TAL effectors specificity stems from negative discrimination

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Wicky, Basile I M ^a   Stenta, Marco ^a   Dal Peraro, Matteo ^a,b  

^a Laboratory of Computational Systems Biology Institute of Bioengineering School of Life Sciences   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; PLANT DNA;

AMINO ACID SEQUENCE; CHEMISTRY; DNA METHYLATION; GENETICS; MICROBIOLOGY; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PHYSIOLOGY; PLANT DISEASE; PROMOTER REGION; TANDEM REPEAT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA METHYLATION; DNA, PLANT; DNA-BINDING PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PROMOTER REGIONS, GENETIC; TANDEM REPEAT SEQUENCES;

EID: 84894261610     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080261     Document Type: Article

References (50)

1. Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13: 394-401.
2. Boch J, Bonas U (2010) Xanthomonas AvrBs3 Family-Type III Effectors: Discovery and Function. Annu Rev Phytopathol 48: 419-436.
3. Scholze H, Boch J (2011) TAL effectors are remote controls for gene activation. Curr Opin Microbiol 14: 47-53.
4. Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326: 1501.
5. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, et al. (2009) Breaking the Code of DNA Binding Specificity of TAL-Type III Effectors. Science 326: 1509-1512.
6. Morbitzer R, Römer P, Boch J, Lahaye T (2010) Regulation of selected genome loci using de novo-engineered transcription activator-like effector (TALE)-type transcription factors. Proc Natl Acad Sci U S A 107: 21617-21622.
7. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143-148.
8. Garg A, Lohmueller JJ, Silver PA, Armel TZ (2012) Engineering synthetic TAL effectors with orthogonal target sites. Nucleic Acids Res 40: 7584-7595.
9. Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, et al. (2011) 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 108: 2623-2628.
10. Mussolino C, Morbitzer R, Lütge F, Dannemann N, Lahaye T, et al. (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39: 9283-9293.
11. Li T, Huang S, Jiang WZ, Wright D, Spalding MH, et al. (2011) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39: 359-372.
12. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, et al. (2010) Targeting DNA Double-Strand Breaks with TAL Effector Nucleases. Genetics 186: 757-761.
13. Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, et al. (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29: 697-698.
14. Tesson L, Usal C, Menoret S, Leung E, Niles BJ, et al. (2011) Knockout rats generated by embryo microinjection of TALENs. Nat Biotechnol 29: 695-696.
15. Zhang F, Cong L, Lodato S, Kosuri S, Church GM, et al. (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat Biotechnol 29: 149-153.
16. Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, et al. (2011) Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 29: 731-734.
17. Murakami MT, Sforça ML, Neves JL, Paiva JH, Domingues MN, et al. (2010) The repeat domain of the type III effector protein PthA shows a TPR-like structure and undergoes conformational changes upon DNA interaction. Proteins 78: 3386-3395.
18. Mak ANS, Bradley P, Cernadas RA, Bogdanove AJ, Stoddard BL (2012) The Crystal Structure of TAL Effector PthXo1 Bound to Its DNA Target. Science 335: 716-719.
19. Deng D, Yan CY, Pan XJ, Mahfouz M, Wang JW, et al. (2012) Structural Basis for Sequence-Specific Recognition of DNA by TAL Effectors. Science 335: 720-723.
20. Bochtler M (2012) Structural basis of the TAL effector-DNA interaction. Biol Chem 393: 1055-1066.
21. Mak AN, Bradley P, Bogdanove AJ, Stoddard BL (2013) TAL effectors: function, structure, engineering and applications. Curr Opin Struct Biol 23: 93-99.
22. Streubel J, Blucher C, Landgraf A, Boch J (2012) TAL effector RVD specificities and efficiencies. Nat Biotechnol 30: 593-595.
23. Deng D, Yin P, Yan CY, Pan XJ, Gong XQ, et al. (2012) Recognition of methylated DNA by TAL effectors. Cell Res 22: 1502-1504.
24. Levitt M (2001) The birth of computational structural biology. Nat Struct Biol 8: 392-393.
25. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802. (Pubitemid 43078511)
26. Perez A, Marchan I, Svozil D, Sponer J, Cheatham TE 3rd, et al. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers. Biophys J 92: 3817-3829. (Pubitemid 46910569)
27. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of Simple Potential Functions for Simulating Liquid Water. J Chem Phys 79: 926-935.
28. Karplus M, McCammon JA (2002) Molecular dynamics simulations of biomolecules. Nat Struct Biol 9: 646-652. (Pubitemid 34977295)
29. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, et al. (2000) Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 33: 889-897. (Pubitemid 32056774)
30. Noskov SY, Lim C (2001) Free energy decomposition of protein-protein interactions. Biophys J 81: 737-750. (Pubitemid 32721449)
31. Rucker R, Oelschlaeger P, Warshel A (2010) A binding free energy decomposition approach for accurate calculations of the fidelity of DNA polymerases. Proteins 78: 671-680.
32. Case DA, Cheatham TE 3rd, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688. (Pubitemid 43076180)
33. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, et al. (2009) Gaussian 09, Revision A.1. Wallingford CT: Gaussian 09, Revision A.1, Gaussian, Inc.
34. Wagner S, Stenta M, Metzger LC, Dal Peraro M, Cornelis GR (2010) Length control of the injectisome needle requires only one molecule of Yop secretion protein P (YscP). Proc Natl Acad Sci U S A 107: 13860-13865.
35. Wong S, Amaro RE, McCammon JA (2009) MM-PBSA Captures Key Role of Intercalating Water Molecules at a Protein-Protein Interface. J Chem Theory Comput 5: 422-429.
36. Chen L, Zheng QC, Yu LY, Chu WT, Zhang JL, et al. (2012) Insights into the thermal stabilization and conformational transitions of DNA by hyperthermophile protein Sso7d: molecular dynamics simulations and MM-PBSA analysis. J Biomol Struct Dyn 30: 716-727.
37. Moroni E, Caselle M, Fogolari F (2007) Identification of DNA-binding protein target sequences by physical effective energy functions: free energy analysis of lambda repressor-DNA complexes. BMC Struct Biol 7: 61.
38. Brice AR, Dominy BN (2011) Analyzing the robustness of the MM/PBSA free energy calculation method: application to DNA conformational transitions. J Comput Chem 32: 1431-1440.
39. Blasco B, Stenta M, Alonso-Sarduy L, Dietler G, Dal Peraro M, et al. (2011) Atypical DNA recognition mechanism used by the EspR virulence regulator of Mycobacterium tuberculosis. Mol Microbiol 82: 251-264.
40. Gao H, Wu X, Chai J, Han Z (2012) Crystal structure of a TALE protein reveals an extended N-terminal DNA binding region. Cell Res 22: 1716-1720.
41. Meckler JF, Bhakta MS, Kim MS, Ovadia R, Habrian CH, et al. (2013) Quantitative analysis of TALE-DNA interactions suggests polarity effects. Nucleic Acids Res 41: 4118-4128.
42. Zou X, Ma W, Solov'yov IA, Chipot C, Schulten K (2012) Recognition of methylated DNA through methyl-CpG binding domain proteins. Nucleic Acids Res 40: 2747-2758.
43. Swindells MB, MacArthur MW, Thornton JM (1995) Intrinsic φ,ψ propensities of amino acids, derived from the coil regions of known structures. Nat Struct Biol 2: 596-603.
44. Best Robert B, de Sancho D, Mittal J (2012) Residue-Specific α-Helix Propensities from Molecular Simulation. Biophys J 102: 1462-1467.
45. Nick Pace C, Martin Scholtz J (1998) A Helix Propensity Scale Based on Experimental Studies of Peptides and Proteins. Biophys J 75: 422-427.
46. Basu G, Sivanesan D, Kawabata T, Go N (2004) Electrostatic potential of nucleotide-free protein is sufficient for discrimination between adenine and guanine-specific binding sites. J Mol Biol 342: 1053-1066. (Pubitemid 39165667)
47. 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.
48. Christian ML, Demorest ZL, Starker CG, Osborn MJ, Nyquist MD, et al. (2012) Targeting G with TAL effectors: a comparison of activities of TALENs constructed with NN and NK repeat variable di-residues. PLoS One 7: e45383.
49. Huang P, Xiao A, Zhou M, Zhu Z, Lin S, et al. (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29: 699-700.
50. Vanyushin BF, Ashapkin VV (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta 1809: 360-368.