E.M., Schellenberg M.J., Garside E.L., George M.M., Macmillan A.M. // Nat. Struct. Mol. Biol. 2011, V.18, №6, P.688-692
- Richter H., Zoephel J., Schermuly J., Maticzka D., Backofen R., Randau L. // Nucleic Acids Res. 2012, V.40, №19, P.9887-9896
- Sashital D.G., Jinek M., Doudna J.A. // Nat. Struct. Mol. Biol. 2011, V.18, №6, P.680-687
- Hale C.R., Zhao P., Olson S., Duff M.O., Graveley B.R., Wells L., Terns R.M., Terns M.P. // Cell. 2009, V.139, №5, P.945-956
- Makarova K.S., Grishin N.V., Shabalina S.A., Wolf Y.I., Koonin E.V. // Biol. Direct. 2006, V.1, P.7
- Marraffini L.A., Sontheimer E.J. // Nature 2010, V.463, №7280, P.568-571
- Bondy-Denomy J., Pawluk A., Maxwell K.L., Davidson A.R. // Nature 2013, V.493, №7432, P.429-432
- Makarova K.S., Aravind L., Wolf Y.I., Koonin E.V. // Biol. Direct. 2011, V.6, P.38
- Sapranauskas R., Gasiunas G., Fremaux C., Barrangou R., Horvath P., Siksnys V. // Nucleic Acids Res. 2011, V.39, №21, P.9275-9282
- Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. // Science. 2012, V.337, №6096, P.816-821
- Deltcheva E., Chylinski K., Sharma C.M., Gonzales K., Chao Y., Pirzada Z.A., Eckert M.R., Vogel J., Charpentier E. // Nature 2011, V.471, №7340, P.602-607
- Mussolino C., Cathomen T. // Curr. Opin. Biotechnol. 2012, V.23, №5, P.644-650
- Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A. // Science. 2013, V.339, №6121, P.819-823
- Hsu P.D., Scott D.A., Weinstein J.A., Ran F.A., Konermann S., Agarwala V., Li Y., Fine E.J., Wu X., Shalem O. // Nat. Biotechnol. 2013, V.31, №9, P.827-832
- Jiang W., Bikard D., Cox D., Zhang F., Marraffini L.A. // Nat. Biotechnol. 2013, V.31, №3, P.233-239
- Fu Y., Foden J.A., Khayter C., Maeder M.L., Reyon D., Joung J.K., Sander J.D. // Nat. Biotechnol. 2013, V.31, №9, P.822-826
- Mali P., Aach J., Stranges P.B., Esvelt K.M., Moosburner M., Kosuri S., Yang L., Church G.M. // Nat. Biotechnol. 2013, V.31, №9, P.833-838
- Ran F.A., Hsu P.D., Lin C., Gootenberg J.S., Konermann S., Trevino A.E., Scott D.A., Inoue A., Matoba S., Zhang Y. // Cell. 2013, V.154, №6, P.1380-1389
- Gasiunas G., Barrangou R., Horvath P., Siksnys V. // Proc. Natl. Acad. Sci. USA. 2012, V.109, №39, P.2579-2586
- Dianov G.L., Hubscher U. // Nucleic Acids Res. 2013, V.41, №6, P.3483-3490
- Doyle E.L., Booher N.J., Standage D.S., Voytas D.F., Brendel V.P., Vandyk J.K., Bogdanove A.J. // Nucleic Acids Res. 2012, V.40, P.117-122
- Fine E.J., Cradick T.J., Zhao C.L., Lin Y., Bao G. // Nucleic Acids Res. 2013, V.42, №6, P.e42
- Grau J., Boch J., Posch S. // Bioinformatics. 2013, V.29, №22, P.2931-2932
- Grau J., Wolf A., Reschke M., Bonas U., Posch S. // PLoS Comput. Biol. 2013, V.9, №3, P.e1002962
- Heigwer F., Kerr G., Walther N., Glaeser K., Pelz O., Breinig M., Boutros M. // Nucleic Acids Res. 2013, V.41, №20, P.e190
- Neff K.L., Argue D.P., Ma A.C., Lee H.B., Clark K.J., Ekker S.C. // BMC Bioinformatics. 2013, V.14, P.1
- Grissa I., Vergnaud G., Pourcel C. // Nucleic Acids Res. 2007, V.35, P.52-57
- Rousseau C., Gonnet M., Le Romancer M., Nicolas J. // Bioinformatics. 2009, V.25, №24, P.3317-3318
- Xiao A., Cheng Z., Kong L., Zhu Z., Lin S., Gao G., Zhang B. // Bioinformatics. 2014, V.30, №8, P.1180-1182
- Sander J.D., Cade L., Khayter C., Reyon D., Peterson R.T., Joung J.K., Yeh J.R. // Nat. Biotechnol. 2011, V.29, №8, P.697-698
- Reyon D., Khayter C., Regan M.R., Joung J.K., Sander J.D. // Curr. Protoc. Mol. Biol. 2012. C.12. U. 12.15. 2012
- Weber E., Engler C., Gruetzner R., Werner S., Marillonnet S. // PLoS One. 2011, V.6, №2, P.e16765
- Engler C., Gruetzner R., Kandzia R., Marillonnet S. // PLoS One. 2009, V.4, №5, P.e5553
- Zhang F., Cong L., Lodato S., Kosuri S., Church G.M., Arlotta P. // Nat. Biotechnol. 2011, V.29, №2, P.149-153
- Sanjana N.E., Cong L., Zhou Y., Cunniff M.M., Feng G., Zhang F. // Nature Protocols 2012, V.7, №1, P.171-192
- Schmid-Burgk J.L., Schmidt T., Kaiser V., Honing K., Hornung V. // Nat. Biotechnol. 2013, V.31, №1, P.76-81
- Cermak T., Doyle E.L., Christian M., Wang L., Zhang Y., Schmidt C., Baller J.A., Somia N.V., Bogdanove A.J., Voytas D.F. // Nucleic Acids Res. 2011, V.39, №12, P.e82
- Ding Q., Lee Y.K., Schaefer E.A., Peters D.T., Veres A., Kim K., Kuperwasser N., Motola D.L., Meissner T.B., Hendriks W.T. // Cell Stem Cell. 2013, V.12, №2, P.238-251
- Reyon D., Tsai S.Q., Khayter C., Foden J.A., Sander J.D., Joung J.K. // Nat. Biotechnol. 2012, V.30, №5, P.460-465
- Briggs A.W., Rios X., Chari R., Yang L., Zhang F., Mali P., Church G.M. // Nucleic Acids Res. 2012, V.40, №15, P.e117
- Wang Z., Li J., Huang H., Wang G., Jiang M., Yin S., Sun C., Zhang H., Zhuang F., Xi J.J. // Angew. Chem. Int. Ed. Engl. 2012, V.51, №34, P.8505-8508
- Jinek M., Doudna J.A. // Nature 2009, V.457, №7228, P.405-412
- Malone C.D., Hannon G.J. // Cell. 2009, V.136, №4, P.656-668
- Meister G., Tuschl T. // Nature 2004, V.431, №7006, P.343-349
- Cho S.W., Kim S., Kim J.M., Kim J.S. // Nat. Biotechnol. 2013, V.31, №3, P.230-232
- Jinek M., East A., Cheng A., Lin S., Ma E., Doudna J. // Elife. 2013, V.2, P.e00471
- Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. // Science. 2013, V.339, №6121, P.823-826
- Chang N., Sun C., Gao L., Zhu D., Xu X., Zhu X., Xiong J.W., Xi J.J. // Cell Res. 2013, V.23, №4, P.465-472
- Hwang W.Y., Fu Y., Reyon D., Maeder M.L., Tsai S.Q., Sander J.D., Peterson R.T., Yeh J.R., Joung J.K. // Nat. Biotechnol. 2013, V.31, №3, P.227-229
- Wang H., Yang H., Shivalia S.C., Dawlaty M.M., Cheng W.A., Zhang F., Jaenisch R. // Cell. 2013, V.153, №4, P.910-918
- Shalem O., Sanjana N.E., Hartenian E., Shi X., Scott D.A., Mikkelsen T.S., Heckl D., Ebert B.L., Root D.E., Doench J.G. // Science. 2014, V.343, №6166, P.84-87
- Wang T., Wei J.J., Sabatini D.M., Lander E.S. // Science. 2014, V.343, №6166, P.80-84
- Shan Q., Wang Y., Li J., Zhang Y., Chen K., Liang Z., Zhang K., Liu J., Xi J.J., Qiu J.L. // Nat. Biotechnol. 2013, V.31, №8, P.686-688
- Mao Y., Zhang H., Xu N., Zhang B., Gao F., Zhu J.K. // Mol. Plant. 2013, V.6, №6, P.2008-2011
- Li J.F., Norville J.E., Aach J., McCormack M., Zhang D., Bush J., Church G.M., Sheen J. // Nat. Biotechnol. 2013, V.31, №8, P.688-691
- Nekrasov V., Staskawicz B., Weigel D., Jones J.D., Kamoun S. // Nat. Biotechnol. 2013, V.31, №8, P.691-369
- Lieber M.R. // Annu. Rev. Biochem. 2010, V.79, P.181-211
- Ousterout D.G., Perez-Pinera P., Thakore P.I., Kabadi A.M., Brown M.T., Qin X., Fedrigo O., Mouly V., Tremblay J.P., Gersbach C.A. // Molecular Therapy 2013, V.21, №9, P.1718-1726
- Kim H., Um E., Cho S.R., Jung C., Kim H., Kim J.S. // Nat. Methods. 2011, V.8, №11, P.941-943
- Guschin D.Y., Waite A.J., Katibah G.E., Miller J.C., Holmes M.C., Rebar E.J. // Methods Mol. Biol. 2010, V.649, P.247-256
- Dahlem T.J., Hoshijima K., Jurynec M.J., Gunther D., Starker C.G., Locke A.S., Weis A.M., Voytas D.F., Grunwald D.J. // PLoS Genet. 2012, V.8, №8, P.e1002861
- Ota S., Hisano Y., Muraki M., Hoshijima K., Dahlem T.J., Grunwald D.J., Kawahara A. // Genes Cells. 2013, V.18, №6, P.450-458
- Kim H.J., Lee H.J., Kim H., Cho S.W., Kim J.S. // Genome Res. 2009, V.19, №7, P.1279-1288
- Hisano Y., Ota S., Arakawa K., Muraki M., Kono N., Oshita K., Sakuma T., Tomita M., Yamamoto T., Okada Y. // Biol. Open. 2013, V.2, №4, P.363-367
- Yang L., Guell M., Byrne S., Yang J.L., De Los Angeles A., Mali P., Aach J., Kim-Kiselak C., Briggs A.W., Rios X. // Nucleic Acids Res. 2013, V.41, №19, P.9049-9061
- Saleh-Gohari N., Helleday T. // Nucleic Acids Res. 2004, V.32, №12, P.3683-3688
- Perez E.E., Wang J., Miller J.C., Jouvenot Y., Kim K.A., Liu O., Wang N., Lee G., Bartsevich V.V., Lee Y.L. // Nat. Biotechnol. 2008, V.26, №7, P.808-816
- Cristea S., Freyvert Y., Santiago Y., Holmes M.C., Urnov F.D., Gregory P.D., Cost G.J. // Biotechnology and Bioengineering 2013, V.110, №3, P.871-880
- Maresca M., Lin V.G., Guo N., Yang Y. // Genome Res. 2013, V.23, №3, P.539-546
- Chen F., Pruett-Miller S.M., Huang Y., Gjoka M., Taunton J., Collinwood T.N., Frodin M., Davis G.D. // Nat. Methods. 2011, V.8, №9, P.753-755
- Moehle E.A., Rock J.M., Lee Y.L., Jouvenot Y., DeKelver R.C., Gregory P.D., Urnov F.D., Holmes M.C. // Proc. Natl. Acad. Sci. USA. 2007, V.104, №9, P.3055-3060
- Orlando S.J., Santiago Y., DeKelver R.C., Freyvert Y., Boydston E.A., Moehle E.A., Choi V.M., Gopalan S.M., Lou J.F., Li J. // Nucleic Acids Res. 2010. V. 38. № 15. 2010, V.38, №15, P.e152
- Hu R., Wallace J., Dahlem T.J., Grunwald D.J., O’Connell R.M. // PLoS One. 2013. V. 8. № 5. 2013, V.8, №5, P.e63074
- Bloom K., Ely A., Mussolino C., Cathomen T., Arbuthnot P. // Molecular Therapy 2013, V.21, №10, P.1889-1897
- Schiffer J.T., Aubert M., Weber N.D., Mintzer E., Stone D., Jerome K.R. // Virology Journal 2012, V.86, №17, P.8920-8936
- Holt N., Wang J., Kim K., Friedman G., Wang X., Taupin V., Crooks G.M., Kohn D.B., Gregory P.D., Holmes M.C. // Nat. Biotechnol. 2010, V.28, №8, P.839-847
- Horii T., Tamura D., Morita S., Kimura M., Hatada I. // Int. J. Mol. Sci. 2013, V.14, №10, P.19774-19781
- Schwank G., Koo B.K., Sasselli V., Dekkers J.F., Heo I., Demircan T., Sasaki N., Boymans S., Cuppen E., van der Ent C.K. // Cell Stem Cell. 2013, V.13, №6, P.653-658
- Gilbert L.A., Larson M.H., Morsut L., Liu Z., Brar G.A., Torres S.E., Stern-Ginossar N., Brandman O., Whitehead E.H., Doudna J.A. // Cell. 2013, V.154, №2, P.442-451
- Bikard D., Jiang W., Samai P., Hochschild A., Zhang F., Marraffini L.A. // Nucleic Acids Res. 2013, V.41, №15, P.7429-7437
- Perez-Pinera P., Kocak D.D., Vockley C.M., Adler A.F., Kabadi A.M., Polstein L.R., Thakore C.A. // Nat. Methods. 2013, V.10, №10, P.973-976
- Farzadfard F., Perli S.D., Lu T.K. // ACS Synth. Biol. 2013, V.2, №10, P.604-613
- Heintze J., Luft C., Ketteler R. // Front Genet. 2013, V.4, P.193
- Chen B., Gilbert L.A., Cimini B.A., Schnitzbauer J., Zhang W., Li. G.W., Park J., Blackburn E.H., Weissman J.S., Qi L.S. // Cell. 2013, V.155, №7, P.1479-1491
- Smith J.R., Maguire S., Davis L.A., Alexander M., Yang F., Chandran S., Ffrench-Constant C., Pedersen R.A. // Stem Cells. 2008, V.26, №2, P.496-504
- Chiu H., Schwartz H.T., Antoshechkin I., Sternberg P.W. // Genetics. 2013, V.195, №3, P.1167-1171
- Cho S.W., Lee J., Carroll D., Kim J., Lee J. // Genetics. 2013, V.195, №3, P.1177-1180
- Katic I., Grosshans H. // Genetics. 2013, V.195, №3, P.1173-1176
- Lo T.W., Pickle C.S., Lin S., Ralston E.J., Gurling M., Schartner C.M., Bian Q., Doudna J.A., Meyer B.J. // Genetics. 2013, V.195, №2, P.331-348
- Tzur Y.B., Friedland A.E., Nadarajan S., Church G.M., Calarco J.A., Colaiácovo M.P. // Genetics. 2013, V.195, №3, P.1181-1185
- Waaijers S., Portegijs V., Kerver J., Lemmens B.B., Tijsterman M., van den Heuvel S., Boxem M. // Genetics. 2013, V.195, №3, P.11887-11891
- Dickinson D.J., Ward J.D., Reiner D.J., Goldstein B. // Nat. Methods. 2013, V.10, №10, P.1028-1034
- Friedland A.E., Tzur Y.B., Esvelt K.M., Colaiácovo M.P., Church G.M., Calarco J.A. // Nat. Methods. 2013, V.10, №8, P.741-743
- Maggert K.A., Gong W.J., Golic K.G. // Methods Mol. Biol. 2008, V.420, P.155-174
- Rong Y.S., Golic K.G. // Science. 2000, V.288, №5473, P.2013-2018
- Venken K.J., Bellen H.J. // Nat. Rev. Genet. 2005, V.6, №3, P.167-178
- Bassett A.R., Tibbit C., Ponting C.P., Liu J. // Cell Rep. 2013, V.4, №1, P.220-228
- Gratz S.J., Cummings A.M., Nguyen J.N., Hamm D.C., Donohue L.K., Harrison M.M., Wildonger J., O’Connor-Giles K.M. // Genetics. 2013, V.194, №4, P.1029-1035
- Yu Z., Ren M., Wang Z., Zhang B., Rong Y.S., Jiao R., Gao G. // Genetics. 2013, V.195, №1, P.289-291
- Ren X., Sun J., Housden B.E., Hu Y., Roesel C., Liu L.P., Yang Z., Mao D., Sun L., Wu Q. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №47, P.19012-19017
- Seth A., Stemple D.L., Barroso I. // Dis. Model. Mech. 2013, V.6, №5, P.1080-1088
- Copeland N.G., Jenkins N.A. // Nat. Rev. Cancer. 2010, V.10, №10, P.696-706
- Kool J., Berns A. // Nat. Rev. Cancer. 2009, V.9, №6, P.389-399
- Bogdanove A.J., Voytas D.F. // Science. 2011, V.333, №6051, P.1843-1846
- Carroll D., Beumer K.J., Morton J.J., Bozas A., Trautman J.K. // Methods Mol. Biol. 2008, V.435, P.63-77
- Urnov F.D., Rebar E.J., Holmes M.C., Zhang H.S., Gregory P.D. // Nat. Rev Genet. 2010, V.11, №9, P.636-646
- Carbery I.D., Ji D., Harrington A., Brown V., Weinstein E.J., Liaw L., Cui X. // Genetics. 2010, V.186, №2, P.451-459
- Geurts A.M., Cost G.J., Freyvert Y., Zeitler B., Miller J.C., Choi V.M., Jenkins S.S., Wood A., Cui X., Meng X. // Science. 2009, V.325, №5939, P.433
- Cui X., Ji D., Fisher D.A., Wu Y., Briner D.M., Weinstein E.J. // Nat. Biotechnol. 2011, V.29, №1, P.64-67
- Meyer M., de Angelis M.H., Wurst W., Kuhn R. // Proc. Natl. Acad. Sci. USA. 2010, V.107, №34, P.15022-15026
- Li D., Qiu Z., Shao Y., Guan Y., Liu M., Li Y., Gao N., Wang L., Lu X., Zao Y. // Nat. Biotechnol. 2013, V.31, №8, P.681-683
- Li W., Teng F., Li T., Zhou Q. // Nat. Biotechnol. 2013, V.31, №8, P.684-686
- Wu Y., Liang D., Wang Y., Bai M., Tang W., Bao S., Yan Z., Li D., Li J. // Cell Stem Cell. 2013, V.13, №6, P.659-662
- Chen K., Gao C. // J. Genet. Genomics. 2013, V.40, №6, P.271-279
- van der Hoorn R.A., Laurent F., Roth R., De Wit P.J. // Mol. Plant. Microbe Interact. 2000, V.13, №4, P.439-446
- Feng Z., Zhang B., Ding W., Liu X., Yang D., Wei P., Cao F., Zhu S., Zhang F., Mao Y. // Cell Res. 2013, V.23, №10, P.1229-1232
- Xie K., Yang Y. // Mol. Plant. 2013, V.6, №6, P.1975-1983
- Miao J., Guo D., Zhang J., Huang Q., Qin G., Zhang X., Wan J., Gu H., Qu L. // Cell Res. 2013, V.23, №10, P.1233-1236
- Jiang W., Zhou H., Bi H., Fromm M., Yang B., Weeks D.P. // Nucleic Acids Res. 2013, V.41, №20, P.e188
- Upadhyay S.K., Kumar J., Alok A., Tuli R. // G3 (Bethesda). 2013, V.3, №12, P.2233-2238
- Shan Q., Wang Y., Chen K., Liang Z., Li J., Zhang Y., Zhang K., Liu J., Voytas D.F., Zheng X. // Mol. Plant. 2013, V.6, №4, P.1365-1368
- Li T., Liu B., Spalding M.H., Weeks D.P., Yang B. // Nat. Biotechnol. 2012, V.30, №5, P.390-392
- Zhang Y., Zhang F., Li X., Baller J.A., Starker C.G., Bogdanove A.J., Voytas D.F. // Plant Physiol. 2013, V.161, №1, P.20-27
- Mahfouz M.M., Li L., Shamimuzzaman M., Wibowo A., Fang X., Zhu J.K. // Proc. Natl. Acad. Sci. USA. 2011, V.108, №6, P.2623-2628
- Beerli R.R., Segal D.J., Dreier B., Barbas C.F. 3rd. // Proc. Natl. Acad. Sci. USA. 1998, V.95, №25, P.14628-14633
- Perez-Pinera P., Ousterout D.G., Brunger J.M., Farin A.M., Guilak F., Crawford G.E., Hartemink A.J., Gersbach C.A. // Nat. Methods. 2013, V.10, №3, P.239-242
- Maeder M.L., Linder S.J., Reyon D., Angstman J.F., Fu Y., Sander J.D., Joung J.K. // Nat. Methods. 2013, V.10, №3, P.243-245
- Li Y., Moore R., Guinn M., Bleris L. // Sci. Rep. 2012, V.2, P.897
- Mahfouz M.M., Li L., Piatek M., Fang X., Mansour H., Bangarusamy D.K., Zhu J.K. // Plant Mol. Biol. 2012, V.78, №3, P.311-321
- Chapdelaine P., Coulombe Z., Chikh A., Gerard C., Tremblay J.P. // Mol. Ther. Nucleic. Acids. 2013, V.2, P.e119
- Gao X., Yang J., Tsang J.C., Ooi J., Wu D., Liu P. // Stem Cell Reports. 2013, V.1, №2, P.183-197
- Mercer A.C., Gaj T., Sirk S.J., Lamb B.M., Barbas C.F. 3rd. // ACS Synth. Biol. 2013
- Konermann S., Brigham M.D., Trevino A.E., Hsu P.D., Heidenreich M., Cong L., Platt R.J., Scott D.A., Church G.M., Zhang F. // Nature 2013, V.500, №7463, P.472-476
- Gaber R., Lebar T., Majerle A., Ster B., Dobnikar A., Bencina M., Jerala R. // Nat. Chem. Biol. 2014, V.10, №3, P.203-208
- Lienert F., Torella J.P., Chen J.H., Norsworthy M., Richardson R.R., Silver P.A. // Nucleic Acids Res. 2013, V.41, №21, P.9967-9975
- Miyanari Y., Ziegler-Birling C., Torres-Padilla M.E. // Nat. Struct. Mol. Biol. 2013, V.20, №11, P.1321-1324
- Thanisch K., Schneider K., Morbitzer R., Solovei I., Lahaye T., Bultmann S., Leonhardt H. // Nucleic Acids Res. 2013, V.42, №6, P.e38
- Ma H., Reyes-Gutierrez P., Pederson T. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №52, P.21048-21053
- Owens J.B., Urschitz J., Stoytchev I., Dang N.C., Stoytcheva Z., Belcaid M., Maragathavally K.J., Coates C.J., Segal D.J., Moisyadi S. // Nucleic Acids Res. 2012, V.40, №14, P.6978-6991
- Mercer A.C., Gaj T., Fuller R.P., Barbas C.F., 3rd. I.O. // Nucleic Acids Res. 2012, V.40, №21, P.11163-11172
- Lamb B.M., Mercer A.C., Barbas C.F., 3rd. I.O. // Nucleic Acids Res. 2013, V.41, №21, P.9779-9785
- Owens J.B., Mauro D., Stoytchev I., Bhakta M.S., Kim M.S., Segal D.J., Moisyadi S. // Nucleic Acids Res. 2013, V.41, №19, P.9197-9207
- Miller J.C., Tan S., Qiao G., Barlow K.A., Wang J., Xia D.F., Meng X., Paschon D.E., Leung E., Hinkley S.J. // Nat. Biotechnol. 2011, V.29, №2, P.143-148
- Mussolino C., Morbitzer R., Lutge F., Dannemann N., Lahaye T., Cathomen T. // Nucleic Acids Res. 2011, V.39, №21, P.9283-9293
- Sun N., Liang J., Abil Z., Zhao H. // Mol. Biosyst. 2012, V.8, №4, P.1255-1263
- Xu L., Zhao P., Mariano A., Han R. // Mol. Ther. Nucleic Acids. 2013, V.2, P.e112
- Hockemeyer D., Wang H., Kiani S., Lai C.S., Gao Q., Cassady J.P., Cost G.J., Zhang L., Santiago Y., Miller J.C. // Nat. Biotechnol. 2011, V.29, №8, P.731-734
- Li T., Huang S., Zhao X., Wright D.A., Carpenter S., Spalding M.H., Weeks D.P., Yang B. // Nucleic Acids Res. 2011, V.39, №14, P.6315-6325
- Wood A.J., Lo T.W., Zeitler B., Pickle C.S., Ralston E.J., Lee A.H., Amora R., Miller J.C., Leung E., Meng X. // Science. 2011, V.333, №6040, P.307
- Liu J., Li C., Yu Z., Huang P., Wu H., Wei C., Zhu N., Chen Y., Zhang B., Deng W.M. // J. Genet. Genomics. 2012, V.39, №5, P.209-215
- Bedell V.M., Wang Y., Campbell J.M., Poshusta T.L., Starker C.G., Krug R.G. 2 nd., Tan W., Penheiter S.G., Ma A.C., Leung A.Y. // Nature 2012, V.491, №7422, P.114-118
- Moore F.E., Reyon D., Sander J.D., Martinez S.A., Blackburn J.S., Khayter C., Ramirez C.L., Joung J.K., Langenau D.M. // PLoS One. 2012. P. 7. № 5. 2012, V.7, №5, P.e37877
- Huang P., Xiao A., Zhou M., Zhu Z., Lin S., Zhang B. // Nat. Biotechnol. 2011, V.29, №8, P.699-700
- Cade L., Reyon D., Hwang W.Y., Tsai S.Q., Patel S., Khayter C., Joung J.K., Sander J.D., Peterson R.T., Yeh J.R. // Nucleic Acids Res. 2012, V.40, №16, P.8001-8010
- Ma S., Zhang S., Wang F., Liu Y., Liu Y., Xu H., Liu C., Lin Y., Zhao P., Xia Q. // PLoS One. 2012, V.7, №9, P.e45035
- Watanabe T., Ochiai H., Sakuma T., Horch H.W., Hamaguchi N., Nakamura T., Bando T., Ohuchi H., Yamamoto T., Noji S. // Nat. Commun. 2012, V.3, P.1017
- Lei Y., Guo X., Liu Y., Cao Y., Deng Y., Chen X., Cheng X., Cheng C.H., Dawid I.B., Chen Y. // Proc. Natl. Acad. Sci. USA. 2012, V.109, №43, P.17484-17489
- Panda S.K., Wefers B., Ortiz O., Floss T., Schmid B., Haass C., Wurst W., Kuhn R. // Genetics. 2013, V.195, №3, P.703-713
- Qiu Z., Liu M., Chen Z., Shao Y., Pan H., Wei G., Yu C., Zhang L., Li X., Wang P. // Nucleic Acids Res. 2013, V.41, №11, P.e120
- Wu J., Huang Z., Ren J., Zhang Z., He P., Li Y., Ma J., Chen W., Zhang Y., Zhou X. // Cell Res. 2013, V.23, №8, P.994-1006
- Sung Y.H., Baek I.J., Kim D.H., Jeon J., Lee J., Lee K., Jeong D., Kim J.S., Lee H.W. // Nat. Biotechnol. 2013, V.31, №1, P.23-24
- Wefers B., Meyer M., Ortiz O., Hrabe de Angelis M., Hansen J., Wurst W., Kuhn R. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №10, P.3782-3787
- Davies B., Davies G., Preece C., Puliyadi R., Szumska D., Bhattacharya S. // PLoS One. 2013, V.8, №3, P.e60216
- Tong C., Huang G., Ashton C., Wu H., Yan H., Ying Q.L. // J. Genet. Genomics. 2012, V.39, №6, P.275-280
- Tesson L., Usal C., Menoret S., Leung E., Niles B.J., Remy S., Santiago Y., Vincent A.I., Meng X., Zhang L. // Nat. Biotechnol. 2011, V.29, №8, P.695-696
- Carlson D.F., Tan W., Lillico S.G., Stverakova D., Proudfoot C., Christian M., Voytas D.F., Long C.R., Whitelaw C.B., Fahrenkrug S.C. // Proc. Natl. Acad. Sci. USA. 2012, V.109, №43, P.17382-17387
- DiCarlo J.E., Norville J.E., Mali P., Rios X., Aach J., Church G.M. // Nucleic Acids Res. 2013, V.41, №7, P.4336-4343
- Hou Z., Zhang Y., Propson N.E., Howden S.E., Chu L., Sontheimer E.J., Thomson J.A. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №39, P.15644-15649
- Ding Q., Regan S.N., Xia Y., Oostrom L.A., Cowan C.A., Musunuru K. // Cell Stem Cell. 2013, V.12, №4, P.393-394
- Hwang W.Y., Fu Y., Reyon D., Maeder M.L., Kaini P., Sander J.D., Joung J.K., Peterson R.T., Yeh J.J. // PLoS One. 2013, V.8, №7, P.e68708
- Jao L.E., Wente S.R., Chen W. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №34, P.13904-13909
- Xiao A., Wang Z., Hu Y., Wu Y., Luo Z., Yang Z., Zu Y., Li W., Huang P., Tong X. // Nucleic Acids Res. 2013, V.41, №14, P.e141
- Hruscha A., Krawitz P., Rechenberg A., Heinrich V., Hecht J., Haass C., Schmid B. // Development. 2013, V.140, №24, P.4982-4987
- Nakayama T., Fish M.B., Fisher M., Oomen-Hajagos J., Thomsen G.H., Grainger R.M. // Genesis. 2013, V.51, №12, P.835-843
- Tan W., Carlson D.F., Lancto C.A., Garbe J.R., Webster D.A., Hackett P.B., Fahrenkrug S.C. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №41, P.16526-16531
- Fujii W., Kawasaki K., Sugiura K., Naito K. // Nucleic Acids Res. 2013, V.41, №20, P.e187
- Shen B., Zhang J., Wu H., Wang J., Ma K., Li Z., Zhang X., Zhang P., Huang X. // Cell Res. 2013, V.23, №5, P.720-723
- Ma Y., Zhang X., Shen B., Lu Y., Chen W., Ma J., Bai L., Huang X., Zhang L. // Cell Res. 2014, V.24, №1, P.122-125