Skip to main content
SpringerLink
Log in

Role of indirect readout mechanism in TATA box binding protein–DNA interaction

  • Published:
Journal of Computer-Aided Molecular Design Aims and scope Submit manuscript

Abstract

Gene expression generally initiates from recognition of TATA-box binding protein (TBP) to the minor groove of DNA of TATA box sequence where the DNA structure is significantly different from B-DNA. We have carried out molecular dynamics simulation studies of TBP–DNA system to understand how the DNA structure alters for efficient binding. We observed rigid nature of the protein while the DNA of TATA box sequence has an inherent flexibility in terms of bending and minor groove widening. The bending analysis of the free DNA and the TBP bound DNA systems indicate presence of some similar structures. Principal coordinate ordination analysis also indicates some structural features of the protein bound and free DNA are similar. Thus we suggest that the DNA of TATA box sequence regularly oscillates between several alternate structures and the one suitable for TBP binding is induced further by the protein for proper complex formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Deremble C, Lavery R (2005) Macromollecullar recognition. Curr Opin Struct Biol 15(2):171–175. doi:10.1016/j.sbi.2005.01.018

    Article  CAS  Google Scholar 

  2. Sarai A, Kono H (2005) Protein–DNA recognition patterns and predictions. Annu Rev Biophys Biomol Struct 34:379–398. doi:10.1146/annurev.biophys.34.040202.144537

    Article  CAS  Google Scholar 

  3. Rhodes D, Schwabe JWR, Chapman L, Fairall L (1996) Towards an understanding of protein–DNA recognition. Philos Trans R Soc Lond Ser B 351(1339):501–509. doi:10.1098/rstb.1996.0048

    Article  CAS  Google Scholar 

  4. Paillard G, Lavery R (2004) Analyzing protein–DNA recognition mechanisms. Structure 12(1):113–122. doi:10.1016/j.str.2003.11.022

    Article  CAS  Google Scholar 

  5. Fischer E (1894) Einfluss der configuration auf die wirkung der enzyme. Ber Dtsch Chem Ges 27:9

    Google Scholar 

  6. Gromiha MM, Siebers JG, Selvaraj S, Kono H, Sarai A (2004) Intermolecular and intramolecular readout mechanisms in protein–DNA recognition. J Mol Biol 337(2):285–294. doi:10.1016/j.jmb.2004.01.033

    Article  Google Scholar 

  7. Gromiha MM, Slebcrs JG, Selvaraj S, Kono H, Sarai A (2005) Role of inter and intramolecular interactions in protein–DNA recognition. Gene 364:108–113. doi:10.1016/j.gene.2005.07.022

    Article  CAS  Google Scholar 

  8. Koshland DE (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 44(2):98–104. doi:10.1073/pnas.44.2.98

    Article  CAS  Google Scholar 

  9. Ma BY, Kumar S, Tsai CJ, Nussinov R (1999) Folding funnels and binding mechanisms. Protein Eng 12(9):713–720. doi:10.1093/protein/12.9.713

    Article  CAS  Google Scholar 

  10. Troyer JM, Cohen FE (1995) Protein conformational landscapes—energy minimization and clustering of a long molecular-dynamics trajectory. Proteins Struct Funct Genet 23(1):97–110. doi:10.1002/prot.340230111

    Article  CAS  Google Scholar 

  11. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254(5038):1598–1603. doi:10.1126/science.1749933

    Article  CAS  Google Scholar 

  12. Boehr DD, Nussinov R, Wright PE (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5(11):789–796. doi:10.1038/nchembio1209-954d

    Article  CAS  Google Scholar 

  13. Kumar S, Ma BY, Tsai CJ, Sinha N, Nussinov R (2000) Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci 9(1):10–19. doi:10.1110/ps.9.1.10

    Article  CAS  Google Scholar 

  14. Grunberg R, Leckner J, Nilges M (2004) Complementarity of structure ensembles in protein–protein binding. Structure 12(12):2125–2136. doi:10.1016/j.str.2004.09.014

    Article  CAS  Google Scholar 

  15. Wlodarski T, Zagrovic B (2009) Conformational selection and induced fit mechanism underlie specificity in noncovalent interactions with ubiquitin. Proc Natl Acad Sci USA 106(46):19346–19351. doi:10.1073/pnas.0906966106

    Article  CAS  Google Scholar 

  16. Csermely P, Palotai R, Nussinov R (2010) Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Trends Biochem Sci 35(10):539–546. doi:10.1016/j.tibs.2010.04.009

    Article  CAS  Google Scholar 

  17. Klug A, Jack A, Viswamitra MA, Kennard O, Shakked Z, Steitz TA (1979) Hypothesis on a specific sequence-dependent conformation of dna and its relation to the binding of the lac-repressor protein. J Mol Biol 131(4):669–680. doi:10.1016/0022-2836(79)90196-7

    Article  CAS  Google Scholar 

  18. Dixit SB, Andrews DQ, Beveridge DL (2005) Induced fit and the entropy of structural adaptation in the complexation of CAP and lambda-repressor with cognate DNA sequences. Biophys J 88(5):3147–3157. doi:10.1529/biophysj.104.053843

    Article  CAS  Google Scholar 

  19. Dragan AI, Read CM, Makeyeva EN, Milgotina EI, Churchill MEA, Crane-Robinson C, Privalov PL (2004) DNA binding and bending by HMG boxes: energetic determinants of specificity. J Mol Biol 343(2):371–393. doi:10.1016/j.jmb.2004.08.035

    Article  CAS  Google Scholar 

  20. Crothers DM (1998) DNA curvature and deformation in protein–DNA complexes: a step in the right direction. Proc Natl Acad Sci USA 95(26):15163–15165. doi:10.1073/pnas.95.26.15163

    Article  CAS  Google Scholar 

  21. Davis NA, Majee SS, Kahn JD (1999) TATA box DNA deformation with and without the TATA box-binding protein. J Mol Biol 291(2):249–265. doi:10.1006/jmbi.1999.2947

    Article  CAS  Google Scholar 

  22. Cherstvy AG (2009) Positively Charged Residues in DNA-binding domains of structural proteins follow sequence-specific positions of DNA phosphate groups. J Phys Chem B 113(13):4242–4247. doi:10.1021/jp810009s

    Article  CAS  Google Scholar 

  23. Garcia-Perez M, Pinto M, Subirana JA (2003) Nonsequence-specific arginine interactions in the nucleosome core particle. Biopolymers 69(4):432–439. doi:10.1002/bip.10389

    Article  CAS  Google Scholar 

  24. Werner MH (1996) Intercalation, DNA kinking, and the control of transcription. Science 271(5250):778–784. doi:10.1126/science.271.5250.778

    Article  CAS  Google Scholar 

  25. Privalov PL, Dragan AI, Crane-Robinson C (2009) The cost of DNA bending. Trends Biochem Sci 34(9):464–470. doi:10.1016/j.tibs.2009.05.005

    Article  CAS  Google Scholar 

  26. Kim YC, Geiger JH, Hahn S, Sigler PB (1993) Crystal-structure of a yeast TBP TATA-box complex. Nature 365(6446):512–520. doi:10.1038/365512a0

    Article  CAS  Google Scholar 

  27. Nikolov DB, Burley SK (1994) 2.1-Angstrom resolution refined structure of a TATA box-binding protein (TBP). Nat Struct Biol 1(9):621–637. doi:10.1038/nsb0994-621

    Article  CAS  Google Scholar 

  28. Osheagreenfield A, Smale ST (1992) Roles of TATA and initiator elements in determining the start site location and direction of rna polymerase-II transcription. J Biol Chem 267(2):1391–1402

    CAS  Google Scholar 

  29. Singer VL, Wobbe CR, Struhl K (1990) A wide variety of DNA-sequences can functionally replace a yeast TATA element for transcriptional activation. Genes Dev 4(4):636–645. doi:10.1101/gad.4.4.636

    Article  CAS  Google Scholar 

  30. Wang Y, Stumph WE (1995) RNA-polymerase II/III transcription specificity determined by TATA box orientation. Proc Natl Acad Sci USA 92(19):8606–8610. doi:10.1073/pnas.92.19.8606

    Article  CAS  Google Scholar 

  31. Wobbe CR, Struhl K (1990) Yeast and human TATA-binding proteins have nearly identical DNA-sequence requirements for transcription invitro. Mol Cell Biol 10(8):3859–3867. doi:10.1128/MCB.10.8.3859

    CAS  Google Scholar 

  32. Kim JL, Nikolov DB, Burley SK (1993) Co-crystal structure of TBP recognizing the minor-groove of a TATA element. Nature 365(6446):520–527. doi:10.1038/365520a0

    Article  CAS  Google Scholar 

  33. Kim JL, Burley SK (1994) 1.9-Angstrom resolution refined structure of TBP recognizing the minor-groove of TATAAAAG. Nat Struct Biol 1(9):638–653. doi:10.1038/nsb0994-638

    Article  CAS  Google Scholar 

  34. Nikolov DB, Chen H, Halay ED, Hoffmann A, Roeder RG, Burley SK (1996) Crystal structure of a human TATA box-binding protein/TATA element complex. Proc Natl Acad Sci USA 93(10):4862–4867. doi:10.1073/pnas.93.10.4862

    Article  CAS  Google Scholar 

  35. Wu J, Parkhurst KM, Powell RM, Brenowitz M, Parkhurst LJ (2001) DNA bends in TATA-binding protein center dot TATA complexes in solution are DNA sequence-dependent. J Biol Chem 276(18):14614–14622. doi:10.1074/jbc.M004402200

    Article  CAS  Google Scholar 

  36. Wu J, Parkhurst KM, Powell RM, Parkhurst LJ (2001) DNA sequence-dependent differences in TATA-binding protein-induced DNA bending in solution are highly sensitive to osmolytes. J Biol Chem 276(18):14623–14627. doi:10.1074/jbc.M004401200

    Article  CAS  Google Scholar 

  37. Geggier S, Vologodskii A (2010) Sequence dependence of DNA bending rigidity. Proc Natl Acad Sci USA 107(35):15421–15426. doi:10.1073/pnas.1004809107

    Article  CAS  Google Scholar 

  38. Du Q, Kotlyar A, Vologodskii A (2008) Kinking the double helix by bending deformation. Nucleic Acids Res 36(4):1120–1128. doi:10.1093/nar/gkm1125

    Article  CAS  Google Scholar 

  39. Vafabakhsh R, Ha T (2012) Extreme bendability of DNA less than 100 base pairs long revealed by single-molecule cyclization. Science 337(6098):1097–1101. doi:10.1126/science.1224139

    Article  CAS  Google Scholar 

  40. Kannan S, Kohlhoff K, Zacharias M (2006) B-DNA under stress: over- and untwisting of DNA during molecular dynamics simulations. Biophys J 91(8):2956–2965. doi:10.1529/biophysj.106.087163

    Article  CAS  Google Scholar 

  41. Starr DB, Hoopes BC, Hawley DK (1995) DNA bending ss an important component of site-specific recognition by the TATA-binding protein. J Mol Biol 250(4):434–446. doi:10.1006/jmbi.1995.0388

    Article  CAS  Google Scholar 

  42. Qian XL, Strahs D, Schlick T (2001) Dynamic simulations of 13 TATA variants refine kinetic hypotheses of sequence/activity relationships. J Mol Biol 308(4):681–703. doi:10.1006/jmbi.2001.4617

    Article  CAS  Google Scholar 

  43. Hancock SP, Ghane T, Cascio D, Rohs R, Di Felice R, Johnson RC (2013) Control of DNA minor groove width and Fis protein binding by the purine 2-amino group. Nucleic Acids Res. doi:10.1093/nar/gkt357

    Google Scholar 

  44. Samanta S, Chakrabarti J, Bhattacharyya D (2010) Changes in thermodynamic properties of DNA base pairs in protein–DNA recognition. J Biomol Struct Dyn 27(4):429–442. doi:10.1080/07391102.2010.10507328

    Article  CAS  Google Scholar 

  45. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28(1):235–242. doi:10.1093/nar/28.1.235

    Article  CAS  Google Scholar 

  46. Chandrasekaran R, Arnott S (1996) The structure of B-DNA in oriented fibers. J Biomol Struct Dyn 13(6):1015–1027. doi:10.1080/07391102.1996.10508916

    Article  CAS  Google Scholar 

  47. Case DA, VB JTB, Betz RM, Cai Q, Cerutti DS, Cheatham III TE, Darden TA, Duke RE, Gohlke H, Goetz AW, Gusarov S, Homeyer N, Janowski P, Kaus J, Kolossvary I, Kovalenko A, Lee TS, LeGrand S, Luchko T, Luo R, Madej B, Merz Jr KM, Paesani F, Roe DR, Roitberg A, Sagui C, Salomon-Ferrer R, Seabra G, Simmerling CL, Smith WL, Swails J, Walker RC, Wang J, Wolf RM, Wu X, Kollman PA (2014) The FF14SB force field. AMBER 14 Reference Manual, pp 29–31

  48. Kale L, Skeel R, Bhandarkar M, Brunner R, Gursoy A, Krawetz N, Phillips J, Shinozaki A, Varadarajan K, Schulten K (1999) NAMD2: greater scalability for parallel molecular dynamics. J Comput Phys 151(1):283–312. doi:10.1006/jcph.1999.6201

    Article  CAS  Google Scholar 

  49. Nelson M, Humphrey W, Kufrin R, Gursoy A, Dalke A, Kale L, Skeel R, Schulten K (1995) MDSCOPE—a visual computing environment for structural biology. Comput Phys Commun 91(1–3):111–133. doi:10.1016/0010-4655(95)00045-h

    Article  CAS  Google Scholar 

  50. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J Am Chem Soc 117(19):5179–5197. doi:10.1021/ja00124a002

    Article  CAS  Google Scholar 

  51. Perez A, Marchan I, Svozil D, Sponer J, Cheatham TE, Laughton CA, Orozco M (2007) Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers. Biophys J 92(11):3817–3829. doi:10.1529/biophysj.106.097782

    Article  CAS  Google Scholar 

  52. Foloppe N, MacKerell AD (2000) All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J Comput Chem 21(2):86–104. doi:10.1002/(SICI)1096-987X(20000130)21:2<86:AID-JCC2>3.0.CO;2-G

    Article  CAS  Google Scholar 

  53. Bansal M, Bhattacharyya D, Ravi B (1995) NUPARM and NUCGEN—software for analysis and generation of sequence-dependent nucleic-acid structures. Comput Appl Biosci 11(3):281–287

    CAS  Google Scholar 

  54. Mukherjee S, Bansal M, Bhattacharyya D (2006) Conformational specificity of non-canonical base pairs and higher order structures in nucleic acids: crystal structure database analysis. J Comput Aided Mol Des 20(10–11):629–645. doi:10.1007/s10822-006-9083-x

    Article  CAS  Google Scholar 

  55. Mukherjee S, Majumdar S, Bhattacharyya D (2005) Role of hydrogen bonds in protein–DNA recognition: effect of nonplanar amino groups. J Phys Chem B 109(20):10484–10492. doi:10.1021/Jp0446231

    Article  CAS  Google Scholar 

  56. Kabsch W, Sander C (1983) Dictionary of protein secondary structure—pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers 22(12):2577–2637. doi:10.1002/bip.360221211

    Article  CAS  Google Scholar 

  57. Bhattacharyya D, Bansal M (1989) A self-consistent formulation for analysis and generation of non-uniform DNA structures. J Biomol Struct Dyn 6(4):635–653. doi:10.1080/07391102.1989.10507727

    Article  CAS  Google Scholar 

  58. Kanhere A, Bansal M (2003) An assessment of three dinucleotide parameters to predict DNA curvature by quantitative comparison with experimental data. Nucleic Acids Res 31(10):2647–2658. doi:10.1093/nar/gkg362

    Article  CAS  Google Scholar 

  59. Dickerson RE (1998) DNA bending: the prevalence of kinkiness and the virtues of normality. Nucleic Acids Res 26(8):1906–1926. doi:10.1093/nar/26.8.1906

    Article  CAS  Google Scholar 

  60. Lavery R, Moakher M, Maddocks JH, Petkeviciute D, Zakrzewska K (2009) Conformational analysis of nucleic acids revisited: curves+. Nucleic Acids Res 37(17):5917–5929. doi:10.1093/nar/gkp608

    Article  CAS  Google Scholar 

  61. Skjaerven L, Martinez A, Reuter N (2011) Principal component and normal mode analysis of proteins; a quantitative comparison using the GroEL subunit. Proteins Struct Funct Bioinf 79(1):232–243. doi:10.1002/prot.22875

    Article  CAS  Google Scholar 

  62. Grant BJ, Rodrigues APC, ElSawy KM, McCammon JA, Caves LSD (2006) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22(21):2695–2696. doi:10.1093/bioinformatics/btl461

    Article  CAS  Google Scholar 

  63. Becker OM (1998) Principal coordinate maps of molecular potential energy surfaces. J Comput Chem 19(11):1255–1267. doi:10.1002/(sici)1096-987x(199808)19:11<1255:aid-jcc5>3.3.co;2-h

    Article  CAS  Google Scholar 

  64. Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338. doi:10.1093/biomet/53.3-4.325

    Article  Google Scholar 

  65. Becker OM (1997) Geometric versus topological clustering: an insight into conformation mapping. Proteins Struct Funct Genet 27(2):213–226. doi:10.1002/(sici)1097-0134(199702)27:2<213:aid-prot8>3.0.co;2-g

    Article  CAS  Google Scholar 

  66. Brandl CJ, Struhl K (1990) A nucleosome-positioning sequence is required for GCN4 to activate transcription in the absence of a TATA element. Mol Cell Biol 10(8):4256–4265. doi:10.1128/MCB.10.8.4256

    CAS  Google Scholar 

  67. Anish R, Hossain MB, Jacobson RH, Takada S (2009) Characterization of transcription from TATA-less promoters: identification of a new core promoter element XCPE2 and analysis of factor requirements. PLoS One. doi:10.1371/Journal.Pone.0005103

    Google Scholar 

  68. Mondal M, Mukherjee S, Bhattacharyya D (2014) Contribution of phenylalanine side chain intercalation to the TATA-box binding protein-DNA interaction: molecular dynamics and dispersion-corrected density functional theory stidies. J Mol Model 20(11):2499. doi:10.1007/s00894-014-2499-7

  69. Calladine CR, Drew HR, Luisi BF, Travers AA (2004) Understanding DNA, the molecule and how it works, 3rd edn. Elsevier, London

Download references

Author information

Authors and Affiliations

  1. Computational Science Division, Saha Institute of Nuclear Physics, 1/AF Bidhannagar, Kolkata, 700064, India

    Manas Mondal & Dhananjay Bhattacharyya

  2. School of Biotechnology, Jawaharlal Nehru University, New Mehrauli Road, New Delhi, 110067, India

    Devapriya Choudhury

  3. S.N. Bose National Center for Basic Sciences, Sector III, Salt Lake, Kolkata, 700098, India

    Jaydeb Chakrabarti

Authors
  1. Manas Mondal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Devapriya Choudhury
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaydeb Chakrabarti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dhananjay Bhattacharyya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jaydeb Chakrabarti or Dhananjay Bhattacharyya.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1425 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mondal, M., Choudhury, D., Chakrabarti, J. et al. Role of indirect readout mechanism in TATA box binding protein–DNA interaction. J Comput Aided Mol Des 29, 283–295 (2015). https://doi.org/10.1007/s10822-014-9828-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10822-014-9828-x

Keywords

Search

Navigation