Recent results on hydrogen and hydration in biology studied by neutron macromolecular crystallography

Cellular and Molecular Life Sciences

Volumn 63, Issue 3, 2006, Pages 285-300

  Niimura, N ^a   Arai, S ^b   Kurihara, K ^b   Chatake, T ^c   Tanaka, I ^a   Bau, R ^d  

^a IBARAKI UNIVERSITY   (Japan)

^b JAPAN ATOMIC ENERGY AGENCY   (Japan)

^c CHIBA INSTITUTE OF SCIENCE   (Japan)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

H D exchange; Hydration; Hydrogen; Hydrogen bond; Neutron diffraction; Protein crystallization; Protonation and deprotonation

Indexed keywords

ALDEHYDE REDUCTASE; AMICYANIN; AMINO ACID; CAMPHOR 5 MONOOXYGENASE; CARBOXYLIC ACID; CONCANAVALIN A; DIHYDROFOLATE REDUCTASE; DNA B; DNA Z; DOUBLE STRANDED DNA; ENDOTHIAPEPSIN; GUANINE; HISTIDINE; HYDROGEN; LYSOZYME; OLIGONUCLEOTIDE; PROTOCATECHUATE 3,4 DIOXYGENASE; WATER; XYLOSE ISOMERASE;

ATOM; BIOLOGY; CORRELATION ANALYSIS; CRYSTAL; CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; DATA BASE; ENZYME ACTIVITY; FRANCE; HYDRATION; HYDROGEN BOND; JAPAN; MACROMOLECULE; MOLECULE; NEUTRON; NEUTRON DIFFRACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; REVIEW; TEMPERATURE; THERMOSTABILITY; UNITED STATES; WATER STRUCTURE; X RAY DIFFRACTION;

BIOLOGY; DEUTERIUM; DEUTERIUM EXCHANGE MEASUREMENT; HYDROGEN; NEUTRON DIFFRACTION; PROTEIN CONFORMATION; PROTEINS; WATER;

DRYOBALANOPS;

EID: 32044434962     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5418-3     Document Type: Review

References (83)

1. Petrova T. and Podjarny A. D. (2004) Protein crystallography at subatomic resolution. Rep. Prog. Phys. 67: 1565-1605
2. Blakeley M. P., Cianci M., Helliwell J. R. and Rizkallah P. J. (2004) Synchrotron and neutron techniques in biological crystallography. Chem. Soc. Rev. 33: 548-557
3. Niimura N., Karasawa Y., Tanaka I., Miyahara J., Takahashi K., Saito H. et al. (1994) An imaging plate neutron detector. Nucl. Instrum. Methods. A349: 521-525
4. Haga Y. K., Kumazawa S. and Niimura N. (1999) Gamma-ray sensitivity and shielding of a neutron imaging plate. J. Appl. Cryst. 32: 878-882
5. Haga Y. K., Neriishi K., Takahashi K. and Niimura N. (2002) Optimization of neutron imaging plate. Nucl. Instrum. Methods Phys. Research A487: 504-510
6. Niimura N., Minezaki Y., Nonaka T., Castagna J. C., Cipriani F., Hoghej P. et al. (1997) Neutron Laue diffractometry with an imaging plate provides an effective data collection regime for neutron protein crystallography. Nat. Struct. Biol. 4: 909-914
7. Helliwell J. R. and Wilkinson C. (1994) X-ray and neutron Laue diffraction. In: Neutron and Synchrotron Radiation for Condensed Matter Studies: Applications to Soft Condensed Matter and Biology, chap. 7, vol. 3, Baruchel J., Hodeau J.-L., Lehmann M., Regnard J. R. and Schlenkar C. (eds.), Springer, Berlin
8. Schoenborn B. P., Saxena A. M., Stamm M., Dimmler G. and Radeka V. (1985) A neutron spectrometer with a two-dimensional detector for time-resolved studies. Australian Journal of Physics: 38: 337-351
9. Schoenborn B. P. and Langan P. (2004) Protein crystallography with spallation neutrons. J. Synchrotron Radiat. 11: 80-82
10. Helliwell J. R. (1997) Neutron Laue diffraction does it faster. Nat. Struct. Biol. 4: 874-876
11. Raghavan N. V. and Woldawer A. (1987) Neutron crystallography of proteins. Methods Exp. Phys. Part C 23: 335-365
12. Schoenborn B. P. (1985) Experimental neutron protein crystallography. Methods Enzymol. 114: 510-529
13. Schoenborn B. P. (ed.) (1984) Neutrons in Biology, Plenum Press, New York
14. Schoenborn B. P. and Knott R. B. (eds.) (1996) Neutrons in Biology, Basic Life Sciences Series, vol. 64, Plenum Press, New York
15. Kossiakoff A. A. (1985) The application of neutron crystallography to the study of dynamic and hydration properties of proteins. Annu. Rev. Biochem. 54: 1195-1227
16. Niimura N. (1999) Neutrons expand the field of structural biology. Curr. Opin. Struct. Biol. 9: 602-608
17. Tsyba I. and Bau R. (2002) Neutron diffraction studies of proteins. Chemtracts 15: 233-257
18. Niimura N., Chatake T., Ostermann A., Kurihara K. and Tanaka I. (2003) High resolution neutron protein crystallography: hydrogen and hydration in proteins. Z. Kristallogr. 218: 96-107
19. Niimura N., Chatake T., Kurihara K. and Maeda M. (2004) Hydrogen and hydration in proteins. Cell Biochem. Biophys. 40: 351-370
20. Meilleur F., Blakeley M. and Myles D. A. A. (2005) Neutron laue analysis of hydrogen and hydration in protein structures. In: Hydrogen- and Hydration-Sensitive Structural Biology, pp. 75-86. Niimura N., Mizuno H., Helliwell J. R. and Westhof E. (eds.), KubaPro, Tokyo
21. Blakeley M., Hazemann I., Myles D. A. A. and Podjarny A. D. (2005) Protonation states in human aldose reductase observed with high-resolution X-ray crystallography and preliminary neutron diffraction results. In: Hydrogen- and Hydration-Sensitive Structural Biology, pp. 87-102, Niimura N., Mizuno H., Helliwell J. R. and Westhof E. (eds.) KubaPro, Tokyo
22. Habash J., Raftery J., Nuttall R., Price H. J., Wilkinson C., Kalb A. J. et al. (2000) Direct determination of the positions of the deuterium atoms of the bound water in concanavalin A by neutron Laue crystallography. Acta Cryst. D56: 541-550
23. Myles D. A. A., Bon C., Langan P., Cipriani F., Castagna J. C., Lehmann, M. S. et al. (1998) Neutron Laue diffraction in macromolecular crystallography. Physica B241&243: 1122-1130
24. Langan P., Greene G. and Schoenborn B. P. (2004) Protein crystallography with spallation neutrons: the User Facility at Los Alamos Neutron Science Center. J. Appl. Cryst. 37: 24-31
25. Langan P. and Greene G. (2004) Protein crystallography with spallation neutrons: collecting and processing wavelength-resolved Laue protein data. J. Appl. Cryst. 37: 253-257
26. Schoenborn B. P. and Langan P. (2004) Protein crystallography with spallation neutrons. J. Synchrotron Rad. 11: 80-82
27. Tanaka I., Kurihara K., Chatake T. and Niimura N. (2002) A high-performance neutron diffractometer for biological crystallography (BIX-3). J. Appl. Cryst. 35: 34-40
28. Kurihara K., Tanaka I., Muslih M. R., Ostermann A. and Niimura N. (2004) A new neutron single-crystal diffractometer dedicated for biological macromolecules (BIX-4). J. Synchrotron Radiat. 11: 68-71
29. Schultz A. J. (1993) Single-crystal time-of-flight neutron diffraction. Trans. Amer. Cryst. Assoc. 29: 29-41
30. Wilson C. C. (1995) A guided tour of ISIS, the UK Spallation Source. Neutron News 23: 313-316
31. Keen, D. A. and Wilson, C. C. (1996) Single Crystal Diffraction at ISIS, User guide for the SXD Instrument, Rutherford Lab Technical Report RAL-TR-96-083
32. Kurihara K., Tanaka I., Chatake T., Adams M. W., Jenney F. E. Jr., Moiseeva N. et al. (2004) Neutron crystallographic study on rubredoxin from Pyrocuccus furiosus by BIX-3, a single-crystal diffractometer for biomacromolecules. Proc. Natl. Acad. Sci. USA 101: 11215-11220
33. Chatake T., Kurihara K., Tanaka I., Tsyba I., Bau R., Jenney F. E. et al. (2004) A neutron crystallographic analysis of a rubredoxin mutant at 1.6 Å resolution. Acta Cryst. D60: 1364-1373
34. Li, X., Langan, P., Bau, R., Tsyba, I., Jenny, F. E. Adams, M. W. W. and Schoenborn, B. P. (2004). A preliminary time-of-flight neutron diffraction study of the W3Y single mutant of Rubredoxin from pyrococcus furiosus. Acta Cryst. D60: 200-202
35. Arai S., Chatake T., Minezaki Y. and Niimura N. (2002) Crystallization of a large single crystal of a B-DNA decamer for a neutron diffraction experiment by the phase-diagram technique. Acta Cryst. D58: 151-153
36. Chatake T., Mizuno N., Voordouw G., Higuchi Y., Arai S., Tanaka I. et al. (2003) Crystallization and preliminary neutron analysis of the dissimilatory sulfite reductase D (DsrD) protein from the sulfate-reducing bacterium Desulfovibrio vulgaris. Acta Cryst. D59: 2306-2309
37. Maeda M., Chatake T., Tanaka I., Ostermann A. and Niimura N. (2004) Crystallization of a large single crystal of cubic insulin for neutron protein crystallography. J. Synchrotron Radiat. 11: 41-44
38. Arai S., Chatake T., Suzuki N., Mizuno H. and Niimura N. (2004) More rapid evaluation of biomacromolecular crystals for diffraction experiments. Acta Cryst. D60: 1032-1039
39. Gamble T. R., Clauser K. R. and Kossiakoff A. A.(1994) The production and X-ray structure determination of perdeuterated Staphylococcal nuclease. Biophys. Chem. 53: 15-25
40. Shu F., Ramakrishnan V. and Schoenborn B. P. (2000) Enhanced visibility of hydrogen atoms by neutron crystallography on fully deuterated myoglobin. Proc. Natl. Acad. Sci. USA 97: 3872-3879
41. Langan P., Bennet B., Dealwis C., Stone D. Li X., Schoenborn B. P. et al. (2004) LANSCE Activity Report, Los Alamos National Laboratory, Los Alamos, New Mexico, USA, March 22
42. Myles D. A. A. (2004) Abstracts of the Amer. Cryst. Assoc. Meeting, Chicago, July
43. Garman E. (1999) Cool data: quantity and quality. Acta Cryst. D55: 1641-1653
44. 43a Hanson B. L. (2004) Getting protein solvent structures down cold: Proc. Natl. Acad. Sci. USA 101: 16393-16394
45. Bon C., Lehmann M. S. and Wilkinson C. (1999) Quasi-Laue neutron-diffraction study of the water arrangement in crystals of triclinic hen egg-white lysozyme. Acta Cryst. D55: 978-987
46. Blakeley M. P., Kalb A. J., Helliwell J. R. and Myles D. A. A. (2004) The 15-K neutron structure of saccharide-free concanavalin A. Proc. Natl. Acad. Sci. USA 101: 16405-16410
47. Ostermann A., Tanaka I., Engler N., Niimura N. and Parak F. G. (2002) Hydrogen and deuterium in myoglobin as seen by a neutron structure determination at 1.5 Å resolution. Biohpys. Chem. 95: 183-193
48. Maeda M., Fujiwara S., Yonezawa Y. and Niiimura N. (2001) Neutron structure analysis of hen egg-white lysozyme at pH4.9. J. Phys. Soc. Jpn. Suppl. A, 70: 403-405
49. 2 observed by neutron diffraction measurements. Nucleic Acids Res. 33: 3017-3024
50. Chatake T., Tanaka I., Umino H., Arai S. and Niimura N. (2005) Neutron crystallographic analysis of the Z-DNA hexamer CGCGCG. Acta Cryst. D61: 1088-1098
51. Baker E. N. and Hubbard R. E. (1984) Hydrogen bonding in globular proteins. Prog. Biophys. Molec. Biol. 44: 97-179
52. Preissner R., Egner U. and Saenger W. (1991) Occurrence of bifurcated three-center hydrogen bonds in proteins. FEBS Lett. 288: 192-196
53. Hiller R., Zhou Z. H., Adams M. W. W. and Englander S. W. (1997) Stability and dynamics in a hyperthermophilic protein with melting temperature close to 200°C. Proc. Natl. Acad. Sci. USA 94: 11329-11332
54. Hernandez G., Jenney F. E. Jr., Adams M. W. W. and LeMaster D. M. (2000) Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature. Proc. Natl. Acad. Sci. USA 97: 3166-3170
55. Matsuo H., Oe M., Sakiyama F. and Narita K. (1972) A new approach to the determination of pKa's of histidine residues in proteins. J. Biochem. 72: 1057-1060
56. Brandes R. and Ehrenberg A. (1986) Kinetics of the proton-deuteron exchange at position H8 of adenine and guanine in DNA. Nucleic Acids Res. 14: 9491-9508
57. Gursky O., Li Y., Badger J.and Casper D. L. D. (1992) Monovalent cation binding to cubic insulin crystals. Biophys. J. 61: 604-611
58. Phillips D. C. (1966) The three-dimensional structure of an enzyme molecule. Sci. Am. 215: 75-80
59. Mason S. A., Bentley G. A. and McIntyre G. J. (1984) Deuterium exchange in lysozyme at 1.4 Å resolution. In: Neutrons in Biology, pp. 323-334, Schoenborn B. P. (ed.), Plenum Press, New York
60. Cooper J. B. and Myles D. A. A. (2000) A preliminary neutron Laue diffraction study of the aspartic proteinase endothiapepsin. Acta Cryst. D56: 246-248
61. Coates L., Erskine P. T., Wood S. P., Myles D. A. A. and Cooper J. B. (2001) A neutron Laue diffraction study of endothiapepsin: implications for the aspartic proteinase mechanism. Biochemistry 40: 13149-13157
62. Hanson B. L., Langan P., Katz A. K., Li X. M., Harp J. M., Glusker J. P. et al. (2004) A preliminary time-of-flight neutron diffraction study of Streptomyces rubiginosus D-xylose isomerase. Acta Cryst. D60: 241-249
63. Fenn T. D., Ringe D. and Petsko G. A. (2004) Xylose isomerase in substrate and inhibitor michaelis states: atomic resolution studies of a metal-mediated hydride shift. Biochemistry 43: 6464-6474
64. Howard E. I., Sanishvili R., Cachau R. E., Mitschler A., Chevrier B., Barth P. et al. (2004) Ultrahigh resolution drug design: details of interactions in human aldose reductase-inhibitor complex at 0.66 Å. Proteins 55: 792-804
65. Meilleur F. (2004) Thesis, University J. Fourier, Grenoble
66. Sukumar N., Langan P., Mathews F. S., Jones L. H., Thiyagarajan P., Schoenborn B. P. et al. (2005) A preliminary time-of-flight neutron diffraction study on amicyanin from Paracoccus denurificans. Acta Cryst. D: 61 (Pt 5): 640-642
67. Zhu Z., Cunane L. M., Chen Z., Durley R. C., Mathews F. S. and Davidson V. L. (1998) Molecular basis for interprotein complex-dependent effects on the redox properties of amicyanin. Biochemistry 37: 17128-17136
68. Elgren T. E., Orville A. M., Kelly K. A., Lipscomb J. D., Ohlendorf D. H. and Que L. Jr. (1997) Crystal structure and resonance Raman studies of protocatechuate 3,4-dioxygenase complexed with 3,4-dihydroxyphenylacetate. Biochemistry 36: 11504-11513
69. Brown C. K., Langan P., Scoenborn B. P., Earhart C. A. and Ohlendorf D. H. (2004) Abstracts of the Amer. Cryst. Assoc. Meeting, Chicago, July
70. Daniels B. V., Myles D. A. A., Forsyth V. T. and Lawson C. L. (2003) Crystals of trp repressor suitable for high-resolution neutron Laue diffraction studies. Acta Cryst. D59: 136-138
71. Chatake T., Ostermann A., Kurihara K., Parak F. G. and Niimura N. (2003) Hydration in proteins observed by high-resolution neutron crystallography. Proteins 50: 516-523
72. Wing W., Drew H., Takano T., Broka C., Tanaka S., Itakura K. et al. (1980) Crystal structure analysis of a complete turn of B-DNA. Nature 287: 755-758
73. Tereshko V., Minasov G. and Egli M. (1999) The Dickerson-Drew B-DNA dodecamer revisited at atomic resolution. J. Am. Chem. Soc. 122: 470-471
74. Minasov G., Tereshko V. and Egli M. (1999) Atomic-resolution crystal structures of B-DNA reveal specific influences of divalent metal ions on conformation and packing. J. Mol. Biol. 291: 83-99
75. Goodsell D. S., Kaczor-Grzeskowiak M. and Dickerson R. E. (1994) The crystal structure of C-C-A-T-T-A-A-T-G-G. Implications for bending of B-DNA at T-A steps. J. Mol. Biol. 239: 79-96
76. Rich A. and Zhang S. (2003) Timeline: Z-DNA: the long road to biological function. Nat. Rev. Genet. 4: 566-572
77. Wang A. H., Quigley G. J., Kolpak F. J., Crawford J. L., van Boom J. H., van der Marel G. et al. (1979) Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282: 680-686
78. Bancroft D., Willians L. D., Rich A. and Egli M. (1994) 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: 1073-1086
79. Egli M., Williams L. D., Gao Q. and Rich A. (1991) Structure of the pure-spermine form of Z-DNA (magnesium free) at 1 Å resolution. Biochemistry 30: 11388-11402
80. Gessner R. V., Quigley G. J. and Egli M. (1994) Comparative studies of high resolution Z-DNA crystal structures. Part 1: Common hydration patterns of alternating dC-dG. J. Mol. Biol. 236: 1154-1168
81. Habash J., Raftery J., Weisgerber S., Cassetta A., Lehmann M. S., Hoghoj P. et al. (1997) Neutron Laue diffraction study of concanavalin A: the proton of Asp-28. J. Chem. Soc. Faraday Trans. 93: 4313-4319
82. Kalb (Gilboa) A. J., Myles D. A. A., Habash J., Raftery J. and Helliwell J. R. (2001) Neutron Laue diffraction experiments on a large unit cell: concanavalin A complexed with methyl-α-D-glucopyranoside. J. Appl. Cryst. 34: 454-457
83. Ahmed H., Blakerly M., Habash J. and Helliwell J. R. (2005) Atomic detail structural studies on concanavalin A and extending the large molecular weight frontier of neutron protein crystallography to virus crystals. In: Hydrogen- and Hydration-Sensitive Structural Biology, pp. 63-74, Niimura N., Mizuno H., Helliwell J. R. and Westhof E. (eds.), KubaPro, Tokyo