Energy landscape of domain motion in glutamate dehydrogenase deduced from cryo-electron microscopy.

Tytuł:: Energy landscape of domain motion in glutamate dehydrogenase deduced from cryo-electron microscopy.
Autorzy:: Oide M; Department of Physics, Faculty of Science and Technology, Keio University, Yokohama, Japan.; RIKEN SPring-8 Center, Sayo-gun, Japan.
Kato T; Graduate School of Frontier Biosciences, Osaka University, Suita, Japan.
Oroguchi T; Department of Physics, Faculty of Science and Technology, Keio University, Yokohama, Japan.; RIKEN SPring-8 Center, Sayo-gun, Japan.
Nakasako M; Department of Physics, Faculty of Science and Technology, Keio University, Yokohama, Japan.; RIKEN SPring-8 Center, Sayo-gun, Japan.
Źródło:: The FEBS journal [FEBS J] 2020 Aug; Vol. 287 (16), pp. 3472-3493. Date of Electronic Publication: 2020 Feb 05.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: Oxford, UK : Published by Blackwell Pub. on behalf of the Federation of European Biochemical Societies, c2005-
MeSH Terms:: Molecular Dynamics Simulation*
Protein Domains*
Archaeal Proteins/*chemistry
Glutamate Dehydrogenase/*chemistry
Thermococcus/*enzymology
Algorithms ; Archaeal Proteins/metabolism ; Archaeal Proteins/ultrastructure ; Cryoelectron Microscopy ; Energy Transfer ; Glutamate Dehydrogenase/metabolism ; Glutamate Dehydrogenase/ultrastructure ; Motion ; Thermodynamics
References:: Marsh JA, Teichmann SA & Forman-Kay JD (2012) Probing the diverse landscape of protein flexibility and binding. Curr Opn Struct Biol 22, 643-650.
Berendsen HJ & Hayward S (2000) Collective protein dynamics in relation to function. Curr Opn Struct Biol 10, 165-169.
Noji H, Yasuda R, Yoshida M & Kinoshita K Jr (1997) Direct observation of the rotation of F1-ATPase. Nature 386, 299-302.
Cornish PV, Emolenko DN, Noller HF & Ha T (2008) Spontaneous intersubunit rotation in single ribosomes. Mol Cell 30, 578-588.
Sasmal DK, Pulido L, Kasal S & Huang J (2016) Single-molecule fluorescence resonance energy transfer in molecular biology. Nanoscale 8, 19928-19944.
Dror RO, Dirks RM, Grossman JP, Xu H & Shaw DE (2012) Biomolecular simulation: a computational microscopy for molecular biology. Annu Rev Biophys 41, 429-452.
Oroguchi T, Hashimoto H, Shimizu T, Sato M & Ikeguchi M (2009) Intrinsic dynamics of restriction endonuclease EcoO109I studied by molecular dynamics simulations and X-Ray scattering data analysis. Biophys J 96, 2808-2822.
Beauchamp KA, Lin Y, Das R & Pande VS (2012) Are protein force fields getting better? A systematic benchmark on 524 diverse NMR measurements. J Chem Theory Comput 8, 1409-1414.
Oroguchi T & Nakasako M (2017) Influences of lone-pair electrons on directionality of hydrogen bonds formed by hydrophilic amino acid side chains in molecular dynamics simulation. Sci Rep 7, 15859.
Frank J (2007) Three-Dimensional Electron Microscopy of Macromolecular Assemblies. Oxford University Press, Oxford.
Carroni M & Saibil HR (2016) Cryo electron microscopy to determine the structure of macromolecular complexes. Methods 95, 78-85.
Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J, McDowall AW & Schultz P (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21, 129-228.
Scheres SHW, Gao H, Valle M, Herman GT, Eggermont PPB, Frank J & Carazo JM (2007) Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat Met 4, 27-29.
Dashti A, Schwander P, Langlois R, Fung R, Li W, Hosseinizadeh A, Liao HY, Pallesen J, Sharma G, Stupina VA et al. (2014) Trajectories of the ribosome as a Brownian nanomachine. Proc Natl Acad Sci USA 111, 17492-17497.
Bai XC, Rajendra E, Yang G, Shi Y & Scheres SHW (2015) Sampling the conformational space of the catalytic subunit of human γ-secretase. eLife 4, 11182.
Schilbach S, Hantsche M, Tegunov D, Dienemann C, Wigge C, Urlaub H & Cramer P (2017) Structures of transcription pre-initiation complex with TFIIH and Mediator. Nature 551, 204-209.
Nakane T, Kimanius D, Lindahl E & Scheres SHW (2018) Characterisation of molecular motions in cryo-EM single-particle data by multi-body refinement in RELION. eLife 7, 36861.
Frank J & Ourmazd A (2016) Continuous changes in structure mapped by manifold embedding of single-particle data in cryo-EM. Methods 100, 61-67.
Nakasako M, Fujisawa T, Adachi S, Kudo T & Higuchi S (2001) Large-scale domain movements and hydration structure changes in the active-site cleft of unligated glutamate dehydrogenase from Thermococcus profundus studied by cryogenic X-ray crystal structure analysis and small-angle X-ray scattering. Biochemistry 40, 3069-3079.
Oroguchi T & Nakasako M (2016) Changes in hydration structure are necessary for collective motions of a multi-domain protein. Sci Rep 6, 26302.
Scheres SHW & Chen S (2012) Prevention of overfitting in cryo-EM structure determination. Nat Met 9, 853-854.
Scheres SHW (2012) RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180, 519-530.
Kitao A, Hayward S & Go N (1998) Energy landscape of a native protein: jumping-among-minima model. Proteins Struct Funct Genet 33, 496-517.
Gerstein M, Lesk AM & Chothia C (1994) Structural mechanisms for domain movements in proteins. Biochemistry 33, 6739-6749.
Zivanov J, Nakane T, Forsberg BO, Kimanius D, Hagen WJ, Lindahl E & Scheres SHW (2018) RELION- 3: new tools for automated high-resolution cryo-EM structure determination. eLife 7, e42166.
Colliex C, Cowley JM, Dudarev SL, Fink M, Gjønnes J, Hilderbrandt R, Howie A, Lynch DF, Peng LM, Ren Get al. (2006) Electron diffraction. In International Tables for Crystallography, Vol. C (Prince E ed), pp. 263-281. International Union of Crystallography, Chester.
Matsuoka D & Nakasako M (2009) Probability distributions of hydration water molecules around polar protein atoms obtained by a database analysis. J Phys Chem B 113, 11274-11292.
Matsuoka D & Nakasako M (2010) Prediction of hydration structures around hydrophilic surfaces of proteins by using the empirical hydration distribution functions from a database analysis. J Phys Chem B 114, 4652-4663.
Stillman TJ, Baker PJ, Britton KL & Rice DW (1993) Conformational flexibility in glutamate dehydrogenase: role of water in substrate recognition and catalysis. J Mol Biol 234, 1131-1139.
Sorzano COS, Jiménez A, Mota J, Vilas JL, Maluenda D, Martínez M, Ramírez-Aportela E, Majtner T, Segura J, Sánchez-Gracía R et al. (2019) Survey of the analysis of continuous conformational variability of biological macromolecules by electron microscopy. Acta Crystallogr F75, 19-32.
Shan H, Wang Z, Zhang F, Xiong Y, Yin CC & Sun F (2016) A local-optimization refinement algorithm in single particle analysis for macromolecular complex with multiple rigid modules. Protein Cell 7, 46-62.
Haselbach D, Komarov I, Agafonov DE, Hartmuth K, Graf B, Dybkov O, Urlaub H, Kastner B, Lührmann R & Stark H (2018) Structure and conformational dynamics of the human spliceosomal Bact complex. Cell 172, 1-11.
Arkhipov A, Freddolino PL, Imada K, Namba K & Schulten K (2006) Coarse-grained molecular dynamics simulations of a rotating bacterial flagellum. Biophys J 91, 4589-4597.
Sugita Y, Kitao A & Okamoto Y (2000) Multidimensional replica-exchange method for free-energy calculations. J Chem Phys 113, 6042-6051.
Harada R & Kitao A (2011) Nontargeted parallel cascade selection molecular dynamics for enhancing the conformational sampling of proteins. J Chem Theory Comp 8, 290-299.
Yoshidome T, Oroguchi T, Nakasako M & Ikeguchi M (2015) Classification of projection images of proteins with structural polymorphism by manifold: A simulation study for X-ray free-electron laser diffraction imaging. Phys Rev E 92, 032710.
Oroguchi T, Yoshidome T, Yamamoto T & Nakasako M (2018) Growth of cuprous oxide particles in liquid-phase synthesis investigated by X-ray laser diffraction. Nano Lett 18, 5192-5197.
Rasmussen BF, Stock AM, Ringe D & Petsko G (1992) Crystalline ribonuclease A loses function below the dynamical transition at 220 K. Nature 357, 423-424.
Ferrand M, Dianoux AJ, Petry W & 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 USA 90, 9668-9672.
Daniel RM, Finney JL, Réat V, Dunn R, Ferrand M & Smith JC (1999) Enzyme dynamics and activity: time-scale dependence of dynamical transition in glutamate dehydrogenase solution. Biophys J 77, 2184-2190.
Zheng SQ, Palovcak E, Armache JP, Verba KA, Cheng Y & Agard DA (2017) MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat Met 14, 331-332.
Zhang K (2016) Gctf: Real-time CTF determination and correction. J Struct Biol 193, 1-12.
Scheres SHW (2015) Semi-automated selection of cryo-EM particles in RELION-1.3. J Struct Biol 189, 114-122.
Kimanius D, Forsberg BO, Scheres SHW & Lindahl E (2016) Accelerated cryo-EM structure determination with parallelization using GPUs in RELION-2. eLife 5, e18722.
Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I & Ludtke SJ (2007) EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157, 38-46.
Chen S, McMullan G, Faruqi AR, Murshudov GN, Short JM, Scheres SHW & Henderson R (2013) High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy 135, 24-35.
Rosenthal PB & Henderson R (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron microscopy. J Mol Biol 333, 721-745.
Heymann JB (2018) Guidelines for using Bsoft for high resolution reconstruction and validation of biomolecular structures from electron micrographs. Protein Sci 27, 159-171.
Cardone G, Heymann JB & Steven AC (2013) One number does not fit all: Mapping local variations in resolution in cryo-EM reconstructions. J Struct Biol 184, 226-236.
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC & Ferrin TE (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.
Goddard TD, Huang CC & Ferring TE (2007) Visualizing density maps with UCSF Chimera. J Struct Biol 157, 281-287.
DeLano WL (2012) The PyMOL Molecular Graphics System, version 1.5.0.1. Schrödinger, LLC, New York, NY.
Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW & Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79, 926-935.
Ikeguchi M (2004) Partial rigid-body dynamics in NPT, NPAT and NPγT ensembles for proteins and membranes. J Comput Chem 25, 529-541.
MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102, 3586-3616.
Essmann U, Perera L, Berkowitz ML, Darden T, Lee H & Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103, 8577-8593.
Martyna GJ, Tobias DJ & Klein ML (1994) Constant pressure molecular dynamics algorithms. J Chem Phys 101, 4177-4189.
Emsley P, Lohkamp B, Scott WG & Cowtan K (2010) Features and development of coot. Acta Crystallogr D 66, 486-501.
Adam PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echol N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D 66, 213-221.
Afonine PV, Poon BK, Read RJ, Sobolev OV, Terwilliger TC, Urzhumtsev A & Adams PD (2018) Real-space refinement in PHENIX for cryo-EM and crystallography. Acta Crystallogr D 74, 531-544.
Contributed Indexing:: Keywords: cryo-electron microscopy; domain motion; energy landscape; glutamate dehydrogenase
Substance Nomenclature:: 0 (Archaeal Proteins)
EC 1.4.1.2 (Glutamate Dehydrogenase)
Entry Date(s):: Date Created: 20200125 Date Completed: 20210517 Latest Revision: 20210517
Update Code:: 20240104
DOI:: 10.1111/febs.15224
PMID:: 31976609
: Czasopismo naukowe

Pełny tekst

Analysis of the conformational changes of protein is important to elucidate the mechanisms of protein motions correlating with their function. Here, we studied the spontaneous domain motion of unliganded glutamate dehydrogenase from Thermococcus profundus using cryo-electron microscopy and proposed a novel method to construct free-energy landscape of protein conformations. Each subunit of the homo-hexameric enzyme comprises nucleotide-binding domain (NAD domain) and hexamer-forming core domain. A large active-site cleft is situated between the two domains and varies from open to close according to the motion of a NAD domain. A three-dimensional map reconstructed from all cryo-electron microscopy images displayed disordered volumes of NAD domains, suggesting that NAD domains in the collected images adopted various conformations in domain motion. Focused classifications on NAD domain of subunits provided several maps of possible conformations in domain motion. To deduce what kinds of conformations appeared in EM images, we developed a novel analysis method that describe the EM maps as a linear combination of representative conformations appearing in a 200-ns molecular dynamics simulation as reference. The analysis enabled us to estimate the appearance frequencies of the representative conformations, which illustrated a free-energy landscape in domain motion. In the open/close domain motion, two free-energy basins hindered the direct transformation from open to closed state. Structure models constructed for representative EM maps in classifications demonstrated the correlation between the energy landscape and conformations in domain motion. Based on the results, the domain motion in glutamate dehydrogenase and the analysis method to visualize conformational changes and free-energy landscape were discussed. DATABASE: The EM maps of the four conformations were deposited to Electron Microscopy Data Bank (EMDB) as accession codes EMD-9845 (open), EMD-9846 (half-open1), EMD-9847 (half-open2), and EMD-9848 (closed), respectively. In addition, the structural models built for the four conformations were deposited to the Protein Data Bank (PDB) as accession codes 6JN9 (open), 6JNA (half-open1), 6JNC (half-open2), and 6JND (closed), respectively.
(© 2020 Federation of European Biochemical Societies.)

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