Conformational exchange of aromatic side chains characterized by L-optimized TROSY-selected 13C CPMG relaxation dispersion

Akke M, Palmer AG (1996) Monitoring macromolecular motions on microsecond–millisecond time scales by R1ρ–R1 constant-relaxation-time NMR spectroscopy. J Am Chem Soc 118:911–912 Baldwin AJ, Religa TL, Hansen DF, Bouvignies G, Kay LE (2010) 13CHD2 methyl group probes of millisecond time scale exchange in proteins by 1H relaxation dispersion: an application to proteasome gating residue dynamics. J Am Chem Soc 132:10992–10995 Bartlett GJ, Porter CT, Borkakoti N, Thornton JM (2002) Analysis of catalytic residues in enzyme active sites. J Mol Biol 324:105–121 Birtalan S, Fisher RD, Sidhu SS (2010) The functional capacity of the natural amino acids for molecular recognition. Mol Bio Syst 6:1186–1194 Boehr DD, McElheny D, Dyson HJ, Wright PE (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313:1638–1642 Bogan AA, Thorn KS (1998) Anatomy of hot spots in protein interfaces. J Mol Biol 280:1–9 Brath U, Akke M, Yang D, Kay LE, Mulder FAA (2006) Functional dynamics of human FKBP12 revealed by methyl 13C rotating frame relaxation dispersion NMR spectroscopy. J Am Chem Soc 128:5718–5727 Brüschweiler S, Schanda P, Kloiber K, Brutscher B, Kontaxis G, Konrat R, Tollinger M (2009) Direct observation of the dynamic process underlying allosteric signal transmission. J Am Chem Soc 131:3063–3068 Carr HY, Purcell EM (1954) Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 94:630–638 Carver JP, Richards RE (1972) A general two-site solution for the chemical exchange produced dependence of T2 upon the carr-purcell pulse separation. J Magn Reson 6:89–105 Cole R, Loria JP (2002) Evidence for flexibility in the function of ribonuclease A. Biochemistry 41:6072–6081 Diehl C, Engström O, Delaine T, Håkansson M, Genheden S, Modig K, Leffler H, Ryde U, Nilsson UJ, Akke M (2010) Protein flexibility and conformational entropy in ligand design targeting the carbohydrate recognition domain of galectin-3. J Am Chem Soc 132:14577–14589 Eisenmesser EZ, Bosco DA, Akke M, Kern D (2002) Enzyme dynamics during catalysis. Science 295:1520–1523 Eletsky A, Atreya HS, Liu GH, Szyperski T (2005) Probing structure and functional dynamics of (large) proteins with aromatic rings: L-GFT-TROSY (4, 3)D HCCHNMR spectroscopy. J Am Chem Soc 127:14578–14579 Geen H, Freeman R (1991) Band-selective radiofrequency pulses. J Magn Reson 93:93–141 Grey MJ, Tang YF, Alexov E, McKnight CJ, Raleigh DP, Palmer AG (2006) Characterizing a partially folded intermediate of the villin headpiece domain under non-denaturing conditions: contribution of His41 to the pH-dependent stability of the N-terminal subdomain. J Mol Biol 355:1078–1094 Gutowsky HS, Saika A (1953) Dissociation, chemical exchange, and the proton magnetic resonance in some aqueous electrolytes. J Chem Phys 21:1688–1694 Hansen AL, Kay LE (2011) Quantifying millisecond time-scale exchange in proteins by CPMG relaxation dispersion NMR spectroscopy of side-chain carbonyl groups. J Biomol NMR 50:347–355 Hansen DF, Vallurupalli P, Lundström P, Neudecker P, Kay LE (2008) Probing chemical shifts of invisible states of proteins with relaxation dispersion NMR spectroscopy: how well can we do? J Am Chem Soc 130:2667–2675 Hansen AL, Lundström P, Velyvis A, Kay LE (2012) Quantifying millisecond exchange dynamics in proteins by cpmg relaxation dispersion NMR using side-chain H-1 probes. J Am Chem Soc 134:3178–3189 Helgstrand M, Allard P (2004) QSim, a program for NMR simulations. J Biomol NMR 30:71–80 Hill RB, Bracken C, DeGrado WF, Palmer AG (2000) Molecular motions and protein folding: characterization of the backbone dynamics and folding equilibrium of alpha D-2 using C-13 NMR spin relaxation. J Am Chem Soc 122:11610–11619 Igumenova TI, Palmer AG (2006) Off-resonance TROSY-selected R1ρ experiment with improved sensitivity for medium—and high-molecular-weight proteins. J Am Chem Soc 128:8110–8111 Igumenova TI, Brath U, Akke M, Palmer AG (2007) Characterization of chemical exchange using residual dipolar coupling. J Am Chem Soc 129:13396–13397 Kay LE, Keifer P, Saarinen T (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J Am Chem Soc 114:10663–10665 Korzhnev DM, Religa TL, Banachewicz W, Fersht AR, Kay LE (2010) A transient and low-populated protein-folding intermediate at atomic resolution. Science 329:1312–1316 Lo Conte L, Chothia C, Janin J (1999) The atomic structure of protein–protein recognition sites. J Mol Biol 285:2177–2198 Loria JP, Rance M, Palmer AG (1999a) A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J Am Chem Soc 121:2331–2332 Loria JP, Rance M, Palmer AG (1999b) A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J Biomol NMR 15:151–155 Lundström P, Akke M (2005a) Microsecond protein dynamics measured by rotating-frame 13Ca spin relaxation. Chem Bio Chem 6:1685–1692 Lundström P, Akke M (2005b) Off-resonance rotating-frame amide proton spin relaxation experiments measuring microsecond chemical exchange in proteins. J Biomol NMR 32:163–173 Lundström P, Hansen DF, Kay LE (2008) Measurement of carbonyl chemical shifts of excited protein states by relaxation dispersion NMR spectroscopy: comparison between uniformly and selectively 13C labeled samples. J Biomol NMR 42:35–47 Lundström P, Hansen DF, Vallurupalli P, Kay LE (2009a) Accurate measurement of alpha proton chemical shifts of excited protein states by relaxation dispersion NMR spectroscopy. J Am Chem Soc 131:1915–1926 Lundström P, Lin H, Kay LE (2009b) Measuring 13Cβ chemical shifts of invisible excited states in proteins by relaxation dispersion NMR spectroscopy. J Biomol NMR 44:139–155 Lundström P, Teilum K, Carstensen T, Bezsonova I, Wiesner S, Hansen F, Religa TL, Akke M, Kay LE (2007) Fractional 13C enrichment of isolated carbons using [1–13C]- or [2–13C]-glucose facilitates the accurate measurement of dynamics at backbone Cα and side-chain methyl positions in proteins. J Biomol NMR 38:122–199 Malmendal A, Evenäs J, Forsén S, Akke M (1999) Structural dynamics in the C-terminal domain of calmodulin at low calcium levels. J Mol Biol 293:883–899 Meiboom S, Gill D (1958) Modified spin-echo method for measuring nuclear spin relaxation times. Rev Sci Instrum 29:688–691 Mulder FAA, Akke M (2003) Carbonyl 13C transverse relaxation measurements to sample protein backbone dynamics. Magn Reson Chem 41:853–865 Mulder FAA, Hon B, Mittermaier A, Dahlquist FW, Kay LE (2002) Slow internal dynamics in proteins: application of NMR relaxation dispersion spectroscopy to methyl groups in a cavity mutant of T4 lysozyme. J Am Chem Soc 124:1443–1451 Neudecker P, Zarrine-Afsar A, Choy WY, Muhandiram DR, Davidson AR, Kay LE (2006) Identification of a collapsed intermediate with non-native long-range interactions on the folding pathway of a pair of Fyn SH3 domain mutants by NMR relaxation dispersion spectroscopy. J Mol Biol 363:958–976 O’Connell NE, Grey MJ, Tang YF, Kosuri P, Miloushev VZ, Raleigh DP, Palmer AG (2009) Partially folded equilibrium intermediate of the villin headpiece HP67 defined by 13C relaxation dispersion. J Biomol NMR 45:85–98 Otten R, Villali J, Kern D, Mulder FAA (2010) Probing microsecond time scale dynamics in proteins by methyl 1H Carr-Purcell-Meiboom-Gill relaxation dispersion NMR measurements. Application to activation of the signaling protein NtrCr. J Am Chem Soc 132:17004–17014 Palmer AG, Cavanagh J, Wright PE, Rance M (1991) Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J Magn Reson 93:151–170 Palmer AG, Kroenke CD, Loria JP (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Meth Enz 339:204–238 Paquin R, Ferrage F, Mulder FAA, Akke M, Bodenhausen G (2008) Multiple-timescale dynamics of side-chain carboxyl and carbonyl groups in proteins by C-13 nuclear spin relaxation. J Am Chem Soc 130:15805 Pervushin K, Riek R, Wider G, Wüthrich K (1998) Transverse relaxation-optimized spectroscopy (TROSY) for NMR studies of aromatic spin systems in 13C-labeled proteins. J Am Chem Soc 120:6394–6400 Pervushin K, Vögeli B, Eletsky A (2002) Longitudinal H-1 relaxation optimization in TROSY NMR spectroscopy. J Am Chem Soc 124:12898–12902 Schindler T, Herrler M, Marahiel MA, Schmid FX (1995) Extremely rapid protein-folding in the absence of intermediates. Nat Struct Biol 2:663–673 Shaka AJ, Barker PB, Freeman R (1985) Computer-optimized decoupling scheme for wideband applications and low-level operation. J Magn Reson 64:547–552 Sprangers R, Gribun A, Hwang PM, Houry WA, Kay LE (2005) Quantitative NMR spectroscopy of supramolecular complexes: dynamic side pores in ClpP are important for product release. Proc Natl Acad Sci USA 102:16678–16683 Teilum K, Brath U, Lundström P, Akke M (2006a) Biosynthetic 13C labeling of aromatic side-chains in proteins for NMR relaxation measurements. J Am Chem Soc 128:2506–2507 Teilum K, Poulsen FM, Akke M (2006b) The inverted chevron plot measured by NMR relaxation reveals a native-like unfolding intermediate in acyl-coA binding protein. Proc Natl Acad Sci USA 103:6877–6882 Vallurupalli P, Hansen DF, Stollar E, Meirovitch E, Kay LE (2007) Measurement of bond vector orientations in invisible excited states of proteins. Procm Natl Acad Sci USA 104:18473–18477 van Ingen H, Korzhnev DM, Kay LE (2009) An analysis of the effects of 1HN-1HN dipolar couplings on the measurement of amide bond vector orientations in invisible protein states by relaxation dispersion NMR. J Phys Chem B 113:9968–9977 Veeman WS (1984) Carbon-13 chemical shift anisotropy. Prog NMR Spectrosc 16:193–235 Weininger U, Diehl C, Akke M (2012) 13C relaxation experiments for aromatic side chains by longitudinal- and transverse-relaxation optimized NMR spectroscopy. J Biomol NMR. doi:10.1007/s10858-012-9650-5 Wüthrich K, Wagner G (1975) NMR investigations of the dynamics of the aromatic amino acid residues in the basic pancreatic trypsin inhibitor. FEBS Lett 50:265–268 Zeeb M, Balbach J (2005) NMR spectroscopic characterization of millisecond protein folding by transverse relaxation dispersion measurements. J Am Chem Soc 127:13207–13212