Nuance in the double-helix and its role in protein-DNA recognition

Current Opinion in Structural Biology

Volumn 19, Issue 2, 2009, Pages 171-177

  Rohs, Remo ^a   West, Sean M ^a   Liu, Peng ^a   Honig, Barry ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEIN; TRANSCRIPTION FACTOR;

BINDING SITE; DNA HELIX; DNA PROTEIN COMPLEX; DNA STRUCTURE; ENERGY TRANSFER; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; MONTE CARLO METHOD; NUCLEOSOME; PREDICTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; REVIEW; SEQUENCE ANALYSIS; SIMULATION;

BINDING SITES; COMPUTER SIMULATION; DNA; MONTE CARLO METHOD; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; PROTEIN CONFORMATION; PROTEINS; TRANSCRIPTION FACTORS;

EID: 64649095501     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2009.03.002     Document Type: Review

References (58)

1. Sarai A., and Kono H. Protein-DNA recognition patterns and predictions. Annu Rev Biophys Biomol Struct 34 (2005) 379-398
2. Joshi R., Passner J.M., Rohs R., Jain R., Sosinsky A., Crickmore M.A., Jacob V., Aggarwal A.K., Honig B., and Mann R.S. Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell 131 (2007) 530-543. This paper establishes sequence-dependent minor groove shape as the molecular basis of Hox specificity. The paper introduces local shape readout as a new mode of protein-DNA recognition.
3. Dixit S.B., Beveridge D.L., Case D.A., Cheatham III T.E., Giudice E., Lankas F., Lavery R., Maddocks J.H., Osman R., Sklenar H., et al. Molecular dynamics simulations of the 136 unique tetranucleotide sequences of DNA oligonucleotides. II: sequence context effects on the dynamical structures of the 10 unique dinucleotide steps. Biophys J 89 (2005) 3721-3740. This work reports structural information on all 136 unique tetranucleotides based on MD simulations with the AMBER94 force field.
4. Fujii S., Kono H., Takenaka S., Go N., and Sarai A. Sequence-dependent DNA deformability studied using molecular dynamics simulations. Nucleic Acids Res 35 (2007) 6063-6074. This study reports structural information on all 136 unique tetranucleotides based on MD simulations with the AMBER99 force field.
5. Rohs R., Sklenar H., and Shakked Z. Structural and energetic origins of sequence-specific DNA bending: Monte Carlo simulations of papillomavirus E2-DNA binding sites. Structure 13 (2005) 1499-1509. This paper provides insights into the molecular basis of indirect readout mechanisms and predicts sequence-dependent DNA bending based on MC simulations.
6. Czapla L., Swigon D., and Olson W.K. Effects of the nucleoid protein HU on the structure, flexibility, and ring-closure properties of DNA deduced from Monte Carlo simulations. J Mol Biol 382 (2008) 353-370. This paper uses MC simulations based on a coarse-grained model to show that the non-specific binding of the histone-like HU protein to DNA stabilizes structural distortions that assist in DNA ring closure.
7. Segal E., Fondufe-Mittendorf Y., Chen L., Thastrom A., Field Y., Moore I.K., Wang J.P., and Widom J. A genomic code for nucleosome positioning. Nature 442 (2006) 772-778. This study determines nucleosome sites in vivo and tries to predict these sites based on an approach that employs dinucleotide occupancy statistics.
8. 31P chemical shift anisotropy. J Biomol NMR 26 (2003) 297-315
9. Nelson H.C., Finch J.T., Luisi B.F., and Klug A. The structure of an oligo(dA)·oligo(dT) tract and its biological implications. Nature 330 (1987) 221-226
10. Hizver J., Rozenberg H., Frolow F., Rabinovich D., and Shakked Z. DNA bending by an adenine-thymine tract and its role in gene regulation. Proc Natl Acad Sci U S A 98 (2001) 8490-8495
11. Crothers D.M., and Shakked Z. DNA bending by adenine-thymine tracts. In: Neidle S. (Ed). Oxford Handbook of Nucleic Acid Structures (1999), Oxford University Press 455-470
12. Gorin A.A., Zhurkin V.B., and Olson W.K. B-DNA twisting correlates with base-pair morphology. J Mol Biol 247 (1995) 34-48
13. Olson W.K., Gorin A.A., Lu X.J., Hock L.M., and Zhurkin V.B. DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc Natl Acad Sci U S A 95 (1998) 11163-11168
14. Burkhoff A.M., and Tullius T.D. Structural details of an adenine tract that does not cause DNA to bend. Nature 331 (1988) 455-457
15. Greenbaum J.A., Pang B., and Tullius T.D. Construction of a genome-scale structural map at single-nucleotide resolution. Genome Res 17 (2007) 947-953. This study uses hydroxyl radical cleavage data to provide genome-wide structural information on the solvent-accessible surface area of DNA.
16. Cheatham III T.E. Simulation and modeling of nucleic acid structure, dynamics and interactions. Curr Opin Struct Biol 14 (2004) 360-367
17. Cheatham III T.E., and Kollman P.A. Molecular dynamics simulation of nucleic acids. Annu Rev Phys Chem 51 (2000) 435-471
18. Perez A., Marchan I., Svozil D., Sponer J., Cheatham III T.E., Laughton C.A., and Orozco M. Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers. Biophys J 92 (2007) 3817-3829. This work attempts to correct the AMBER force field imbalance regarding α/γ-backbone torsion angle flips.
19. Lankas F., Lavery R., and Maddocks J.H. Kinking occurs during molecular dynamics simulations of small DNA minicircles. Structure 14 (2006) 1527-1534
20. Perez A., Luque F.J., and Orozco M. Dynamics of B-DNA on the microsecond time scale. J Am Chem Soc 129 (2007) 14739-14745
21. Orozco M., Noy A., and Perez A. Recent advances in the study of nucleic acid flexibility by molecular dynamics. Curr Opin Struct Biol 18 (2008) 185-193
22. Babin V., Baucom J., Darden T.A., and Sagui C. Molecular dynamics simulations of DNA with polarizable force fields: convergence of an ideal B-DNA structure to the crystallographic structure. J Phys Chem B 110 (2006) 11571-11581
23. Chocholousova J., and Feig M. Implicit solvent simulations of DNA and DNA-protein complexes: agreement with explicit solvent vs experiment. J Phys Chem B 110 (2006) 17240-17251
24. Prabhu N.V., Panda M., Yang Q., and Sharp K.A. Explicit ion, implicit water solvation for molecular dynamics of nucleic acids and highly charged molecules. J Comput Chem 29 (2008) 1113-1130
25. Bomble Y.J., and Case D.A. Multiscale modeling of nucleic acids: insights into DNA flexibility. Biopolymers 89 (2008) 722-731
26. Sklenar H., Wustner D., and Rohs R. Using internal and collective variables in Monte Carlo simulations of nucleic acid structures: chain breakage/closure algorithm and associated Jacobians. J Comput Chem 27 (2006) 309-315
27. Rohs R., Bloch I., Sklenar H., and Shakked Z. Molecular flexibility in ab initio drug docking to DNA: binding-site and binding-mode transitions in all-atom Monte Carlo simulations. Nucleic Acids Res 33 (2005) 7048-7057. This paper presents the first ab initio drug-DNA docking method with complete flexibility of both the ligand and receptor molecule throughout the docking process.
28. Mackerell Jr. A.D., and Nilsson L. Molecular dynamics simulations of nucleic acid-protein complexes. Curr Opin Struct Biol 18 (2008) 194-199
29. Pan Y., and Nussinov R. Structural basis for p53 binding-induced DNA bending. J Biol Chem 282 (2007) 691-699. This paper used MD simulations to provide insights into the architecture of the complex formed by the p53 tetramer with its consensus DNA binding site.
30. Pan Y., and Nussinov R. p53-Induced DNA bending: the interplay between p53-DNA and p53-p53 interactions. J Phys Chem B 112 (2008) 6716-6724
31. Ma B., Pan Y., Gunasekaran K., Venkataraghavan R.B., Levine A.J., and Nussinov R. Comparison of the protein-protein interfaces in the p53-DNA crystal structures: towards elucidation of the biological interface. Proc Natl Acad Sci U S A 102 (2005) 3988-3993
32. Kitayner M., Rozenberg H., Kessler N., Rabinovich D., Shaulov L., Haran T.E., and Shakked Z. Structural basis of DNA recognition by p53 tetramers. Mol Cell 22 (2006) 741-753. This study presents the first crystal structures of p53 tetramer-DNA complexes.
33. Swigon D., Coleman B.D., and Olson W.K. Modeling the Lac repressor-operator assembly: the influence of DNA looping on Lac repressor conformation. Proc Natl Acad Sci U S A 103 (2006) 9879-9884
34. Arya G., and Schlick T. Role of histone tails in chromatin folding revealed by a mesoscopic oligonucleosome model. Proc Natl Acad Sci U S A 103 (2006) 16236-16241
35. Rocchia W., Sridharan S., Nicholls A., Alexov E., Chiabrera A., and Honig B. Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects. J Comput Chem 23 (2002) 128-137
36. Honig B., and Nicholls A. Classical electrostatics in biology and chemistry. Science 268 (1995) 1144-1149
37. Paillard G., and Lavery R. Analyzing protein-DNA recognition mechanisms. Structure 12 (2004) 113-122. This work suggests that optimal base sequences of protein binding sites can be derived from the relative energetic contributions of direct and indirect readout.
38. Gromiha M.M., Siebers J.G., Selvaraj S., Kono H., and Sarai A. Role of inter and intramolecular interactions in protein-DNA recognition. Gene 364 (2005) 108-113
39. Morozov A.V., Havranek J.J., Baker D., and Siggia E.D. Protein-DNA binding specificity predictions with structural models. Nucleic Acids Res 33 (2005) 5781-5798. This approach includes inter- and intra-base pair deformation energy in the development of a knowledge-based potential to predict protein-DNA binding specificity.
40. Ahmad S., Kono H., Arauzo-Bravo M.J., and Sarai A. ReadOut: structure-based calculation of direct and indirect readout energies and specificities for protein-DNA recognition. Nucleic Acids Res 34 (2006) W124-W127
41. Jamal Rahi S., Virnau P., Mirny L.A., and Kardar M. Predicting transcription factor specificity with all-atom models. Nucleic Acids Res 36 (2008) 6209-6217
42. Siggers T.W., Silkov A., and Honig B. Structural alignment of protein-DNA interfaces: insights into the determinants of binding specificity. J Mol Biol 345 (2005) 1027-1045
43. 2 zinc-finger binding specificity: sensitivity to docking geometry. Nucleic Acids Res 35 (2007) 1085-1097. This paper reports the use of protein-DNA structures to predict binding specificity and considers the possibility of predicting position weight matrices (PWM) for an entire protein family based on the structures of just a few family members.
44. Havranek J.J., Duarte C.M., and Baker D. A simple physical model for the prediction and design of protein-DNA interactions. J Mol Biol 344 (2004) 59-70
45. Ashworth J., Havranek J.J., Duarte C.M., Sussman D., Monnat Jr. R.J., Stoddard B.L., and Baker D. Computational redesign of endonuclease DNA binding and cleavage specificity. Nature 441 (2006) 656-659
46. Morozov A.V., and Siggia E.D. Connecting protein structure with predictions of regulatory sites. Proc Natl Acad Sci U S A 104 (2007) 7068-7073. This work integrates homology modeling of transcription factors with a database of protein-DNA contact geometry in genome-wide transcription factor binding site prediction.
47. Lu X.J., and Olson W.K. 3DNA: a versatile, integrated software system for the analysis, rebuilding and visualization of three-dimensional nucleic-acid structures. Nat Protoc 3 (2008) 1213-1227
48. Tolstorukov M.Y., Colasanti A.V., McCandlish D.M., Olson W.K., and Zhurkin V.B. A novel roll-and-slide mechanism of DNA folding in chromatin: implications for nucleosome positioning. J Mol Biol 371 (2007) 725-738. This paper reveals the detailed relationship between dinucleotide geometry and nucleosomal topology and superhelical pitch.
49. Tolstorukov M.Y., Choudhary V., Olson W.K., Zhurkin V.B., and Park P.J. nuScore: a web-interface for nucleosome positioning predictions. Bioinformatics 24 (2008) 1456-1458
50. Kaplan N., Moore I.K., Fondufe-Mittendorf Y., Gossett A.J., Tillo D., Field Y., Leproust E.M., Hughes T.R., Lieb J.D., Widom J., et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458 (2009) 362-366
51. Gabdank I., Barash D., and Trifonov E.N. Nucleosome DNA Bendability Matrix (C. elegans). J Biomol Struct Dyn 26 (2009) 403-412
52. Iwahara J., Zweckstetter M., and Clore G.M. NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA. Proc Natl Acad Sci U S A 103 (2006) 15062-15067. This NMR study shows that, while the HoxD9 homeodomain binds to DNA both specifically and non-specifically with a similar binding geometry, arginine side chains at the interface are more flexible when in contact with the non-specific sequence.
53. Gorman J., and Greene E.C. Visualizing one-dimensional diffusion of proteins along DNA. Nat Struct Mol Biol 15 (2008) 768-774
54. Givaty O., and Levy Y. Protein sliding along DNA: dynamics and structural characterization. J Mol Biol 385 (2009) 1087-1097
55. Lavery R., and Sklenar H. Defining the structure of irregular nucleic acids: conventions and principles. J Biomol Struct Dyn 6 (1989) 655-667
56. Petrey D., and Honig B. GRASP2: visualization, surface properties, and electrostatics of macromolecular structures and sequences. Methods Enzymol 374 (2003) 492-509
57. Parker SC, Hansen L, Abaan HO, Tullius TD, Margulies EH: Local DNA topography correlates with functional noncoding regions of the human genome. Science, doi:10.1126/science.1169050, published online 12 March 2009. This paper uses hydroxyl radical cleavage data to show that there is evolutionary pressure to conserve DNA shape.
58. Locasale J.W., Napoli A.A., Chen S., Berman H.M., and Lawson CL:. Signatures of protein-DNA recognition in free DNA binding sites. J Mol Biol 386 (2009) 1054-1065. Based on crystal structures of DNA sequences, which were previously crystallized in protein-DNA complexes (MetR, PurR, and Zif268), this study suggests that structural features observed in free-DNA are conserved upon protein binding.