Positive and negative impacts of nonspecific sites during target location by a sequence-specific DNA-binding protein: Origin of the optimal search at physiological ionic strength

Nucleic Acids Research

Volumn 42, Issue 11, 2014, Pages 7039-7046

  Esadze, Alexandre ^a   Kemme, Catherine A ^a   Kolomeisky, Anatoly B ^b   Iwahara, Junji ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1;

ARTICLE; BINDING KINETICS; BINDING SITE; DNA DETERMINATION; DNA SEQUENCE; FLUORESCENCE SPECTROSCOPY; GENE TARGETING; IONIC STRENGTH; PRIORITY JOURNAL; PROTEIN DISSOCIATION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN SLIDING; PROTEIN TARGETING; STOPPED FLOW FLUORESCENCE ASSAY;

DNA; EARLY GROWTH RESPONSE PROTEIN 1; HUMANS; KINETICS; OSMOLAR CONCENTRATION;

EID: 84903191631     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku418     Document Type: Article

References (53)

1. Berg O.G. Winter R.B. and von Hippel P.H. (1981) Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 20 6929-6948.
2. Gorman J. and Greene E.C. (2008) Visualizing one-dimensional diffusion of proteins along DNA. Nat. Struct.Mol. Biol. 15 768-774.
3. Halford S.E. (2009) An end to 40 years of mistakes in DNA-protein association kinetics Biochem. Soc. Trans. 37 343-348.
4. Halford S.E. and Marko J.F. (2004) How do site-specific DNA-binding proteins find their targets Nucleic Acids Res. 32 3040-3052.
5. Kolomeisky A.B. (2011) Physics of protein-DNA interactions: mechanisms of facilitated target search. Phys. Chem. Chem. Phys. 13 2088-2095.
6. Mirny L. Slutsky M. Wunderlich Z. Tafvizi A. Leith J. and Kosmrlj A. (2009) How a protein searches for its site on DNA: the mechanism of facilitated diffusion. J. Phys. A: Math. Theor. 42 401335.
7. Monico C. Capitanio M. Belcastro G. Vanzi F. and Pavone F.S. (2013) Optical methods to study protein-DNA interactions in vitro and in living cells at the single-molecule level. Int. J. Mol. Sci. 14 3961-3992.
8. Sheinman M. Benichou O. Kafri Y. and Voituriez R. (2012) Classes of fast and specific search mechanisms for proteins on DNA. Rep. Prog. Phys. 75 026601.
9. Tafvizi A. Mirny L.A. and van Oijen A.M. (2011) Dancing on DNA: kinetic aspects of search processes on DNA. Chemphyschem 12 1481-1489.
10. von Hippel P.H. and Berg O.G. (1989) Facilitated target location in biological systems. J. Biol. Chem. 264 675-678.
11. Winter R.B. Berg O.G. and von Hippel P.H. (1981) Diffusion-driven mechanisms of protein translocation on nucleic acids. 3. The Escherichia coli lac repressor-operator interaction: kinetic measurements and conclusions. Biochemistry 20 6961-6977.
12. Lewin B. (2000) Genes VII. Oxford Univ Press Oxford.
13. Valouev A. Johnson S.M. Boyd S.D. Smith C.L. Fire A.Z. and Sidow A. (2011) Determinants of nucleosome organization in primary human cells. Nature 474 516-520.
14. Elrod-Erickson M. Rould M.A. Nekludova L. and Pabo C.O. (1996) Zif268 protein-DNA complex refined at 1.6 A : a model system for understanding zinc finger-DNA interactions. Structure 4 1171-1180.
15. Pavletich N.P. and Pabo C.O. (1991) Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A . Science 252 809-817.
16. Bozon B. Davis S. and Laroche S. (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40 695-701.
17. Lee J.L. Everitt B.J. and Thomas K.L. (2004) Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304 839-843.
18. Khachigian L.M. Lindner V. Williams A.J. and Collins T. (1996) Egr-1-induced endothelial gene expression: a common theme in vascular injury. Science 271 1427-1431.
19. Yan S.F. Fujita T. Lu J. Okada K. Shan Zou Y. Mackman N. Pinsky D.J. and Stern D.M. (2000) Egr-1 a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat. Med. 6 1355-1361.
20. Esadze A. and Iwahara J. (2014) Stopped-flow fluorescence kinetic study of protein sliding and intersegment transfer in the target DNA search process. J. Mol. Biol. 426 230-244.
21. Iwahara J. and Levy Y. (2013) Speed-stability paradox in DNA-scanning by zinc-finger proteins. Transcription 4 58-61.
22. Takayama Y. Sahu D. and Iwahara J. (2010) NMR studies of translocation of the Zif268 protein between its target DNA Sites. Biochemistry 49 7998-8005.
23. Zandarashvili L. Vuzman D. Esadze A. Takayama Y. Sahu D. Levy Y. and Iwahara J. (2012) Asymmetrical roles of zinc fingers in dynamic DNA-scanning process by the inducible transcription factor Egr-1. Proc. Natl. Acad. Sci. U.S.A. 109 E1724-E1732.
24. Pollard T.D. and De La Cruz E.M. (2013) Take advantage of time in your experiments: a guide to simple informative kinetics assays. Mol. Biol. Cell 24 1103-1110.
25. Redner S. (2001) A Guide to First-Passage Processes. Cambridge University Press Cambridge.
26. Veksler A. and Kolomeisky A.B. (2013) Speed-selectivity paradox in the protein search for targets on DNA: is it real or not J. Phys. Chem. B 117 12695-12701.
27. Manning G.S. (1978) Molecular theory of polyelectrolyte solutions with applications to electrostatic properties of polynucleotides. Q. Rev. Biophys. 11 179-246.
28. Record M.T. Anderson C.F. and Lohman T.M. (1978) Thermodynamic analysis of ion effects on binding and conformational equilibria of proteins and nucleic-acids-roles of ion association or release screening and ion effects on water activity. Q. Rev. Biophys. 11 103-178.
29. Berg O.G. and Ehrenberg M. (1982) Association kinetics with coupled three-and one-dimensional diffusion. Chain-length dependence of the association rate of specific DNA sites. Biophys. Chem. 15 41-51.
30. Kim J.G. Takeda Y. Matthews B.W. and Anderson W.F. (1987) Kinetic studies on Cro repressor-operator DNA interaction. J. Mol. Biol. 196 149-158.
31. Stanford N.P. Szczelkun M.D. Marko J.F. and Halford S.E. (2000) One-and three-dimensional pathways for proteins to reach specific DNA sites. EMBO J. 19 6546-6557.
32. Terry B.J. Jack W.E. and Modrich P. (1985) Facilitated diffusion during catalysis by EcoRI endonuclease. Nonspecific interactions in EcoRI catalysis. J. Biol. Chem. 260 13130-13137.
33. Zhou H.X. (2005) A model for the mediation of processivity of DNA-targeting proteins by nonspecific binding: dependence on DNA length and presence of obstacles. Biophys. J. 88 1608-1615.
34. Barkley M.D. (1981) Salt dependence of the kinetics of the lac repressor-operator interaction: role of nonoperator deoxyribonucleic acid in the association reaction. Biochemistry 20 3833-3842.
35. Rau D.C. and Sidorova N.Y. (2010) Diffusion of the restriction nuclease EcoRI along DNA. J. Mol. Biol. 395 408-416.
36. Tafvizi A. Huang F. Leith J.S. Fersht A.R. Mirny L.A. and van Oijen A.M. (2008) Tumor suppressor p53 slides on DNA with low friction and high stability. Biophys. J. 95 L01-L03.
37. Bresloff J.L. and Crothers D.M. (1975) DNA-ethidium reaction kinetics: demonstration of direct ligand transfer between DNA binding sites. J. Mol. Biol. 95 103-123.
38. Fried M.G. and Crothers D.M. (1984) Kinetics and mechanism in the reaction of gene regulatory proteins with DNA. J. Mol. Biol. 172 263-282.
39. Iwahara J. and Clore G.M. (2006) Direct observation of enhanced translocation of a homeodomain between DNA cognate sites by NMR exchange spectroscopy. J. Am. Chem. Soc. 128 404-405.
40. Iwahara J. Zweckstetter M. and Clore G.M. (2006) NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA. Proc. Natl. Acad. Sci. U.S.A. 103 15062-15067.
41. Lieberman B.A. and Nordeen S.K. (1997) DNA intersegment transfer how steroid receptors search for a target site. J. Biol. Chem. 272 1061-1068.
42. Sidorova N.Y. Scott T. and Rau D.C. (2013) DNA concentration-dependent dissociation of EcoRI: direct transfer or reaction during hopping. Biophys. J. 104 1296-1303.
43. Takayama Y. and Clore G.M. (2012) Interplay between minor and major groove-binding transcription factors Sox2 and Oct1 in translocation on DNA studied by paramagnetic and diamagnetic NMR. J. Biol. Chem. 287 14349-14363.
44. Lohman T.M. DeHaseth P.L. and Record M.T. Jr (1978) Analysis of ion concentration effects of the kinetics of protein-nucleic acid interactions. Application to lac repressor-operator interactions. Biophys. Chem. 8 281-294.
45. Bonnet I. Biebricher A. Porte P.L. Loverdo C. Benichou O. Voituriez R. Escude C. Wende W. Pingoud A. and Desbiolles P. (2008) Sliding and jumping of single EcoRV restriction enzymes on non-cognate DNA. Nucleic Acids Res. 36 4118-4127.
46. Givaty O. and Levy Y. (2009) Protein sliding along DNA: dynamics and structural characterization. J. Mol. Biol. 385 1087-1097.
47. Terakawa T. Kenzaki H. and Takada S. (2012) p53 searches on DNA by rotation-uncoupled sliding at C-terminal tails and restricted hopping of core domains. J. Am. Chem. Soc. 134 14555-14562.
48. Blainey P.C. van Oijen A.M. Banerjee A. Verdine G.L. and Xie X.S. (2006) A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc. Natl. Acad. Sci. U.S.A. 103 5752-5757.
49. Gorman J. Wang F. Redding S. Plys A.J. Fazio T. Wind S. Alani E.E. and Greene E.C. (2012) Single-molecule imaging reveals target-search mechanisms during DNA mismatch repair. Proc. Natl. Acad. Sci. U.S.A. 109 E3074-E3083.
50. Anderson K.M. Esadze A. Manoharan M. Br schweiler R. Gorenstein D.G. and Iwahara J. (2013) Direct observation of the ion-pair dynamics at a protein-DNA interface by NMR spectroscopy. J. Am. Chem. Soc. 135 3613-3619.
51. Luger K. Mader A.W. Richmond R.K. Sargent D.F. and Richmond T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 251-260.
52. Schreiber G. and Fersht A.R. (1996) Rapid electrostatically assisted association of proteins. Nat. Struct. Biol. 3 427-431.
53. Vijayakumar M. Wong K.Y. Schreiber G. Fersht A.R. Szabo A. and Zhou H.X. (1998) Electrostatic enhancement of diffusion-controlled protein-protein association: comparison of theory and experiment on barnase and barstar. J. Mol. Biol. 278 1015-1024.