Probing the flexibility of the bacterial reaction center: The wild-type protein is more rigid than two site-specific mutants

Biochemistry

Volumn 46, Issue 51, 2007, Pages 14960-14968

  Sacquin Mora, Sophie ^a   Sebban, Pierre ^b   Derrien, Valérie ^b   Frick, Bernhard ^c   Lavery, Richard ^a   Alba Simionesco, Christiane ^b  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^b UNIVERSITÉ PARIS SUD   (France)

^c INSTITUT LAUE LANGEVIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACKSCATTERING; BACTERIA; BROWNIAN MOVEMENT; CRYSTALLOGRAPHY; MUTAGENESIS; NEUTRON SCATTERING;

ANHARMONICITY; POINT GENETIC MUTATIONS; PROTEIN MECHANICS; QUASIELASTIC NEUTRON SCATTERING;

PROTEINS;

ALANINE; ASPARTIC ACID; BACTERIAL PROTEIN; GLUTAMIC ACID; MUTANT PROTEIN; TYROSINE;

AMINO ACID SUBSTITUTION; ARTICLE; CRYSTALLOGRAPHY; DIFFUSION; MOLECULAR DYNAMICS; NEUTRON SCATTERING; NONHUMAN; PHOTOSYNTHESIS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; RHODOBACTER SPHAEROIDES; TEMPERATURE;

BACTERIAL PROTEINS; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RHODOBACTER SPHAEROIDES; SENSITIVITY AND SPECIFICITY; TEMPERATURE;

BACTERIA (MICROORGANISMS); PHOTOBACTERIA; RHODOBACTER SPHAEROIDES;

EID: 37349030789     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7004416     Document Type: Article

References (66)

1. Frauenfelder, H., Sligar, S. G., and Wolynes, P. G. (1991) The energy landscapes and motions of proteins, Science 254, 1598-603.
2. Elber, R., and Karplus, M. (1987) Multiple conformational states of proteins: a molecular dynamics analysis of myoglobin, Science 235, 318-21.
3. Daniel, R. M., Dunn, R. V., Finney, J. L., and Smith, J. C. (2003) The role of dynamics in enzyme activity, Annu. Rev. Biophys. Biomol. Struct. 32, 69-92.
4. Parak, F. G. (2003) Proteins in action: the physics of structural fluctuations and conformational changes, Curr. Opin. Struct. Biol. 13, 552-7.
5. Caliskan, G., Kisliuk, A., Tsai, A. M., Soles, C. L., and Sokolov, A. P. (2003) Protein dynamics in viscous solvents, J. Chem. Phys. 118, 4230-4236.
6. Cordone, L., Ferrand, M., Vitrano, E., and Zaccai, G. (1999) Harmonic behavior of trehalose-coated carbon-monoxy-myoglobin at high temperature, Biophys. J. 76, 1043-7.
7. Fitter, J., Lechner, R. E., Buldt, G., and Dencher, N. A. (1996) Internal molecular motions of bacteriorhodopsin: hydration-induced flexibility studied by quasielastic incoherent neutron scattering using oriented purple membranes, Proc. Natl. Acad. Sci. U.S.A. 93, 7600-5.
8. Zaccai, G. (2000) How soft is a protein? A protein dynamics force constant measured by neutron scattering, Science 288, 1604-7.
9. Reat, V., Patzelt, H., Ferrand, M., Pfister, C., Oesterhelt, D., and Zaccai, G. (1998) Dynamics of different functional parts of bacteriorhodopsin: H-2H labeling and neutron scattering, Proc. Natl. Acad. Sci. U.S.A. 95, 4970-5.
10. Hayward, J. A., and Smith, J. C. (2002) Temperature dependence of protein dynamics: computer simulation analysis of neutron scattering properties, Biophys. J. 82, 1216-25.
11. Tournier, A. L., and Smith, J. C. (2003) Principal components of the protein dynamical transition, Phys. Rev. Lett. 91, 208106.
12. Bartlett, G. J., Porter, C. T., Borkakoti, N., and Thornton, J. M. (2002) Analysis of catalytic residues in enzyme active sites, J. Mol. Biol. 324, 105-21.
13. Kurkal-Siebert, V., and Smith, J. C. (2006) Low-temperature protein dynamics: a simulation analysis of interprotein vibrations and the boson peak at 150 k, J. Am. Chem. Soc. 128, 2356-64.
14. Sacquin-Mora, S., and Lavery, R. (2006) Investigating the local flexibility of functional residues in hemoproteins, Biophys. J. 90, 2706-17.
15. Sacquin-Mora, S., and Lavery, R. (2007) Locating the active sites of enzymes using mechanical properties, Proteins 67, 350-359.
16. Tehei, M., Smith, J. C., Monk, C., Ollivier, J., Oettl, M., Kurkal, V., Finney, J. L., and Daniel, R. M. (2006) Dynamics of immobilized and native Escherichia coli dihydrofolate reductase by quasielastic neutron scattering, Biophys. J. 90, 1090-7.
17. Yang, L. W., and Bahar, I. (2005) Coupling between catalytic site and collective dynamics: a requirement for mechanochemical activity of enzymes, Structure 13, 893-904.
18. Yuan, Z., Zhao, J., and Wang, Z. X. (2003) Flexibility analysis of enzyme active sites by crystallographic temperature factors, Protein Eng. 16, 109-14.
19. Paddock, M. L., Feher, G., and Okamura, M. Y. (2003) Proton transfer pathways and mechanism in bacterial reaction centers, FEBS Lett. 555, 45-50.
20. Rutherford, A. W., and Faller, P. (2003) Photosystem II: evolutionary perspectives, Philos. Trans. R. Soc. Land. B Biol. Sci. 358, 245-53.
21. Wraight, C. A. (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides, Front. Biosci. 9, 309-37.
22. Ermler, U., Fritzsch, G., Buchanan, S. K., and Michel, H. (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 Å resolution: cofactors and protein-cofactor interactions, Structure 2, 925-36.
23. Fritzsch, G., Koepke, J., Diem, R., Kuglstatter, A., and Baciou, L. (2002) Charge separation induces conformational changes in the photosynthetic reaction centre of purple bacteria, Acta Crystallogr. Sect. D: Biol. Crystallogr. 58, 1660-3.
24. Pokkuluri, P. R., Laible, P. D., Deng, Y. L., Wong, T. N., Hanson, D. K., and Schiffer, M. (2002) The structure of a mutant photosynthetic reaction center shows unexpected changes in main chain orientations and quinone position, Biochemistry 41, 5998-6007.
25. Stowell, M. H., McPhillips, T. M., Rees, D. C., Soltis, S. M., Abresch, E., and Feher, G. (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer, Science 276, 812-6.
26. Miksovska, J., Schiffer, M., Hanson, D. K., and Sebban, P. (1999) Proton uptake by bacterial reaction centers: the protein complex responds in a similar manner to the reduction of either quinone acceptor, Proc. Natl. Acad. Sci. U.S.A. 96, 14348-53.
27. Paddock, M. L., Rongey, S. H., Feher, G., and Okamura, M. Y. (1989) Pathway of proton transfer in bacterial reaction centers: replacement of glutamic acid 212 in the L subunit by glutamine inhibits quinone (secondary acceptor) turnover, Proc. Natl. Acad. Sci. U.S.A. 86, 6602-6.
28. Takahashi, E., and Wraight, C. A. (1990) A crucial role for AspL213 in the proton transfer pathway to the secondary quinone of reaction centers from Rhodobacter sphaeroides, Biochim. Biophys. Acta 1020, 107-111.
29. Tandori, J., Baciou, L., Alexov, E., Maroti, P., Schiffer, M., Hanson, D. K., and Sebban, P. (2001) Revealing the Involvment of Extended Hydrogen-Bond Networks in the Cooperative Function between Distant Sites in Bacterial Centers, J. Biol. Chem. 276, 45513-15.
30. Hanson, D. K., Tiede, D. M., Nance, S. L., Chang, C. H., and Schiffer, M. (1993) Site-specific and compensatory mutations imply unexpected pathways for proton delivery to the QB binding site of the photosynthetic reaction center, Proc. Natl. Acad. Sci. U.S.A. 90, 8929-33.
31. Hanson, D. K., Baciou, L., Tiede, D. M., Nance, S. L., Schiffer, M., and Sebban, P. (1992) In bacterial reaction centers protons can diffuse to the secondary quinone by alternative pathways, Biochim. Biophys. Acta 1102, 260-5.
32. Gall, A., Seguin, J., Robert, B., and Bellissent-Funel, M. C. (2002) Membrane Proteins in Bulk Solution Can Be Used for Quasi-Elastic Neutron Scattering Studies: The Case for the Photochemical Reaction Center, J. Phys. Chem. B 106, 6303-6309.
33. Zacharias, M. (2003) Protein-protein docking with a reduced protein model accounting for side-chain flexibility, Protein Sci. 12, 1271-82.
34. Atilgan, A. R., Durell, S. R., Jernigan, R. L., Demirel, M. C., Keskin, O., and Bahar, I. (2001) Anisotropy of fluctuation dynamics of proteins with an elastic network model, Biophys. J. 80, 505-15.
35. Doruker, P., Jernigan, R. L., and Bahar, I. (2002) Dynamics of large proteins through hierarchical levels of coarse-grained structures, J. Comput. Chem. 23, 119-27.
36. Berman, H. M., Battistuz, T., Bhat, T. N., Bluhm, W. F., Bourne, P. E., Burkhardt, K., Feng, Z., Gilliland, G. L., Iype, L., Jain, S., Fagan, P., Marvin, J., Padilla, D., Ravichandran, V., Schneider, B., Thanki, N., Weissig, H., Westbrook, J. D., and Zardecki, C. (2002) The Protein Data Bank, Acta Crystallogr. Sect. D: Biol. Crystallogr. 58, 899-907.
37. Cusack, S., and Doster, W. (1990) Temperature dependence of the low frequency dynamics of myoglobin. Measurement of the vibrational frequency distribution by inelastic neutron scattering, Biophys. J. 58, 243-51.
38. Xu, Q., and Gunner, M. R. (2001) Trapping conformational intermediate states in the reaction center protein from photosynthetic bacteria, Biochemistry 40, 3232-3241.
39. Diehl, M., Doster, W., Petry, W., and Schober, H. (1997) Water-coupled low-frequency modes of myoglobin and lysozyme observed by inelastic neutron scattering. Biophys. J. 73, 2726-32.
40. Giordano, R., Grasso, A., Teixeira, J., Wanderlingh, F., and Wanderlingh, U. (1991) Small-angle neutron scattering in lysozyme solutions, Phys. Rev. A 43, 6894-6899.
41. Smith, J., Kuczera, K., and Karplus, M. (1990) Dynamics of myoglobin: comparison of simulation results with neutron scattering spectra, Proc. Natl. Acad. Sci. U.S.A. 87, 1601-5.
42. Bicout, D. J., and Zaccai, G. (2001) Protein Flexibility from the Dynamical Transition: A Force Constant Analysis, Biophys. J. 80, 1115-23.
43. Kurkal, V., Daniel, R. M., Finney, J. L., Tehei, M., Dunn, R. V., and Smith, J. C. (2005) Low frequency enzyme dynamics as a function of temperature and hydration: A neutron scattering study. Chem. Phys. 317, 267-73.
44. Begen, B., Kisliuk, A., Novikov, V., Sokolov, A., Niss, K., Chauty-Cailliaux, A., Alba-Simionesco, C., and Frick, B. (2006) Influence of pressure on fast dynamics in polyisobutylene, J. Non-Cryst. Solids (in press).
45. Frick, B., and Alba-Simionesco, C. (1999) Comparison of the pressure and temperature dependence of the elastic incoherent scattering for the polymers polybutadiene and polyisobutylene, Phys. B 266, 13-19.
46. Frick, B., and Alba-Simionesco, C. (2002) Pressure dependence of the Boson peak in poly (butadiene), Appl. Phys. A 74.
47. Leonforte, F., Tanguy, A., Wittmer, J. P., and Barrat, J. L. (2006) Inhomogeneous elastic response of silica glass, Phys. Rev. Lett. 97, 055501.
48. Lubchenko, V., and Wolynes, P. G. (2003) The origin of the boson peak and thermal conductivity plateau in low-temperature glasses, Proc. Natl. Acad. Sci. U.S.A. 100, 1515-8.
49. Monaco, A., Chumakov, A. I., Monaco, G., Crichton, W. A., Meyer, A., Comez, L., Fioretto, D., Korecki, J., and Ruffer, R. (2006) Effect of Densification on the Density of Vibrational States of Glasses, Phys. Rev. Lett. 97.
50. Niss, K., and Alba-Simionesco, C. (2006) Effect of density and temperature on correlations between fragility and glassy properties, Phys. Rev. B 74, 024205.
51. Schirmacher, W., Ruocco, G., and Scopigno, T. (2007) Acoustic Attenuation in Glasses and its Relation with the Boson Peak, Phys. Rev. Lett. 98, 25501.
52. Brown, K. G., Erfurth, S. C., Small, E. W., and Peticolas, W. L. (1972) Conformationally dependent low-frequency motions of proteins by laser Raman spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 69, 1467-9.
53. Fenimore, P. W., Frauenfelder, H., McMahon, B. H., and Young, R. D. (2004) 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. 101, 14408-13.
54. Ferrand, M., Dianoux, A. J., Petry, W., and Zaccai, G. (1993) Thermal motions and function of bacteriorhodopsin in purple membranes: effects of temperature and hydration studied by neutron scattering, Proc. Natl. Acad. Sci. U.S.A. 90, 9668-72.
55. Fitter, J. (1999) The temperature dependence of internal molecular motions in hydrated and dry alpha-amylase: the role of hydration water in the dynamical transition of proteins, Biophys. J. 76, 1034-42.
56. Paciaroni, A., Stroppolo, M. E., Arcangeli, C., Bizzarri, A. R., Desideri, A., and Cannistraro, S. (1999) Incoherent neutron scattering of copper azurin: a comparison with molecular dynamics simulation results, Eur Biophys. J. 28, 447-56.
57. Roh, J. H., Curtis, J. E., Azzam, S., Novikov, V. N., Peral, I., Chowdhuri, Z., Gregory, R. B., and Sokolov, A. P. (2006) Influence of hydration on the dynamics of lysozyme, Biophys. J. 91, 2573-88.
58. Daniel, R. M., Finney, J. L., Réat, V., Dunn, R., Ferrand, M., and Smith, J. C. (1999) Enzyme Dynamics and Activity: Time-Scale Dependence of Dynamical Transitions in Glutamate Dehydrogenase Solution, Biophys. J. 77, 2184-90.
59. Gabel, F.. Weik, M., Doctor, B. P., Saxena, A., Fournier, D., Brochier, L., Renault, F., Masson, P., Silman, I., and Zaccai, G. (2004) The Influence of Solvent Composition on Global Dynamics of Human Butyrylcholinesterase Powders: A Neutron-Scattering Study, 86, 3152-65.
60. Tirion, M. M. (1996) Large Amplitude Elastic Motions in Proteins from a Single-Parameter, Atomic Analysis, Phys. Rev. Lett. 77, 1905-1908.
61. Tozzini, V. (2005) Coarse-grained models for proteins, Curr. Opin. Struct. Biol. 15, 144-50.
62. Zachariae, U., and Lancaster, C. R. (2001) Proton uptake associated with the reduction of the primary quinone Q(A) influences the binding site of the secondary quinone Q(B) in Rhodopseudomonas viridis photosynthetic reaction centers, Biochim. Biophys. Acta 1505, 280-90.
63. Baciou, L., and Sebban, P. (1995) Heterogeneity of the quinone electron acceptor system in bacterial reaction centers, Photochem. Photobiol. 62, 271-278.
64. Spitz, J. A., Derrien, V., Baciou, L., and Sebban, P. (2005) Specific triazine resistance in bacterial reaction ceters induced by a single mutation in the QA protein pocket, Biochemistry 44, 1338-43.
65. Frick, F., Combet, J., Pfister, C. (2001) Neutron backscattering and its application in soft matter investigation, J. Phys. Soc. Jpn. 70 (Suppl. A), 311-316.
66. Gabel, F. (2006) Protein dynamics in solution and powder measured by incoherent elastic neutron scattering: the influence of Q-range and energy resolution, Eur. Biophys. J. 34, 1-12.