Biopolym. Cell. 2010; 26(5):360-372.
http://dx.doi.org/10.7124/bc.00016A
Reviews
Variability of DNA structure and protein-nucleic acid reconginition
1Boryskina O. P., 1Tkachenko M. Yu., 1Shestopalova A. V.
  1. A. Usikov Institute of Radio Physics and Electronics, NAS of Ukraine
    12, Proskura Str., Kharkov, Ukraine, 61085

Abstract

Revealing molecular mechanisms of sequence-specific recognition of DNA by proteins is one of the key tasks of biology. The current review presents the results of statistical analysis of the structural databases obtained by different scientific groups studying the conformational features of free and protein-bound DNA fragments that could be used for clarifying the mechanisms of protein-nucleic acid recognition. The analysis of the published data allowed us to make the following generalizations. The ability of DNA double helix to adopt alternative conformations, including the ones of sugar-phosphate backbone, is an intrinsic characteristic of certain DNA sequences. Such conformational transitions are the potential sources of formation of unique geometry of the dinucleotide steps and/or individual nucleotides and lead to alteration of base stacking and/or changes of the assessable surface area of atoms, and can be the criteria of recognition of DNA by protein as well. Changes in the physical properties that depend on the DNA structure, i. e. the polar/unpolar profile and electrostatic potential of the grooves, can also be used by protein for DNA readout.
Keywords: protein-nucleic acid recognition, variability of DNA structure, sugar-phosphate DNA backbone, alternative conformations
Full text: (PDF, in English) (PDF, in Russian)

References

[1] Gromiha M. M., Siebers J. G., Selvaraj S., Kono H., Sarai A. Intermolecular and intramolecular readout mechanisms in protein-DNA recognition J. Mol. Biol 2004 337, N 1:285–294.
[2] Steitz T. A. Structural studies of protein-nucleic acid interaction: the sources of sequence-specific binding Q. Rev. Biophys 1990 23, N 3:205–280.
[3] Marathe A., Karandur D., Bansal M. Small local variations in B-form DNA lead to a large variety of global geometries which can accommodate most DNA-binding protein motifs BMC Struct. Biol 2009 9:24.
[4] Kono H., Sarai A. Structure-based prediction of DNA target sites by regulatory proteins PROTEINS: Structure, Function, and Genetics 1999 35, N 1 P.114–131.
[5] Bernstein F. C., Koetzle T. F., Williams G. J., Meyer E. F. Jr., Brice M. D., Rodgers J. R., Kennard O., Shimanouchi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures J. Mol. Biol 1977 112, N 3:535–542.
[6] Sarai A., Kono H. Protein-DNA recognition patterns and predictions Annu. Rev. Biophys. Biomol. Struct 2005 34:379–398.
[7] Wang A. H., Quigley G. J., Kolpak F. J., Crawford J. L., van Boom J. H., van der Marel G. A., Rich A. Molecular structure of a lefthanded double helical DNA fragment at atomic resolution Nature 1979 282, N 5740:680–686.
[8] Shakked Z., Rabinovich D., Kennard O., Cruse W. B., Salisbury S. A., Viswamitra M. A. Sequence-dependent conformation of an A-DNA double helix. The crystal structure of the octamer d(G-G-T-A-T-A-C-C) J. Mol. Biol 1983 166, N 2:183–201.
[9] Wing R., Drew H., Takano T., Broka C., Tanaka S., Itakura K., Dickerson R. E. Crystal structure analysis of a complete turn of B-DNA Nature 1980 287, N 5784:755–758.
[10] Dickerson R. E., Drew H. R. Structure of a B-DNA dodecamer. II. Influence of base sequence on helix structure J. Mol. Biol 1981 149, N 4:761–786.
[11] Dickerson R. E. What do we really know about B-DNA? Structure and methods DNA and RNA: Proceedings of the Sixth Conversation in Biomolecular Stereodynamics. Eds R. H. Sarma, M. H. Sarma New York: Adenine press, 1990 Vol. 3:1–38.
[12] Drew H. R., Dickerson R. E. Structure of a B-DNA dodecamer. III. Geometry of hydration J. Mol. Biol 1981 151, N 3:535–556.
[13] Kopka M. L., Fratini A. V., Drew H. R., Dickerson R. E. Ordered water structure of a B-DNA dodecamer. A quantitative study J. Mol. Biol 1983 163, N 1:129–146.
[14] Jones S., van Heyningen P., Berman H. M., Thornton J. M. Protein-DNA interactions: A structural analysis J. Mol. Biol 1999 287, N 5:877–896.
[15] Luscombe N. M., Laskowski R. A., Thornton J. M. Amino acids-base interaction: a three-dimensional analysis of protein-DNA interactions at an atomic level Nucl. Acids Res 2001 29, N 13:2860–2874.
[16] Ahmad S., Gromiha M. M., Sarai A. Analysis and prediction of DNA-binding proteins and their binding residues based on composition, sequence and structural information Bioinformatics 2004 20, N 4:477–486.
[17] Berman H. M. The Protein Data Bank: a historical perspective Acta Crystallogr. A 2008 64, pt 1:88–95.
[18] Berman H. M., Olson W. K., Beveridge D. L., Westbrook J., Gelbin A., Demeny T., Hsieh S. H., Srinivasan A. R., Schneider B. The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids Biophys. J 1992 63, N 3:751–759.
[19] Reddy C. K., Das A., Jayaram B. Do water molecules mediate protein-DNA recognition? J. Mol. Biol 2001 314, N 3:619–632.
[20] Ahmad S., Keskin O., Sarai A., Nussinov R. Protein–DNA interactions: structural, thermodynamic and clustering patterns of conserved residues in DNA-binding proteins Nucl. Acids Res 2008 36, N 18:5922–5932.
[21] Wellenzohn B., Flader W., Winger R. H., Hallbrucker A., Mayer E., Liedl K. R. Complex of B-DNA with polyamides freezes DNA backbone flexibility J. Am. Chem. Soc 2001 123, N 21:5044–5049.
[22] Wellenzohn B., Flader W., Winger R. H., Hallbrucker A., Mayer E., Liedl K. R. Indirect readout of the trp-repressoroperator complex by B-DNA's backbone conformation transitions Biochemistry 2004 41, N 12:4088–4095.
[23] Hartmann B., Sullivan M. R., Harris L. F. Operator recognition by the phage 434 cI repressor: MD simulations of free and bound 50-bp DNA reveal important differences between the OR1 and OR2 sites Biopolymers 2003 68, N 2:250–264.
[24] Rohs R., West S. M., Liu P., Honig B. Nuance in the doublehelix and its role in protein-DNA recognotion Curr. Opin. Struct. Biol 2009 19, N 2:171–177.
[25] Pabo C. O., Nekludova L. Geometric analysis and comparison of protein-DNA interfaces: why is there no simple code for recognition J. Mol. Biol 2000 301, N 3:597–624.
[26] Lankas F., Sponer J., Langowski J., Cheatham T. E. 3rd. DNA basepair step deformability inferred from molecular dynamics simulations Biophys. J 2003 85, N 5:2872–2883.
[27] Dickerson R. E. DNA bending: the prevalence of kinkiness and the virtues of normality Nucl. Acids Res 1998 26, N 8:1906–1926.
[28] Aeling K. A., Opel M. L., Steffen N. R., Tretyachenko-Ladokhina V., Hatfield G. W., Lathrop R. H., Senear D. F. Indirect recognition in sequence-specific DNA binding by E. coli integration host factor: the role of DNA deformation energy J. Biol. Chem 2006 281, N 51:39236–39248.
[29] Ahmad S., Sarai A. Moment-based prediction of DNA-binding proteins J. Mol. Biol 2004 341, N 1:65–71.
[30] Nadassy K., Wodak S. J., Janin J. Structural features of protein-nucleic acid recognition sites Biochemistry 1999 38, N 7:1999–2017.
[31] Matthew J. B., Ohlendorf D. H. Electrostatic deformation of DNA by a DNA-binding protein. J. Biol. Chem. 1985; 260, N 10:5860–5862.
[32] Lejeune D., Delsaux N., Charloteaux B., Thomas A., Brasseur R. Protein-nucleic acid recognition: statistical analysis of atomic interactions and influence of DNA structure Proteins 2005 61, N 2:258–271.
[33] Mandel-Gutfreund Y., Schueler O., Margalit H. Comprehensive analysis of hydrogen bonds in regulatory protein–DNA complexes: in search of common principles J. Mol. Biol 1995 253, N 2:370–382.
[34] Mandel-Gutfreund Y., Margalit H., Jernigan R. L., Zhurkin V. B. A role for CH...O interactions in protein-DNA recognition J. Mol. Biol 1998 277, N 5:1129–1140.
[35] Gromiha M. M., Santhosh C., Ahmad S. Structural analysis of cation-pi interactions in DNA binding proteins Int. J. Biol. Macromol 2004 34, N 3:203–211.
[36] Davey C. A., Sargent D. F., Luger K., Maeder A. W., Richmond T. J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 C resolution J. Mol. Biol 2002 319, N 5:1097–1113.
[37] Prabakaran P., Siebers J. G., Ahmad S., Gromiha M. M., Singarayan M. G., Sarai A. Classification of protein-DNA complexes based on structural descriptors Structure 2006 14, N 9:1355–1367.
[38] Svozil D., Kalina J., Omelka M., Schneider B. DNA conformations and their sequence preferences Nucl. Acids Res 2008 36, N 11:3690–3706.
[39] Schultz S. C., Shields G. C., Steitz T. A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees Science 1991 253, N 5023:1001–1007.
[40] Luger K., Mader A. W., Richmond R. K., Sargent D. F., Richmond T. J. Crystal structure of the nucleosome core particle at 2.8 C resolution Nature 1997 389, N 6648:251–260.
[41] Matthews B. W. No code for recognition Nature 1988 335, N 6188:294–295.
[42] Seeman N. C., Rosenberg J. M., Rich A. Sequence specific recognition of double helical nucleic acids by proteins Proc. Nat. Acad. Sci. USA 1976 73, N 3:804–808.
[43] Saenger W. Principles of nucleic acid structure. New York: Springer, 1984; 556 p.
[44] Arnott S., Hukins D. W. Refinement of the structure of BDNA and implications for the analysis of X-ray diffraction data from fibers of biopolymers J. Mol. Biol 1973 81, N 2:93–105.
[45] Chandrasekaran R., Wang M., He R.-G., Puigianer L. G., Byler M. A., Milliane R. P., Arnott S. A re-examination of the crystal structure of A-DNA using fiber diffraction data J. Biomol. Struct. Dyn 1986 6, N 6:1189–1202.
[46] Arnott S., Hukins D. W. Optimised parameters for A-DNA and B-DNA Biochem. Biophys. Res. Communs 1972 47, N 6:1504–1509.
[47] Dickerson R. E. Definitions and nomenclature of nucleic acid structure components Nucl. Acids Res 1989 17, N 5:1797–1803.
[48] Sinden R. R. DNA structure and function New York: Acad. press, 1994 398 p.
[49] Rich A., Norheim A., Wang A. H. J. The chemistry and biology of left-handed Z-DNA Ann. Rev. Biochem 1984 53:791–846.
[50] Lu X.-J., Shakked Z., Olson W. K. A-form conformational motifs in ligand-bound DNA structures J. Mol. Biol 2000 300, N 4:819–840.
[51] van Dam L., Levitt M. H. BI Nucleotides in the B and C forms of natural-sequence polymeric DNA: a new model for the C form of DNA J. Mol. Biol. – 2000 304, N 4:541–561.
[52] Tolstorukov M. Y., Jernigan R. L., Zhurkin V. B. Protein– DNA hydrophobic recognition in the minor groove is facilitated by sugar switching J. Mol. Biol 2004 337, N 1:65–76.
[53] Conner B. N., Yun C., Dickerson J. L., Dickerson R. E. Helix geometry and hydration in an A-DNA tetramer: IC-C-G-G J. Mol. Biol 1984 174, N 4:663–695.
[54] Dickerson R. E. Base sequence and helix structure variation in B and A DNA J. Mol. Biol 1983 166, N 3:419–441.
[55] Bhattacharyya D., Bansal M. Groove width and depth of BDNA structures depend on local variation in slide J. Biomol. Struct. Dyn 1992 10, N 1:213–226.
[56] Dickerson R. E., Ng H. L. DNA structure from A to B Proc. Nat. Acad. Sci. USA 2001 98, N 13:6986–6988.
[57] Bingman C., Li X., Zon G., Sundaralingam M. Crystal and molecular structure of d(GTGCG CAC): investigation of the effects of base sequence on the conformation of octamer duplexes Biochemistry 1992 31, N 51:12803–12812.
[58] Olson W. K., Bansal M., Burley S. K., Dickerson R. E., Gerstein M., Harvey S. C., Heinemann U., Lu X. J., Neidle S., Shakked Z., Sklenar H., Suzuki M., Tung C. S., Westhof E., Wolberger C., Berman H. M. A standard reference frame for the description of nucleic acid base-pair geometry J. Mol. Biol 2001 313, N 1:229–233.
[59] Gorin A. A., Zhurkin V. B., Olson W. K. B-DNA Twisting correlates with base-pair morphology J. Mol. Biol 1995 247, N 1:34–48.
[60] Lu X., Olson W. K. 3DNA: software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structure Nucl. Acids Res 2003 31, N 17:5108–5121.
[61] Sims G. E., Kim S.-H. Global mapping of nucleic acid conformational space: dinucleoside monophosphate conformations and transition pathways among conformational classes Nucl. Acids Res 2003 31, N 19:5607–5616.
[62] Wenz C., Jeltsch A., Pingoud A. Probing the indirect readout of the restriction enzyme EcoRV mutational analysis of contacts to the DNA backbone J. Biol. Chem 1996 271, N 10:5565–5573.
[63] Zhang Y., Zhiqun X., Hegde R. S., Shakked Z., Crothers D. M. Predicting indirect readout effects in protein-DNA interactions Proc. Nat. Acad. Sci. USA 2004 101, N 22:8337–8341.
[64] Schneider B., Neidle S., Berman H. M. Conformations of the sugar–phosphate backbone in helical DNA crystal structures Biopolymers 1997 42, N 1:113–124.
[65] Fratini A. V., Kopka M. L., Drew H. R., Dickerson R. E. Reversible bending and helix geometry in a B-DNA dodecamer: CGCGAATTBrCGCG* J. Biol. Chem 1982 257, N 24:14686–14707.
[66] Varnai P., Djuranovic D., Lavery R., Hartmann B. transitions in the B-DNA backbone Nucl. Acids Res 2002 30, N 24:5398–5406.
[67] Dixit S. B., Beveridge D. L., Case D. A., Cheatham T. E. 3rd, Giudice E., Lankas F., Lavery R., Maddocks J. H., Osman R., Sklenar H., Thayer K. M., Varnai P. 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 2005 89, N 6:3721–3740.
[68] Grzeskowiak K., Yanagi K., Prive G. G., Dickerson R. E. The structure of B-helical C-G-A-T-C-G-A-T-C-G and comparison with C-C-A-A-C-G-T-T-G-G. The effect of base pair reversals. J. Biol. Chem. 1991; 266, N 14:8861–8883.
[69] Hartmann B., Piazzola D., Lavery R. BI-BII transitions in BDNA Nucl. Acids Res 1993 21, N 3:561–568.
[70] Bertrand H., Ha-Duong T., Fermandjian S., Hartmann B. Flexibility of the B-DNA backbone: effects of local and neighbouring sequences on pyrimidine-purine steps Nucleic Acids Res. 1998;26(5):1261-7.
[71] Djuranovic D., Hartmann B. Conformational characteristics and correlations in crystal structures of nucleic acid oligonucleotides: evidence for sub-states J. Biomol. Struc. Dyn 2003 20, N 6:771–788.
[72] Haran T. E., Shakked Z., Wang A. H., Rich A. The crystal structure of d(CCCCGGGG): a new A-form variant with an extended backbone conformation J. Biomol. Struct. Dyn 1987 2, N 2:199–217.
[73] Wang A. H.-J., Fujii S., van Boom J. H., Rich A. Molecular structure of the octamer d(G-G-C-C-G-G-C-C): modified ADNA Proc. Nat. Acad. Sci. USA 1982 79, N 13:3968–3972.
[74] Shakked Z., Rabinovich D., Kennard O., Cruse W. B. T., Salisbury S. A., Viswamitra M. A. Sequence-dependent conformation of an A-DNA double helix. The crystal structure of the octamer d(G-G-T-A-T-A-C-C) J. Mol. Biol 1983 166, N 2:183–201.
[75] Tkachenko M. Y., Boryskina O. P., Shestopalova A. V., Tolstorukov M. Y. ProtNA-ASA: Protein-nucleic acid structural database with information on accessible surface area Int. J. Quant. Chem 2010 110, N 1:230–232.
[76] Boryskina O. P., Tkachenko M. Y., Shestopalova A. V., Tolstorukov M. Y. DNA accessible surface area and indirect protein-DNA recognition: study by bioinformatical approach: Proc. 7th EBSA Eur. Biophys. Congr. (Genova, Italy, July 11–15 2009) Eur. Biophys. J 2009 38 (Suppl. 1):S62.
[77] Rozenberg H., Rabinovich D., Frolow F., Hegde R. S., Shakked Z. Structural code for DNA recognition revealed in crystal structures of papillomavirus E2-DNA targets Proc. Nat. Acad. Sci. USA 1998 95, N 26:5194–5199.
[78] Devarakonda S., Harp J. M., Kim Y., Ozyhar A., Rastinejad F. Structure of the heterodimeric ecdysone receptor DNAbinding complex EMBO J 2003 22, N 21:5827–5840.
[79] Sierk M. L., Zhao Q., Rastinejad F. DNA deformability as a recognition feature in the reverb response element Biochemistry 2001 40, N 43:12833–12843.
[80] Joshi R., Passner J. M., Rohs R., Jain R., Sosinsky A., Crickmore M. A., Jacob V., Aggarwal A. K., Honig B., Mann R. S. Functional specificity of a Hox protein mediated by the recognition of minor groove structure Cell 2007 131, N 3:530–543.