How proteins bind to DNA: target discrimination and dynamic sequence search by the telomeric protein TRF1 - Publication - Bridge of Knowledge

Search

How proteins bind to DNA: target discrimination and dynamic sequence search by the telomeric protein TRF1

Abstract

Target search as performed by DNA-binding proteins is a complex process, in which multiple factors contribute to both thermodynamic discrimination of the target sequence from overwhelmingly abundant off-target sites and kinetic acceleration of dynamic sequence interrogation. TRF1, the protein that binds to telomeric tandem repeats, faces an intriguing variant of the search problem where target sites are clustered within short fragments of chromosomal DNA. In this study, we use extensive (>0.5 ms in total) MD simulations to study the dynamical aspects of sequence-specific binding of TRF1 at both telomeric and non-cognate DNA. For the first time, we describe the spontaneous formation of a sequence-specific native protein–DNA complex in atomistic detail, and study the mechanism by which proteins avoid off-target binding while retaining high affinity for target sites. Our calculated free energy landscapes reproduce the thermodynamics of sequence-specific binding, while statistical approaches allow for a comprehensive description of intermediate stages of complex formation.

Citations

  • 1 9

    CrossRef

  • 0

    Web of Science

  • 1 7

    Scopus

Cite as

Full text

download paper
downloaded 24 times
Publication version
Accepted or Published Version
License
Creative Commons: CC-BY-NC open in new tab

Keywords

Details

Category:
Articles
Type:
artykuł w czasopiśmie wyróżnionym w JCR
Published in:
NUCLEIC ACIDS RESEARCH no. 45, edition 13, pages 7643 - 7654,
ISSN: 0305-1048
Language:
English
Publication year:
2017
Bibliographic description:
Wieczór M., Czub J.: How proteins bind to DNA: target discrimination and dynamic sequence search by the telomeric protein TRF1// NUCLEIC ACIDS RESEARCH. -Vol. 45, iss. 13 (2017), s.7643-7654
DOI:
Digital Object Identifier (open in new tab) 10.1093/nar/gkx534
Bibliography: test
  1. von Hippel,P. (1994) protein-DNA recognition: new perspectives and underlying themes. Science, 263, 769-770. open in new tab
  2. Rohs,R., Jin,X., West,S.M., Joshi,R., Honig,B. and Mann,R.S. (2010) Origins of Specificity in protein-DNA Recognition. Annu. Rev. Biochem., 79, 233-269. open in new tab
  3. Oda,M., Furukawa,K., Ogata,K., Sarai,A. and Nakamura,H. (1998) Thermodynamics of specific and non-specific DNA binding by the c-myb DNA-binding domain. J. Mol. Biol., 276, 571-590. open in new tab
  4. Holbrook,J.A., Tsodikov,O.V., Saecker,R.M. and Record,M. (2001) Specific and non-specific interactions of integration host factor with DNA: thermodynamic evidence for disruption of multiple IHF surface salt-bridges coupled to DNA binding. J. Mol. Biol., 310, 379-401. open in new tab
  5. Zhang,Y., Larsen,C.A., Stadler,H.S. and Ames,J.B. (2011) Structural Basis for Sequence Specific DNA Binding and Protein Dimerization of HOXA13. PLoS ONE, 6, e23069. open in new tab
  6. Pinto,U.M., Flores-Mireles,A.L., Costa,E.D. and Winans,S.C. (2011) RepC protein of the octopine-type Ti plasmid binds to the probable origin of replication within repC and functions only in cis. Mol. Microbiol., 81, 1593-1606. open in new tab
  7. Pelossof,R., Singh,I., Yang,J.L., Weirauch,M.T., Hughes,T.R. and Leslie,C.S. (2015) Affinity regression predicts the recognition code of nucleic acid-binding proteins. Nat. Biotechnol., 33, 1242-1249. open in new tab
  8. Si,J., Zhao,R. and Wu,R. (2015) An overview of the prediction of protein DNA-binding sites. Int. J. Mol. Sci., 16, 5194-5215. open in new tab
  9. Yamasaki,S., Terada,T., Kono,H., Shimizu,K. and Sarai,A. (2012) A new method for evaluating the specificity of indirect readout in protein-DNA recognition. Nucleic Acids Res., 40, e129. open in new tab
  10. van der Vaart,A. (2015) Coupled binding-bending-folding: the complex conformational dynamics of protein-DNA binding studied by atomistic molecular dynamics simulations. Biochim. Biophys. Acta (BBA) -Gen. Subj., 1850, 1091-1098. open in new tab
  11. Graneli,A., Yeykal,C.C., Robertson,R.B. and Greene,E.C. (2006) Long-distance lateral diffusion of human Rad51 on double-stranded DNA. Proc. Natl. Acad. Sci. U.S.A., 103, 1221-1226. open in new tab
  12. Lin,J., Countryman,P., Buncher,N., Kaur,P., E,L., Zhang,Y., Gibson,G., You,C., Watkins,S.C., Piehler,J. et al. (2013) TRF1 and TRF2 use different mechanisms to find telomeric DNA but share a novel mechanism to search for protein partners at telomeres. Nucleic Acids Res., 42, 2493-2504. open in new tab
  13. Izeddin,I., Recamier,V., Bosanac,L., Cisse,I.I., Boudarene,L., Dugast-Darzacq,C., Proux,F., Benichou,O., Voituriez,R., Bensaude,O. et al. (2014) Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus. eLife, 3, doi:10.7554/eLife.02230. open in new tab
  14. Givaty,O. and Levy,Y. (2009) Protein sliding along DNA: dynamics and structural characterization. J. Mol. Biol., 385, 1087-1097. open in new tab
  15. Florescu,A.-M. and Joyeux,M. (2010) Comparison of kinetic and dynamical models of DNA-protein interaction and facilitated diffusion. J. Phys. Chem. A, 114, 9662-9672. open in new tab
  16. Khazanov,N., Marcovitz,A. and Levy,Y. (2013) Asymmetric DNA-search dynamics by symmetric dimeric proteins. Biochemistry, 52, 5335-5344. open in new tab
  17. Tan,C., Terakawa,T. and Takada,S. (2016) Dynamic coupling among protein binding, sliding, and DNA bending revealed by molecular dynamics. J. Am. Chem. Soc., 138, 8512-8522. open in new tab
  18. Kolomeisky,A.B. (2011) Physics of protein-DNA interactions: mechanisms of facilitated target search. Phys. Chem. Chem. Phys., 13, 2088-2095. open in new tab
  19. Zandarashvili,L., Esadze,A., Vuzman,D., Kemme,C.A., Levy,Y. and Iwahara,J. (2015) Balancing between affinity and speed in target DNA search by zinc-finger proteins via modulation of dynamic conformational ensemble. Proc. Natl. Acad. Sci. U.S.A., 112, E5142-E5149. open in new tab
  20. Lange,M., Kochugaeva,M. and Kolomeisky,A.B. (2015) Protein search for multiple targets on DNA. J. Chem. Phys., 143, 105102. open in new tab
  21. Iwahara,J. and Clore,G.M. (2006) Detecting transient intermediates in macromolecular binding by paramagnetic NMR. Nature, 440, 1227-1230. open in new tab
  22. Gao,M. and Skolnick,J. (2009) From nonspecific DNA-protein encounter complexes to the prediction of DNA-protein interactions. PLoS Comput. Biol., 5, e1000341. open in new tab
  23. Marcovitz,A. and Levy,Y. (2011) Frustration in protein-DNA binding influences conformational switching and target search kinetics. Proc. Natl. Acad. Sci. U.S.A., 108, 17957-17962. open in new tab
  24. Etheve,L., Martin,J. and Lavery,R. (2015) Dynamics and recognition within a protein-DNA complex: a molecular dynamics study of the SKN-1/DNA interaction. Nucleic Acids Res., 44, 1440-1448. open in new tab
  25. Gowers,D.M., Wilson,G.G. and Halford,S.E. (2005) From The Cover: Measurement of the contributions of 1D and 3D pathways to the translocation of a protein along DNA. Proc. Natl. Acad. Sci. U.S.A., 102, 15883-15888. open in new tab
  26. Ryu,K.-S., Tugarinov,V. and Clore,G.M. (2014) Probing the rate-limiting step for intramolecular transfer of a transcription factor between specific sites on the same DNA molecule by 15 N z -exchange NMR spectroscopy. J. Am. Chem. Soc., 136, 14369-14372. open in new tab
  27. Ganji,M., Docter,M., Le Grice,S.F. and Abbondanzieri,E.A. (2016) DNA binding proteins explore multiple local configurations during docking via rapid rebinding. Nucleic Acids Res., 44, 8376-8384. open in new tab
  28. Buch,I., Giorgino,T. and De Fabritiis,G. (2011) Complete reconstruction of an enzyme-inhibitor binding process by molecular dynamics simulations. Proc. Natl. Acad. Sci. U.S.A., 108, 10184-10189. open in new tab
  29. Mattern,K.A., Swiggers,S.J., Nigg,A.L., Lowenberg,B., Houtsmuller,A.B. and Zijlmans,J.M. (2004) Dynamics of protein binding to telomeres in living cells: implications for telomere structure and function. Mol. Cell. Biol., 24, 5587-5594. open in new tab
  30. Nishikawa,T., Okamura,H., Nagadoi,A., König,P., Rhodes,D. and Nishimura,Y. (2001) Solution structure of a telomeric DNA complex of human TRF1. Structure, 9, 1237-1251. open in new tab
  31. Burglin,T.R. and Affolter,M. (2015) Homeodomain proteins: an update. Chromosoma, 125, 497-521. open in new tab
  32. Colasanti,A.V., Lu,X.-J. and Olson,W.K. (2013) Analyzing and building nucleic acid structures with 3DNA. JoVE, e4401. open in new tab
  33. Furini,S., Domene,C. and Cavalcanti,S. (2010) Insights into the sliding movement of the Lac repressor nonspecifically bound to DNA. J. Phys. Chem. B, 114, 2238-2245. open in new tab
  34. Maffeo,C., Schopflin,R., Brutzer,H., Stehr,R., Aksimentiev,A., Wedemann,G. and Seidel,R. (2010) DNA-DNA interactions in tight supercoils are described by a small effective charge density. Phys. Rev. Lett., 105, 158101. open in new tab
  35. Marklund,E.G., Mahmutovic,A., Berg,O.G., Hammar,P., van der Spoel,D., Fange,D. and Elf,J. (2013) Transcription-factor binding and sliding on DNA studied using micro-and macroscopic models. Proc. Natl. Acad. Sci. U.S.A., 110, 19796-19801. open in new tab
  36. Yoo,J. and Aksimentiev,A. (2016) Improved parameterization of amine-carboxylate and amine-phosphate interactions for molecular dynamics simulations using the CHARMM and AMBER force fields. J. Chem. Theory Comput., 12, 430-443. open in new tab
  37. Abraham,M.J., Murtola,T., Schulz,R., Pall,S., Smith,J.C., Hess,B. and Lindahl,E. (2015) GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1-2, 19-25. open in new tab
  38. Perez,A., Marchan,I., Svozil,D., Sponer,J., Cheatham,T.E., Laughton,C.A. and Orozco,M. (2007) Refinement of the amber force field for nucleic acids: improving the description of ␣/␥ conformers. Biophys. J., 92, 3817-3829. open in new tab
  39. Wieczor,M., Tobiszewski,A., Wityk,P., Tomiczek,B. and Czub,J. (2014) Molecular recognition in complexes of TRF proteins with telomeric DNA. PLoS ONE, 9, e89460. open in new tab
  40. Torrie,G. and Valleau,J. (1977) Nonphysical sampling distributions in Monte Carlo free-energy estimation: umbrella sampling. J. Comput. Phys., 23, 187-199. open in new tab
  41. Kumar,S., Rosenberg,J.M., Bouzida,D., Swendsen,R.H. and Kollman,P.A. (1992) THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem., 13, 1011-1021. open in new tab
  42. Tribello,G.A., Bonomi,M., Branduardi,D., Camilloni,C. and Bussi,G. (2014) PLUMED 2: new feathers for an old bird. Comput. Phys. Commun., 185, 604-613. open in new tab
  43. Ogata,K., Morikawa,S., Nakamura,H., Sekikawa,A., Inoue,T., Kanai,H., Sarai,A., Ishii,S. and Nishimura,Y. (1994) Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell, 79, 639-648. open in new tab
  44. Hanaoka,S., Nagadoi,A. and Nishimura,Y. (2005) Comparison between TRF2 and TRF1 of their telomeric DNA-bound structures and DNA-binding activities. Protein Sci., 14, 119-130. open in new tab
  45. Ivani,I., Dans,P.D., Noy,A., Pérez,A., Faustino,I., Hospital,A., Walther,J., Andrio,P., Goñi,R., Balaceanu,A. et al. (2016) Parmbsc1: a refined force field for DNA simulations. Nat. Methods, 13, 55-58. open in new tab
  46. Blainey,P.C., Luo,G., Kou,S.C., Mangel,W.F., Verdine,G.L., Bagchi,B. and Xie,X.S. (2009) Nonspecifically bound proteins spin while diffusing along DNA. Nat. Struct. Mol. Biol., 16, 1224-1229. open in new tab
  47. Slutsky,M. and Mirny,L.A. (2004) Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential. Biophys. J., 87, 4021-4035. open in new tab
  48. Dahirel,V., Paillusson,F., Jardat,M., Barbi,M. and Victor,J.-M. (2009) Nonspecific DNA-protein interaction: why proteins can diffuse along DNA. Phys. Rev. Lett., 102, 228101. open in new tab
  49. Condamin,S., Tejedor,V., Voituriez,R., Benichou,O. and Klafter,J. (2008) Probing microscopic origins of confined subdiffusion by first-passage observables. Proc. Natl. Acad. Sci. U.S.A., 105, 5675-5680. open in new tab
  50. Furini,S. and Domene,C. (2014) DNA recognition process of the lactose repressor protein studied via metadynamics and umbrella sampling simulations. J. Phys. Chem. B, 118, 13059-13065. open in new tab
  51. Merino,F., Bouvier,B. and Cojocaru,V. (2015) Cooperative DNA recognition modulated by an interplay between protein-protein interactions and DNA-mediated allostery. PLoS Comput. Biol., 11, e1004287. open in new tab
  52. Chen,C. and Pettitt,B.M. (2011) The binding process of a nonspecific enzyme with DNA. Biophys. J., 101, 1139-1147. open in new tab
  53. Furini,S., Barbini,P. and Domene,C. (2013) DNA-recognition process described by MD simulations of the lactose repressor protein on a specific and a non-specific DNA sequence. Nucleic Acids Res., 41, 3963-3972. open in new tab
  54. Ghosh,S., Chandra,N. and Vishveshwara,S. (2015) Mechanism of iron-dependent repressor (IdeR) activation and DNA binding: a molecular dynamics and protein structure network study. PLoS Comput. Biol., 11, e1004500. open in new tab
  55. Vuzman,D., Azia,A. and Levy,Y. (2010) Searching DNA via a 'Monkey Bar' mechanism: the significance of disordered tails. J. Mol. Biol., 396, 674-684. open in new tab
  56. Kophengnavong,T., Carroll,A.S. and Blackwell,T.K. (1999) The SKN-1 amino-terminal arm is a DNA specificity segment. Mol. Cell. Biol., 19, 3039-3050. open in new tab
  57. Vuzman,D. and Levy,Y. (2012) Intrinsically disordered regions as affinity tuners in protein-DNA interactions. Mol. BioSyst., 8, 47-57. open in new tab
  58. Kamberaj,H. and van der Vaart,A. (2009) Extracting the causality of correlated motions from molecular dynamics simulations. Biophys. J., 97, 1747-1755. open in new tab
  59. Suarez,E., Adelman,J.L. and Zuckerman,D.M. (2016) Accurate estimation of protein folding and unfolding times: beyond Markov State models. J. Chem. Theory Comput., 12, 3473-3481. open in new tab
Verified by:
Gdańsk University of Technology

seen 127 times

Recommended for you

Meta Tags