Protein-DNA complexation: contact profiles in DNA grooves

M. Yu. Zhitnikova, A. V. Shestopalova

Анотація


Background: Investigation of the specific protein-DNA complexation mechanisms allows to establish general principles of molecular recognition, which must be taken into account while developing artificial nanostructures based on DNA, and to improve the prediction efficiency of the protein binding sites on DNA. One of the main characteristics of the protein-DNA complexes are the number and type of contacts in the binding sites of DNA and proteins. Conformational changes in the DNA double helix can cause changes in these characteristics.

Objectives: The purpose of our study is to establish the features of the interactions between nucleotides and amino acid residues in the binding sites of protein-DNA complexes and their dependence on the conformation of deoxyribose and the angle γ of the polynucleotide chain.

Materials and methods: At research of protein-DNA recognition process we have analyzed the contacts between amino acids and nucleotides of the 128 protein-DNA complexes from the structural databases. Conformational parameters of DNA backbone were calculated using the 3DNA/CompDNA program. The number of contacts was determined using a geometric criterion. Two protein and DNA atoms were considered to be in contact if the distance between their centers is less than 4.5 Å. Amino acid residues were arranged according to hydrophobicity scale as hydrophobic or nonpolar and polar.

Results: The analysis of contacts between polar and hydrophobic residues and nucleotides with different conformations of the sugar-phosphate backbone showed that nucleotides form more contacts with polar amino acids in both grooves than with hydrophobic ones regardless of nucleotide conformation. But the profile of such contacts differs in minor and major grooves and depends on the conformation of both deoxyribose and γ angle. The contact profiles are characterized by the sequence-specificity or the different propensity of nucleotides to form contacts with the residues in both grooves.

Conclusions: Our analysis have shown, that the amount and type of protein-nucleic contacts and their distribution in the grooves depend on the conformation of the sugar-phosphate backbone, the nucleotide sequence and the type of amino acids in the binding sites.


Ключові слова


protein-DNA recognition; protein-DNA contacts; DNA structure; binding site prediction; structural variations

Повний текст:

PDF (English)

Посилання


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Література


Si J., Zhao R., Wu R. An Overview of the Prediction of Protein DNA-Binding Sites // Int. J. Mol. Sci. 2015. No 16. P. 5194-5215.

Mandel-Gutfreund Y., Margalit H. Quantitative parameters for amino acid–base interaction: implications for prediction of protein–DNA binding sites // Nucleic Acids Res. 1998. Vol. 26. No 10. P. 2306–2312.

Jones S., Shanahan H.P., Berman H.M., Thornton J.M. Using electrostatic potentials to predict DNA-binding sites on DNA-binding proteins // Nucleic Acids Res. 2003. No 31. P. 7189–7198.

Shanahan H.P., Garcia M.A., Jones S., Thornton J.M. Identifying DNA-binding proteins using structural motifs and the electrostatic potential // Nucleic Acids Res. 2004. No 32. P. 4732–4741.

Ofran Y., Mysore V., Rost B. Prediction of DNA-binding residues from sequence // Bioinformatics. 2007. Vol. 23. No 13. P. i347–i353.

Luscombe N.M., Laskowski R.A., Thornton J.M. Amino acid–base interactions: a three-dimensional analysis of protein–DNA interactions at an atomic level // Nucleic Acids Research. 2001. Vol. 29. No 13. P. 2860–2874.

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. Vol. 61. No 2. P. 258–271.

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. No 337. P. 65–76.

Rohs R., Jin X., West S.M., Joshi R., Honig B., Mann R.S. Origins of specificity in protein-DNA recognition // Annual review of biochemistry. 2010. No 79. P. 233–26.

10. Schneider B., Cerny J., Svozil D., Cech P., Gelly J.-C., de Brevern A. G. Bioinformatic analysis of the protein/DNA interface // Nucleic Acids Research. 2014. Vol. 42. No 5. P. 3381–3394.

11. Locasale J.W., Napoli A.A., Chen S., Berman H.M., Lawson,C.L. Signatures of protein-DNA recognition in free DNA binding sites // J. Mol. Biol. 2009. No 386. P. 1054–1065.

12. Zhao J., Bacolla A., Wang G., Vasquez K.M. Non-B DNA structure-induced genetic instability and evolution // Cell. Mol. Life Sci. 2010. No 67. P. 43–62.

13. Schneider B., Neidle S., Berman H. M. Conformations of the sugar–phosphate backbone in helical DNA crystal structures // Biopolymers. 1997. Vol. 42. No 1. P. 113–124.

14. Varnai P., Djuranovic D., Lavery R., Hartmann B. -γ transitions in the B-DNA backbone // Nucl. Acids Res. 2002. Vol. 30. No 24. P. 5398–5406.

15. Zhitnikova M.Yu., Boryskina O.P., Shestopalova A.V. Sequence-specific transitions of the torsion angle gamma change the polar-hydrophobic profile of the DNA grooves: implication for indirect protein-DNA recognition // J. Biomol. Struct. Dyn. 2014. Vol. 32. No 10. P. 1670-1685.

16. Berman H. M., Olson W. K., Beveridge D. L., 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 // Biophysical Journal. 1992. No 63. P. 751–759.

17. Lu X. J., Olson W. K. 3DNA: A software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures // Nucleic Acids Research. 2003. No 31. P. 5108–5121.

18. 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. No 20. P. 477–486.

19. Kuznetsov I.B., Gou Z., Li R., Hwang S. Using evolutionary and structural information to predict DNA-binding sites on DNA-binding proteins // Proteins. 2006. No 64. P. 19–27.

20. Bartlett G.J., Porter C.T., Borkakoti N., Thornton J.M. Analysis of catalytic residues in enzyme active sites // J. Mol. Biol. 2002. No 324. P. 105–121.

21. Faucher J., Pliska V. Hydrophobic parameters pi of amino acid side chains from the partitioning of N-acetyl-amino-acid amides // Eur. J. Med. Chem. 1983. No 18. P. 369–375.

22. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein // J. Mol. Biol. 1982. No 157. P. 105–132.

23. Corona R. I., Guo J.T. Statistical analysis of structural determinants for protein-DNA binding specificity // Proteins. 2016. Vol. 84. No 8. P. 1147–1161.

24. Bewley C.A., Gronenborn A.M., Clore G.M. Minor groove-binding architectural proteins: structure, function, and DNA recognition // Annu Rev. Biophys. Biomol. Struct. 1998. Vol. 27. P. 105–131.

25. Huang J., Zhao Y., Liu H., Huang D., Cheng X., Zhao W., Taylor I.A., Liu J., Peng Y.L. Substitution of tryptophan 89 with tyrosine switches the DNA binding mode of PC4 // Scientific Reports. 2015. Vol. 5. P. 8789.

26. Schneider T.D., Stormo G.D., Gold L. Information content of binding sites on nucleotide sequences // J. Mol. Biol. 1986. No 188. P. 415–431.

27. Berg O.G., von Hippel P.H. Selection of DNA binding sites by regulatory proteins—statistical-mechanical theory and application to operators and promoters // J. Mol. Biol. 1987. No 193. P. 723–750.

28. Takeda Y., Sarai A., Rivera V.M. Analysis of the sequence-specific interactions between Cro repressor and operator DNA by systematic base substitution experiments // Proc. Natl. Acad. Sci. USA. 1989. No 86. P. 439–443.

29. Sarai A., Takeda Y. λ repressor recognizes the approximately 2-fold symmetric half-operator sequences asymmetrically // Proc. Natl. Acad. Sci. USA. 1989. No 86. P. 6513–6517.

30. Tanikawa J., Yasukawa T., Enari M., Ogata K., Nishimura Y., Ishii S., Sarai A. Recognition of specific DNA sequences by the c-Myb proto-oncogen product: Role of three repeat units in the DNA-binding domain // Proc. Natl. Acad. Sci. USA. 1993. No 90. P. 9320–9324.

31. Kono H., Sarai A. Structure-based prediction of DNA target sites by regulatory proteins // Proteins. 1999. No 35. P. 114–131.


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