Thermodynamic and structural basis for relaxation of specificity in protein-DNA recognition

Journal of Molecular Biology

Volumn 426, Issue 1, 2014, Pages 84-104

  Sapienza, Paul J ^a   Niu, Tianyi ^a   Kurpiewski, Michael R ^a   Grigorescu, Arabela ^a   Jen Jacobson, Linda ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

cosolute effect; heat capacity; indirect readout; osmolyte; restriction endonuclease

Indexed keywords

5' PURINE PYRIMIDINE; A138T ENDONUCLEASE; DNA; ECORI ENDONUCLEASE; ENDONUCLEASE; MUTANT PROTEIN; PYRIMIDINE DERIVATIVE; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE I; DNA BINDING PROTEIN; OLIGODEOXYNUCLEOTIDE; PHOSPHOPROTEIN; PURINE; PURINE DERIVATIVE; PYRIMIDINE; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA CLEAVAGE; DNA STRAND; ENZYME SPECIFICITY; HEAT; MACROMOLECULE; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA INTERACTION; THERMODYNAMICS; WILD TYPE; BASE PAIRING; COMPLEX FORMATION; DNA FLANKING REGION; DNA PROTEIN COMPLEX; DNA SEQUENCE; DNA STRUCTURE; ENZYME STABILITY; NUCLEOTIDE BINDING SITE; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN MOTIF; PROTEIN STRUCTURE;

EID: 84890859461     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.09.005     Document Type: Article

References (90)

1. D.R. Lesser, M.R. Kurpiewski, and L. Jen-Jacobson The energetic basis of specificity in the Eco RI endonuclease-DNA interaction Science 250 1990 776 786
2. L. Jen-Jacobson Protein-DNA recognition complexes: conservation of structure and binding energy in the transition state Biopolymers 44 1997 153 180
3. P.J. Sapienza, C.A. Dela Torre, W.H. McCoy III, S.V. Jana, and L. Jen-Jacobson Thermodynamic and kinetic basis for the relaxed DNA sequence specificity of "promiscuous" mutant EcoRI endonucleases J Mol Biol 348 2005 307 324
4. A. Pingoud, M. Fuxreiter, V. Pingoud, and W. Wende Type II restriction endonucleases: structure and mechanism Cell Mol Life Sci 62 2005 685 707
5. R. Rohs, H. Sklenar, and Z. Shakked Structural and energetic origins of sequence-specific DNA bending: Monte Carlo simulations of papillomavirus E2-DNA binding sites Structure 13 2005 1499 1509
6. D.R. Lesser, M.R. Kurpiewski, T. Waters, B.A. Connolly, and L. Jen-Jacobson Facilitated distortion of the DNA site enhances EcoRI endonuclease-DNA recognition Proc Natl Acad Sci U S A 90 1993 7548 7552
7. S.P. Hancock, D.A. Hiller, J.J. Perona, and L. Jen-Jacobson The energetic contribution of induced electrostatic asymmetry to DNA bending by a site-specific protein J Mol Biol 406 2011 285 312
8. Z. Otwinowski, R.W. Schevitz, R.G. Zhang, C.L. Lawson, A. Joachimiak, and R.Q. Marmorstein et al. Crystal structure of trp repressor/operator complex at atomic resolution Nature 335 1988 321 329
9. R. Rohs, X. Jin, S.M. West, R. Joshi, B. Honig, and R.S. Mann Origins of specificity in protein-DNA recognition Annu Rev Biochem 79 2010 233 269
10. C.L. Lawson, and H.M. Berman Indirect readout of DNA sequence by proteins P.A. Rice, C. Correll, Structural biology of protein-nucleic acid interactions 2008 Royal Society of Chemistry Publishing Cambridge, UK 66 90
11. M.C. Mossing, and M.T. Record Jr. Thermodynamic origins of specificity in the lac repressor-operator interaction. Adaptability in the recognition of mutant operator sites J Mol Biol 186 1985 295 305
12. L. Jen-Jacobson Structural-perturbation approaches to thermodynamics of site-specific protein-DNA interactions Methods Enzymol 259 1995 305 344
13. D.A. Hiller, A.M. Rodriguez, and J.J. Perona Non-cognate enzyme-DNA complex: structural and kinetic analysis of EcoRV endonuclease bound to the EcoRI recognition site GAATTC J Mol Biol 354 2005 121 136
14. D.E. Frank, R.M. Saecker, J.P. Bond, M.W. Capp, O.V. Tsodikov, and S.E. Melcher et al. Thermodynamics of the interactions of lac repressor with variants of the symmetric lac operator: effects of converting a consensus site to a non-specific site J Mol Biol 267 1997 1186 1206
15. L.E. Engler, K.K. Welch, and L. Jen-Jacobson Specific binding by EcoRV endonuclease to its DNA recognition site GATATC J Mol Biol 269 1997 82 101
16. Engler, L. E. (1998). Specificity determinants in the BamHI-DNA interaction. Ph.D. Thesis, University of Pittsburgh.
17. Grigorescu, A. (2003). Structural and Energetic Determinants of the Binding Specificity of EcoRI Endonuclease. Ph.D. Thesis, University of Pittsburgh.
18. C.G. Kalodimos, N. Biris, A.M. Bonvin, M.M. Levandoski, M. Guennuegues, and R. Boelens et al. Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes Science 305 2004 386 389
19. J. Romanuka, G.E. Folkers, N. Biris, E. Tishchenko, H. Wienk, and A.M. Bonvin et al. Specificity and affinity of Lac repressor for the auxiliary operators O2 and O3 are explained by the structures of their protein-DNA complexes J Mol Biol 390 2009 478 489
20. C.A. Frederick, J. Grable, M. Melia, C. Samudzi, L. Jen-Jacobson, and B.C. Wang et al. Kinked DNA in crystalline complex with EcoRI endonuclease Nature 309 1984 327 331
21. 2 + binding to the active site of EcoRV endonuclease: a crystallographic study of complexes with substrate and product DNA at 2 Å resolution Biochemistry 34 1995 683 696
22. M. Newman, T. Strzelecka, L.F. Dorner, I. Schildkraut, and A.K. Aggarwal Structure of Bam HI endonuclease bound to DNA: partial folding and unfolding on DNA binding Science 269 1995 656 663
23. 2 + sites in a DNA-modifying enzyme to reveal determinants of catalytic specificity Proc Natl Acad Sci U S A 109 2012 E993 E1000
24. A. Grigorescu, M. Horvath, P.A. Wilkosz, K. Chandrasekhar, and J.M. Rosenberg The integration of recognition and cleavage: X-ray structures of pre-transition state complex, post reactive complex and the DNA-free endonuclease A.M. Pingoud, Restriction endonucleases 2003 Springer Berlin, Germany 137 173
25. K.M. Stone, J.E. Townsend, J. Sarver, P.J. Sapienza, S. Saxena, and L. Jen-Jacobson Electron spin resonance shows common structural features for different classes of EcoRI-DNA complexes Angew Chem Int Ed Engl 47 2008 10192 10194
26. J. Alves, T. Ruter, R. Geiger, A. Fliess, G. Maass, and A. Pingoud Changing the hydrogen-bonding potential in the DNA binding site of EcoRI by site-directed mutagenesis drastically reduces the enzymatic activity, not, however, the preference of this restriction endonuclease for cleavage within the site-GAATTC Biochemistry 28 1989 2678 2684
27. L.F. Dorner, J. Bitinaite, R.D. Whitaker, and I. Schildkraut Genetic analysis of the base-specific contacts of BamHI restriction endonuclease J Mol Biol 285 1999 1515 1523
28. A. Fritz, W. Kuster, and J. Alves Asn141 is essential for DNA recognition by EcoRI restriction endonuclease FEBS Lett 438 1998 66 70
29. T. Ivanenko, J. Heitman, and A. Kiss Mutational analysis of the function of Met137 and Ile197, two amino acids implicated in sequence-specific DNA recognition by the EcoRI endonuclease Biol Chem 379 1998 459 465
30. M.C. Needels, S.R. Fried, R. Love, J.M. Rosenberg, H.W. Boyer, and P.J. Greene Determinants of EcoRI endonuclease sequence discrimination Proc Natl Acad Sci U S A 86 1989 3579 3583
31. J. Osuna, H. Flores, and X. Soberon Combinatorial mutagenesis of three major groove-contacting residues of EcoRI: single and double amino acid replacements retaining methyltransferase-sensitive activities Gene 106 1991 7 12
32. Z. Zhu, J. Zhou, A.M. Friedman, and S.Y. Xu Isolation of BsoBI restriction endonuclease variants with altered substrate specificity J Mol Biol 330 2003 359 372
33. J. Heitman, and P. Model Mutants of the EcoRI endonuclease with promiscuous substrate specificity implicate residues involved in substrate recognition EMBO J 9 1990 3369 3378
34. P.J. Sapienza, J.M. Rosenberg, and L. Jen-Jacobson Structural and thermodynamic basis for enhanced DNA binding by a promiscuous mutant EcoRI endonuclease Structure 15 2007 1368 1382
35. L. Jen-Jacobson, and L.A. Jacobson The role of water and the effects of small ions in site-specific protein-DNA interactions P.A. Rice, C. Correll, Structural biology of protein-nucleic acid interactions 2008 Royal Society of Chemistry Publishing Cambridge, UK 13 46
36. Cao, D. F. (2001). Co-solute effects as probes of the role of water release in DNA binding and catalysis by three restriction endonucleases. Ph.D. Thesis, University of Pittsburgh.
37. J.A. Schellman A simple-model for solvation in mixed-solvents - applications to the stabilization and destabilization of macromolecular structures Biophys Chem 37 1990 121 140
38. H. Eisenberg Protein and nucleic-acid hydration and cosolvent interactions - establishment of reliable base-line values at high cosolvent concentrations Biophys Chem 53 1994 57 68
39. M.T. Record, and C.F. Anderson Interpretation of preferential interaction coefficients of nonelectrolytes and of electrolyte ions in terms of a 2-domain model Biophys J 68 1995 786 794
40. D.J. Windsor, and P.R. Wills Thermodynamic nonideality and protein solvation R.B. Gregory, Protein-solvation interactions 1995 Marcel Dekker, Inc. New York, NY 483
41. M.T. Record, W.T. Zhang, and C.F. Anderson Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: A practical guide to recognizing and interpreting polyelectrolyte effects, Hofmeister effects, and osmotic effects of salts Adv Protein Chem 51 51 1998 281 353
42. S.N. Timasheff Control of protein stability and reactions by weakly interacting cosolvents: the simplicity of the complicated Adv Protein Chem 51 51 1998 355 432
43. B.L. Neal, D. Asthagiri, and A.M. Lenhoff Molecular origins of osmotic second virial coefficients of proteins Biophys J 75 1998 2469 2477
44. A.P. Minton Molecular crowding: analysis of effects of high concentrations of inert cosolutes on biochemical equilibria and rates in terms of volume exclusion Methods Enzymol 295 1998 127 149
45. V.A. Parsegian, R.P. Rand, and D.C. Rau Osmotic stress, crowding, preferential hydration, and binding: a comparison of perspectives Proc Natl Acad Sci U S A 97 2000 3987 3992
46. R. Chitra, and P.E. Smith Preferential interactions of cosolvents with hydrophobic solutes J Phys Chem B 105 2001 11513 11522
47. P.R. Davis-Searles, A.J. Saunders, D.A. Erie, D.J. Winzor, and G.J. Pielak Interpreting the effects of small uncharged solutes on protein-folding equilibria Annu Rev Biophys Biomol Struct 30 2001 271 306
48. S.N. Timasheff Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components Proc Natl Acad Sci U S A 99 2002 9721 9726
49. C.F. Anderson, D.J. Felitsky, J. Hong, and M.T. Record Generalized derivation of an exact relationship linking different coefficients that characterize thermodynamic effects of preferential interactions Biophys Chem 101 2002 497 511
50. J.A. Schellman Protein stability in mixed solvents: a balance of contact interaction and excluded volume Biophys J 85 2003 108 125
51. J.M. Schurr, D.P. Rangel, and S.R. Aragon A contribution to the theory of preferential interaction coefficients Biophys J 89 2005 2258 2276
52. J.A. Schellman Destabilization and stabilization of proteins Q Rev Biophys 38 2005 351 361
53. S. Shimizu, and N. Matubayasi Preferential hydration of proteins: a Kirkwood-Buff approach Chem Phys Lett 420 2006 518 522
54. I.L. Shulgin, and E. Ruckenstein A protein molecule in a mixed solvent: the preferential binding parameter via the Kirkwood-Buff theory Biophys J 90 2006 704 707
55. P.E. Smith Chemical potential derivatives and preferential interaction parameters in biological systems from Kirkwood-Buff theory Biophys J 91 2006 849 856
56. J. Rosgen, B.M. Pettitt, and D.W. Bolen An analysis of the molecular origin of osmolyte-dependent protein stability Protein Sci 16 2007 733 743
57. V. Pierce, M. Kang, M. Aburi, S. Weerasinghe, and P.E. Smith Recent applications of Kirkwood-Buff theory to biological systems Cell Biochem Biophys 50 2008 1 22
58. J.G. Kirkwood, and F.P. Buff The statistical mechanical theory of solutions. 1 J Chem Phys 19 1951 774 777
59. A. Ben-Naim Statistical thermodynamics for chemists and biochemists 1992 Plenum New York, NY 372 382 [and 448-457]
60. L. Jen-Jacobson, L.E. Engler, J.T. Ames, M.R. Kurpiewski, and A. Grigorescu Thermodynamic parameters of specific and nonspecific protein-DNA binding Supramol Chem 12 2000 143 160
61. Y. Takeda, P.D. Ross, and C.P. Mudd Thermodynamics of Cro protein-DNA interactions Proc Natl Acad Sci U S A 89 1992 8180 8184
62. J.E. Ladbury, J.G. Wright, J.M. Sturtevant, and P.B. Sigler A thermodynamic study of the trp repressor-operator interaction J Mol Biol 238 1994 669 681
63. C. Berger, I. Jelesarov, and H.R. Bosshard Coupled folding and site-specific binding of the GCN4-bZIP transcription factor to the AP-1 and ATF/CREB DNA sites studied by microcalorimetry Biochemistry 35 1996 14984 14991
64. J.M. Sturtevant Heat capacity and entropy changes in processes involving proteins Proc Natl Acad Sci U S A 74 1977 2236 2240
65. J.R. Livingstone, R.S. Spolar, and M.T. Record Jr. Contribution to the thermodynamics of protein folding from the reduction in water-accessible nonpolar surface area Biochemistry 30 1991 4237 4244
66. R.S. Spolar, J.R. Livingstone, and M.T. Record Jr. Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water Biochemistry 31 1992 3947 3955
67. R.S. Spolar, and M.T. Record Coupling of local folding to site-specific binding of proteins to DNA Science 263 1994 777 784
68. I. Haq, R. O'Brien, A. Lagunavicius, V. Siksnys, and J.E. Ladbury Specific DNA recognition by the type II restriction endonuclease MunI: the effect of pH Biochemistry 40 2001 14960 14967
69. K.J. Laidler, and M.C. King The development of transition-state theory J Phys Chem 87 1983 2657 2664
70. J.M. Rosenberg Structure and function of restriction endonucleases Curr Opin Struct Biol 1 1991 104 113
71. M.R. Kurpiewski, L.E. Engler, L.A. Wozniak, A. Kobylanska, M. Koziolkiewicz, and W.J. Stec et al. Mechanisms of coupling between DNA recognition specificity and catalysis in EcoRI endonuclease Structure (Camb) 12 2004 1775 1788
72. P.J. Sapienza, and A.L. Lee Using NMR to study fast dynamics in proteins: methods and applications Curr Opin Pharmacol 10 2010 723 730
73. N.V. Nucci, M.S. Pometun, and A.J. Wand Site-resolved measurement of water-protein interactions by solution NMR Nat Struct Mol Biol 18 2011 245 249
74. S.R. Tzeng, and C.G. Kalodimos Protein activity regulation by conformational entropy Nature 488 2012 236 240
75. A.J. Wand The dark energy of proteins comes to light: conformational entropy and its role in protein function revealed by NMR relaxation Curr Opin Struct Biol 23 2013 75 81
76. D.D. Boehr, R. Nussinov, and P.E. Wright The role of dynamic conformational ensembles in biomolecular recognition Nat Chem Biol 5 2009 789 796
77. L. Jen-Jacobson, M. Kurpiewski, D. Lesser, J. Grable, H.W. Boyer, and J.M. Rosenberg et al. Coordinate ion pair formation between EcoRI endonuclease and DNA J Biol Chem 258 1983 14638 14646
78. M.M. Warshaw, and C.R. Cantor Oligonucleotide interactions. IV. Conformational differences between deoxy- and ribodinucleoside phosphates Biopolymers 9 1970 1079 1103
79. M. Senior, R.A. Jones, and K.J. Breslauer Influence of dangling thymidine residues on the stability and structure of two DNA duplexes Biochemistry 27 1988 3879 3885
80. D.R. Lesser, A. Grajkowski, M.R. Kurpiewski, M. Koziolkiewicz, W.J. Stec, and L. Jen-Jacobson Stereoselective interaction with chiral phosphorothioates at the central DNA kink of the EcoRI endonuclease-GAATTC complex J Biol Chem 267 1992 24810 24818
81. H. Fukada, and K. Takahashi Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride Proteins 33 1998 159 166
82. B.M. Baker, and K.P. Murphy Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry Biophys J 71 1996 2049 2055
83. A.G. Kozlov, and T.M. Lohman Large contributions of coupled protonation equilibria to the observed enthalpy and heat capacity changes for ssDNA binding to Escherichia coli SSB protein Proteins Suppl 4 2000 8 22
84. J.R. Horn, J.F. Brandts, and K.P. Murphy van't Hoff and calorimetric enthalpies II: effects of linked equilibria Biochemistry 41 2002 7501 7507
85. W.J. Becktel, and J.A. Schellman Protein stability curves Biopolymers 26 1987 1859 1877
86. J.H. Ha, R.S. Spolar, and M.T. Record Jr. Role of the hydrophobic effect in stability of site-specific protein-DNA complexes J Mol Biol 209 1989 801 816
87. S.F. Dec, and S.J. Gill Temperature dependence of errors in parameters derived from van't Hoff studies J Chem Educ 62 1985 879 881
88. E.C.W. Clarke, and D.N. Glew Evaluation of thermodynamic functions from equilibrium constants Trans Faraday Soc 62 1966 539 547
89. W. Zhang, M.W. Capp, J.P. Bond, C.F. Anderson, and M.T. Record Jr. Thermodynamic characterization of interactions of native bovine serum albumin with highly excluded (glycine betaine) and moderately accumulated (urea) solutes by a novel application of vapor pressure osmometry Biochemistry 35 1996 10506 10516
90. U. Siebenlist, and W. Gilbert Contacts between Escherichia coli RNA polymerase and an early promoter of phage T7 Proc Natl Acad Sci U S A 77 1980 122 126