Probing anisotropic structure changes in proteins with picosecond time-resolved small-angle X-ray scattering

Journal of Physical Chemistry B

Volumn 117, Issue 49, 2013, Pages 15825-15832

  Cho, Hyun Sun ^a   Schotte, Friedrich ^a   Dashdorj, Naranbaatar ^a   Kyndt, John ^b   Anfinrud, Philip A ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b BELLEVUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOTROPIC STRUCTURE; ELECTRONIC TRANSITION; ORTHOGONAL DIRECTIONS; PHOTOACTIVE YELLOW PROTEINS; SMALL ANGLE X-RAY SCATTERING; SOLUTION SCATTERINGS; STRUCTURAL INFORMATION; STRUCTURE TRANSITIONS;

CHROMOPHORES; CRYSTALLINE MATERIALS; STRUCTURAL DYNAMICS; X RAY SCATTERING;

PROTEINS;

4-COUMARIC ACID; BACTERIAL PROTEIN; COUMARIC ACID; PARA COUMARIC ACID; PHOTOACTIVE YELLOW PROTEIN, BACTERIA; RECOMBINANT PROTEIN; VISUAL PROTEINS AND PIGMENTS;

ARTICLE; BIOSYNTHESIS; CHEMISTRY; ELECTRON; GENETICS; METABOLISM; SMALL ANGLE SCATTERING; TIME; X RAY DIFFRACTION;

BACTERIAL PROTEINS; COUMARIC ACIDS; ELECTRONS; PHOTORECEPTORS, MICROBIAL; RECOMBINANT PROTEINS; SCATTERING, SMALL ANGLE; TIME FACTORS; X-RAY DIFFRACTION;

EID: 84890523124     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp407593j     Document Type: Article

References (40)

1. Srajer, V.; Teng, T. Y.; Ursby, T.; Pradervand, C.; Ren, Z.; Adachi, S.; Schildkamp, W.; Bourgeois, D.; Wulff, M.; Moffat, K. Photolysis of the Carbon Monoxide Complex of Myoglobin: Nanosecond Time-Resolved Crystallography Science 1996, 274 (5293) 1726-1729
2. Schotte, F.; Lim, M. H.; Jackson, T. A.; Smirnov, A. V.; Soman, J.; Olson, J. S.; Phillips, G. N.; Wulff, M.; Anfinrud, P. A. Watching a Protein as it Functions with 150-ps Time-resolved X-ray Crystallography Science 2003, 300 (5627) 1944-1947
3. Schotte, F.; Cho, H. S.; Kaila, V. R.; Kamikubo, H.; Dashdorj, N.; Henry, E. R.; Graber, T. J.; Henning, R.; Wulff, M.; Hummer, G. Watching a Signaling Protein Function in Real Time via 100-ps Time-resolved Laue Crystallography Proc. Natl. Acad. Sci. U.S.A. 2012, 109 (47) 19256-61
4. Salcedo, J. R.; Siegman, A. E.; Dlott, D. D.; Fayer, M. D. Dynamics of Energy Transport in Molecular Crystals: The Picosecond Transient-Grating Method Phys. Rev. Lett. 1978, 41 (2) 131-134
5. Goodno, G. D.; Miller, R. J. D. Femtosecond Heterodyne-Detected Four-Wave-Mixing Studies of Deterministic Protein Motions. 1. Theory and Experimental Technique of Diffractive Optics-Based Spectroscopy J. Phys. Chem. A 1999, 103 (49) 10619-10629
6. Goodno, G. D.; Astinov, V.; Miller, R. J. D. Femtosecond Heterodyne-detected four-wave-mixing Studies of Deterministic Protein Motions. 2. Protein Response J. Phys. Chem. A 1999, 103 (49) 10630-10643
7. 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 (10) 881-6
8. Cho, H. S.; Dashdorj, N.; Schotte, F.; Graber, T.; Henning, R.; Anfinrud, P. Protein Structural Dynamics in Solution Unveiled via 100-ps Time-resolved X-ray Scattering Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (16) 7281-6
9. Kim, T. W.; Lee, J. H.; Choi, J.; Kim, K. H.; van Wilderen, L. J.; Guerin, L.; Kim, Y.; Jung, Y. O.; Yang, C.; Kim, J. Protein Structural Dynamics of Photoactive Yellow Protein in Solution Revealed by Pump-Probe X-ray Solution Scattering J. Am. Chem. Soc. 2012, 134 (6) 3145-3153
10. 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 (20) 7145-7150
11. Jung, Y. O.; Lee, J. H.; Kim, J.; Schmidt, M.; Moffat, K.; Srajer, V.; Ihee, H. Volume-conserving trans-cis isomerization Pathways in Photoactive Yellow Protein Visualized by Picosecond X-ray Crystallography Nat. Chem. 2013, 5 (3) 212-20
12. Tripathi, S.; Srajer, V.; Purwar, N.; Henning, R.; Schmidt, M. pH Dependence of the Photoactive Yellow Protein Photocycle Investigated by Time-Resolved Crystallography Biophys. J. 2012, 102 (2) 325-332
13. Hellingwerf, K. J.; Hendriks, J.; Gensch, T. Photoactive Yellow Protein, a new type of Photoreceptor Protein: Will this "yellow lab" bring us where we want to go? J. Phys. Chem. A 2003, 107 (8) 1082-1094
14. Imamoto, Y.; Kataoka, M. Structure and Photoreaction of Photoactive Yellow Protein, a Structural Prototype of the PAS Domain Superfamily Photochem. Photobiol. 2007, 83 (1) 40-49
15. Meyer, T. E. Isolation and Characterization of Soluble Cytochromes, Ferredoxins and Other Chromophoric Proteins from the Halophilic Phototrophic Bacterium Ectothiorhodospira-Halophila Biochim. Biophys. Acta 1985, 806 (1) 175-183
16. Hustede, E.; Liebergesell, M.; Schlegel, H. G. The Photophobic Response of Various Sulfur and Nonsulfur Purple Bacteria Photochem. Photobiol. 1989, 50 (6) 809-815
17. Sprenger, W. W.; Hoff, W. D.; Armitage, J. P.; Hellingwerf, K. J. The Eubacterium Ectothiorhodospira-Halophila Is Negatively Phototactic, with a Wavelength Dependence That Fits the Absorption-Spectrum of the Photoactive Yellow Protein J. Bacteriol. 1993, 175 (10) 3096-3104
18. Ujj, L.; Devanathan, S.; Meyer, T. E.; Cusanovich, M. A.; Tollin, G.; Atkinson, G. H. New photocycle intermediates in the Photoactive Yellow Protein from Ectothiorhodospira halophila: Picosecond transient Absorption Spectroscopy Biophys. J. 1998, 75 (1) 406-412
19. Imamoto, Y.; Kataoka, M.; Tokunaga, F.; Asahi, T.; Masuhara, H. Primary Photoreaction of Photoactive Yellow Protein Studied by Subpicosecond-nanosecond spectroscopy Biochemistry 2001, 40 (20) 6047-6052
20. Larsen, D. S.; van Stokkum, I. H. M.; Vengris, M.; van der Horst, M. A.; de Weerd, F. L.; Hellingwerf, K. J.; van Grondelle, R. Incoherent Manipulation of the Photoactive Yellow Protein Photocycle with Dispersed pump-dump-probe Spectroscopy Biophys. J. 2004, 87 (3) 1858-1872
21. van Wilderen, L. J. G. W.; Van der Horst, M. A.; van Stokkum, I. H. M.; Hellingwerf, K. J.; van Grondelle, R.; Groot, M. L. Ultrafast Infrared Spectroscopy r\Reveals a Key Step for Successful Entry into the Photocycle for Photoactive Yellow Protein Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (41) 15050-15055
22. Heyne, K.; Mohammed, O. F.; Usman, A.; Dreyer, J.; Nibbering, E. T. J.; Cusanovich, M. A. Structural Evolution of the Chromophore in the Primary Stages of trans/cis isomerization in Photoactive Yellow Protein J. Am. Chem. Soc. 2005, 127 (51) 18100-18106
23. Meyer, T. E.; Yakali, E.; Cusanovich, M. A.; Tollin, G. Properties of a Water-Soluble, Yellow Protein Isolated from a Halophilic Phototrophic Bacterium that has Photochemical Activity Analogous to Sensory Rhodopsin Biochemistry 1987, 26 (2) 418-23
24. Meyer, T. E.; Tollin, G.; Hazzard, J. H.; Cusanovich, M. A. Photoactive Yellow Protein from the Purple Phototrophic Bacterium, Ectothiorhodospira- Halophila-Quantum Yield of Photobleaching and Effects of Temperature, Alcohols, Glycerol, and Sucrose on Kinetics of Photobleaching and Recover Biophys. J. 1989, 56 (3) 559-564
25. Meyer, T. E.; Tollin, G.; Causgrove, T. P.; Cheng, P.; Blankenship, R. E. Picosecond Decay Kinetics and Quantum Yield of Fluorescence of the Photoactive Yellow Protein from the Halophilic Purple Phototrophic Bacterium, Ectothiorhodospira-Halophila Biophys. J. 1991, 59 (5) 988-991
26. Anderson, S.; Crosson, S.; Moffat, K. Short hydrogen bonds in Photoactive Yellow Protein Acta Crystallogr., D 2004, 60, 1008-1016
27. Kaila, V. R.; Schotte, F.; Cho, H. S.; Hummer, G.; Anfinrud, P. Reconciling Contradictions in Time-resolved x-ray Structures of early Intermediates in the Photocycle of Photoactive Yellow Protein. Nat. Chem., in press.
28. Ansari, A.; Szabo, A. Theory of photoselection by Intense Light Pulses. Influence of Reorientational Dynamics and Chemical Kinetics on Absorbance Measurements Biophys. J. 1993, 64 (3) 838-51
29. Lakowicz, J. R. Principles of fluorescence spectroscopy, 3 rd ed.; Springer: New York, 2006; p xxvi.
30. Ansari, A.; Jones, C. M.; Henry, E. R.; Hofrichter, J.; Eaton, W. A. Photoselection in Polarized Photolysis Experiments on Heme Proteins Biophys. J. 1993, 64 (3) 852-68
31. Lim, M.; Jackson, T. A.; Anfinrud, P. A. Binding of CO to Myoglobin from a Heme Pocket Docking site to form nearly Linear Fe-C-O Science 1995, 269 (5226) 962-6
32. Lim, M.; Jackson, T. A.; Anfinrud, P. A. Ultrafast Rotation and Trapping of Carbon Monoxide Dissociated from Myoglobin Nat. Struct. Biol. 1997, 4 (3) 209-14
33. Moore, J. N.; Hansen, P. A.; Hochstrasser, R. M. Iron-carbonyl bond Geometries of Carboxymyoglobin and Carboxyhemoglobin in Solution Determined by Picosecond Time-resolved Infrared Spectroscopy Proc. Natl. Acad. Sci. U.S.A. 1988, 85 (14) 5062-6
34. Kim, J.; Kim, K. H.; Kim, J. G.; Kim, T. W.; Kim, Y.; Ihee, H. Anisotropic Picosecond X-ray Solution Scattering from Photo-selectively Aligned Protein Molecules J. Phys. Chem. Lett. 2011, 2 (5) 350-356
35. Kyndt, J. A.; Vanrobaeys, F.; Fitch, J. C.; Devreese, B. V.; Meyer, T. E.; Cusanovich, M. A.; Van Beeumen, J. J. Heterologous Production of Halorhodospira halophila holo-photoactive Yellow Protein through Tandem Expression of the Postulated Biosynthetic Genes Biochemistry 2003, 42 (4) 965-970
36. Porod, G. General Theory. In Small Angle X-ray Scattering; Glatter, O.; Kratky, O., Eds.; Academic Press, Inc.: New York, 1982; pp 17-51.
37. Otto, H.; Hoersch, D.; Meyer, T. E.; Cusanovich, M. A.; Heyn, M. P. Time-resolved Single tryptophan Fluorescence in Photoactive Yellow Protein Monitors Changes in the Chromophore Structure during the Photocycle via Energy Transfer Biochemistry 2005, 44 (51) 16804-16816
38. Jones, C. M.; Ansari, A.; Henry, E. R.; Christoph, G. W.; Hofrichter, J.; Eaton, W. A. Speed of Intersubunit Communication in Proteins Biochemistry 1992, 31 (29) 6692-702
39. McCalley, R. C.; Shimshick, E. J.; McConnell, H. M. Effect of Slow Rotational Motion on Paramagnetic-Resonance Spectra Chem. Phys. Lett. 1972, 13 (2) 115
40. Hofrichter, J.; Henry, E. R.; Szabo, A.; Murray, L. P.; Ansari, A.; Jones, C. M.; Coletta, M.; Falcioni, G.; Brunori, M.; Eaton, W. A. Dynamics of the Quaternary Conformational change in Trout Hemoglobin Biochemistry 1991, 30 (26) 6583-98