SunnyTALEN: A second-generation TALEN system for human genome editing

Biotechnology and Bioengineering

Volumn 111, Issue 4, 2014, Pages 683-691

  Sun, Ning ^a,c   Bao, Zehua ^a   Xiong, Xiong ^a   Zhao, Huimin ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Directed evolution; Double strand break; Gene therapy; Genome editing; Synthetic biology

Indexed keywords

BIOLOGY; GENE THERAPY;

DIRECTED EVOLUTION; DNA DOUBLE-STRAND BREAKS; DOUBLE-STRAND BREAKS; GENETIC MODIFICATIONS; HOMOLOGOUS RECOMBINATION; NONHOMOLOGOUS END JOINING; SYNTHETIC BIOLOGY; THERAPEUTIC APPLICATION;

GENES;

DNA FRAGMENT; HETERODIMER; HISTONE H2AX; HOMODIMER; NUCLEASE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA BINDING; DNA CLEAVAGE; DNA DAMAGE; DNA MODIFICATION; FLUORESCENCE ACTIVATED CELL SORTING; GENE LOCUS; GENOME; HIGH THROUGHPUT SCREENING; HISTONE PHOSPHORYLATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; HUMAN GENOME; INDEL MUTATION; MUTAGENESIS; NUCLEAR LOCALIZATION SIGNAL; POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; WESTERN BLOTTING;

DIRECTED EVOLUTION; DOUBLE-STRAND BREAK; GENE THERAPY; GENOME EDITING; SYNTHETIC BIOLOGY;

DEOXYRIBONUCLEASES; DIRECTED MOLECULAR EVOLUTION; DNA BREAKS, DOUBLE-STRANDED; GENOME, HUMAN; GENOMICS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MODELS, MOLECULAR; SYNTHETIC BIOLOGY;

EID: 84894252630     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25154     Document Type: Article

References (44)

1. Andersson S, Davis DL, Dahlback H, Jornvall H, Russell DW. 1989. Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme. J Biol Chem 264(14):8222-8229.
2. Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug RG II, Tan W, Penheiter SG, Ma AC, Leung AY, Fahrenkrug SC, Carlson DF, Voytas DF, Clark KJ, Essner JJ, Ekker SC. 2012. In vivo genome editing using a high-efficiency TALEN system. Nature 491(7422):114-118.
3. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326(5959):1509-1512.
4. Cade L, Reyon D, Hwang WY, Tsai SQ, Patel S, Khayter C, Joung JK, Sander JD, Peterson RT, Yeh JR. 2012. Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Res 40(16):8001-8010.
5. Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C, Christian M, Voytas DF, Long CR, Whitelaw CB, Fahrenkrug SC. 2012. Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci USA 109(43):17382-17387.
6. Carroll D. 2011. Genome engineering with zinc-finger nucleases. Genetics 188(4):773-782.
7. Check E. 2002. A tragic setback. Nature 420(6912):116-118.
8. Cherry AB, Daley GQ. 2013. Reprogrammed cells for disease modeling and regenerative medicine. Annu Rev Med 64:277-290.
9. Choi SM, Kim Y, Shim JS, Park JT, Wang RH, Leach SD, Liu JO, Deng CX, Ye Z, Jang YY. 2013. Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 57(6):2458-2468.
10. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF. 2010. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186(2):757-761.
11. Cong L, Zhou R, Kuo YC, Cunniff M, Zhang F. 2012. Comprehensive interrogation of natural TALE DNA-binding modules and transcriptional repressor domains. Nat Commun 3:968.
12. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819-823.
13. Ding Q, Lee YK, Schaefer EA, Peters DT, Veres A, Kim K, Kuperwasser N, Motola DL, Meissner TB, Hendriks WT, Trevisan M, Gupta RM, Moisan A, Banks E, Friesen M, Schinzel RT, Xia F, Tang A, Xia Y, Figueroa E, Wann A, Ahfeldt T, Daheron L, Zhang F, Rubin LL, Peng LF, Chung RT, Musunuru K, Cowan CA. 2013. A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell 12(2):238-251.
14. Dow LE, Lowe SW. 2012. Life in the fast lane: Mammalian disease models in the genomics era. Cell 148(6):1099-1109.
15. Doyle EL, Booher NJ, Standage DS, Voytas DF, Brendel VP, Vandyk JK, Bogdanove AJ. 2012. TAL effector-nucleotide targeter (TALE-NT) 2.0: Tools for TAL effector design and target prediction. Nucleic Acids Res 40(Web Server issue):W117-W122.
16. Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC. 2011. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Methods 8(1):74-79.
17. Gietz RD, Schiestl RH. 2007. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2(1):31-34.
18. Guo J, Gaj T, Barbas CF III. 2010. Directed evolution of an enhanced and highly efficient FokI cleavage domain for zinc finger nucleases. J Mol Biol 400(1):96-107.
19. Huang P, Xiao A, Zhou M, Zhu Z, Lin S, Zhang B. 2011. Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29(8):699-700.
20. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK. 2013. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31(3):227-229.
21. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31(3):233-239.
22. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. 2013. RNA-programmed genome editing in human cells. Elife 2:e00471.
23. Joung JK, Sander JD. 2013. TALENs: A widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14(1):49-55.
24. Kim H, Um E, Cho SR, Jung C, Kim H, Kim JS. 2011. Surrogate reporters for enrichment of cells with nuclease-induced mutations. Nat Methods 8(11):941-943.
25. Kim Y, Kweon J, Kim A, Chon JK, Yoo JY, Kim HJ, Kim S, Lee C, Jeong E, Chung E, Kim D, Lee MS, Go EM, Song HJ, Kim H, Cho N, Bang D, Kim S, Kim JS. 2013a. A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 31(3):251-258.
26. Kim Y, Kweon J, Kim JS. 2013b. TALENs and ZFNs are associated with different mutation signatures. Nat Methods 10(3):185.
27. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339(6121):823-826.
28. Marshall E. 1999. Gene therapy death prompts review of adenovirus vector. Science 286(5448):2244-2245.
29. Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA, Gregory PD, Pabo CO, Rebar EJ. 2007. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25(7):778-785.
30. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, Dulay GP, Hua KL, Ankoudinova I, Cost GJ, Urnov FD, Zhang HS, Holmes MC, Zhang L, Gregory PD, Rebar EJ. 2011. A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29(2):143-148.
31. Moscou MJ, Bogdanove AJ. 2009. A simple cipher governs DNA recognition by TAL effectors. Science 326(5959):1501.
32. Mussolino C, Cathomen T. 2012. TALE nucleases: Tailored genome engineering made easy. Curr Opin Biotechnol 23(5):644-6450.
33. Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T. 2011. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39(21):9283-9293.
34. Osborn MJ, Starker CG, McElroy AN, Webber BR, Riddle MJ, Xia L, Defeo AP, Gabriel R, Schmidt M, Von Kalle C, Carlson DF, Maeder ML, Joung JK, Wagner JE, Voytas DF, Blazar BR, Tolar J. 2013. TALEN-based gene correction for epidermolysis bullosa. Mol Ther 21(6):1151-1159.
35. Pattanayak V, Ramirez CL, Joung JK, Liu DR. 2011. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat Methods 8(9):765-770.
36. Perez-Pinera P, Ousterout DG, Gersbach CA. 2012. Advances in targeted genome editing. Curr Opin Chem Biol 16(3-4):268-277.
37. Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK. 2012. FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30(5):460-465.
38. Silva G, Poirot L, Galetto R, Smith J, Montoya G, Duchateau P, Paques F. 2011. Meganucleases and other tools for targeted genome engineering: Perspectives and challenges for gene therapy. Curr Gene Ther 11(1):11-27.
39. Streubel J, Blucher C, Landgraf A, Boch J. 2012. TAL effector RVD specificities and efficiencies. Nat Biotechnol 30(7):593-595.
40. Sun N, Zhao H. 2013a. Seamless correction of the sickle cell disease mutation of the HBB gene in human induced pluripotent stem cells using TALENs. Biotechnol Bioeng doi: 10.1002/bit.25018
41. Sun N, Zhao H. 2013b. Transcription activator-like effector nucleases (TALENs): A highly efficient and versatile tool for genome editing. Biotechnol Bioeng 110(7):1811-1821.
42. Sun N, Abil Z, Zhao H. 2012a. Recent advances in targeted genome engineering in mammalian systems. Biotechnol J 7(9):1074-1087.
43. Sun N, Liang J, Abil Z, Zhao H. 2012b. Optimized TAL effector nucleases (TALENs) for use in treatment of sickle cell disease. Mol Biosyst 8(4):1255-1263.
44. Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ, Cathomen T. 2007. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25(7):786-793.