The redundancy of NMR restraints can be used to accelerate the unfolding behavior of an SH3 domain during molecular dynamics simulations

BMC Structural Biology

Thérèse E Malliavin²  Michael Nilges²  Leandro Martínez¹  Nathalie Duclert-Savatier² 

[1] Instituto de Física de São Carlos, Universidade de São Paulo. Av. Trabalhador São-carlense 400, 13566-590 São Carlos, SP, Brasil;Institut Pasteur, CNRS URA 2185, Unité de Bioinformatique Structurale, 25-28 rue du Dr Roux, F-75724 Paris Cedex 15, France

关键词: contact order: Gaussian Network Model;    QUEEN;    molecular dynamics simulation;    SH3 domain;    protein folding;    NMR;   

Others  :  1092492
DOI  :  10.1186/1472-6807-11-46

 received in 2011-06-13, accepted in 2011-11-24,  发布年份 2011

【 授权许可】

   
2011 Duclert-Savatier et al; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Ding F, Dokholyan N, Buldyrev S, Stanley H, Shakhnovich E: Molecular dynamics simulation of the SH3 domain aggregation suggest a generic amyloidogenesis mechanism. J Mol Biol 2002, 324:851-857.
• [2]Hubner I, Edmonds K, Shakhnovich E: Nucleation and the transition state of the SH3 domain. J Mol Biol 2005, 349:424-434.
• [3]Day R, Bennion B, Ham S, Daggett V: Increasing temperature accelerates protein unfolding without changing the pathway of unfolding. J Mol Biol 2002, 322:189-203.
• [4]Gsponer J, Caflisch A: Role of Native Topology Investigated by Multiple Unfolding Simulations of Four SH3 Domains. J Mol Biol 2001, 309:285-298.
• [5]Gsponer J, Caflisch A: Molecular dynamics simulations of protein folding from the transition state. Proc Natl Acad Sci 2002, 99:6719-6724.
• [6]Settanni G, Gsponer J, Caflisch A: Formation of the folding nucleus of an SH3 do-main investigated by loosely coupled molecular dynamics simulations. Biophys J 2004, 86:1691-1701.
• [7]Settanni G, Rao F, Caflisch A: Φ-value analysis by molecular dynamics simulations of reversible folding. Proc Natl Acad Sci 2005, 102:628-633.
• [8]Parisi M, Bennett C, Eckert M, Dobyns W, Gleeson J, Shaw D, McDonald R, Eddy A, Chance P, Glass I: The NPHP1 gene deletion associated with juvenile nephronophthisis is present in a subset of individuals with Joubert syndrome. Am J Hum Genet 2004, 75:82-91.
• [9]le Maire A, Weber T, Saunier S, Broutin I, Antignac C, Ducruix A, Dardel F: Solution NMR structure of the SH3 domain of human nephrocystin and analysis of a mutation-causing juvenile nephronophthisis. Proteins 2005, 59:347-355.
• [10]DeLano W: The PyMOL Molecular Graphics System. [http://www.pymol.org] webcite 2002.
• [11]Nabuurs S, Spronk C, Krieger E, Maassen H, Vriend G, Vuister G: Quantitative evaluation of experimental NMR restraints. J Am Chem Soc 2003, 125:12026-12034.
• [12]Brunger APDA, Clore G, DeLano W, Gross P, Grosse-Kunstleve R, Jiang J, Kuszewski J, Nilges M, Pannu N, Read R, Rice L, Simonson T, Warren G: Crystal-lography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998, 54:905-921.
• [13]Rieping W, Habeck M, Bardiaux B, Bernard A, Malliavin T, Nilges M: ARIA2: automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 2006, 23:381-382.
• [14]Doreleijers J, Rullmann J, Kaptein R: Quality assessment of NMR structures: a statistical survey. J Mol Biol 1998, 281:149-164.
• [15]Laskowski R, MacArthur M, Moss D, Thornton J: PROCHECK: a program to check the stereochemical quality of protein structure. J Appl Cryst 1993, 26:283-291.
• [16]Hooft R, Vriend G, Sander C, Abola E: Errors in protein structures. Nature 1996, 381:272-272.
• [17]Case D, Darden T, Cheatham T, Simmerling C, Wang J, Duke R, Merz K, Wang B, Pearlman D, Crowley M, Brozell S, Tsui V, Gohlke H, Mongan J, Hornak V, Cui G, Beroza P, Schafmeister JW, Caldwell RossWS, Kollman P: AMBER 9. 2004.
• [18]Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C: Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 2006, 65:712-725.
• [19]Darden T, York D, Pedersen L: Particule mesh Ewald. J Chem Phys 1993, 98:10089-10092.
• [20]Loncharich R, Brooks B, Pastor R: Langevin dynamics of peptides: the fric-tional dependence of isomerization rates of N-acetylalanyl-N'-methylamide. Biopolymers 1992, 32:523-535.
• [21]Berendsen H, Postma J, van Gunsteren W, DiNola A, Haak J: Molecular dynamics with coupling to an external bath. J Chem Phys 1984, 81:3684-3690.
• [22]Ryckaert J, Ciccotti G, Berendsen H: Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of n-Alkanes. J Comp Phys 1977, 23:327-341.
• [23]Lee M, Duan Y, Kollman P: Use of MM-PB/SA in estimating the free energies of proteins: Application to native, intermediates, and unfolded vilin headpiece. Proteins 2000, 39:309-316.
• [24]Onufriev A, Bashford D, Case D: Exploring protein native states and large-scale conformational changes with a modified generalized Born model. Proteins 2004, 55:383-394.
• [25]Case D, Darden T, Cheatham T, Simmerling C, Wang J, Duke R, Merz K, Wang B, Pearlman D, Crowley M, Brozell S, Tsui V, Gohlke H, Mongan J, Hornak V, Cui G, Beroza P, Schafmeister JC, Caldwell , Ross W, Kollman P: AMBER 10 User's Manual. 2009.
• [26]Andreani R, Birgin E, Martinez J, Schuvert M: On Augmented Lagrangian Methods with general lower-level constraints. SIAM Journal on Optimization 2007, 18:1286-1309.
• [27]Andreani R, Birgin E, Martinez J, Schuvert M: Augmented Lagrangian methods under the Constant Positive Linear Dependence constraint qualification. Mathematical Programming 2008, 111:5-32.
• [28]Crippen G, Havel T: Distance Geometry and Molecular Conformation. 1988.
• [29]Plaxco K, Simons K, Baker D: Contact order, transition state placement and the refolding rates of single domain proteins. J Mol Biol 1998, 277:985-994.
• [30]Makarov D, Keller C, Plaxco K, Metiu H: How the folding rate constant of simple, single-domain proteins depends on the number of native contacts. Proc Natl Acad Sci USA 2002, 99:3535-3539.
• [31]Paci E, Lindorff-Larsen K, Dobson C, Karplus M, Vendruscolo M: Transition State Contact Orders Correlate with Protein Folding Rates. J Mol Biol 2005, 352:495-500.
• [32]Bonneau R, Ruczinski I, Tsai J, Baker D: Contact order and ab initio protein structure prediction. Protein Sci 2002, 11:1937-1944.
• [33]Mirny L, Shakhnovich E: Protein folding theory: from lattice to all-atom models. Ann Rev Biophys Biomolec Struct 2001, 30:361-396.
• [34]Dill K, Chan H: From Levinthal to pathways to funnels. Nature Structural Biology 1997, 4:10-19.
• [35]Shannon C: A Mathematical Theory of Communication. Bell System Technical Journal 1948, 27:379-423. & 623-656
• [36]Lee A, Wand A: Microscopic origins of entropy, heat capacity and the glass transition in proteins. Nature 2001, 411:501-504.
• [37]Yang D, Mok Y, Forman-Kay J, Farrow N, Kay L: Contributions to protein entropy and heat capacity from bond vector motions measured by NMR spin relaxation. J Mol Biol 1997, 272:790-804.
• [38]Bahar I, Wallqvist A, Covell D, Jernigan R: Correlation between native-state hydrogen exchange and cooperative residue fluctuations from a simple model. Biochemistry 1998, 37:1067-1075.
• [39]Bahar I, Altigan A, Erman B: Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Folding Des 1997, 2:173-181.
• [40]Su J, Li C, Hao R, Chen W, Wang C: Protein unfolding behavior studied by elastic network model. Biophys J 2008, 94:4586-4596.
• [41]Humphrey WAAD, Schulten K: VMD - Visual Molecular Dynamics. J Mol Graphics 1996, 14:333-38.
• [42]Periole X, Vendruscolo M, Mark A: Molecular dynamics simulations from putative transition states of alpha-spectrin SH3 domain. Proteins 2007, 69:536-550.
• [43]Lam A, Borreguero J, Ding F, Dokholyan N, Buldyrev S, Stanley H, Shakhnovich E: Parallel Folding Pathways in the SH3 Domain Protein. J Mol Biol 2007, 373:1348-1360.
• [44]Ding F, Guo W, Dokholyan N, Shakhnovich E, Shea J: Reconstruction of the src-SH3 Protein Domain Transition State Ensemble using Multiscale Molecular Dynamics Simulations. J Mol Biol 2005, 350:1035-1050.
• [45]Borreguero J, Ding F, Buldyrev S, Stanley H, Dokholyan N: Multiple folding pathways of the SH3 domain. Biophys J 2004, 87:521-533.
• [46]Ding F, Dokholyan N, Buldyrev S, Stanley H, Shakhnovich E: Molecular dynamics simulation of the SH3 domain aggregation suggests a generic amyloidogenesis mechanism. J Mol Biol 2002, 324:851-857.
• [47]Shea J, Onuchic JCB III: Probing the folding free energy landscape of the src-SH3 protein domain. Proc Natl Acad Sci 2002, 99:16064-16068.
• [48]Lindorff-Larsen K, Vendruscolo M, Paci E, Dobson C: Transition states for protein folding have native topologies despite high structural variability. Nature Struct Molec Biol 2004, 11:443-449.
• [49]Tollinger M, Neale C, Kay L, Forman-Kay J: Characterization of the Hydrodynamic Properties of the Folding Transition State of an SH3 Domain by Magnetization Transfer NMR Spectroscopy. Biochemistry 2006, 45:6434-6445.
• [50]Neudecker P, Zarrine-Afsar A, Davidson A, Kay L: Φ-Value analysis of a three-state protein folding pathway by NMR relaxation dispersion spectroscopy. Proc Natl Acad Sci 2007, 104:15717-15722.
• [51]Korzhnev D, Salvatella X, Vendruscolo M, Nardo AD, Davidson A, Dobson C, Kay L: Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 2004, 430:586-590.
• [52]Martinez J, Pisabarro M, Serrano L: Obligatory steps in protein folding and the conformational diversity of the transition state. Nature Struct Molec Biol 1998, 5:721-729.
• [53]Riddle D, Grantcharova V, Santiago J, Alm E, Ruczinski I, Baker D: Experiment and theory highlight role of native state topology in SH3 folding. Nature Struct Biol 1999, 6:1016-1024.
• [54]Lindorff-Larsen K, Paci E, Serrano L, Dobson C, Vendruscolo M: Calculation of mutational free energy changes in transition states for protein folding. Biophys J 2003, 85:1207-1214.
• [55]Guerois R, Serrano L: The SH3-fold family: experimental evidence and prediction of variations in the folding pathways. J Mol Biol 2000, 304:967-982.
• [56]Ding F, Dokholyan N, Buldyrev S, Stanley H, Shakhnovich E: Direct Molecular Dynamics Observation of Protein Folding Transition State Ensemble. Biophys J 2002, 83:3525-3532.
• [57]Mitomo D, Nakamura H, Ikeda K, Yamagishi A, Higo J: Transition State of a SH3 Domain Detected with Principle Component Analysis and a Charge Neutralized All-Atom Protein Model. PROTEINS: Structure, Function, and Bioinformatics 2006, 64:883-894.
• [58]Vendruscolo M, Paci E, Dobson C, Karplus M: Three key residues form a critical contact network in a protein folding transition state. Nature 2001, 409:641-645.
• [59]Tsai J, Levitt M, Baker D: Hierarchy of structure loss in MD simulations of src SH3 domain unfolding. J Mol Biol 1999, 291:215-225.
• [60]Krivov S, Karplus M: Hidden complexity of free energy surface for peptide (protein) folding. Proc Natl Acad Sci 2004, 101:14766-14770.
• [61]Gō N, Abe H: Noninteracting local-structure model of folding and unfolding transition in globular proteins. I. Formulation. Biopolymers 1981, 20:991-1011.
• [62]Kleiner A, Shakhnovich E: The mechanical unfolding of ubiquitin through all atom Monte Carlo simulation with a Gō-type potential. Biophysical J 2007, 92:2054-2061.
• [63]Vendruscolo M, Paci E, Dobson C, Karplus M: Rare fluctuations of native proteins sampled by equilibrium hydrogen exchange. J Am Chem Soc 2003, 125:15686-15687.
• [64]Laskowski R: PDBsum new things. Nucleic Acids Res 2009, 37:D355-359.