Multi-Timescale Dynamics Study of FKBP12 Along the Rapamycin–mTOR Binding Coordinate

Journal of Molecular Biology - Tập 405 - Trang 378-394 - 2011
Paul J. Sapienza1, Randall V. Mauldin2, Andrew L. Lee1,2
1Division of Medicinal Chemistry and Natural Products, Eshelman School of Pharmacy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
2Department of Biochemistry and Biophysics, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA

Tài liệu tham khảo

Frederick, 2007, Conformational entropy in molecular recognition by proteins, Nature, 448, 325, 10.1038/nature05959 Petit, 2009, Hidden dynamic allostery in a PDZ domain, Proc. Natl Acad. Sci. USA, 106, 18249, 10.1073/pnas.0904492106 Tzeng, 2009, Dynamic activation of an allosteric regulatory protein, Nature, 462, 368, 10.1038/nature08560 Marlow, 2010, The role of conformational entropy in molecular recognition by calmodulin, Nat. Chem. Biol., 6, 352, 10.1038/nchembio.347 Volkman, 2001, Two-state allosteric behavior in a single-domain signaling protein, Science, 291, 2429, 10.1126/science.291.5512.2429 Zhang, 2009, Domain-elongation NMR spectroscopy yields new insights into RNA dynamics and adaptive recognition, RNA, 15, 1941, 10.1261/rna.1806909 Boehr, 2006, The dynamic energy landscape of dihydrofolate reductase catalysis, Science, 313, 1638, 10.1126/science.1130258 Eisenmesser, 2002, Enzyme dynamics during catalysis, Science, 295, 1520, 10.1126/science.1066176 Eisenmesser, 2005, Intrinsic dynamics of an enzyme underlies catalysis, Nature, 438, 117, 10.1038/nature04105 Watt, 2007, The mechanism of rate-limiting motions in enzyme function, Proc. Natl Acad. Sci. USA, 104, 11981, 10.1073/pnas.0702551104 Foloppe, 2009, Conformational sampling and energetics of drug-like molecules, Curr. Med. Chem., 16, 3381, 10.2174/092986709789057680 Perola, 2004, Conformational analysis of drug-like molecules bound to proteins: an extensive study of ligand reorganization upon binding, J. Med. Chem., 47, 2499, 10.1021/jm030563w Siekierka, 1989, A cytosolic binding protein for the immunosuppressant FK506 has peptidyl–prolyl isomerase activity but is distinct from cyclophilin, Nature, 341, 755, 10.1038/341755a0 Siekierka, 1989, FK-506, a potent novel immunosuppressive agent, binds to a cytosolic protein which is distinct from the cyclosporin A-binding protein, cyclophilin, J. Immunol., 143, 1580, 10.4049/jimmunol.143.5.1580 Bierer, 1990, Two distinct signal transmission pathways in T lymphocytes are inhibited by complexes formed between an immunophilin and either FK506 or rapamycin, Proc. Natl Acad. Sci. USA, 87, 9231, 10.1073/pnas.87.23.9231 Harding, 1989, A receptor for the immunosuppressant FK506 is a cis–trans peptidyl–prolyl isomerase, Nature, 341, 758, 10.1038/341758a0 Bierer, 1990, Probing immunosuppressant action with a nonnatural immunophilin ligand, Science, 250, 556, 10.1126/science.1700475 Griffith, 1995, X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12–FK506 complex, Cell, 82, 507, 10.1016/0092-8674(95)90439-5 Heitman, 1991, Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast, Science, 253, 905, 10.1126/science.1715094 Liu, 1991, Calcineurin is a common target of cyclophilin–cyclosporin A and FKBP–FK506 complexes, Cell, 66, 807, 10.1016/0092-8674(91)90124-H Brown, 1994, A mammalian protein targeted by G1-arresting rapamycin–receptor complex, Nature, 369, 756, 10.1038/369756a0 Janus, 2005, The mammalian target of the rapamycin (mTOR) kinase pathway: its role in tumourigenesis and targeted antitumour therapy, Cell. Mol. Biol. Lett., 10, 479 Easton, 2006, mTOR and cancer therapy, Oncogene, 25, 6436, 10.1038/sj.onc.1209886 Okuno, 2006, Mammalian target of rapamycin inhibitors in sarcomas, Curr. Opin. Oncol., 18, 360, 10.1097/01.cco.0000228742.72165.cf Chen, 1995, Identification of an 11-kDa FKBP12–rapamycin-binding domain within the 289-kDa FKBP12–rapamycin-associated protein and characterization of a critical serine residue, Proc. Natl Acad. Sci. USA, 92, 4947, 10.1073/pnas.92.11.4947 Lorenz, 1995, TOR mutations confer rapamycin resistance by preventing interaction with FKBP12–rapamycin, J. Biol. Chem., 270, 27531, 10.1074/jbc.270.46.27531 Lipari, 1982, Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules: 1. Theory and range of validity, J. Am. Chem. Soc., 104, 4546, 10.1021/ja00381a009 Lipari, 1982, Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules: 2. Analysis of experimental results, J. Am. Chem. Soc., 104, 4559, 10.1021/ja00381a010 Keating, 2009, StoneHinge: hinge prediction by network analysis of individual protein structures, Protein Sci., 18, 359, 10.1002/pro.38 Choi, 1996, Structure of the FKBP12–rapamycin complex interacting with the binding domain of human FRAP, Science, 273, 239, 10.1126/science.273.5272.239 Liang, 1999, Refined structure of the FKBP12–rapamycin–FRB ternary complex at 2.2 Å resolution, Acta Crystallogr. Sect. D, 55, 736, 10.1107/S0907444998014747 Igumenova, 2006, Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution, Chem. Rev., 106, 1672, 10.1021/cr040422h Muhandiram, 1995, Measurement of H-2 T-1 and T-1p relaxation-times in uniformly C-13-labeled and fractionally H-2-labeled proteins in solution, J. Am. Chem. Soc., 117, 11536, 10.1021/ja00151a018 Millet, 2002, Deuterium spin probes of side-chain dynamics in proteins: 1. Measurement of five relaxation rates per deuteron in (13)C-labeled and fractionally (2)H-enriched proteins in solution, J. Am. Chem. Soc., 124, 6439, 10.1021/ja012497y Clarkson, 2004, Long-range dynamic effects of point mutations propagate through side chains in the serine protease inhibitor eglin c, Biochemistry, 43, 12448, 10.1021/bi0494424 Lee, 2000, Redistribution and loss of side chain entropy upon formation of a calmodulin–peptide complex, Nat. Struct. Biol., 7, 72, 10.1038/71280 Millet, 2003, The effects of mutations on motions of side-chains in protein L studied by 2H NMR dynamics and scalar couplings, J. Mol. Biol., 329, 551, 10.1016/S0022-2836(03)00471-6 Namanja, 2007, Substrate recognition reduces side-chain flexibility for conserved hydrophobic residues in human Pin1, Structure, 15, 313, 10.1016/j.str.2007.01.014 Teilum, 2006, Biosynthetic 13C labeling of aromatic side chains in proteins for NMR relaxation measurements, J. Am. Chem. Soc., 128, 2506, 10.1021/ja055660o Boyer, 2008, Monitoring aromatic picosecond to nanosecond dynamics in proteins via 13C relaxation: expanding perturbation mapping of the rigidifying core mutation, V54A, in eglin c, Biochemistry, 47, 4876, 10.1021/bi702330t Clore, 1990, Deviations from the simple 2-parameter model-free approach to the interpretation of N-15 nuclear magnetic-relaxation of proteins, J. Am. Chem. Soc., 112, 4989, 10.1021/ja00168a070 d'Auvergne, 2003, The use of model selection in the model-free analysis of protein dynamics, J. Biomol. NMR, 25, 25, 10.1023/A:1021902006114 Mandel, 1995, Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme, J. Mol. Biol., 246, 144, 10.1006/jmbi.1994.0073 Jin, 1998, Propagation of experimental uncertainties using the Lipari–Szabo model-free analysis of protein dynamics, J. Biomol. NMR, 12, 471, 10.1023/A:1008313319334 Hubbard, 1993 Brath, 2009, Differential responses of the backbone and side-chain conformational dynamics in FKBP12 upon binding the transition-state analog FK506: implications for transition-state stabilization and target protein recognition, J. Mol. Biol., 387, 233, 10.1016/j.jmb.2009.01.047 Brath, 2006, Functional dynamics of human FKBP12 revealed by methyl 13C rotating frame relaxation dispersion NMR spectroscopy, J. Am. Chem. Soc., 128, 5718, 10.1021/ja0570279 Loria, 1999, A TROSY CPMG sequence for characterizing chemical exchange in large proteins, J. Biomol. NMR, 15, 151, 10.1023/A:1008355631073 Palmer, 2001, Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules, Methods Enzymol., 339, 204, 10.1016/S0076-6879(01)39315-1 Yang, 1996, Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: application to protein folding, J. Mol. Biol., 263, 369, 10.1006/jmbi.1996.0581 Recht, 2001, Central domain assembly: thermodynamics and kinetics of S6 and S18 binding to an S15–RNA complex, J. Mol. Biol., 313, 35, 10.1006/jmbi.2001.5018 Li, 2006, A mutation in the S-switch region of the Runt domain alters the dynamics of an allosteric network responsible for CBFbeta regulation, J. Mol. Biol., 364, 1073, 10.1016/j.jmb.2006.10.002 McAlpine, 1991, Revised NMR assignments for rapamycin, J. Antibiot. (Tokyo), 44, 688, 10.7164/antibiotics.44.688 Nishikawa, 1994, Reversible isomerization of rapamycin demonstrated by liquid chromatography, J. Antibiot. (Tokyo), 47, 1554, 10.7164/antibiotics.47.1554 Lindorff-Larsen, 2005, Simultaneous determination of protein structure and dynamics, Nature, 433, 128, 10.1038/nature03199 Materese, 2008, Hierarchical organization of eglin c native state dynamics is shaped by competing direct and water-mediated interactions, Proc. Natl Acad. Sci. USA, 105, 10659, 10.1073/pnas.0801850105 Hamelberg, 2004, Accelerated molecular dynamics: a promising and efficient simulation method for biomolecules, J. Chem. Phys., 120, 11919, 10.1063/1.1755656 Fraser, 2009, Hidden alternative structures of proline isomerase essential for catalysis, Nature, 462, 669, 10.1038/nature08615 Rosen, 1990, Inhibition of FKBP rotamase activity by immunosuppressant FK506: twisted amide surrogate, Science, 248, 863, 10.1126/science.1693013 Mauldin, 2009, Dynamic dysfunction in dihydrofolate reductase results from antifolate drug binding: modulation of dynamics within a structural state, Structure, 17, 386, 10.1016/j.str.2009.01.005 Henzler-Wildman, 2007, A hierarchy of timescales in protein dynamics is linked to enzyme catalysis, Nature, 450, 913, 10.1038/nature06407 Wittekind, 1993, HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha-carbon and beta-carbon resonances in proteins, J. Magn. Reson. Ser. B, 101, 201, 10.1006/jmrb.1993.1033 Muhandiram, 1994, Gradient-enhanced triple-resonance 3-dimensional NMR experiments with improved sensitivity, J. Magn. Reson. Ser. B, 103, 203, 10.1006/jmrb.1994.1032 Uhrin, 2000, 3D HCCH3-TOCSY for resonance assignment of methyl-containing side chains in C-13-labeled proteins, J. Magn. Reson., 142, 288, 10.1006/jmre.1999.1951 Bax, 1994, Resonance assignment of methionine methyl groups and chi 3 angular information from long-range proton–carbon and carbon–carbon J correlation in a calmodulin–peptide complex, J. Biomol. NMR, 4, 787, 10.1007/BF00398409 Yamazaki, 1993, 2-Dimensional NMR experiments for correlating C-13-beta and H-1-delta/epsilon chemical-shifts of aromatic residues in C-13-labeled proteins via scalar couplings, J. Am. Chem. Soc., 115, 11054, 10.1021/ja00076a099 Farrow, 1994, Backbone dynamics of a free and a phosphopeptide-complexed Src homology-2 domain studied by N-15 NMR relaxation, Biochemistry, 33, 5984, 10.1021/bi00185a040 Dosset, 2000, Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data, J. Biomol. NMR, 16, 23, 10.1023/A:1008305808620 Lee, 1997, Rotational diffusion anisotropy of proteins from simultaneous analysis of 15N and 13C alpha nuclear spin relaxation, J. Biomol. NMR, 9, 287, 10.1023/A:1018631009583 Fuentes, 2004, Ligand-dependent dynamics and intramolecular signaling in a PDZ domain, J. Mol. Biol., 335, 1105, 10.1016/j.jmb.2003.11.010 Bremi, 1994, Side-chain motion with 2 degrees of freedom in peptides—an NMR-study of phenylalanine side-chains in antamanide, J. Phys. Chem., 98, 9322, 10.1021/j100088a038 LeMaster, 1996, Dynamical mapping of E. coli thioredoxin via C-13 NMR relaxation analysis, J. Am. Chem. Soc., 118, 9255, 10.1021/ja960877r Palmer, 1993, Characterization of amino-acid side-chain dynamics in a zinc-finger peptide using C-13 NMR-spectroscopy and time-resolved fluorescence spectroscopy, J. Am. Chem. Soc., 115, 6333, 10.1021/ja00067a057 Delaglio, 1995, NMRPipe—a multidimensional spectral processing system based on Unix pipes, J. Biomol. NMR, 6, 277, 10.1007/BF00197809 Mulder, 2001, Measurement of slow (μs–ms) time scale dynamics in protein side chains by N-15 relaxation dispersion NMR spectroscopy: application to Asn and Gln residues in a cavity mutant of T4 lysozyme, J. Am. Chem. Soc., 123, 967, 10.1021/ja003447g