TALE: A tale of genome editing

Progress in Biophysics and Molecular Biology

Volumn 114, Issue 1, 2014, Pages 25-32

  Zhang, Mingjie ^a   Wang, Feng ^b   Li, Shifei ^a   Wang, Yan ^a   Bai, Yun ^a   Xu, Xueqing ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Gene targeting; Genome editing; TALE nucleases; TALE transcription factors; Transcription activator like effectors

Indexed keywords

BACTERIA (MICROORGANISMS); XANTHOMONAS;

DEOXYRIBONUCLEASE; DNA; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETIC ENGINEERING; GENETIC TRANSCRIPTION; GENETICS; GENOME; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROCEDURES;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DEOXYRIBONUCLEASES; DNA; GENETIC ENGINEERING; GENOME; HUMANS; MOLECULAR SEQUENCE DATA; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84897958499     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2013.11.006     Document Type: Review

References (84)

1. Aravind L., Anantharaman V., Balaji S., Babu M.M., Iyer L.M. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol. Rev. 2005, 29:231-262.
2. Bennetzen J.L., Ma J. The genetic colinearity of rice and other cereals on the basis of genomic sequence analysis. Curr. Opin. Plant Biol. 2003, 6:128-133.
3. Bibikova M., Carroll D., Segal D.J., Trautman J.K., Smith J., Kim Y.-G., Chandrasegaran S. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell Biol. 2001, 21:289-297.
4. Boch J., Bonas U. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 2010, 48:419-436.
5. Boch J., Scholze H., Schornack S., Landgraf A., Hahn S., Kay S., Lahaye T., Nickstadt A., Bonas U. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 2009, 326:1509-1512.
6. Bogdanove A.J., Schornack S., Lahaye T. TAL effectors: finding plant genes for disease and defense. Curr. Opin. Plant Biol. 2010, 13:394-401.
7. Bogdanove A.J., Voytas D.F. TAL effectors: customizable proteins for DNA targeting. Science 2011, 333:1843-1846.
8. Bonas U., Stall R.E., Staskawicz B. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 1989, 218:127-136.
9. Bradley P. Structural modeling of TAL effector-DNA interactions. Protein Sci. 2012, 21:471-474.
10. Briggs A.W., Rios X., Chari R., Yang L., Zhang F., Mali P., Church G.M. Iterative capped assembly: rapid and scalable synthesis of repeat-module DNA such as TAL effectors from individual monomers. Nucleic Acids Res. 2012, 40:e117.
11. Carlson D.F., Tan W., Lillico S.G., Stverakova D., Proudfoot C., Christian M., Voytas D.F., Long C.R., Whitelaw C.B.A., Fahrenkrug S.C. Efficient TALEN-mediated gene knockout in livestock. Proc. Natl. Acad. Sci. U S A 2012, 109:17382-17387.
12. Cathomen T., Joung J.K. Zinc-finger nucleases: the next generation emerges. Mol. Ther. 2008, 16:1200-1207.
13. 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. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucl. Acids Res. 2011, 39:e82.
14. Cho S.W., Kim S., Kim J.M., Kim J.S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 2013, 31:230-232.
15. Christian M., Cermak T., Doyle E.L., Schmidt C., Zhang F., Hummel A., Bogdanove A.J., Voytas D.F. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 2010, 186:757-761.
16. 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. Targeting G with TAL effectors: a comparison of activities of TALENs constructed with NN and NK repeat variable di-residues. PLoS One 2012, 7:e45383.
17. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
18. Cong L., Zhou R., Kuo Y.C., Cunniff M., Zhang F. Comprehensive interrogation of natural TALE DNA-binding modules and transcriptional repressor domains. Nat. Commun. 2012, 3:968.
19. Cornelis G.R., Van Gijsegem F. Assembly and function of type Iii secretory systems. Annu. Rev. Microbiol. 2000, 54:735-774.
20. de Souza T.A., Soprano A.S., de Lira N.P., Quaresma A.J., Pauletti B.A., Paes Leme A.F., Benedetti C.E. The TAL effector PthA4 interacts with nuclear factors involved in RNA-dependent processes including a HMG protein that selectively binds poly(U) RNA. PLoS One 2012, 7:e32305.
21. DeFrancesco L. Move over ZFNs. Nat. Biotechnol. 2011, 29:681-684.
22. Deng D., Yin P., Yan C., Pan X., Gong X., Qi S., Xie T., Mahfouz M., Zhu J.-K., Yan N., Shi Y. Recognition of methylated DNA by TAL effectors. Cell Res. 2012, 22:1502-1504.
23. Domingues M.N., de Campos B.M., de Oliveira M.L., de Mello U.Q., Benedetti C.E. TAL effectors target the C-terminal domain of RNA polymerase II (CTD) by inhibiting the prolyl-isomerase activity of a CTD-associated cyclophilin. PLoS One 2012, 7:e41553.
24. Domingues M.N., De Souza T.A., Cernadas R.A., de Oliveira M.L., Docena C., Farah C.S., Benedetti C.E. The Xanthomonas citri effector protein PthA interacts with citrus proteins involved in nuclear transport, protein folding and ubiquitination associated with DNA repair. Mol. Plant Pathol. 2010, 11:663-675.
25. Elhiti M., Stasolla C. Structure and function of homodomain-leucine zipper (HD-Zip) proteins. Plant Signal Behav. 2009, 4:86-88.
26. Fu Y., Foden J.A., Khayter C., Maeder M.L., Reyon D., Joung J.K., Sander J.D. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 2013, 31:822-826. (advance online publication).
27. Galetto R., Duchateau P., Pâques F. Targeted approaches for gene therapy and the emergence of engineered meganucleases. Expert. Opin. Biol. Ther. 2009, 9:1289-1303.
28. Garg A., Lohmueller J.J., Silver P.A., Armel T.Z. Engineering synthetic TAL effectors with orthogonal target sites. Nucleic Acids Res. 2012, 40:7584-7595.
29. Geissler R., Scholze H., Hahn S., Streubel J., Bonas U., Behrens S.-E., Boch J. Transcriptional activators of human genes with programmable DNA-specificity. PloS One 2011, 6:e19509.
30. Gommans W.M., Haisma H.J., Rots M.G. Engineering zinc finger protein transcription factors: the therapeutic relevance of switching endogenous gene expression on or off at command. J.Mol. Biol. 2005, 354:507-519.
31. Hall D.B., Struhl K. The VP16 activation domain interacts with multiple transcriptional components as determined by protein-protein Cross-linking invivo. J.Biol. Chem. 2002, 277:46043-46050.
32. Heuer H., Yin Y.-N., Xue Q.-Y., Smalla K., Guo J.-H. Repeat domain diversity of avrBs3-like genes in Ralstonia solanacearum strains and association with host preferences in the field. Appl. Environ. Microbiol. 2007, 73:4379-4384.
33. Hockemeyer D., Wang H., Kiani S., Lai C.S., Gao Q., Cassady J.P., Cost G.J., Zhang L., Santiago Y., Miller J.C., Zeitler B., Cherone J.M., Meng X., Hinkley S.J., Rebar E.J., Gregory P.D., Urnov F.D., Jaenisch R. Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 2011, 29:731-734.
34. Hsu P.D., Zhang F. Dissecting neural function using targeted genome engineering technologies. ACS Chem. Neurosci. 2012, 3:603-610.
35. Huertas P. DNA resection in eukaryotes: deciding how to fix the break. Nat. Struct. Mol. Biol. 2010, 17:11-16.
36. Jones S. An overview of the basic helix-loop-helix proteins. Genome. Biol. 2004, 5:226.
37. Kleinstiver B.P., Wolfs J.M., Kolaczyk T., Roberts A.K., Hu S.X., Edgell D.R. Monomeric site-specific nucleases for genome editing. Proc. Natl. Acad. Sci. U S A 2012, 109:8061-8066.
38. Li L., Piatek M.J., Atef A., Piatek A., Wibowo A., Fang X., Sabir J.S.M., Zhu J.-K., Mahfouz M.M. Rapid and highly efficient construction of TALE-based transcriptional regulators and nucleases for genome modification. Plant Mol. Biol. 2012, 78:407-416.
39. Li T., Huang S., Jiang W.Z., Wright D., Spalding M.H., Weeks D.P., Yang B. TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucl. Acids Res. 2011, 39:359-372.
40. Li T., Huang S., Zhao X., Wright D.A., Carpenter S., Spalding M.H., Weeks D.P., Yang B. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucl. Acids Res. 2011, 39:6315-6325.
41. Lieber M.R. The mechanism of human nonhomologous DNA end joining. J.Biol. Chem. 2008, 283:1-5.
42. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end joining pathway. Annu. Rev. Biochem. 2010, 79:181-211.
43. Liu J., Li C., Yu Z., Huang P., Wu H., Wei C., Zhu N., Shen Y., Chen Y., Zhang B., Deng W.-M., Jiao R. Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy. J.Genet. Genomics 2012, 39:209-215.
44. Ma S., Zhang S., Wang F., Liu Y., Liu Y., Xu H., Liu C., Lin Y., Zhao P., Xia Q. Highly efficient and specific genome editing in silkworm using custom TALENs. PLoS One 2012, 7:e45035.
45. Mahfouz M.M., Li L. TALE nucleases and next generation GM crops. GM Crops 2011, 2:99-103.
46. Mahfouz M.M., Li L., Piatek M., Fang X., Mansour H., Bangarusamy D.K., Zhu J.K. Targeted transcriptional repression using a chimeric TALE-SRDX repressor protein. Plant Mol. Biol. 2012, 78:311-321.
47. Mahfouz M.M., Li L., Shamimuzzaman M., Wibowo A., Fang X., Zhu J.-K. De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc. Natl. Acad. Sci. U S A 2011, 108:2623-2628.
48. Mak A.N.-S., Bradley P., Cernadas R.A., Bogdanove A.J., Stoddard B.L. The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 2012, 335:716-719.
49. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
50. Mannervik M. Target genes of homeodomain proteins. Bioessays 1999, 21:267-270.
51. McMahon M.A., Rahdar M., Porteus M. Gene editing: not just for translation anymore. Nat. Methods 2012, 9:28-31.
52. 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., Dulay G.P., Hua K.L., Ankoudinova I., Cost G.J., Urnov F.D., Zhang H.S., Holmes M.C., Zhang L., Gregory P.D., Rebar E.J. ATALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 2011, 29:143-148.
53. Morbitzer R., Elsaesser J., Hausner J., Lahaye T. Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res. 2011, 39:5790-5799.
54. Morbitzer R., Romer P., Boch J., Lahaye T. Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. Proc. Natl. Acad. Sci. U S A 2010, 107:21617-21622.
55. Moscou M.J., Bogdanove A.J. Asimple cipher governs DNA recognition by TAL effectors. Science 2009, 326:1501.
56. Mussolino C., Morbitzer R., Lutge F., Dannemann N., Lahaye T., Cathomen T. Anovel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res. 2011, 39:9283-9293.
57. Römer P., Hahn S., Jordan T., Strauß T., Bonas U., Lahaye T. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 2007, 318:645-648.
58. Ramirez C.L., Foley J.E., Wright D.A., Müller-Lerch F., Rahman S.H., Cornu T.I., Winfrey R.J., Sander J.D., Fu F., Townsend J.A., Cathomen T., Voytas D.F., Joung J.K. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods 2008, 5:374-375.
59. Reyon D., Tsai S.Q., Khayter C., Foden J.A., Sander J.D., Joung J.K. FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 2012, 30:460-465.
60. Romer P., Recht S., Lahaye T. Asingle plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc. Natl. Acad. Sci. U S A 2009, 106:20526-20531.
61. Romer P., Strauss T., Hahn S., Scholze H., Morbitzer R., Grau J., Bonas U., Lahaye T. Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol. 2009, 150:1697-1712.
62. Ronald P., Leung H. The rice genome. The most precious things are not jade and pearls. Science 2002, 296:58-59.
63. Sander J.D., Cade L., Khayter C., Reyon D., Peterson R.T., Joung J.K., Yeh J.-R.J. Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat. Biotechnol. 2011, 29:697-698.
64. Sanjana N.E., Cong L., Zhou Y., Cunniff M.M., Feng G., Zhang F. Atranscription activator-like effector toolbox for genome engineering. Nat. Protoc. 2012, 7:171-192.
65. Schiffer J.T., Aubert M., Weber N.D., Mintzer E., Stone D., Jerome K.R. Targeted DNA mutagenesis for the cure of chronic viral infections. J.Virol. 2012, 86:8920-8936.
66. Schmid-Burgk J.L., Schmidt T., Kaiser V., Honing K., Hornung V. Aligation-independent cloning technique for high-throughput assembly of transcription activator-like effector genes. Nat. Biotechnol. 2013, 31:76-81.
67. Scholze H., Boch J. TAL effector-DNA specificity. Virulence 2010, 1:428-432.
68. Schornack S., Meyer A., Römer P., Jordan T., Lahaye T. Gene-for-gene-mediated recognition of nuclear-targeted AvrBs3-like bacterial effector proteins. J.Plant Physiol. 2006, 163:256-272.
69. Singh N., Ma Z., Gemmill T., Wu X., Defiglio H., Rossettini A., Rabeler C., Beane O., Morse R.H., Palumbo M.J., Hanes S.D. The Ess1 prolyl isomerase is required for transcription termination of small noncoding RNAs via the Nrd1 pathway. Mol. Cell. 2009, 36:255-266.
70. Streubel J., Blücher C., Landgraf A., Boch J. TAL effector RVD specificities and efficiencies. Nat. Biotechnol. 2012, 30:593-595.
71. Sun N., Liang J., Abil Z., Zhao H. Optimized TAL effector nucleases (TALENs) for use in treatment of sickle cell disease. Mol. Biosyst. 2012, 8:1255-1263.
72. Szurek B., Marois E., Bonas U., Van den Ackerveken G. Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 2001, 26:523-534.
73. Szurek B., Rossier O., Hause G., Bonas U. Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol. Microbiol. 2002, 46:13-23.
74. Tesson L., Usal C., Ménoret S., Leung E., Niles B.J., Remy S., Santiago Y., Vincent A.I., Meng X., Zhang L., Gregory P.D., Anegon I., Cost G.J. Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol. 2011, 29:695-696.
75. Urnov F.D., Rebar E.J., Holmes M.C., Zhang H.S., Gregory P.D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 2010, 11:636-646.
76. Van den Ackerveken G., Marois E., Bonas U. Recognition of the bacterial a virulence protein AvrBs3 occurs inside the host plant cell. Cell 1996, 87:1307-1316.
77. van der Oost J. Molecular biology. New tool for genome surgery. Science 2013, 339:768-770.
78. Voytas D.F., Joung J.K. Plant science. DNA binding made easy. Science 2009, 326:1491-1492.
79. Watanabe T., Ochiai H., Sakuma T., Horch H.W., Hamaguchi N., Nakamura T., Bando T., Ohuchi H., Yamamoto T., Noji S., Mito T. Non-transgenic genome modifications in a hemimetabolous insect using zinc-finger and TAL effector nucleases. Nat. Commun. 2012, 3:1017.
80. Weber E., Engler C., Gruetzner R., Werner S., Marillonnet S. Amodular cloning system for standardized assembly of multigene constructs. PLoS One 2011, 6:e16765.
81. 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., Zhang L., Rebar E.J., Gregory P.D., Urnov F.D., Meyer B.J. Targeted genome editing across species using ZFNs and TALENs. Science 2011, 333:307.
82. Yin P., Deng D., Yan C., Pan X., Xi J.J., Yan N., Shi Y. Specific DNA-RNA hybrid recognition by TAL effectors. Cell Rep. 2012, 2:707-713.
83. Zhang F., Cong L., Lodato S., Kosuri S., Church G.M., Arlotta P. Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat. Biotechnol. 2011, 29:149-153.
84. Zhu W., Yang B., Chittoor J.M., Johnson L.B., White F.F. AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol. Plant Microbe. Interact. 1998, 11:824-832.