Reintroducing electrostatics into macromolecular crystallographic refinement: Application to neutron crystallography and DNA hydration

Structure

Volumn 19, Issue 4, 2011, Pages 523-533

  Fenn, Timothy D ^a   Schnieders, Michael J ^a   Mustyakimov, Marat ^b   Wu, Chuanjie ^c   Langan, Paul ^b   Pande, Vijay S ^a   Brunger, Axel T ^a  

^a STANFORD UNIVERSITY   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c SCHRÖDINGER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA B; DNA Z; HYDROGEN; XYLOSE ISOMERASE;

ARTICLE; ATOM; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA HYDRATION; DNA STRUCTURE; ENTROPY; GEOMETRY; HYDRATION; HYDROGEN BOND; MACROMOLECULAR CRYSTALLOGRAPHIC REFINEMENT; MACROMOLECULE; NEUTRON; NEUTRON CRYSTALLOGRAPHY; ORIENTATION; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; STATIC ELECTRICITY; THERMODYNAMICS; X RAY ANALYSIS; X RAY DIFFRACTION;

ALDOSE-KETOSE ISOMERASES; CRYSTALLOGRAPHY; DNA; DNA, Z-FORM; HYDROGEN BONDING; MODELS, MOLECULAR; NEUTRON DIFFRACTION; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; STATIC ELECTRICITY; THERMODYNAMICS; WATER; X-RAY DIFFRACTION;

EID: 79953902483     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.01.015     Document Type: Article

References (97)

1. P.D. Adams, N.S. Pannu, R.J. Read, and A.T. Brünger Cross-validated maximum likelihood enhances crystallographic simulated annealing refinement Proc. Natl. Acad. Sci. USA 94 1997 5018 5023 (Pubitemid 27214728)
2. P.D. Adams, M. Mustyakimov, P.V. Afonine, and P. Langan Generalized X-ray and neutron crystallographic analysis: more accurate and complete structures for biological macromolecules Acta Crystallogr. D Biol. Crystallogr. 65 2009 567 573
3. K.N. Allen, A. Lavie, G.K. Farber, A. Glasfeld, G.A. Petsko, and D. Ringe Isotopic exchange plus substrate and inhibition kinetics of D-xylose isomerase do not support a proton-transfer mechanism Biochemistry 33 1994 1481 1487 (Pubitemid 24093696)
4. K.N. Allen, A. Lavie, A. Glasfeld, T.N. Tanada, D.P. Gerrity, S.C. Carlson, G.K. Farber, G.A. Petsko, and D. Ringe Role of the divalent metal ion in sugar binding, ring opening, and isomerization by D-xylose isomerase: replacement of a catalytic metal by an amino acid Biochemistry 33 1994 1488 1494 (Pubitemid 24093697)
5. S. Arai, T. Chatake, T. Ohhara, K. Kurihara, I. Tanaka, N. Suzuki, Z. Fujimoto, H. Mizuno, and N. Niimura Complicated water orientations in the minor groove of the B-DNA decamer d(CCATTAATGG)2 observed by neutron diffraction measurements Nucleic Acids Res. 33 2005 3017 3024 (Pubitemid 41511239)
6. G.E. Bacon, and K. Lonsdale Neutron diffraction Rep. Prog. Phys. 16 1953 1 61
7. E. Baker, and R.E. Hubbard Hydrogen bonding in globular proteins Prog. Biophys. Mol. Biol. 44 1984 97 179
8. D. Bancroft, L.D. Williams, A. Rich, and M. Egli the low-temperature crystal structure of the pure-spermine form of Z-DNA reveals binding of a spermine molecule in the minor groove Biochemistry 33 1994 1073 1086 (Pubitemid 24072435)
9. S. Bhosale, M. Rao, and V. Deshpande Molecular and industrial aspects of glucose isomerase Microbiol. Rev. 60 1996 280 300 (Pubitemid 26170908)
10. M.P. Blakeley, P. Langan, N. Niimura, and A. Podjarny Neutron crystallography: opportunities, challenges, and limitations Curr. Opin. Struct. Biol. 18 2008 593 600
11. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM: A program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
12. A.T. Brünger, J. Kuriyan, and M. Karplus Crystallographic R factor refinement by molecular dynamics Science 235 1987 458 460 (Pubitemid 17009580)
13. A.T. Brunger Low-resolution crystallography is coming of age Structure 13 2005 171 172 (Pubitemid 40247693)
14. T. Chatake, A. Ostermann, K. Kurihara, F.G. Parak, and N. Niimura Hydration in proteins observed by high-resolution neutron crystallography Proteins 50 2003 516 523 (Pubitemid 36158463)
15. T. Chatake, I. Tanaka, H. Umino, S. Arai, and N. Niimura The hydration structure of a Z-DNA hexameric duplex determined by a neutron diffraction technique Acta Crystallogr. D Biol. Crystallogr. 61 2005 1088 1098 (Pubitemid 43958398)
16. X. Chen, I. Weber, and R.W. Harrison Hydration water and bulk water in proteins have distinct properties in radial distributions calculated from 105 atomic resolution crystal structures J. Phys. Chem. B 112 2008 12073 12080
17. T.K. Chiu, M. Kaczor-Grzeskowiak, and R.E. Dickerson Absence of minor groove monovalent cations in the crosslinked dodecamer C-G-C-G-A-T-T-C-G-C-G J. Mol. Biol. 292 1999 589 608 (Pubitemid 29457321)
18. V.P. Chuprina, U. Heinemann, A.A. Nurislamov, P. Zielenkiewicz, R.E. Dickerson, and W. Saenger Molecular dynamics simulation of the hydration shell of a B-DNA decamer reveals two main types of minor-groove hydration depending on groove width Proc. Natl. Acad. Sci. USA 88 1991 593 597 (Pubitemid 21915512)
19. C.A. Collyer, and D.M. Blow Observations of reaction intermediates and the mechanism of aldose-ketose interconversion by D-xylose isomerase Proc. Natl. Acad. Sci. USA 87 1990 1362 1366
20. C.A. Collyer, K. Henrick, and D.M. Blow Mechanism for aldose-ketose interconversion by xylose isomerase involving ring opening followed by a 1,2-hydride shift J. Mol. Biol. 212 1990 211 235
21. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an N • log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
22. Z. Dauter, and D.A. Adamiak Anomalous signal of phosphorus used for phasing DNA oligomer: importance of data redundancy Acta Crystallogr. D Biol. Crystallogr. 57 2001 990 995 (Pubitemid 32620890)
23. W.L. Davidson, G.A. Morton, C.G. Shull, and E.O. Wollan Neutron Diffraction Analysis of NaH and NaD 1947 Atomic Energy Commission Washington, DC
24. G.R. Desiraju, and T. Steiner The weak hydrogen bond Structural Chemistry and Biology 2001 Oxford University Press New York
25. H.R. Drew, and R.E. Dickerson Structure of a B-DNA dodecamer: III. Geometry of hydration J. Mol. Biol. 151 1981 535 556 (Pubitemid 12252694)
26. M. Egli, L.D. Williams, Q. Gao, and A. Rich Structure of the pure-spermine form of Z-DNA (magnesium free) at 1-.ANG. resolution Biochemistry 30 1991 11388 11402
27. R.A. Engh, and R. Huber Accurate bond and angle parameters for X-ray protein structure refinement Acta Crystallogr. A 47 1991 392 400
28. M.A.L. Eriksson, and A. Laaksonen A molecular dynamics study of conformational changes and hydration of left-handed d (CGCGCGCGCGCG)2 in a nonsalt solution Biopolymers 32 1992 1035 1059
29. P.P. Ewald Die Berechnung optischer und elektrostatischer Gitterpotentiale Annalen der Physik 369 1921 253 287
30. G.K. Farber, A. Glasfeld, G. Tiraby, D. Ringe, and G.A. Petsko Crystallographic studies of the mechanism of xylose isomerase Biochemistry 28 1989 7289 7297
31. S.A. Fawthrop, J. Yang, and J. Fisher Structural and dynamic studies of a non-selfcomplementary dodecamer DNA duplex Nucleic Acids Res. 21 1993 4860 4866 (Pubitemid 23330158)
32. T.D. Fenn, D. Ringe, and G.A. Petsko POVScript+: a program for model and data visualization using persistence of vision ray-tracing J. Appl. Crystallogr. 36 2003 944 947
33. T.D. Fenn, D. Ringe, and G.A. Petsko Xylose isomerase in substrate and inhibitor michaelis states: atomic resolution studies of a metal-mediated hydride shift Biochemistry 43 2004 6464 6474 (Pubitemid 38697546)
34. T.D. Fenn, M.J. Schnieders, A.T. Brunger, and V.S. Pande Polarizable atomic multipole X-Ray refinement: hydration geometry and application to macromolecules Biophys. J. 98 2010 2984 2992
35. A.R. Fersht, and L. Serrano Principles of protein stability derived from protein engineering experiments Curr. Opin. Struct. Biol. 3 1993 75 83 (Pubitemid 23058386)
36. J.S. Finer-Moore, A.A. Kossiakoff, J.H. Hurley, T. Earnest, and R.M. Stroud Solvent structure in crystals of trypsin determined by X-ray and neutron diffraction Proteins 12 1992 203 222
37. M.A. Fuertes, V. Cepeda, C. Alonso, and J.M. Pérez Molecular Mechanisms for the B-Z transition in the example of poly[d(G-C)·d(G-C)] polymers. A critical review Chem. Rev. 106 2006 2045 2064
38. M. Fuxreiter, Ö. Farkas, and G. Náray-Szabó Molecular modelling of xylose isomerase catalysis: the role of electrostatics and charge transfer to metals Protein Eng. 8 1995 925 933 (Pubitemid 26002479)
39. R.V. Gessner, G.J. Quigley, and M. Egli Comparative studies of high resolution Z-DNA crystal structures Part 1: Common hydration patterns of alternating dC-dG J. Mol. Biol. 236 1994 1154 1168
40. P.S. Ho, and B.H.M. Mooers Z-DNA crystallography Biopolymers 44 1997 65 90
41. M.H. Hou, S. Lin, J.P. Yuann, W. Lin, A.H. Wang, and L. Kan Effects of polyamines on the thermal stability and formation kinetics of DNA duplexes with abnormal structure Nucleic Acids Res. 29 2001 5121 5128 (Pubitemid 34065430)
42. H. Hu, H. Liu, and Y. Shi The reaction pathway of the isomerization of d-xylose catalyzed by the enzyme d-xylose isomerase: A theoretical study Proteins 27 1997 545 555 (Pubitemid 27212353)
43. K.K. Irikura, B. Tidor, B. Brooks, and M. Karplus Transition from B to Z DNA: contribution of internal fluctuations to the configurational entropy difference Science 229 1985 571 572 (Pubitemid 16239338)
44. B. Jana, S. Pal, P.K. Maiti, S. Lin, J.T. Hynes, and B. Bagchi Entropy of water in the hydration layer of major and minor grooves of DNA J. Phys. Chem. B 110 2006 19611 19618 (Pubitemid 44626446)
45. W.L. Jorgensen, and J. Tirado-Rives The OPLS [optimized potentials for liquid simulations] potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin JACS 110 1988 1657 1666
46. M. Karttunen, J. Rottler, I. Vattulainen, and C. Sagui Electrostatics in biomolecular simulations: Where are we now and where are we heading? S. Feller, Computational Modeling of Membrane Bilayers 2008 Academic Press New York 49 89
47. A. Korostelev, M.O. Fenley, and M.S. Chapman Impact of a Poisson-Boltzmann electrostatic restraint on protein structures refined at medium resolution Acta Crystallogr. D Biol. Crystallogr. 60 2004 1786 1794 (Pubitemid 41079700)
48. A.Y. Kovalevsky, L. Hanson, S.Z. Fisher, M. Mustyakimov, S.A. Mason, V. Trevor Forsyth, M.P. Blakeley, D.A. Keen, T. Wagner, and H. Carrell Metal ion roles and the movement of hydrogen during reaction catalyzed by D-xylose isomerase: a joint X-ray and neutron diffraction study Structure 18 2010 688 699
49. E.B. Krissinel, M.D. Winn, C.C. Ballard, A.W. Ashton, P. Patel, E.A. Potterton, S.J. McNicholas, K.D. Cowtan, and P. Emsley The new CCP4 Coordinate Library as a toolkit for the design of coordinate-related applications in protein crystallography Acta Crystallogr. D Biol. Crystallogr. 60 2004 2250 2255 (Pubitemid 41742777)
50. M.G. Kubinec, and D.E. Wemmer NMR evidence for DNA bound water in solution J. Am. Chem. Soc. 114 1992 8739 8740
51. A. Laaksonen, L.G. Nilsson, B. Jönsson, and O. Teleman Molecular dynamics simulation of double helix Z-DNA in solution Chem. Phys. 129 1989 175 183
52. P. Langan, X. Li, B.L. Hanson, L. Coates, and M. Mustyakimov Synthesis, capillary crystallization and preliminary joint X-ray and neutron crystallographic study of Z-DNA without polyamine at low pH Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62 2006 453 456 (Pubitemid 43810024)
53. P. Langan, Z. Fisher, A. Kovalevsky, M. Mustyakimov, A. Sutcliffe Valone, C. Unkefer, M.J. Waltman, L. Coates, P.D. Adams, and P.V. Afonine Protein structures by spallation neutron crystallography J. Synchrotron Radiat. 15 2008 215 218 (Pubitemid 351571005)
54. T. Lan, and L.W. McLaughlin minor groove hydration is critical to the stability of DNA duplexes J. Am. Chem. Soc. 122 2000 6512 6513 (Pubitemid 30481761)
55. A. Lavie, K.N. Allen, G.A. Petsko, and D. Ringe X-ray crystallographic structures of D-xylose isomerase-substrate complexes position the substrate and provide evidence for metal movement during catalysis Biochemistry 33 1994 5469 5480 (Pubitemid 24162982)
56. C.Y. Lee, M. Bagdasarian, M.H. Meng, and J.G. Zeikus Catalytic mechanism of xylose (glucose) isomerase from Clostridium thermosulfurogenes. Characterization of the structural gene and function of active site histidine J. Biol. Chem. 265 1990 19082 19090
57. E. Liepinsh, G. Otting, and K. Wuthrich NMR observation of individual molecules of hydration water bound to DNA duplexes: direct evidence for a spine of hydration water present in aqueous solution Nucleic Acids Res. 20 1992 6549 6553 (Pubitemid 23052674)
58. J.P. Linge, M.A. Williams, C.A. Spronk, A.M.J.J. Bonvin, and M. Nilges Refinement of protein structures in explicit solvent Proteins 50 2003 496 506 (Pubitemid 36158461)
59. A. Luzar, and D. Chandler Hydrogen-bond kinetics in liquid water Nature 379 1996 55 57 (Pubitemid 126532744)
60. G. Minasov, V. Tereshko, and M. Egli Atomic-resolution crystal structures of B-DNA reveal specific influences of divalent metal ions on conformation and packing J. Mol. Biol. 291 1999 83 99 (Pubitemid 29391407)
61. A.V. Morozov, T. Kortemme, K. Tsemekhman, and D. Baker Close agreement between the orientation dependence of hydrogen bonds observed in protein structures and quantum mechanical calculations Proc. Natl. Acad. Sci. USA 101 2004 6946 6951 (Pubitemid 38596423)
62. L. Moulinier, D.A. Case, and T. Simonson Reintroducing electrostatics into protein X-ray structure refinement: bulk solvent treated as a dielectric continuum Acta Crystallogr. D Biol. Crystallogr. 59 2003 2094 2103 (Pubitemid 38024844)
63. S. Nozinovic, B. Fürtig, H.R.A. Jonker, C. Richter, and H. Schwalbe High-resolution NMR structure of an RNA model system: the 14-mer cUUCGg tetraloop hairpin RNA Nucleic Acids Res. 38 2010 683 694
64. G. Otting, E. Liepinsh, and K. Wuthrich Protein hydration in aqueous solution Science 254 1991 974 980 (Pubitemid 21917420)
65. C. Pace, B. Shirley, M. McNutt, and K. Gajiwala Forces contributing to the conformational stability of proteins FASEB J. 10 1996 75 83 (Pubitemid 26035509)
66. G. Parkinson, J. Vojtechovsky, L. Clowney, A.T. Brünger, and H.M. Berman New parameters for the refinement of nucleic acid-containing structures Acta Crystallogr. D Biol. Crystallogr. 52 1996 57 64 (Pubitemid 126512683)
67. F.M. Pohl, and T.M. Jovin Salt-induced co-operative conformational change of a synthetic DNA: Equilibrium and kinetic studies with poly(dG-dC) J. Mol. Biol. 67 1972 375 396
68. J.W. Ponder, and D.A. Case Force fields for protein simulations Adv. Protein Chem. 66 2003 27 85 (Pubitemid 37392314)
69. J.W. Ponder, C. Wu, P. Ren, V.S. Pande, J.D. Chodera, M.J. Schnieders, I. Haque, D.L. Mobley, D.S. Lambrecht, and R.A. DiStasio Current status of the AMOEBA polarizable force field J. Phys. Chem. B 114 2010 2549 2564
70. P. Ren, and J.W. Ponder Polarizable atomic multipole water model for molecular mechanics simulation J. Phys. Chem. B 107 2003 5933 5947
71. P. Ren, and J.W. Ponder Temperature and pressure dependence of the AMOEBA water model J. Phys. Chem. B 108 2004 13427 13437
72. L.M. Rice, Y. Shamoo, and A.T. Brünger Phase Improvement by Multi-Start Simulated Annealing Refinement and Structure-Factor Averaging J. Appl. Crystallogr. 31 1998 798 805 (Pubitemid 128477508)
73. C. Sagui, and T.A. Darden Molecular dynamics simulations of biomolecules: long-range electrostatic effects Annu. Rev. Biophys. Biomol. Struct. 28 1999 155 179 (Pubitemid 29319256)
74. C. Sagui, L.G. Pedersen, and T.A. Darden Towards an accurate representation of electrostatics in classical force fields: Efficient implementation of multipolar interactions in biomolecular simulations J. Chem. Phys. 120 2004 73
75. M.J. Schnieders, and J.W. Ponder Polarizable atomic multipole solutes in a generalized Kirkwood continuum J. Chem. Theory Comput. 3 2007 2083 2097
76. M.J. Schnieders, N.A. Baker, P. Ren, and J.W. Ponder Polarizable atomic multipole solutes in a Poisson-Boltzmann continuum J. Chem. Phys. 126 2007 124114 124121
77. M.J. Schnieders, T.D. Fenn, V.S. Pande, and A.T. Brunger Polarizable atomic multipole X-ray refinement: application to peptide crystals Acta Crystallogr. D Biol. Crystallogr. 65 2009 952 965
78. K.J. Schray, and I.A. Rose Anomeric specificity and mechanism of two pentose isomerases Biochemistry 10 1971 1058 1062
79. H. Schreiber, and O. Steinhauser Cutoff size does strongly influence molecular dynamics results on solvated polypeptides Biochemistry 31 1992 5856 5860
80. G.F. Schroder, M. Levitt, and A.T. Brunger Super-resolution biomolecular crystallography with low-resolution data Nature 464 2010 1218 1222
81. M. Soler-Lopez, L. Malinina, and J.A. Subirana Solvent organization in an oligonucleotide crystal. The structure of d(GCGAATTCG)2 at atomic resolution J. Biol. Chem. 275 2000 23034 23044 (Pubitemid 30646193)
82. A.K. Soper Joint structure refinement of x-ray and neutron diffraction data on disordered materials: application to liquid water J. Phys. Condens. Matter 19 2007 335206
83. T. Steinel, J.B. Asbury, J. Zheng, and M.D. Fayer Watching Hydrogen Bonds Break:A Transient Absorption Study of Water J. Phys. Chem. A 108 2004 10957 10964 (Pubitemid 40011119)
84. D. Sticke, L. Presta, K. Dill, and G. Rose Hydrogen bonding in globular proteins J. Mol. Biol. 226 1992 1143 1159
85. M. Suekane, M. Tamura, and C. Tomimura Physicochemical and enzymatic properties of purified glucose isomerases from Streptomyces olivochromogenes and Bacillus stearothermophilus Agric. Biol. Chem. 42 1978 909 917 (Pubitemid 8365977)
86. K.N. Swamy, and E. Clement Hydration structure and dynamics of B- and Z-DNA in the presence of counterions via molecular dynamics simulations Biopolymers 26 1987 1901 1927
87. N. Valls, G. Wright, R.A. Steiner, G.N. Murshudov, and J.A. Subirana DNA variability in five crystal structures of d(CGCAATTGCG) Acta Crystallogr. D Biol. Crystallogr. 60 2004 680 685 (Pubitemid 41184818)
88. P. van Bastelaere, W. Vangrysperre, and H. Kersters-Hilderson Kinetic studies of Mg(2+)-, Co(2+)- and Mn(2+)-activated D-xylose isomerases Biochem. J. 278 1991 285 292
89. A.H. Wang, T. Hakoshima, G. van der Marel, J.H. van Boom, and A. Rich AT base pairs are less stable than GC base pairs in Z-DNA: The crystal structure of d(m5CGTAm5CG) Cell 37 1984 321 331 (Pubitemid 14079864)
90. A. Warshel, and A. Papazyan Electrostatic effects in macromolecules: fundamental concepts and practical modeling Curr. Opin. Struct. Biol. 8 1998 211 217 (Pubitemid 28221053)
91. W.I. Weis, A.T. Brünger, J.J. Skehel, and D.C. Wiley Refinement of the influenza virus hemagglutinin by simulated annealing J. Mol. Biol. 212 1990 737 761
92. R. Wing, H. Drew, T. Takano, C. Broka, S. Tanaka, K. Itakura, and R.E. Dickerson Crystal structure analysis of a complete turn of B-DNA Nature 287 1980 755 758
93. K.K. Woods, T. Maehigashi, S.B. Howerton, C.C. Sines, S. Tannenbaum, and L.D. Williams High-resolution structure of an extended A-tract: [d(CGCAAATTTGCG)]2 J. Am. Chem. Soc. 126 2004 15330 15331 (Pubitemid 39577438)
94. D.M. York, T.A. Darden, and L.G. Pedersen The effect of long-range electrostatic interactions in simulations of macromolecular crystals: a comparison of the Ewald and truncated list methods J. Chem. Phys. 99 1993 8345
95. D.M. York, W. Yang, H. Lee, T. Darden, and L.G. Pedersen Toward the accurate modeling of DNA: the importance of long-range electrostatics J. Am. Chem. Soc. 117 1995 5001 5002
96. M. Young, G. Ravishanker, and D. Beveridge A 5-nanosecond molecular dynamics trajectory for B-DNA: analysis of structure, motions, and solvation Biophys. J. 73 1997 2313 2336 (Pubitemid 27471443)
97. M.A. Young, B. Jayaram, and D.L. Beveridge Intrusion of counterions into the spine of hydration in the minor groove of B-DNA: fractional occupancy of electronegative pockets J. Am. Chem. Soc. 119 1997 59 69 (Pubitemid 27064483)