Programmable DNA-binding proteins from Burkholderia provide a fresh perspective on the TALE-like repeat domain

Nucleic Acids Research

Volumn 42, Issue 11, 2014, Pages 7436-7449

  Lahaye, Thomas ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; BAT1 PROTEIN; BAT2 PROTEIN; BAT3 PROTEIN; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BURKHOLDERIA; BURKHOLDERIA RHIZOXINICA; CARBOXY TERMINAL SEQUENCE; CHIMERA; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; GENETIC CODE; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN POLYMORPHISM; PROTEIN PROCESSING; PROTEIN TARGETING; TANDEM REPEAT; TRANSCRIPTION INITIATION; VARIABLE NUMBER OF TANDEM REPEAT; WILD TYPE;

BACTERIAL PROTEINS; BURKHOLDERIA; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA; DNA CLEAVAGE; DNA-BINDING PROTEINS; GENOME, BACTERIAL; HEK293 CELLS; HUMANS; NUCLEAR LOCALIZATION SIGNALS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84903213705     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku329     Document Type: Article

References (35)

1. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A. and Bonas, U. (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science, 326, 1509-1512.
2. Moscou, M.J. and Bogdanove, A.J. (2009) A simple cipher governs DNA recognition by TAL effectors. Science, 326, 1501.
3. Boch, J. and Bonas, U. (2010) Xanthomonas AvrBs3 family-type III effectors: Discovery and function. Annu. Rev. Phytopathol., 418, 419-436.
4. Deng, D., Yan, C., Pan, X., Mahfouz, M., Wang, J., Zhu, J.-K., Shi, Y. and Yan, N. (2012) Structural basis for sequence-specific recognition of DNA by TAL effectors. Science, 335, 720-723.
5. Mak, A.N.-S., Bradley, P., Cernadas, R.A., Bogdanove, A.J. and Stoddard, B.L. (2012) The crystal structure of TAL effector PthXo1 bound to its DNA target. Science, 335, 716-719.
6. Doyle, E.L., Stoddard, B.L., Voytas, D.F. and Bogdanove, A.J. (2013) TAL effectors: Highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol., 23, 390-398.
7. Mendenhall, E.M., Williamson, K.E., Reyon, D., Zou, J.Y., Ram, O., Joung, J.K. and Bernstein, B.E. (2013) Locus-specific editing of histone modifications at endogenous enhancers. Nat. Biotechnol., 31, 1133-1136.
8. Maeder, M.L., Angstman, J.F., Richardson, M.E., Linder, S.J., Cascio, V.M., Tsai, S.Q., Ho, Q.H., Sander, J.D., Reyon, D., Bernstein, B.E. et al. (2013) Targeted DNA demethylation and activation of endogenous genes using programmable TALE-TET1 fusion proteins. Nat. Biotechnol., 31, 1137-1142.
9. Konermann, S., Brigham, M.D., Trevino, A.E., Hsu, P.D., Heidenreich, M., Cong, L., Platt, R.J., Scott, D.A., Church, G.M. and Zhang, F. (2013) Optical control of mammalian endogenous transcription and epigenetic states. Nature, 500, 472-476.
10. de Lange, O., Schreiber, T., Schandry, N., Radeck, J., Braun, K.H., Koszinowski, J., Heuer, H., Strauß, A. and Lahaye, T. (2013) Breaking the DNA binding code of Ralstonia solanacearum TAL effectors provides new possibilities to generate plant resistance genes against bacterial wilt disease. New Phytol., 199, 773-786.
11. Lackner, G., Moebius, N., Partida-Martinez, L.P., Boland, S. and Hertweck, C. (2011) Evolution of an endofungal lifestyle: Deductions from the Burkholderia rhizoxinica genome. BMC Genomics, 12, 210.
12. Lackner, G., Moebius, N., Partida-Martinez, L. and Hertweck, C. (2011) Complete genome sequence of Burkholderia rhizoxinica, an endosymbiont of Rhizopus microsporus. J. Bacteriol., 193, 783-784.
13. Stella, S., Molina, R., Bertonatti, C., Juillerrat, A. and Montoya, G. (2014). Expression, purification, crystallization and preliminary X-ray diffraction analysis of the novel modular DNA-binding protein BurrH in its apo form and in complex with its target DNA. Acta Crystallogr. F, 70, 87-91.
14. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675.
15. Morbitzer, R., Elsaesser, J., Hausner, J. and Lahaye, T. (2011) Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res., 39, 5790-5799.
16. Nakamura, S., Mano, S., Tanaka, Y., Ohnishi, M., Nakamori, C., Araki, M., Niwa, T., Nishimura, M., Kaminaka, H., Nakagawa, T. et al. (2010) Gateway binary vectors with the bialaphos resistance gene, bar, as a selection marker for plant tranformation. Biosci. Biotechnol. Biochem., 74, 1315-1319.
17. Meckler, J.F., Bhakta, M.S., Kim, M.-S., Ovadia, R., Habrian, C.H., Zykovich, A., Yu, A., Lockwood, S.H., Morbitzer, R., Els̈aesser, J. et al. (2013) Quantitative analysis of TALE-DNA interactions suggests polarity effects. Nucleic Acids Res., 41, 4118-4128.
18. Mussolino, C., Morbitzer, R., L̈utge, F., Dannemann, N., Lahaye, T. and Cathomen, T. (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res., 39, 9283-9293.
19. Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J. and Lopez, R. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res., 38, W695-W699.
20. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Soding, J. et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7, 539.
21. Strauß, T., Van Poecke, R., Strauß, A., R̈omer, P., Minsavage, G.V., Singh, S., Wolf, C., Strauß, A., Kim, S., Lee, H.-A. et al. (2012) RNA-seq pinpoints a Xanthomonas TAL-effector activated resistance gene in a large crop genome. Proc. Natl. Acad. Sci. U.S.A., 109, 19480-19485.
22. Juillerat, A., Bertonati, C., Dubois, G., Guyot, V., Thomas, S., Valton, J., Beurdeley, M., Silva, G.H., Daboussi, F. and Duchateau, P. (2014). BurrH: A new modular DNA binding protein for genome engineering. Sci. Rep., 4, 3831.
23. 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. et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol., 29, 143-148.
24. Lamb, B.M., Mercer, A.C. and Barbas, C.F. III. (2013) Directed evolution of the TALE N-terminal domain for recognition of all 5' bases. Nucleic Acids Res., 41, 9779-9785.
25. Tsuji, S., Futaki, S. and Imanishi, M. (2013) Creating a TALE protein with unbiased 5'-T binding. Biochem. Biophys. Res. Commun., 1, 262-265.
26. Gao, H., Wu, X., Chai, J. and Han, Z. (2012) Crystal structure of a TALE protein reveals an extended N-terminal DNA binding region. Cell Res., 22, 1716-1720.
27. Garg, A., Lohmueller, J.J., Silver, P.A. and Armel, T.Z. (2012) Engineering synthetic TAL effectors with orthogonal target sites. Nucleic Acids Res., 40, 7584-7595.
28. Perez-Quintero, A.L., Rodriguez, R.L., Dereeper, A., Lopez, C., Koebnik, R., Szurek, B. and Cunnac, S. (2013) An improved method for TAL effectors DNA-binding sites prediction reveals functional convergence in TAL repertoires of Xanthomonas oryzae strains. PLoS One, 8, e68464.
29. Mali, P., Aach, J., Stranges, P.B., Esvelt, K.M., Moosburner, M., Kosuri, S., Yang, L. and Church, G.M. (2013) CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol., 31, 833-838.
30. Zhang, F., Cong, L., Lodato, S., Kosuri, S., Church, G.M. and Arlotta, P. (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat. Biotechnol., 29, 149-153.
31. Wicky, B.I., Stenta, M. and Dal Peraro, M. (2013) TAL effectors specificity stems from negative discrimination. PLoS One, 8, e80261.
32. Holkers, M., Maggio, I., Liu, J., Janssen, J.M., Miselli, F., Mussolino, C., Recchia, A., Cathomen, T. and Gonçalves, M.A.F.V. (2013) Differential integrity of TALE nuclease genes following adenoviral and lentiviral vector gene transfer into human cells. Nucleic Acids Res., 41, e63.
33. Sakuma, T., Ochiai, H., Kaneko, T., Mashimo, T., Tokumasu, D., Sakane, Y., Suzuki, K. I., Miyamoto, T., Sakamoto, N., Matsuura, S. et al. (2013) Repeating pattern of non-RVD variations in DNA-binding modules enhances TALEN activity. Sci. Rep., 3.
34. Yang, Y. and Gabriel, D.W. (1995) Intragenic recombination of a single plant pathogen gene provides a mechanism for the evolution of new host specificities. J. Bacteriol., 177, 4963-4968.
35. Yang, B., Sugio, A. and White, F.F. (2005) Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 18, 142-149.