Kinetic protein crystallography: A tool to watch proteins in action

Crystallography Reviews

Volumn 15, Issue 2, 2009, Pages 87-118

  Bourgeois, D ^a,b   Weik, M ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

Caged compounds; Enzyme mechanism; Intermediate states; Kinetic crystallography; Light sensitive proteins; Microspectrophotometry; Protein dynamics; Time resolved crystallography; Trapping methods

Indexed keywords

CAGED COMPOUNDS; ENZYME MECHANISM; INTERMEDIATE STATES; KINETIC CRYSTALLOGRAPHY; MICROSPECTROPHOTOMETRY; PROTEIN DYNAMICS; TIME-RESOLVED CRYSTALLOGRAPHY; TRAPPING METHODS;

BIOLOGICAL SYSTEMS; CRYSTALLINE MATERIALS; DIFFRACTION; ENZYMES; LIGHT; MINERALOGY; OXYGEN; PHOTOSENSITIVITY; RAMAN SPECTROSCOPY;

X RAY CRYSTALLOGRAPHY;

EID: 70349327495     PISSN: 0889311X     EISSN: 14763508     Source Type: Journal    
DOI: 10.1080/08893110802604868     Document Type: Article

References (146)

1. Henzler-Wildman, K.; Kern, D. Dynamic Personalities of Proteins. Nature 2007, 450, 964-972
2. Cruickshank, D.W.J.; Helliwell, J.R.; Johnson, L.N. Time-resolved Macromolecular Crystallography; The Royal Society and Oxford University Press: New York, USA, 1992.
3. Ren, Z.; Bourgeois, D.; Helliwell, J.R.; Moffat, K.; Srajer, V.; Stoddard, B.L. Laue Crystallography: Coming of Age. J. Synch. Rad. 1999, 6, 891-917.
4. Moffat, K. Time-resolved Biochemical Crystallography: A Mechanistic Perspective. Chem. Rev. 2001, 101, 1569-1581.
5. Schlichting, I. Crystallographic Structure Determination of Unstable Species. Acc. Chem. Res. 2000, 33, 532-538.
6. Schlichting, I.; Chu, K. Trapping Intermediates in the Crystal: Ligand Binding to Myoglobin. Curr. Opin. Struct. Biol. 2000, 10, 744-752.
7. Stoddard, B.L. Trapping Reaction Intermediates in Macromolecular Crystals for Structural Analyses. Methods. 2001, 24, 125-138.
8. Bourgeois, D.; Royant, A. Advances in Kinetic Protein Crystallography. Curr. Opin. Struct. Biol. 2005, 15, 538-547.
9. Hajdu, J.; Neutze, R.; Sjogren, T.; Edman, K.; Szoke, A.; Wilmouth, R.C.; Wilmot, C.M. Analyzing Protein Functions in Four Dimensions. Nat. Struct. Biol. 2000, 7, 1006-1012.
10. Wilmot, C.M.; Pearson, A.R. Cryocrystallography of Metalloprotein Reaction Intermediates. Curr. Opin. Chem. Biol. 2002, 6, 202-207.
11. Petsko, G.A.; Ringe, D. Observation of Unstable Species in Enzyme-catalyzed Transformations using Protein Crystallography. Curr. Opin. Chem. Biol. 2000, 4, 89-94.
12. Frauenfelder, H.; Sligar, S.G.; Wolynes, P.G. The Energy Landscapes and Motions of Proteins. Science 1991, 254, 1598-1603.
13. Rasmussen, B.F.; Stock, A.M.; Ringe, D.; Petsko, G.A. Crystalline Ribonuclease A Loses Function below the Dynamical Transition at 220 K. Nature 1992, 357, 423-424.
14. Tilton, R.F. Jr.; Dewan, J.C.; Petsko, G.A. Effects of Temperature on Protein Structure and Dynamics: X-Ray Crystallographic Studies of the Protein Ribonuclease-A at Nine Different Temperatures from 98 to 320 K. Biochemistry. 1992, 31, 2469-2481.
15. Ansari, A.; Berendzen, J.; Bowne, S.F.; Frauenfelder, H.; Iben, I.E.; Sauke, T.B.; Shyamsunder, E.; Young, R.D. Protein States and Proteinquakes. Proc. Natl. Acad. Sci. U. S. A. 1985, 82, 5000-5004.
16. Henzler-Wildman, K.A.; Thai, V.; Lei, M.; Ott, M.; Wolf-Watz, M.; Fenn, T.; Pozharski, E.; Wilson, M.A.; Petsko, G.A.; Karplus, M.; Hubler, C.; Kem, D. Intrinsic Motions along an Enzymatic Reaction Trajectory. Nature 2007, 450, 838-844.
17. Eisenmesser, E.Z.; Millet, O.; Labeikovsky, W.; Korzhnev, D.M.; Wolf-Watz, M.; Bosco, D.A.; Skalicky, J.J.; Kay, L.E.; Kern, D. Intrinsic Dynamics of an Enzyme Underlies Catalysis. Nature 2005, 438, 117-121. (Pubitemid 41599831)
18. Tobi, D.; Bahar, I. Structural Changes Involved in Protein Binding Correlate with Intrinsic Motions of Proteins in the Unbound State. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 18908-18913.
19. Lange, O.F.; Lakomek, N.A.; Fares, C.; Schroder, G.F.; Walter, K.F.; Becker, S.; Meiler, J.; Grubmuller, H.; Griesinger, C.; De Groot, B.L. Recognition Dynamics up to Microseconds Revealed from an RDC-Derived Ubiquitin Ensemble in Solution. Science 2008, 320, 1471-1475.
20. Sullivan, S.M.; Holyoak, T. Enzymes with Lid-Gated Active Sites Must Operate By an Induced Fit Mechanism instead of Conformational Selection. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 13829-13834.
21. Dai, S.; Friemann, R.; Glauser, D.A.; Bourquin, F.; Manieri, W.; Schurmann, P.; Eklund, H. Structural Snapshots along the Reaction Pathway of Ferredoxin-Thioredoxin Reductase. Nature 2007, 448, 92-96.
22. Ramakrishnan, B.; Ramasamy, V.; Qasba, P.K. Structural Snapshots of Beta-1, 4-Galactosyltransferase-I along the Kinetic Pathway. J. Mol. Biol. 2006, 357, 1619-1633.
23. Zhu, X.; Dickerson, T.J.; Rogers, C.J.; Kaufmann, G.F.; Mee, J.M.; McKenzie, K.M.; Janda, K.D.; Wilson, I.A. Complete Reaction Cycle of a Cocaine Catalytic Antibody at Atomic Resolution. Structure. 2006, 14, 205-216.
24. Parker, J.B.; Bianchet, M.A.; Krosky, D.J.; Friedman, J.I.; Amzel, L.M.; Stivers, J.T. Enzymatic Capture of an Extrahelical Thymine in the Search for Uracil in DNA. Nature 2007, 449, 433-437.
25. Oldham, M.L.; Khare, D.; Quiocho, F.A.; Davidson, A.L.; Chen, J. Crystal Structure of a Catalytic Intermediate of the Maltose Transporter. Nature 2007, 450, 515-521.
26. Olesen, C.; Picard, M.; Winther, A.M.; Gyrup, C.; Morth, J.P.; Oxvig, C.; Moller, J.V.; Nissen, P. The Structural Basis of Calcium Transport by the Calcium Pump. Nature 2007, 450, 1036-1042.
27. Numata, T.; Ikeuchi, Y.; Fukai, S.; Suzuki, T.; Nureki, O. Snapshots of tRNA Sulphuration Via an Adenylated Intermediate. Nature 2006, 442, 419-424.
28. Mozzarelli, A.; Rossi, G.L. Protein Function in the Crystal. Annu. Rev. Biophys. Biomol. Struct. 1996, 25, 343-365.
29. Efremov, R.; Gordeliy, V.I.; Heberle, J.; Buldt, G. Time-resolved Microspectroscopy on a Single Crystal of Bacteriorhodopsin Reveals Lattice-Induced Differences in the Photocycle Kinetics. Biophys. J. 2006, 91, 1441-1451.
30. Yeremenko, S.; van Stokkum, I.H.; Moffat, K.; Hellingwerf, K.J. Influence of the Crystalline State on Photoinduced Dynamics of Photoactive Yellow Protein Studied by Ultraviolet-Visible Transient Absorption Spectroscopy. Biophys. J. 2006, 90, 4224-4235.
31. Katona, G.; Carpentier, P.; Niviere, V.; Amara, P.; Adam, V.; Ohana, J.; Tsanov, N.; Bourgeois, D. Raman-assisted Crystallography Reveals End-on Peroxide Intermediates in a Nonheme Iron Enzyme. Science 2007, 316, 449-453.
32. Kovaleva, E.G.; Lipscomb, J.D. Crystal Structures of Fe2+ Dioxygenase Superoxo, Alkylperoxo, and Bound Product Intermediates. Science 2007, 316, 453-457.
33. Wang, Y.; Guo, H.C. Crystallographic Snapshot of a Productive Glycosylasparaginase- Substrate Complex. J. Mol. Biol. 2007, 366, 82-92.
34. Wang, J.; Kantrowitz, E.R. Trapping the Tetrahedral Intermediate in the Alkaline Phosphatase Reaction by Substitution of the Active Site Serine with Threonine. Protein Sci. 2006, 15, 2395-2401.
35. Berthold, C.L.; Toyota, C.G.; Moussatche, P.; Wood, M.D.; Leeper, F.; Richards, N.G.; Lindqvist, Y. Crystallographic Snapshots of Oxalyl-Coa Decarboxylase Give Insights into Catalysis by Nonoxidative Thdp-Dependent Decarboxylases. Structure. 2007, 15, 853-861.
36. Hartmann, M.D.; Bourenkov, G.P.; Oberschall, A.; Strizhov, N.; Bartunik, H.D. Mechanism of Phosphoryl Transfer Catalyzed by Shikimate Kinase from Mycobacterium Tuberculosis. J. Mol. Biol. 2006, 364, 411-423.
37. Roujeinikova, A.; Hothi, P.; Masgrau, L.; Sutcliffe, M.J.; Scrutton, N.S.; Leys, D. New Insights into the Reductive Half-Reaction Mechanism of Aromatic Amine Dehydrogenase Revealed by Reaction with Carbinolamine Substrates. J. Biol. Chem. 2007, 282, 23766-23777.
38. Masgrau, L.; Roujeinikova, A.; Johannissen, L.O.; Hothi, P.; Basran, J.; Ranaghan, K.E.; Mulholland, A.J.; Sutcliffe, M.J.; Scrutton, N.S.; Leys, D. Atomic Description of an Enzyme Reaction Dominated by Proton Tunneling. Science 2006, 312, 237-241.
39. Kuhnel, K.; Derat, E.; Terner, J.; Shaik, S.; Schlichting, I. Structure and Quantum Chemical Characterization of Chloroperoxidase Compound 0, A Common Reaction Intermediate of Diverse Heme Enzymes. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 99-104.
40. Moniot, S.; Bruno, S.; Vonrhein, C.; Didierjean, C.; Boschi-Muller, S.; Vas, M.; Bricogne, G.; Branlant, G.; Mozzarelli, A.; Corbier, C. Trapping of the Thioacylglyceraldehyde-3-Phosphate Dehydrogenase Intermediate from Bacillus stearothermophilus. Direct Evidence for a Flip-Flop Mechanism. J. Biol. Chem. 2008, 283, 21693-21702.
41. Padayatti, P.S.; Sheri, A.; Totir, M.A.; Helfand, M.S.; Carey, M.P.; Anderson, V.E.; Carey, P.R.; Bethel, C.R.; Bonomo, R.A.; Buynak, J.D.; Van Der Akker, F. Rational Design of a Beta-Lactamase Inhibitor Achieved Via Stabilization of the Trans-Enamine Intermediate: 1.28 Angstrom Crystal Structure of Wt SHV-1 Complex with a Penam Sulfone. J. Am. Chem. Soc. 2006, 128, 13235-13242.
42. Roujeinikova, A.; Scrutton, N.S.; Leys, D. Atomic Level Insight into the Oxidative Half- Reaction of Aromatic Amine Dehydrogenase. J. Biol. Chem. 2006, 281, 40264-40272.
43. Totir, M.A.; Padayatti, P.S.; Helfand, M.S.; Carey, M.P.; Bonomo, R.A.; Carey, P.R.; Van Den Akker, F. Effect of the inhibitor-Resistant M69V Substitution on the Structures and Populations of Trans-Enamine Beta-Lactamase Intermediates. Biochemistry. 2006, 45, 11895-11904.
44. Cavazza, C.; Contreras-Martel, C.; Pieulle, L.; Chabriere, E.; Hatchikian, E.C.; Fontecilla- Camps, J.C. Flexibility of Thiamine Diphosphate Revealed by Kinetic Crystallographic Studies of the Reaction of Pyruvate-Ferredoxin Oxidoreductase with Pyruvate. Structure. 2006, 14, 217-224.
45. Colletier, J.P.; Fournier, D.; Greenblatt, H.M.; Stojan, J.; Sussman, J.L.; Zaccai, G.; Silman, I.; Weik, M. Structural Insights into Substrate Traffic and Inhibition in Acetylcholinesterase. Embo. J. 2006, 25, 2746-2756, Epub 2006 Jun 8.
46. Jung, A.; Reinstein, J.; Domratcheva, T.; Shoeman, R.L.; Schlichting, I. Crystal Structures of the Appa BLUF Domain Photoreceptor Provide Insights into Blue Light-Mediated Signal Transduction. J. Mol. Biol. 2006, 362, 717-732.
47. Moglich, A.; Moffat, K. Structural Basis for Light-Dependent Signaling in the Dimeric LOV Domain of the Photosensor YtvA. J. Mol. Biol. 2007, 373, 112-126.
48. Halavaty, A.S.; Moffat, K. N- and C-terminal Flanking Regions Modulate Light-Induced Signal Transduction in the LOV2 Domain of the Blue Light Sensor Phototropin 1 from Avena Sativa. Biochemistry. 2007, 46, 14001-14009.
49. Bourgeois, D.; Vallone, B.; Arcovito, A.; Sciara, G.; Schotte, F.; Anfinrud, P.A.; Brunori, M. Extended Subnanosecond Structural Dynamics of Myoglobin Revealed by Laue Crystallography. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 4924-4929.
50. Ihee, H.; Rajagopal, S.; Srajer, V.; Pahl, R.; Anderson, S.; Schmidt, M.; Schotte, F.; Anfinrud, P.A.; Wulff, M.; Moffat, K. Visualizing Reaction Pathways in Photoactive Yellow Protein from Nanoseconds to Seconds. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 7145-7150.
51. Baxter, R.H.; Ponomarenko, N.; Srajer, V.; Pahl, R.; Moffat, K.; Norris, J.R. Time-resolved Crystallographic Studies of Light-induced Structural Changes in the Photosynthetic Reaction Center. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 5982-5987. (Pubitemid 38520514)
52. Moukhametzianov, R.; Klare, J.P.; Efremov, R.; Baeken, C.; Goppner, A.; Labahn, J.; Engelhard, M.; Buldt, G.; Gordeliy, V.I. Development of the Signal in Sensory Rhodopsin and its Transfer to the Cognate Transducer. Nature 2006, 440, 115-119.
53. Van Thor, J.J.; Georgiev, G.Y.; Towrie, M.; Sage, J.T. Ultrafast and Low Barrier Motions in the Photoreactions of the Green Fluorescent Protein. J. Biol. Chem. 2005, 280, 33652-33659.
54. Nakamichi, H.; Okada, T. Local Peptide Movement in the Photoreaction Intermediate of Rhodopsin. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 12729-12734.
55. Klink, B.U.; Goody, R.S.; Scheidig, A.J. A Newly Designed Microspectrofluorometer for Kinetic Studies on Protein Crystals in Combination with X-Ray Diffraction. Biophys. J. 2006, 91, 981-992.
56. Ursby, T.; Weik, M.; Fioravanti, E.; Delarue, M.; Goeldner, M.; Bourgeois, D. Cryophotolysis of Caged Compounds: a Technique for Trapping Intermediate States in Protein Crystals. Acta Crystallogr. D Biol. Crystallogr. 2002, 58, 607-614.
57. Bourgeois, D.; Weik, M. In Dynamic Studies in Biology; Goeldner, M., Givens, R., Eds.; Wileyvch: Weinham, 2005; pp. 410-434.
58. Colletier, J.-P.; Royant, A.; Specht, A.; Sanson, B.; Nachon, F.; Masson, P.; Zaccai, G.; Sussman, J.L.; Goeldner, M.; Silman, I.; Bourgeois, D.; Weik, M. Use of a 'caged' Analogue to Study the Traffic of Choline within Acetylcholinesterase by Kinetic Crystallography. Acta Crystallogr. D 2007, 63, 1115-1128.
59. Cherepanov, A.V.; Doroshenko, E.V.; Matysik, J.; De Vries, S.; De Groot, H.J. The Associative Nature of Adenylyl Transfer Catalyzed by T4 DNA Ligase. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 8563-8568.
60. Strickland, D.; Moffat, K.; Sosnick, T.R. Light-activated DNA Binding in a Designed Allosteric Protein. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 10709-10714.
61. Brunori, M.; Bourgeois, D.; Vallone, B. Structural Dynamics of Myoglobin. Method Enzymol. 2008, 437, 397-416.
62. Schotte, F.; Soman, J.; Olson, J.S.; Wulff, M.; Anfinrud, P.A. Picosecond Time-Resolved X-Ray Crystallography: Probing Protein Function in Real Time. J. Struct. Biol. 2004, 147, 235-246. (Pubitemid 39144389)
63. Colletier, J.P.; Bourgeois, D.; Sanson, B.; Fournier, D.; Sussman, J.L.; Silman, I.; Weik, M. Shoot-and-Trap: Use of Specific X-Ray Damage to Study Structural Protein Dynamics by Temperature-Controlled Cryo-Crystallography. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 11742-11747, Epub 2008 Aug 13.
64. Schlichting, I.; Berendzen, J.; Chu, K.; Stock, A.M.; Maves, S.A.; Benson, D.E.; Sweet, R.M.; Ringe, D.; Petsko, G.A.; Sligar, S.G. The Catalytic Pathway of Cytochrome P450cam at Atomic Resolution. Science 2000, 287, 1615-1622.
65. Berglund, G.I.; Carlsson, G.H.; Smith, A.T.; Szoke, H.; Henriksen, A.; Hajdu, J. The Catalytic Pathway of Horseradish Peroxidase at High Resolution. Nature 2002, 417, 463-468.
66. Adam, V.; Royant, A.; Niviere, V.; Molina-Heredia, F.P.; Bourgeois, D. Structure of Superoxide Reductase Bound to Ferrocyanide and Active Site Expansion upon X-Ray- Induced Photo-reduction. Structure (Camb). 2004, 12, 1729-1740.
67. Yano, J.; Kern, J.; Irrgang, K.D.; Latimer, M.J.; Bergmann, U.; Glatzel, P.; Pushkar, Y.; Biesiadka, J.; Loll, B.; Sauer, K.; Messinger, J.; Zouni, A.; Yachandra, V.K. X-ray Damage to the Mn4Ca Complex in Single Crystals of Photosystem II: A Case Study for Metalloprotein Crystallography. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 12047-12052.
68. Beitlich, T.; Kuhnel, K.; Schulze-Briese, C.; Shoeman, R.L.; Schlichting, I. Cryoradiolytic Reduction of Crystalline Heme Proteins: Analysis by UV-Vis Spectroscopy and X-Ray Crystallography. J. Synchrotron. Radiat. 2007, 14, 11-23.
69. Hough, M.A.; Antonyuk, S.V.; Strange, R.W.; Eady, R.R.; Hasnain, S.S. Crystallography with online Optical and X-Ray Absorption Spectroscopies Demonstrates an Ordered Mechanism in Copper Nitrite Reductase. J. Mol. Biol. 2008, 378, 353-361.
70. Pearson, A.R.; Pahl, R.; Kovaleva, E.G.; Davidson, V.L.; Wilmot, C.M. Tracking X-ray-derived Redox Changes in Crystals of a Methylamine Dehydrogenase/Amicyanin Complex using Single-Crystal UV/Vis Microspectrophotometry. J. Synchrotron. Radiat. 2007, 14, 92-98.
71. Echalier, A.; Goodhew, C.F.; Pettigrew, G.W.; Fulop, V. Activation and Catalysis of the Di-Heme Cytochrome C Peroxidase from Paracoccus Pantotrophus. Structure. 2006, 14, 107-117.
72. Dubnovitsky, A.P.; Ravelli, R.B.; Popov, A.N.; Papageorgiou, A.C. Strain Relief at the Active Site of Phosphoserine Aminotransferase Induced by Radiation Damage. Protein Sci. 2005, 14, 1498-1507.
73. Weik, M.; Ravelli, R.B.; Silman, I.; Sussman, J.L.; Gros, P.; Kroon, J. Specific Protein Dynamics near the Solvent Glass Transition Assayed by Radiation-induced Structural Changes. Protein Sci. 2001, 10, 1953-19561.
74. Mees, A.; Klar, T.; Gnau, P.; Hennecke, U.; Eker, A.P.; Carell, T.; Essen, L.O. Crystal Structure of a Photolyase Bound to a CPD-Like DNA Lesion after In Situ Repair. Science 2004, 306, 1789-1793.
75. Murray, J.W.; Rudino-Pinera, E.; Owen, R.L.; Grininger, M.; Ravelli, R.B.; Garman, E.F. Parameters Affecting the X-Ray Dose Absorbed by Macromolecular Crystals. J. Synchrotron. Radiat. 2005, 12, 268-275.
76. Bourgeois, D.; Vallone, B.; Schotte, F.; Arcovito, A.; Miele, A.E.; Sciara, G.; Wulff, M.; Anfinrud, P.; Brunori, M. Complex Landscape of Protein Structural Dynamics Unveiled by Nanosecond Laue Crystallography. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 8704-8709.
77. Schmidt, M.; Krasselt, A.; Reuter, W. Local Protein Flexibility as a Prerequisite for Reversible Chromophore Isomerization in Alpha- Phycoerythrocyanin. Biochim. Biophys. Acta. 2006, 1764, 55-62.
78. Schmidt, M.; Nienhaus, K.; Pahl, R.; Krasselt, A.; Anderson, S.; Parak, F.; Nienhaus, G.U.; Srajer, V. Ligand Migration Pathway and Protein Dynamics in Myoglobin: a Time-Resolved Crystallographic Study on L29W MbCO. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 11704-11709.
79. Key, J.; Srajer, V.; Pahl, R.; Moffat, K. Time-resolved Crystallographic Studies of the Heme Domain of the Oxygen Sensor Fixl: Structural Dynamics of Ligand Rebinding and their Relation to Signal Transduction. Biochemistry. 2007, 46, 4706-4715.
80. Knapp, J.E.; Pahl, R.; Srajer, V.; Royer, W.E., Jr. Allosteric Action in Real Time: Time- Resolved Crystallographic Studies of a Cooperative Dimeric Hemoglobin. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 7649-7654.
81. Teng, T.; Moffat, K. Cooling Rates during Flash Cooling. J. Appl. Cryst. 1998, 31, 252-257.
82. Walker, L.J.; Moreno, P.O.; Hope, H. Cryocrystallography: Effect of Cooling Medium on Sample Cooling Rate. J. Appl. Cryst. 1998, 31, 954-956.
83. Halle, B. Biomolecular Cryocrystallography: Structural Changes during Flash-Cooling. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 4793-4798.
84. Fenimore, P.W.; Frauenfelder, H.; McMahon, B.H.; Parak, F.G. Slaving: Solvent Fluctuations Dominate Protein Dynamics and Functions. Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 16047-16051.
85. Fenimore, P.W.; Frauenfelder, H.; McMahon, B.H.; Young, R.D. Bulk-solvent and Hydration- Shell Fluctuations, Similar to Alpha- and Beta-Fluctuations in Glasses, Control Protein Motions and Functions. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 14408-14413.
86. Angell, C.A. Formation of Glasses from Liquids and Biopolymers. Science (Washington, DC). 1995, 267, 1924-1935.
87. Ostermann, A.; Waschipky, R.; Parak, F.G.; Nienhaus, G.U. Ligand Binding and Conformational Motions in Myoglobin. Nature 2000, 404, 205-208.
88. Genick, U.K.; Soltis, S.M.; Kuhn, P.; Canestrelli, I.L.; Getzoff, E.D. Structure at 0.85A Resolution of an Early Protein Photocycle Intermediate. Nature 1998, 392, 206-209.
89. Anderson, S.; Srajer, V.; Moffat, K. Structural Heterogeneity of Cryotrapped Intermediates in the Bacterial Blue Light Photoreceptor, Photoactive Yellow Protein. Photochem. Photobiol. 2004, 80, 7-14.
90. Schmidt, M.; Rajagopal, S.; Ren, Z.; Moffat, K. Application of Singular Value Decomposition to the Analysis of Time-resolved Macromolecular X-ray Data. Biophys. J. 2003, 84, 2112-2129.
91. Rajagopal, S.; Schmidt, M.; Anderson, S.; Ihee, H.; Moffat, K. Analysis of Experimental Time-Resolved Crystallographic Data by Singular Value Decomposition. Acta Crystallogr. D Biol. Crystallogr. 2004, 60, 860-871.
92. Barstow, B.; Ando, N.; Kim, C.U.; Gruner, S.M. Alteration of Citrine Structure by Hydrostatic Pressure Explains the Accompanying Spectral Shift. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 13362-13366.
93. Coureux, P.D.; Fan, Z.P.; Stojanoff, V.; Genick, U.K. Picometer-scale Conformational Heterogeneity Separates Functional from Nonfunctional States of a Photoreceptor Protein. Structure. 2008, 16, 863-872.
94. De La Mora-Rey, T.; Wilmot, C.M. Synergy within Structural Biology of Single Crystal Optical Spectroscopy and X-Ray Crystallography. Curr. Opin. Struct. Biol. 2007, 17, 580-586.
95. Hadfield, A.; Hajdu, J. A Fast and Portable Microspectrophotometer for Protein Crystallography. J. Appl. Cryst. 1993, 26, 839-842.
96. Royant, A.; Carpentier, P.; Ohana, J.; McGeehan, J.; Paetzold, B.; Noirclerc-Savoye, M.; Vernede, X.; Adam, V.; Bourgeois, D. Advances in Spectroscopic Methods for Biological Crystals. Part 1. Fluorescence Lifetime Measurements. J. Appl. Cryst. 2007, 40, 1105-1112. (Pubitemid 350100308)
97. Carpentier, P.; Royant, A.; Ohana, J.; Bourgeois, D. Advances in Spectroscopic Methods for Biological Crystals. Part 2. Raman Spectroscopy. J. Appl. Cryst. 2007, 40, 1113-1122. (Pubitemid 350100309)
98. Ellis, M.J.; Buffey, S.G.; Hough, M.A.; Hasnain, S.S. On-line Optical and X-Ray Spectroscopies with Crystallography: an Integrated Approach for Determining Metalloprotein Structures in Functionally Well Defined States. J. Synchrotron. Radiat. 2008, 15, 433-439.
99. Sakai, K.; Matsui, Y.; Kouyama, T.; Shiro, Y.; Adachi, S. Optical Monitoring of Freeze- Trapped Reaction Intermediates in Protein Crystals: A Microspectro-Photometer for Cryogenic Protein Crystallography. J. Appl. Cryst. 2002, 35, 270-273.
100. Chen, Y.; Srajer, V.; Ng, K.; Legrand, A.; Moffat, K. Optical Monitoring of Protein Crystals in Time-Resolved X-Ray Experiments: Microspectrophotometer Design and Performance. Rev. Sci. Instrum. 1994, 65, 1506-1511.
101. McGeehan, J.E.; Carpentier, P.; Royant, A.; Bourgeois, D.; Ravelli, R.B. X-ray Radiationinduced Damage in DNA Monitored by Online Raman. J. Synchrotron. Radiat. 2007, 14, 99-108.
102. Pascal, A.A.; Liu, Z.; Broess, K.; Van Oort, B.; Van Amerongen, H.; Wang, C.; Horton, P.; Robert, B.; Chang, W.; Ruban, A. Molecular Basis of Photoprotection and Control of Photosynthetic Light-Harvesting. Nature 2005, 436, 134-137. (Pubitemid 40966199)
103. Enami, N.; Yoshimura, K.; Murakami, M.; Okumura, H.; Ihara, K.; Kouyama, T. Crystal Structures of Archaerhodopsin-1 and -2: Common Structural Motif in Archaeal Light-Driven Proton Pumps. J. Mol. Biol. 2006, 358, 675-685.
104. Sukumar, N.; Chen, Z.W.; Ferrari, D.; Merli, A.; Rossi, G.L.; Bellamy, H.D.; Chistoserdov, A.; Davidson, V.L.; Mathews, F.S. Crystal Structure of an Electron Transfer Complex Between Aromatic Amine Dehydrogenase and Azurin from Alcaligenes Faecalis. Biochemistry. 2006, 45, 13500-13510.
105. Gall, A.; Gardiner, A.T.; Cogdell, R.J.; Robert, B. Carotenoid Stoichiometry in the LH2 Crystal: No Spectral Evidence for the Presence of the Second Molecule in the Alpha/Beta- Apoprotein Dimer. FEBS Lett. 2006, 580, 3841-3844.
106. Baxter, R.H.; Krausz, E.; Norris, J.R. Photoactivation of the Photosynthetic Reaction Center of Blastochloris Viridis in the Crystalline State. J. Phys. Chem. B. 2006, 110, 1026-1032.
107. Carey, P.R. Raman Crystallography and Other Biochemical Applications of Raman Microscopy. Annu. Rev. Phys. Chem. 2006, 57, 527-554.
108. Arcovito, A.; Moschetti, T.; D'Angelo, P.; Mancini, G.; Vallone, B.; Brunori, M.; Della Longa, S. An X-ray Diffraction and X-Ray Absorption Spectroscopy Joint Study of Neuroglobin. Arch. Biochem. Biophys. 2008, 475, 7-13.
109. Arcovito, A.; Benfatto, M.; Cianci, M.; Hasnain, S.S.; Nienhaus, K.; Nienhaus, G.U.; Savino, C.; Strange, R.W.; Vallone, B.; Della Longa, S. X-ray Structure Analysis of a Metalloprotein with Enhanced Active-Site Resolution using In Situ X-Ray Absorption near Edge Structure Spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 6211-6216.
110. Van Gastel, M.; Stein, M.; Brecht, M.; Schroder, O.; Lendzian, F.; Bittl, R.; Ogata, H.; Higuchi, Y.; Lubitz, W. A Single-Crystal ENDOR and Density Functional theory Study of the Oxidized States of the [Nife] Hydrogenase from Desulfovibrio Vulgaris Miyazaki F. J. Biol. Inorg. Chem. 2006, 11, 41-51.
111. Halavaty, A.; Muller, J.J.; Contzen, J.; Jung, C.; Hannemann, F.; Bernhardt, R.; Galander, M.; Lendzian, F.; Heinemann, U. Light-induced Reduction of Bovine Adrenodoxin Via the Covalently Bound Ruthenium(II) Bipyridyl Complex: Intramolecular Electron Transfer and Crystal Structure. Biochemistry. 2006, 45, 709-718.
112. Galander, M.; Uppsten, M.; Uhlin, U.; Lendzian, F. Orientation of the Tyrosyl Radical in Salmonella Typhimurium Class Ib Ribonucleotide Reductase Determined by High Field EPR of R2F Single Crystals. J. Biol. Chem. 2006, 281, 31743-31752.
113. Utschig, L.M.; Chemerisov, S.D.; Tiede, D.M.; Poluektov, O.G. Electron Paramagnetic Resonance Study of Radiation Damage in Photosynthetic Reaction Center Crystals. Biochemistry. 2008, 47, 9251-9257.
114. Andresen, M.; Wahl, M.C.; Stiel, A.C.; Grater, F.; Schafer, L.V.; Trowitzsch, S.; Weber, G.; Eggeling, C.; Grubmuller, H.; Hell, S.W.; Jakobs, S. Structure and Mechanism of the Reversible Photoswitch of a Fluorescent Protein. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 13070-13074.
115. Hummer, G.; Schotte, F.; Anfinrud, P.A. Unveiling Functional Protein Motions with Picosecond X-Ray Crystallography and Molecular Dynamics Simulations. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 15330-15334.
116. Bossa, C.; Anselmi, M.; Roccatano, D.; Amadei, A.; Vallone, B.; Brunori, M.; Di Nola, A. Extended Molecular Dynamics Simulation of the Carbon Monoxide Migration in Sperm Whale Myoglobin. Biophys. J. 2004, 86, 3855-3862.
117. Cammarata, M.; Levantino, M.; Schotte, F.; Anfinrud, P.A.; Ewald, F.; Choi, J.; Cupane, A.; Wulff, M.; Ihee, H. Tracking the Structural Dynamics of Proteins in Solution using Time- Resolved Wide-Angle X-Ray Scattering. Nat. Methods. 2008, 5, 881-886.
118. Wulff, M.; Plech, A.; Eybert, L.; Randler, R.; Schotte, F.; Anfinrud, P.A. The Realization of Sub-Nanosecond Pump and Probe Experiments at the ESRF. Faraday Discussions. 2002, 122, 13-26.
119. Bourgeois, D.; Schotte, F.; Brunori, M.; Vallone, B. Time-resolved Methods in Biophysics. 6. Time-Resolved Laue Crystallography As a tool to Investigate Photo-Activated Protein Dynamics. Photochem. Photobiol. Sci. 2007, 6, 1047-1056.
120. Srajer, V.; Royer, W.E., Jr. Time-resolved X-Ray Crystallography of Heme Proteins. Methods Enzymol. 2008, 437, 379-395.
121. Nozawa, S.; Adachi, S.; Takahashi, J.; Tazaki, R.; Guerin, L.; Daimon, M.; Tomita, A.; Sato, T.; Chollet, M.; Collet, E.; Cailleau, H.; Yamamoto, S.; Tsuchiya, K.; Shioya, T.; Sasaki, H.; Mori, T.; Ichiyanagi, K.; Sawa, H.; Kawata, H.; Koshihara, S.Y. Developing 100 ps-Resolved X-Ray Structural Analysis Capabilities on Beamline NW14A at the Photon Factory Advanced Ring. J. Synchrotron. Radiat. 2007, 14, 313-319.
122. Knapp, J.E.; Srajer, V.; Pahl, R.; Royer, W.E., Jr. Immobilization of Scapharca HbI Crystals Improves Data Quality in Time-Resolved Crystallographic Experiments. Micron. 2004, 35, 107-108.
123. Nieh, Y.P.; Raftery, J.; Weisgerber, S.; Habash, J.; Schotte, F.; Ursby, T.; Wulff, M.; Haedener, A.; Campbell, J.W.; Hao, Q.; Helliwell, J.R. Accurate and Highly Complete Synchrotron Protein Crystal Laue Diffraction Data using the ESRF CCD and the Daresbury Laue software. J. Synchrotron. Rad. 1999, 6, 995-1006.
124. Bourgeois, D.; Wagner, U.; Wulff, M. Towards Automated Laue Data Processing: Application to the Choice of Optimal X-Ray Spectrum. Acta Crystallogr. D Biol. Crystallogr. 2000, 56 (Pt 8), 973-985.
125. Ren, Z. Precognition user guide with reference and tutorials, http://renzresearch.com/ Precognition (2006).
126. Arzt, S.; Campbell, J.W.; Harding, M.M.; Hao, Q.; Helliwell, J.R. LSCALE - the New Normalization, Scaling and Absorption Correction Program in the Daresbury Laue Software Suite. J. Appl. Cryst. 1999, 32, 554-562.
127. Ren, Z.; Moffat, K. Quantitative-analysis of Synchrotron Laue Diffraction Patterns in Macromolecular Crystallography. J. Appl. Cryst. 1995, 28, 461-481.
128. Ren, Z.; Moffat, K. Deconvolution of Energy Overlaps in Laue Diffraction. J. Appl. Cryst. 1995, 28, 482-493.
129. Bourgeois, D.; Nurizzo, D.; Kahn, R.; Cambillau, C. An Integration Routine Based on Profile Fitting with Optimized Fitting Area for the Evaluation of Weak and/or Overlapped 2-Dimensional Laue or Monochromatic Patterns. J. Appl. Cryst. 1998, 31, 22-35.
130. Ren, Z.; Perman, B.; Srajer, V.; Teng, T.Y.; Pradervand, C.; Bourgeois, D.; Schotte, F.; Ursby, T.; Kort, R.; Wulff, M.; Moffat, K. A Molecular Movie at 1.8A Resolution Displays the Photocycle of Photoactive Yellow Protein, a Eubacterial Blue-Light Receptor, from Nanoseconds to Seconds. Biochemistry. 2001, 40, 13788-13801.
131. Ursby, T.; Bourgeois, D. Improved Estimation of Structure Factor Difference Amplitudes from Poorly Accurate Data. Acta Crystallogr. A. 1997, 53, 564-575.
132. Schotte, F.; Lim, M.; Jackson, T.A.; Smirnov, A.V.; Soman, J.; Olson, J.S.; Phillips, G.N., Jr.; Wulff, M.; Anfinrud, P.A. Watching a Protein as It Functions with 150-Ps Time-Resolved X-Ray Crystallography. Science 2003, 300, 1944-1947.
133. Terwilliger, T.C.; Berendzen, J. Difference Refinement: Obtaining Differences Between Two Related Structures. Acta Crystallogr. D Biol. Crystallogr. 1995, 51, 609-618.
134. Silman, I.; Sussman, J.L. Acetylcholinesterase: 'Classical' and 'Non-Classical' Functions and Pharmacology. Curr. Opin. Pharmacol. 2005, 5, 293-302.
135. Sussman, J.L.; Harel, M.; Frolow, F.; Oefner, C.; Goldman, A.; Toker, L.; Silman, I. Atomic Structure of Acetylcholinesterase from Torpedo californica: A Prototypic Acetylcholine- Binding Protein. Science 1991, 253, 872-879.
136. Gilson, M.K.; Straatsma, T.P.; McCammon, J.A.; Ripoll, D.R.; Faerman, C.H.; Axelsen, P.H.; Silman, I.; Sussman, J.L. Open ''Back Door'' in a Molecular Dynamics Simulation of Acetylcholinesterase. Science 1994, 263, 1276-1278.
137. Peng, L.; Silman, I.; Sussman, J.; Goeldner, M. Biochemical Evaluation of Photolabile Precursors of Choline and of Carbamylcholine for Potential Time-Resolved Crystallographic Studies on Cholinesterases. Biochemistry. 1996, 35, 10854-10861.
138. Ravelli, R.B.; Raves, M.L.; Ren, Z.; Bourgeois, D.; Roth, M.; Kroon, J.; Silman, I.; Sussman, J.L. Static Laue Diffraction Studies on Acetylcholinesterase. Acta Crystallogr. D Biol. Crystallogr. 1998, 54, 1359-1366.
139. Specht, A.; Ursby, T.; Weik, M.; Peng, L.; Kroon, J.; Bourgeois, D.; Goeldner, M. Cryophotolysis of Ortho-Nitrobenzyl Derivatives of Enzyme Ligands for the Potential Kinetic Crystallography of Macromolecules. Chembiochem. 2001, 2, 845-848.
140. Corrie, J.E.; Barth, A.; Munasinghe, V.R.; Trentham, D.R.; Hutter, M.C. Photolytic Cleavage of 1-(2-Nitrophenyl)Ethyl Ethers involves Two Parallel Pathways and Product Release Is Rate-Limited by Decomposition of a Common Hemiacetal Intermediate. J. Am. Chem. Soc. 2003, 125, 8546-8554.
141. Weik, M.; Vernede, X.; Royant, A.; Bourgeois, D. Temperature Derivative Fluorescence Spectroscopy As a Tool to Study Dynamical Changes in Protein Crystals. Biophys. J. 2004, 86, 3176-3185.
142. Jenney, F.E., Jr.; Verhagen, M.F.; Cui, X.; Adams, M.W. Anaerobic Microbes: Oxygen Detoxification without Superoxide Dismutase. Science 1999, 286, 306-309.
143. Mathe, C.; Weill, C.O.; Mattioli, T.A.; Berthomieu, C.; Houee-Levin, C.; Tremey, E.; Niviere, V. Assessing the Role of the Active-Site Cysteine Ligand in the Superoxide Reductase from Desulfoarculus Baarsii. J. Biol. Chem. 2007, 282, 22207-22216.
144. Hersleth, H.P.; Ryde, U.; Rydberg, P.; Gorbitz, C.H.; andersson, K.K. Structures of the High- Valent Metal-Ion Haem-Oxygen Intermediates in Peroxidases, Oxygenases and Catalases. J. Inorg. Biochem. 2006, 100, 460-476.
145. Blakeley, M.P.; Ruiz, F.; Cachau, R.; Hazemann, I.; Meilleur, F.; Mitschler, A.; Ginell, S.; Afonine, P.; Ventura, O.N.; Cousido-Siah, A.; Haertlein, M.; Joachimiak, A.; Myles, D.; Podjarny, A. Quantum Model of Catalysis Based on a Mobile Proton Revealed by Subatomic X-Ray and Neutron Diffraction Studies of H-Aldose Reductase. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 1844-1848.
146. Neutze, R.; Huldt, G.; Hajdu, J.; Van Der Spoel, D. Potential Impact of an X-Ray Free Electron Laser on Structural Biology. Rad. Phys. Chem. 2004, 71, 905-916. (Pubitemid 39119721)