TALEN and CRISPR/Cas Genome Editing Systems: Tools of Discovery

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  • 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:
    1. Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences
    2. Institute of Chemical Biology and Fundamental Medicine, Siberian Branch of the Russian Academy of Sciences
    3. Meshalkin Novosibirsk State Research Institute of Circulation Pathology, Ministry of Health of the Russian Federation
    4. Novosibirsk State University
  • Issue: Vol 6, No 3 (2014)
  • Pages: 19-40
  • Section: Reviews
  • URL: http://actanaturae.ru/2075-8251/article/view/10529
  • DOI: https://doi.org/10.32607/20758251-2014-6-3-19-40
  • 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.


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

Russian Federation

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

Russian Federation

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

Russian Federation

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

Russian Federation

  1. Capecchi M.R. // Nat. Rev. Genet. 2005, V.6, №6, P.507-512
  2. Kim Y.G., Cha J., Chandrasegaran S. // Proc. Natl. Acad. Sci. USA. 1996, V.93, №3, P.1156-1160
  3. Bibikova M., Golic M., Golic K.G., Carroll D. // Genetics. 2002, V.161, №3, P.1169-1175
  4. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. Becker M. // Nat. Methods. 2012, V.9, №1, P.1
  10. Schornack S., Meyer A., Römer P., Jordan T., Lahaye T. // J. Plant Physiol. 2006, V.163, №3, P.256-272
  11. Romer P., Hahn S., Jordan T., Strauss T., Bonas U., Lahaye T. // Science. 2007, V.318, №5850, P.645-648
  12. 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
  13. Moscou M.J., Bogdanove A.J. // Science. 2009, V.326, №5959, P.1501
  14. Lamb B.M., Mercer A.C., Barbas C.F. // Nucleic Acids Res. 2013, V.41, №21, P.9779-9785
  15. 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
  16. Cong L., Zhou R., Kuo Y.C., Cunniff M.M., Zhang F. // Nat. Commun. 2012, V.3, P.968
  17. 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
  18. Streubel J., Blucher C., Landgraf A., Boch J. // Nat. Biotechnol. 2012, V.30, №7, P.593-595
  19. Mak A.N., Bradley P., Cernadas R.A., Bogdanove A.J., Stoddard B.L. // Science. 2012, V.335, №6069, P.716-719
  20. Ishino Y., Shinagawa H., Makino K., Amemura M., Nakata A. // Journal of Bacteriology 1987, V.169, №2, P.5429-5433
  21. Haft D.H., Selengut J., Mongodin E.F., Nelson K.E. // PLoS Comput. Biol. 2005, V.1, №6, P.e60
  22. Bolotin A., Quinguis B., Sorokin A., Ehrlich S.D. // Microbiology. 2005, V.151, P.2551-2561
  23. Mojica F.J., Diez-Villasenor C., Garcia-Martinez J., Soria E. // J. Mol. Evol. 2005, V.60, №2, P.174-182
  24. Pourcel C., Salvignol G., Vergnaud G. // Microbiology. 2005, V.151, P.653-663
  25. 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
  26. Grissa I., Vergnaud G., Pourcel C. // BMC Bioinformatics. 2007, V.8, P.172
  27. 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
  28. Mojica F.J., Diez-Villasenor C., Garcia-Martinez J., Almendros C. // Microbiology. 2009, V.155, P.733-740
  29. Swarts D.C., Mosterd C., van Passel M.W., Brouns S.J. // PLoS One. 2012. V. 7. № 4. 2012, V.7, №4, P.e35888
  30. 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
  31. 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
  32. Carte J., Wang R., Li H., Terns R.M., Terns M.P. // Genes. Dev. 2008, V.22, №24, P.3489-3496
  33. Haurwitz R.E., Jinek M., Wiedenheft B., Zhou K., Doudna J.A. // Science. 2010, V.329, №5997, P.1355-1358
  34. 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
  35. Richter H., Zoephel J., Schermuly J., Maticzka D., Backofen R., Randau L. // Nucleic Acids Res. 2012, V.40, №19, P.9887-9896
  36. Sashital D.G., Jinek M., Doudna J.A. // Nat. Struct. Mol. Biol. 2011, V.18, №6, P.680-687
  37. 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
  38. Makarova K.S., Grishin N.V., Shabalina S.A., Wolf Y.I., Koonin E.V. // Biol. Direct. 2006, V.1, P.7
  39. Marraffini L.A., Sontheimer E.J. // Nature 2010, V.463, №7280, P.568-571
  40. Bondy-Denomy J., Pawluk A., Maxwell K.L., Davidson A.R. // Nature 2013, V.493, №7432, P.429-432
  41. Makarova K.S., Aravind L., Wolf Y.I., Koonin E.V. // Biol. Direct. 2011, V.6, P.38
  42. Sapranauskas R., Gasiunas G., Fremaux C., Barrangou R., Horvath P., Siksnys V. // Nucleic Acids Res. 2011, V.39, №21, P.9275-9282
  43. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. // Science. 2012, V.337, №6096, P.816-821
  44. 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
  45. Mussolino C., Cathomen T. // Curr. Opin. Biotechnol. 2012, V.23, №5, P.644-650
  46. 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
  47. 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
  48. Jiang W., Bikard D., Cox D., Zhang F., Marraffini L.A. // Nat. Biotechnol. 2013, V.31, №3, P.233-239
  49. 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
  50. 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
  51. 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
  52. Gasiunas G., Barrangou R., Horvath P., Siksnys V. // Proc. Natl. Acad. Sci. USA. 2012, V.109, №39, P.2579-2586
  53. Dianov G.L., Hubscher U. // Nucleic Acids Res. 2013, V.41, №6, P.3483-3490
  54. 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
  55. Fine E.J., Cradick T.J., Zhao C.L., Lin Y., Bao G. // Nucleic Acids Res. 2013, V.42, №6, P.e42
  56. Grau J., Boch J., Posch S. // Bioinformatics. 2013, V.29, №22, P.2931-2932
  57. Grau J., Wolf A., Reschke M., Bonas U., Posch S. // PLoS Comput. Biol. 2013, V.9, №3, P.e1002962
  58. Heigwer F., Kerr G., Walther N., Glaeser K., Pelz O., Breinig M., Boutros M. // Nucleic Acids Res. 2013, V.41, №20, P.e190
  59. 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
  60. Grissa I., Vergnaud G., Pourcel C. // Nucleic Acids Res. 2007, V.35, P.52-57
  61. Rousseau C., Gonnet M., Le Romancer M., Nicolas J. // Bioinformatics. 2009, V.25, №24, P.3317-3318
  62. Xiao A., Cheng Z., Kong L., Zhu Z., Lin S., Gao G., Zhang B. // Bioinformatics. 2014, V.30, №8, P.1180-1182
  63. 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
  64. Reyon D., Khayter C., Regan M.R., Joung J.K., Sander J.D. // Curr. Protoc. Mol. Biol. 2012. C.12. U. 12.15. 2012
  65. Weber E., Engler C., Gruetzner R., Werner S., Marillonnet S. // PLoS One. 2011, V.6, №2, P.e16765
  66. Engler C., Gruetzner R., Kandzia R., Marillonnet S. // PLoS One. 2009, V.4, №5, P.e5553
  67. Zhang F., Cong L., Lodato S., Kosuri S., Church G.M., Arlotta P. // Nat. Biotechnol. 2011, V.29, №2, P.149-153
  68. Sanjana N.E., Cong L., Zhou Y., Cunniff M.M., Feng G., Zhang F. // Nature Protocols 2012, V.7, №1, P.171-192
  69. Schmid-Burgk J.L., Schmidt T., Kaiser V., Honing K., Hornung V. // Nat. Biotechnol. 2013, V.31, №1, P.76-81
  70. 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
  71. 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
  72. 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
  73. 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
  74. 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
  75. Jinek M., Doudna J.A. // Nature 2009, V.457, №7228, P.405-412
  76. Malone C.D., Hannon G.J. // Cell. 2009, V.136, №4, P.656-668
  77. Meister G., Tuschl T. // Nature 2004, V.431, №7006, P.343-349
  78. Cho S.W., Kim S., Kim J.M., Kim J.S. // Nat. Biotechnol. 2013, V.31, №3, P.230-232
  79. Jinek M., East A., Cheng A., Lin S., Ma E., Doudna J. // Elife. 2013, V.2, P.e00471
  80. 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
  81. 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
  82. 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
  83. 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
  84. 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
  85. Wang T., Wei J.J., Sabatini D.M., Lander E.S. // Science. 2014, V.343, №6166, P.80-84
  86. 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
  87. Mao Y., Zhang H., Xu N., Zhang B., Gao F., Zhu J.K. // Mol. Plant. 2013, V.6, №6, P.2008-2011
  88. 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
  89. Nekrasov V., Staskawicz B., Weigel D., Jones J.D., Kamoun S. // Nat. Biotechnol. 2013, V.31, №8, P.691-369
  90. Lieber M.R. // Annu. Rev. Biochem. 2010, V.79, P.181-211
  91. 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
  92. Kim H., Um E., Cho S.R., Jung C., Kim H., Kim J.S. // Nat. Methods. 2011, V.8, №11, P.941-943
  93. 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
  94. 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
  95. 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
  96. Kim H.J., Lee H.J., Kim H., Cho S.W., Kim J.S. // Genome Res. 2009, V.19, №7, P.1279-1288
  97. 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
  98. 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
  99. Saleh-Gohari N., Helleday T. // Nucleic Acids Res. 2004, V.32, №12, P.3683-3688
  100. 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
  101. 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
  102. Maresca M., Lin V.G., Guo N., Yang Y. // Genome Res. 2013, V.23, №3, P.539-546
  103. 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
  104. 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
  105. 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
  106. 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
  107. Bloom K., Ely A., Mussolino C., Cathomen T., Arbuthnot P. // Molecular Therapy 2013, V.21, №10, P.1889-1897
  108. Schiffer J.T., Aubert M., Weber N.D., Mintzer E., Stone D., Jerome K.R. // Virology Journal 2012, V.86, №17, P.8920-8936
  109. 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
  110. Horii T., Tamura D., Morita S., Kimura M., Hatada I. // Int. J. Mol. Sci. 2013, V.14, №10, P.19774-19781
  111. 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
  112. 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
  113. Bikard D., Jiang W., Samai P., Hochschild A., Zhang F., Marraffini L.A. // Nucleic Acids Res. 2013, V.41, №15, P.7429-7437
  114. 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
  115. Farzadfard F., Perli S.D., Lu T.K. // ACS Synth. Biol. 2013, V.2, №10, P.604-613
  116. Heintze J., Luft C., Ketteler R. // Front Genet. 2013, V.4, P.193
  117. 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
  118. 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
  119. Chiu H., Schwartz H.T., Antoshechkin I., Sternberg P.W. // Genetics. 2013, V.195, №3, P.1167-1171
  120. Cho S.W., Lee J., Carroll D., Kim J., Lee J. // Genetics. 2013, V.195, №3, P.1177-1180
  121. Katic I., Grosshans H. // Genetics. 2013, V.195, №3, P.1173-1176
  122. 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
  123. 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
  124. 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
  125. Dickinson D.J., Ward J.D., Reiner D.J., Goldstein B. // Nat. Methods. 2013, V.10, №10, P.1028-1034
  126. 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
  127. Maggert K.A., Gong W.J., Golic K.G. // Methods Mol. Biol. 2008, V.420, P.155-174
  128. Rong Y.S., Golic K.G. // Science. 2000, V.288, №5473, P.2013-2018
  129. Venken K.J., Bellen H.J. // Nat. Rev. Genet. 2005, V.6, №3, P.167-178
  130. Bassett A.R., Tibbit C., Ponting C.P., Liu J. // Cell Rep. 2013, V.4, №1, P.220-228
  131. 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
  132. Yu Z., Ren M., Wang Z., Zhang B., Rong Y.S., Jiao R., Gao G. // Genetics. 2013, V.195, №1, P.289-291
  133. 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
  134. Seth A., Stemple D.L., Barroso I. // Dis. Model. Mech. 2013, V.6, №5, P.1080-1088
  135. Copeland N.G., Jenkins N.A. // Nat. Rev. Cancer. 2010, V.10, №10, P.696-706
  136. Kool J., Berns A. // Nat. Rev. Cancer. 2009, V.9, №6, P.389-399
  137. Bogdanove A.J., Voytas D.F. // Science. 2011, V.333, №6051, P.1843-1846
  138. Carroll D., Beumer K.J., Morton J.J., Bozas A., Trautman J.K. // Methods Mol. Biol. 2008, V.435, P.63-77
  139. 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
  140. Carbery I.D., Ji D., Harrington A., Brown V., Weinstein E.J., Liaw L., Cui X. // Genetics. 2010, V.186, №2, P.451-459
  141. 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
  142. Cui X., Ji D., Fisher D.A., Wu Y., Briner D.M., Weinstein E.J. // Nat. Biotechnol. 2011, V.29, №1, P.64-67
  143. Meyer M., de Angelis M.H., Wurst W., Kuhn R. // Proc. Natl. Acad. Sci. USA. 2010, V.107, №34, P.15022-15026
  144. 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
  145. Li W., Teng F., Li T., Zhou Q. // Nat. Biotechnol. 2013, V.31, №8, P.684-686
  146. 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
  147. Chen K., Gao C. // J. Genet. Genomics. 2013, V.40, №6, P.271-279
  148. van der Hoorn R.A., Laurent F., Roth R., De Wit P.J. // Mol. Plant. Microbe Interact. 2000, V.13, №4, P.439-446
  149. 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
  150. Xie K., Yang Y. // Mol. Plant. 2013, V.6, №6, P.1975-1983
  151. 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
  152. Jiang W., Zhou H., Bi H., Fromm M., Yang B., Weeks D.P. // Nucleic Acids Res. 2013, V.41, №20, P.e188
  153. Upadhyay S.K., Kumar J., Alok A., Tuli R. // G3 (Bethesda). 2013, V.3, №12, P.2233-2238
  154. 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
  155. Li T., Liu B., Spalding M.H., Weeks D.P., Yang B. // Nat. Biotechnol. 2012, V.30, №5, P.390-392
  156. 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
  157. 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
  158. Beerli R.R., Segal D.J., Dreier B., Barbas C.F. 3rd. // Proc. Natl. Acad. Sci. USA. 1998, V.95, №25, P.14628-14633
  159. 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
  160. 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
  161. Li Y., Moore R., Guinn M., Bleris L. // Sci. Rep. 2012, V.2, P.897
  162. 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
  163. Chapdelaine P., Coulombe Z., Chikh A., Gerard C., Tremblay J.P. // Mol. Ther. Nucleic. Acids. 2013, V.2, P.e119
  164. Gao X., Yang J., Tsang J.C., Ooi J., Wu D., Liu P. // Stem Cell Reports. 2013, V.1, №2, P.183-197
  165. Mercer A.C., Gaj T., Sirk S.J., Lamb B.M., Barbas C.F. 3rd. // ACS Synth. Biol. 2013
  166. 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
  167. Gaber R., Lebar T., Majerle A., Ster B., Dobnikar A., Bencina M., Jerala R. // Nat. Chem. Biol. 2014, V.10, №3, P.203-208
  168. 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
  169. Miyanari Y., Ziegler-Birling C., Torres-Padilla M.E. // Nat. Struct. Mol. Biol. 2013, V.20, №11, P.1321-1324
  170. Thanisch K., Schneider K., Morbitzer R., Solovei I., Lahaye T., Bultmann S., Leonhardt H. // Nucleic Acids Res. 2013, V.42, №6, P.e38
  171. Ma H., Reyes-Gutierrez P., Pederson T. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №52, P.21048-21053
  172. 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
  173. Mercer A.C., Gaj T., Fuller R.P., Barbas C.F., 3rd. I.O. // Nucleic Acids Res. 2012, V.40, №21, P.11163-11172
  174. Lamb B.M., Mercer A.C., Barbas C.F., 3rd. I.O. // Nucleic Acids Res. 2013, V.41, №21, P.9779-9785
  175. 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
  176. 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
  177. Mussolino C., Morbitzer R., Lutge F., Dannemann N., Lahaye T., Cathomen T. // Nucleic Acids Res. 2011, V.39, №21, P.9283-9293
  178. Sun N., Liang J., Abil Z., Zhao H. // Mol. Biosyst. 2012, V.8, №4, P.1255-1263
  179. Xu L., Zhao P., Mariano A., Han R. // Mol. Ther. Nucleic Acids. 2013, V.2, P.e112
  180. 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
  181. 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
  182. 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
  183. 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
  184. 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
  185. 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
  186. Huang P., Xiao A., Zhou M., Zhu Z., Lin S., Zhang B. // Nat. Biotechnol. 2011, V.29, №8, P.699-700
  187. 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
  188. 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
  189. 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
  190. 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
  191. 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
  192. 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
  193. 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
  194. 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
  195. 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
  196. Davies B., Davies G., Preece C., Puliyadi R., Szumska D., Bhattacharya S. // PLoS One. 2013, V.8, №3, P.e60216
  197. Tong C., Huang G., Ashton C., Wu H., Yan H., Ying Q.L. // J. Genet. Genomics. 2012, V.39, №6, P.275-280
  198. 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
  199. 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
  200. 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
  201. 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
  202. 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
  203. 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
  204. Jao L.E., Wente S.R., Chen W. // Proc. Natl. Acad. Sci. USA. 2013, V.110, №34, P.13904-13909
  205. 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
  206. Hruscha A., Krawitz P., Rechenberg A., Heinrich V., Hecht J., Haass C., Schmid B. // Development. 2013, V.140, №24, P.4982-4987
  207. Nakayama T., Fish M.B., Fisher M., Oomen-Hajagos J., Thomsen G.H., Grainger R.M. // Genesis. 2013, V.51, №12, P.835-843
  208. 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
  209. Fujii W., Kawasaki K., Sugiura K., Naito K. // Nucleic Acids Res. 2013, V.41, №20, P.e187
  210. 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
  211. 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

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