13C relaxation experiments for aromatic side chains employing longitudinal-and transverse-relaxationoptimized NMR spectroscopy

Journal of Biomolecular NMR

Volumn 53, Issue 3, 2012, Pages 181-190

  Weininger, Ulrich ^a   Diehl, Carl ^a   Akke, Mikael ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Aromatic side chain; Protein dynamics; Relaxation; Sensitivity enhancement; TROSY

Indexed keywords

AROMATIC COMPOUND; CARBON 13; HYDROGEN; CARBON; HISTAMINE; PHENYLALANINE; PROTEIN; TYROSINE;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONFORMATIONAL TRANSITION; ISOTOPE LABELING; MAGNETIC FIELD; MAGNETISM; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; SIGNAL NOISE RATIO; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; METHODOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

BINDING SITES; CARBON ISOTOPES; HISTAMINE; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHENYLALANINE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEINS; TYROSINE;

EID: 84865179944     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-012-9650-5     Document Type: Article

References (45)

1. Bartlett GJ, Porter CT, Borkakoti N, Thornton JM (2002) Analysis of catalytic residues in enzyme active sites. J Mol Biol 324: 105-121 (Pubitemid 35352183)
2. Berglund H, Baumann H, Knapp S, Ladenstein R, Härd T (1995) Flexibility of an arginine side chain at a DNA-protein interface. J Am Chem Soc 117:12883-12884 (Pubitemid 126635389)
3. Birtalan S, Fisher RD, Sidhu SS (2010) The functional capacity of the natural amino acids for molecular recognition. Mol BioSyst 6: 1186-1194
4. Bogan AA, Thorn KS (1998) Anatomy of hot spots in protein interfaces. J Mol Biol 280:1-9 (Pubitemid 28312802)
5. Boyd J (1995) Measurement of 15N relaxation data from the side chains of asparagine and glutamine residues in proteins. J Magn Reson B 107:279-285
6. Boyer JA, Lee AL (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 47:4876-4886 (Pubitemid 351574994)
7. Cavanagh J, Fairbrother WJ, Palmer AG, Rance M, Skelton NJ (2007) Protein NMR spectroscopy: principles and practice. Elsevier Academic Press, San Diego
8. Chen K, Tjandra N (2011) Water proton spin saturation affects measured protein backbone 15N spin relaxation rates. J Magn Reson 213:151-157
9. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293
10. Diehl C, Genheden S, Modig K, Ryde U, Akke M (2009) Conformational entropy changes upon lactose binding to the carbohydrate recognition domain of galectin-3. J Biomol NMR 45: 157-169
11. Diehl C, Engström O, Delaine T, Hakansson 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
12. 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 (Pubitemid 41510991)
13. Ferrage F, Piserchio A, Cowburn D, Ghose R (2008) On the measurement of N-15-{H-1} nuclear Overhauser effects. J Magn Reson 192:302-313
14. Ferrage F, Cowburn D, Ghose R (2009) Accurate sampling of highfrequency motions in proteins by steady-state N-15-{H-1} nuclear Overhauser effect measurements in the presence of cross-correlated relaxation. J Am Chem Soc 131:6048-6049
15. Geen H, Freeman R (1991) Band-selective radiofrequency pulses. J Magn Reson 93:93-141
16. Igumenova TI, Frederick KK, Wand AJ (2006) Characterization of the fast dynamics of protein amino acid side chains using NMR relaxation in solution. Chem Rev 106:1672-1699 (Pubitemid 43792776)
17. Ishima R, Petkova AP, Louis JM, Torchia DA (2001) Comparison of methyl rotation axis order parameters derived from model-free analyses of H-2 and C-13 longitudinal and transverse relaxation rates measured in the same protein sample. J Am Chem Soc 123:6164-6171 (Pubitemid 32888486)
18. Iwahara J, Jung YS, Clore GM (2007) Heteronuclear NMR spectroscopy for lysine NH3 groups in proteins: unique effect of water exchange on N-15 transverse relaxation. J Am Chem Soc 129:2971-2980 (Pubitemid 46417975)
19. Jarymowycz VA, Stone MJ (2006) Fast time scale dynamics of protein backbones: NMR relaxation methods, applications, and functional consequences. Chem Rev 106:1624-1671 (Pubitemid 43792775)
20. Johnson BA, Blevins RA (1994) NMRView: a computer program for the visualization and analysis of NMR data. J Biomol NMR 4:603-614
21. Kaski J, Vaara J, Jokisaari J (1996) C-13-C-13 spin-spin coupling tensors in benzene as determined experimentally by liquid crystal NMR and theoretically by ab initio calculations. J Am Chem Soc 118:8879-8886 (Pubitemid 26325146)
22. 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
23. Kupce E, Boyd J, Campbell ID (1995) Short selective pulses for biochemical applications. J Magn Reson B 106:300-303
24. Levy RM, Sheridan RP (1983) Combined effect of restricted rotational diffusion plus jumps on nuclear magnetic resonance and fluorescence probes of aromatic ring motions in proteins. Biophys J 41:217-221
25. Lo Conte L, Chothia C, Janin J (1999) The atomic structure of protein-protein recognition sites. J Mol Biol 285:2177-2198 (Pubitemid 29078179)
26. 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 Ca and side-chain methyl positions in proteins. J Biomol NMR 38:199-222
27. Millet O, Muhandiram DR, Skrynnikov NR, Kay LE (2002) Deuterium spin probes of side-chain dynamics in proteins. 1. Measurement of five relaxation rates per deuteron in 13C-labeled and fractionally 2H-enriched proteins in solution. J Am Chem Soc 124:6439-6448 (Pubitemid 34579397)
28. Muhandiram DR, Yamazaki T, Sykes BD, Kay LE (1995) Measurement of 2H T1 and T1q relaxation times in uniformly 13C-labeled and fractionally 2H-labeled proteins in solution. J Am Chem Soc 117:11536-11544 (Pubitemid 3006291)
29. Palmer AG (2004) NMR characterization of the dynamics of biomacromolecules. Chem Rev 104:3623-3640
30. 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
31. Palmer AG, Hochstrasser RA, Millar DP, Rance M, Wright PE (1993) Characterization of amino acid side chain dynamics in a zincfinger peptide using 13C NMR spectroscopy and time-resolved fluorescence spectroscopy. J Am Chem Soc 115:6333-6345
32. 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?
33. Pervushin K, Riek R, Wider G, Wüthrich K (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci USA 94:12366-12371
34. 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 (Pubitemid 28346415)
35. Pervushin K, Vogeli B, Eletsky A (2002) Longitudinal H-1 relaxation optimization in TROSY NMR spectroscopy. J Am Chem Soc 124:12898-12902 (Pubitemid 35216013)
36. Sapienza PJ, Mauldin RV, Lee AL (2011) Multi-timescale dynamics study of FKBP12 along the rapamycin-mTOR binding coordinate. J Mol Biol 405:378-394
37. Separovic F, Hayamizu K, Smith R, Cornell BA (1991) C-13 chemical-shift tensor of L-tryptophan and its application to polypeptide structure determination. Chem Phys Lett 181: 157-162
38. Separovic F, Ashida J, Woolf T, Smith R, Terao T (1999) Determination of chemical shielding tensor of an indole carbon and application to tryptophan orientation of a membrane peptide. Chem Phys Lett 303:493-498 (Pubitemid 129593917)
39. Sklenar V, Piotto M, Leppik R, Saudek V (1993) Gradient-tailored water suppression for H-1-N-15 Hsqc experiments optimized to retain full sensitivity. J Magn Reson A 102:241-245
40. Teilum K, Brath U, Lundström P, Akke M (2006) Biosynthetic 13C labeling of aromatic side-chains in proteins for NMR relaxation measurements. J Am Chem Soc 128:2506-2507 (Pubitemid 43327906)
41. Veeman WS (1984) Carbon-13 chemical shift anisotropy. Prog NMR Spectrosc 16:193-235
42. Witanowski M, Kamienska-Trela K, Biedrzycka Z (2007) Indirect carbon-carbon couplings across one, two and three bonds in substituted benzenes: experiment and theory. J Mol Struct 844: 13-20 (Pubitemid 47576103)
43. 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
44. Yang DW, Mittermaier A, Mok YK, Kay LE (1998) A study of protein side-chain dynamics from new H-2 auto-correlation and C-13 cross-correlation NMR experiments: application to the N-terminal SH3 domain from drk. J Mol Biol 276:939-954 (Pubitemid 28130266)
45. Yip GNB, Zuiderweg ERP (2004) A phase cycle scheme that significantly suppresses offset-dependent artifacts in the R-2- CPMG N-15 relaxation experiment. J Magn Reson 171:25-36