Use of H/D isotope effects to gather information about hydrogen bonding and hydrogen exchange rates

Journal of Magnetic Resonance

Volumn 241, Issue 1, 2014, Pages 148-154

  Takeda, Mitsuhiro ^a   Miyanoiri, Yohei ^a   Terauchi, Tsutomu ^b,c   Yang, Chun Jiun ^a   Kainosho, Masatsune ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b TOKYO METROPOLITAN UNIVERSITY   (Japan)

^c SAIL Technologies Co Inc   (Japan)

Author keywords

13C chemical shifts; H D isotope effect; Hydrogen bonding; Hydrogen exchange rate; Isotope labeling

Indexed keywords

AMINO ACIDS; ATOMS; CARRIER MOBILITY; CHAINS; DEUTERIUM; FINANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS; PROTONS;

BIOLOGICAL FUNCTIONS; BIOLOGICAL IMPLICATIONS; EXCHANGEABLE PROTONS; HYDROGEN EXCHANGE; HYDROGEN-DEUTERIUM EXCHANGE; ISOTOPE EFFECT; ISOTOPE LABELING; THREE-DIMENSIONAL STRUCTURE;

HYDROGEN BONDS;

CARBON; DEUTERIUM; DEUTERIUM OXIDE; PROTEIN; PROTON;

13C-CHEMICAL SHIFTS; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; DEUTERIUM HYDROGEN EXCHANGE; H/D ISOTOPE EFFECT; HYDROGEN BOND; HYDROGEN EXCHANGE RATE; ISOTOPE LABELING; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION;

13C-CHEMICAL SHIFTS; H/D ISOTOPE EFFECT; HYDROGEN BONDING; HYDROGEN EXCHANGE RATE; ISOTOPE LABELING;

CARBON ISOTOPES; DEUTERIUM; DEUTERIUM EXCHANGE MEASUREMENT; DEUTERIUM OXIDE; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS; PROTONS;

EID: 84896985217     PISSN: 10907807     EISSN: 10960856     Source Type: Journal    
DOI: 10.1016/j.jmr.2013.10.001     Document Type: Article

References (51)

1. S. Ohki, and M. Kainosho Stable isotope labeling methods for protein NMR spectroscopy Prog. Nucl. Magn. Reson. Spectrosc. 53 2008 208 226
2. M. Kainosho, T. Torizawa, Y. Iwashita, T. Terauchi, A.M. Ono, and P. Güntert Optimal isotope labelling for NMR protein structure determinations Nature 440 2006 52 57 (Pubitemid 43336263)
3. M. Kainosho, and P. Güntert SAIL-stereo-array isotope labeling Quart. Rev. Biophys. 42 2009 247 300
4. K. Linderstrom-Lang Deuterium exchange between peptides and water Chem. Soc. Spec. Publ. 2 1955 1 20
5. A. Hvidt, and S.O. Nielsen Hydrogen exchange in proteins Adv. Protein Chem. 21 1966 287 386
6. S.W. Englander, N.W. Downer, and H. Teitelbaum Hydrogen exchange Ann. Rev. Biochem. 41 1972 903 924
7. C. Woodward, I. Simon, and E. Tuchsen Hydrogen exchange and the dynamic structure of proteins Mol. Cell. Biochem. 48 1982 135 160
8. G. Wagner, and K. Wüthrich Structural interpretation of the amide proton exchange in the basic pancreatic trypsin inhibitor and related proteins J. Mol. Biol. 134 1979 75 94
9. G. Otting, and K. Wüthrich Studies of protein hydration in aqueous solution by direct NMR observation of individual protein-bound water molecules J. Am. Chem. Soc. 111 1989 1871 1875
10. E. Liepinsh, G. Otting, and K. Wüthrich NMR spectroscopy of hydroxyl protons in aqueous solutions of peptides and proteins J. Biomol. NMR 2 1992 447 465
11. E. Liepinsh, and G. Otting Proton exchange rates from amino acid side chains - implications for image contrast Magn. Reson. Med. 35 1996 30 42 (Pubitemid 26017917)
12. G. Otting, E. Liepinsh, and K. Wüthrich Proton exchange with internal water molecules in the protein BPTI in aqueous solution J. Am. Chem. Soc. 113 1991 4363 4364
13. Y. Takayama, C.A. Castañeda, M. Chimenti, B. García-Moreno, and J. Iwahara Direct evidence for deprotonation of a lysine side chain buried in the hydrophobic core of a protein J. Am. Chem. Soc. 130 2008 6714 6715 (Pubitemid 351748401)
14. F. Löhr, S.G. Mayhew, and H. Rüterjans Detection of scalar couplings across NH...OP and OH...OP hydrogen bonds in a flavoprotein J. Am. Chem. Soc. 122 2000 9289 9295
15. M.J. Plevin, I. Hayashi, and M. Ikura Characterization of a conserved "Threonine Clasp" in CAP-Gly domains: role of a functionally critical OH/π interaction in protein recognition J. Am. Chem. Soc. 130 2008 14918 14919
16. S.J. Baturin, M. Okon, and L.P. McIntosh Structure, dynamics, and ionization equilibria of the tyrosine residues in Bacillus circulans xylanase J. Biomol. NMR 51 2011 379 394
17. M. Takeda, J. Jee, A.M. Ono, T. Terauchi, and M. Kainosho Hydrogen exchange rate of tyrosine hydroxyl groups in proteins as studied by the deuterium isotope effect on Cζ chemical shifts J. Am. Chem. Soc. 131 2009 18556 18562
18. 13Cβ NMR signals J. Am. Chem. Soc. 132 2010 6254 6260
19. M. Takeda, J. Jee, A.M. Ono, T. Terauchi, and M. Kainosho Hydrogen exchange study on the hydroxyl groups of serine and threonine residues in proteins and structure refinement using NOE restraints with polar side-chain groups J. Am. Chem. Soc. 133 2011 17420 17427
20. P.E. Hansen Isotope effects on nuclear shielding Annu. Rep. NMR Spectrosc. 15 1983 105 234
21. 13Cα chemical shifts and protein backbone conformation J. Am. Chem. Soc. 119 1997 8070 8075 (Pubitemid 27380269)
22. 13C chemical shifts Prog. Nucl. Magn. Reson. Spectrosc. 45 2004 1 29
23. 1Hα nuclei in proteins J. Biomol. NMR 56 2013 169 182
24. J. Feeney, P. Partington, and G.C.K. Roberts The assignment of carbon-13 resonances from carbonyl groups in peptides J. Magn. Reson. 13 1974 268 274
25. G.E. Hawkes, E.W. Randall, W.E. Hull, D. Gattegno, and F. Conti Qualitative aspects of hydrogen-deuterium exchange in the proton, carbon-13, and nitrogen-15 nuclear magnetic resonance spectra of viomycin in aqueous solution Biochemistry 17 1978 3986 3993
26. M. Kainosho, and T. Tsuji Assignment of the three methionyl carbonyl carbon resonances in Streptomyces subtilisin inhibitor by a carbon-13 and nitrogen-15 double-labeling technique. A new strategy for structural studies of proteins in solution Biochemistry 21 1982 6273 6279 (Pubitemid 13141631)
27. M. Kainosho, H. Nagao, and T. Tsuji Local structural features around the C-terminal segment of Streptomyces subtilisin inhibitor studied by carbonyl carbon nuclear magnetic resonances three phenylalanyl residues Biochemistry 26 1987 1068 1075
28. J.L. Markley, and M. Kainosho Stable isotope labeling and resonance assignments in larger proteins NMR of Macromolecules 1993 Oxford University Press 101 152
29. K. Uchida, J.L. Markley, and M. Kainosho Carbon-13 NMR method for the detection of correlated hydrogen exchange at adjacent backbone peptide amides and its application to hydrogen exchange in five antiparallel beta strands within the hydrophobic core of Streptomyces subtilisin inhibitor (SSI) Biochemistry 44 2005 11811 11820 (Pubitemid 41262715)
30. H. Sun, and V. Tugarinov Precision measurements of deuterium isotope effects on the chemical shifts of backbone nuclei in proteins: correlations with secondary structure J. Phys. Chem. B 116 2012 7436 7448
31. 1H chemical shifts in proteins J. Am. Chem. Soc. 117 1995 3556 3564
32. 15N transverse relaxation J. Am. Chem. Soc. 129 2007 2971 2980 (Pubitemid 46417975)
33. 15N heteronuclear correlation spectroscopy J. Am. Chem. Soc. 128 2006 15388 15389 (Pubitemid 44876011)
34. J.A. Ippolito, R.S. Alexander, and D.W. Christianson Hydrogen bond stereochemistry in protein structure and function J. Mol. Biol. 215 1990 457 471 (Pubitemid 20364477)
35. L.M. Gregoret, S.D. Rader, R.J. Fletterick, and F.E. Cohen Hydrogen bonds involving sulfur atoms in proteins Proteins 9 1991 99 107
36. B.K. Ho, and D.A. Agard Identification of new, well-populated amino-acid sidechain rotamers involving hydroxyl-hydrogen atoms and sulfhydryl-hydrogen atoms BMC Struct. Biol. 8 2008 41
37. N. Eswar, and C. Ramakrishnan Secondary structures without backbone: an analysis of backbone mimicry by polar side chains in protein structures Protein Eng. 12 1999 447 455 (Pubitemid 29322442)
38. P. Zhou, F. Tian, F. Lv, and Z. Shang Geometric characteristics of hydrogen bonds involving sulfur atoms in proteins Proteins 76 2009 151 163
39. C.L. Worth, and T.L. Blundell Satisfaction of hydrogen-bonding potential influences the conservation of polar side-chains Proteins 75 2009 413 429
40. 2O mixtures Adv. Phys. Org. Chem. 7 1969 259 331
41. R.M. Jarret, and M. Saunders A new method for obtaining isotopic fractionation data at multiple sites in rapidly exchanging systems J. Am. Chem. Soc. 107 1985 2648 2654
42. S.W. Loh, and J.L. Markley Hydrogen bonding in proteins as studied by amide hydrogen D/H fractionation factors: application to staphylococcal nuclease Biochemistry 33 1994 1029 1036 (Pubitemid 24058443)
43. 15N labeled human ubiquitin by triple resonance NMR J. Am. Chem. Soc. 118 1996 12864 12865 (Pubitemid 27042028)
44. 2H and temperature Biochemistry 24 1985 7396 7407 (Pubitemid 16165357)
45. G. Wagner A novel application of nuclear overhauser enhancement (NOE) in proteins: analysis of correlated events in the exchange of internal labile protons Biochim. Biophys. Rev. Commun. 97 1980 614 620
46. V.P. Denisov, B. Halle, J. Peters, and H.D. Hörlein Residence times of the buried water molecules in bovine pancreatic trypsin inhibitor and its G36S mutant Biochemistry 34 1995 9046 9051
47. K. Wüthrich, and G. Wagner NMR investigations of the dynamics of the aromatic amino acid residues in the basic pancreatic trypsin inhibitor FEBS Lett. 50 1975 265 268
48. I.D. Campbell, C.M. Dobson, G.R. Moore, S.J. Perkins, and R.J. Williams Temperature dependent molecular motion of a tyrosine residue of ferrocytochrome C FEBS Lett. 70 1976 96 100
49. J.J. Skalicky, J.L. Mills, S. Sharma, and T. Szyperski Aromatic ring-flipping in supercooled water: implications for NMR-based structural biology of proteins J. Am. Chem. Soc. 123 2001 388 397 (Pubitemid 32105128)
50. M.A.L. Erriksson, T. Haerd, and L. Nilsson On the pH dependence of amide proton exchange rates in proteins Biophys. J. 69 1995 329 339
51. D.C.J. Williams, D.C. Benjamin, R.J. Poljak, and G.S. Rule Global changes in amide hydrogen exchange rates for a protein antigen in complex with three different antibodies J. Mol. Biol. 257 1996 866 876 (Pubitemid 26117074)