Abildgaard J, Hansen PE, Manalo MN, LiWang A (2009) Deuterium isotope effects on 15N backbone chemical shifts in proteins. J Biomol NMR 44:119–126. https://doi.org/10.1007/s10858-009-9316-0

Article  Google Scholar 

Adalsteinsson H, Maulitz AH, Bruice TC (1996) Calculation of the potential energy surface for intermolecular amide hydrogen bonds using semiempirical and ab initio methods. J Am Chem Soc 118:7689–7693

Article  Google Scholar 

Alexandrescu AT, Ulrich EL, Markley JL (1989) Hydrogen-1 NMR evidence for three interconverting forms of staphylococcal nuclease: effects of mutations and solution conditions on their distribution. Biochemistry 28:204–211. https://doi.org/10.1021/bi00427a028

Article  Google Scholar 

Alexandrescu AT, Hinck AP, Markley JL (1990) Coupling between local structure and global stability of a protein: mutants of staphylococcal nuclease. Biochemistry 29:4516–4525. https://doi.org/10.1021/bi00471a003

Article  Google Scholar 

Alexandrescu AT, Snyder DR, Abildgaard F (2001) NMR of hydrogen bonding in cold-shock protein A and an analysis of the influence of crystallographic resolution on comparisons of hydrogen bond lengths. Protein Sci 10:1856–1868. https://doi.org/10.1110/ps.14301

Article  Google Scholar 

Berger S, Künzer H (1983) Extremely long-range 2H isotope effects on the chemical shifts in the 13C-NMR spectra of compounds with conjugated double bonds. Angew Chem Int Ed Engl 22:321–322

Article  Google Scholar 

Bowers PM, Klevit RE (1996) Hydrogen bonding and equilibrium isotope enrichment in histidine-containing proteins. Nat Struct Biol 3:522–531. https://doi.org/10.1038/nsb0696-522

Article  Google Scholar 

Bowers PM, Klevit RE (2000) Hydrogen bond geometry and 2H/1H fractionation in proteins. J Am Chem Soc 122:1030–1033

Article  Google Scholar 

Cao Z, Bowie JU (2014) An energetic scale for equilibrium H/D fractionation factors illuminates hydrogen bond free energies in proteins. Protein Sci 23:566–575. https://doi.org/10.1002/pro.2435

Article  Google Scholar 

Cavanagh J, Fairbrother WJ, Palmer AG III, Skelton NJ (2006) Protein NMR Spectroscopy Principles and Practice. Protein NMR Spectroscopy, 2nd edn. Elsevier Inc., Amsterdam

Google Scholar 

Chevelkov V, Xue Y, Rao DK, Forman-Kay JD, Skrynnikov NR (2010) 15N H/D-SOLEXSY experiment for accurate measurement of amide solvent exchange rates: application to denatured drkN SH3. J Biomol NMR 46:227–244. https://doi.org/10.1007/s10858-010-9398-8

Article  Google Scholar 

Cordier F, Grzesiek S (2002) Temperature-dependence of protein hydrogen bond properties as studied by high-resolution NMR. J Mol Biol 317:739–752. https://doi.org/10.1006/jmbi.2002.5446

Article  Google Scholar 

Dempsey CE (2001) Hydrogen exchange in peptides and proteins using NMR spectroscopy. Prog Nucl Magn Reson Spectrosc 39:135–170

Article  Google Scholar 

Feng W, Tejero R, Zimmerman DE, Inouye M, Montelione GT (1998) Solution NMR structure and backbone dynamics of the major cold-shock protein (CspA) from Escherichia coli: evidence for conformational dynamics in the single-stranded RNA-binding site. Biochemistry 37:10881–10896. https://doi.org/10.1021/bi980269j

Article  Google Scholar 

Garland CW, Nibler JW, Shoemaker DP (2009) Experiments in Physical Chemistry, 8th edn. McGraw-Hill, New York

Google Scholar 

Hansen PE (1988) Isotope effects in nuclear shielding. Prog in NMR Spectrosc 20:207–255

Article  Google Scholar 

Hong J, Jing Q, Yao L (2013) The protein amide (1)H(N) chemical shift temperature coefficient reflects thermal expansion of the N-H O=C hydrogen bond. J Biomol NMR 55:71–78. https://doi.org/10.1007/s10858-012-9689-3

Article  Google Scholar 

Jaravine VA, Rathgeb-Szabo K, Alexandrescu AT (2000) Microscopic stability of cold shock protein A examined by NMR native state hydrogen exchange as a function of urea and trimethylamine N-oxide. Protein Sci 9:290–301. https://doi.org/10.1110/ps.9.2.290

Article  Google Scholar 

Kainosho M, Tsuji T (1982) 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 21:6273–6279. https://doi.org/10.1021/bi00267a036

Article  Google Scholar 

Kainosho M, Nagao H, Imamura Y, Uchida K, Tomonaga N, Nakamura Y, Tsuji T (1985) Structural studies of a protein using the assigned back-bone carbonyl carbon-13 NMR resonances. J Mol Struct 126:549–562

Article  ADS  Google Scholar 

Kaplan AR, Maciejewski M, Olson R, Alexandrescu AT (2013) NMR assignments for the cis and trans forms of the hemolysin II C-terminal domain. Biomol NMR Assign 8:419–423

Article  Google Scholar 

Kaplan AR, Olson R, Alexandrescu AT (2021) Protein yoga: conformational versatility of the Hemolysin II C-terminal domain detailed by NMR structures for multiple states. Protein Sci 30:990–1005. https://doi.org/10.1002/pro.4066

Article  Google Scholar 

Kateb F, Pelupessy P, Bodenhausen G (2007) Measuring fast hydrogen exchange rates by NMR spectroscopy. J Magn Reson 184:108–113. https://doi.org/10.1016/j.jmr.2006.09.022

Article  ADS  Google Scholar 

Khare D, Alexander P, Orban J (1999) Hydrogen bonding and equilibrium protium-deuterium fractionation factors in the immunoglobulin G binding domain of protein G. Biochemistry 38:3918–3925. https://doi.org/10.1021/bi9827114

Article  Google Scholar 

Lambert JB, Greifenstein LG (1974) Origin of the chemical-shift isotope effect stereochemical evidence. J Amer Chem Soc 96:5120–5124

Article  Google Scholar 

LeMaster DM, LaIuppa JC, Kushlan DM (1994) Differential deuterium isotope shifts and one-bond 1H–13C scalar couplings in the conformational analysis of protein glycine residues. J Biomol NMR 4:863–870. https://doi.org/10.1007/BF00398415

Article  Google Scholar 

Liu A, Wang J, Lu Z, Yao L, Li Y, Yan H (2008) Hydrogen-bond detection, configuration assignment and rotamer correction of side-chain amides in large proteins by NMR spectroscopy through protium/deuterium isotope effects. Chembiochem 9:2860–2871. https://doi.org/10.1002/cbic.200800467

Article  Google Scholar 

LiWang AC, Bax A (1996) Equilibrium protium/deuterium dractionation of backbone amides in U-13C/15N labeled human ubiquitin by triple resonance NMR. J Am Chem Soc 118:12864–12865

Article  Google Scholar 

Loh SN, Markley JL (1994) Hydrogen bonding in proteins as studied by amide hydrogen D/H fractionation factors: application to staphylococcal nuclease. Biochemistry 33:1029–1036. https://doi.org/10.1021/bi00170a023

Article  Google Scholar 

Lohr F, Ruterjans H (1999) Alternative E.COSY techniques for the measurement of 3J(C (i) (') (-1), C (i) (beta) ) and (3) J(H (i) (N), C (i) (beta) ) coupling constants in proteins. J Biomol NMR 13:263–274. https://doi.org/10.1023/A:1008378719908

Article  Google Scholar 

Mal TK, Matthews SJ, Kovacs H, Campbell ID, Boyd J (1998) Some NMR experiments and a structure determination employing a [15N,2H] enriched protein. J Biomol NMR 12:259–276. https://doi.org/10.1023/a:1008238009056

Article  Google Scholar 

Maltsev AS, Ying J, Bax A (2012) Deuterium isotope shifts for backbone (1)H, (1)(5)N and (1)(3)C nuclei in intrinsically disordered protein alpha-synuclein. J Biomol NMR 54:181–191. https://doi.org/10.1007/s10858-012-9666-x

Article  Google Scholar 

Nguyen D, Chen C, Pettitt BM, Iwahara J (2019) NMR methods for characterizing the basic side chains of proteins: electrostatic interactions hydrogen bonds, and conformational dynamics. Methods Enzymol 615:285–332. https://doi.org/10.1016/bs.mie.2018.08.017

Article  Google Scholar 

Ottiger M, Bax A (1997) An empirical correlation between amide deuterium isotope effects on 13Calpha chemical shifts and protein backbone conformation. J Am Chem Soc 119:8070–8075

Article  Google Scholar 

Roder H, Wagner G, Wuthrich K (1985) Amide proton exchange in proteins by EX1 kinetics: studies of the basic pancreatic trypsin inhibitor at variable p2H and temperature. Biochemistry 24:7396–7407. https://doi.org/10.1021/bi00346a055

Article  Google Scholar 

Schindelin H, Jiang W, Inouye M, Heinemann U (1994) Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 91:5119–5123. https://doi.org/10.1073/pnas.91.11.5119

Article  ADS  Google Scholar 

Schmidt JM, Hua Y, Lohr F (2010) Correlation of (2)J couplings with protein secondary structure. Proteins 78:1544–1562. https://doi.org/10.1002/prot.22672

Article  Google Scholar 

Shan SO, Loh S, Herschlag D (1996) The energetics of hydrogen bonds in model systems: implications for enzymatic catalysis. Science 272:97–101. https://doi.org/10.1126/science.272.5258.97

Article  ADS  Google Scholar 

Sun H, Tugarinov V (2012) Precision measurements of deuterium isotope effects on the chemical shifts of backbone nuclei in proteins: correlations with secondary structure. J Phys Chem B 116:7436–7448. https://doi.org/10.1021/jp304300n

Article  Google Scholar 

Takeda M, Jee J, Ono AM, Terauchi T, Kainosho M (2009) Hydrogen exchange rate of tyrosine hydroxyl groups in proteins as studied by the deuterium isotope effect on C(zeta) chemical shifts. J Am Chem Soc 131:18556–18562. https://doi.org/10.1021/ja907911y

Article  Google Scholar 

Takeda M, Miyanoiri Y, Terauchi T, Yang CJ, Kainosho M (2014) Use of H/D isotope effects to gather information about hydrogen bonding and hydrogen exchange rates. J Magn Reson 241:148–154. https://doi.org/10.1016/j.jmr.2013.10.001

Article  ADS  Google Scholar 

Theis K, Dingley AJ, Hoffmann A, Omichinski JG, Grzesiek S (1997) Determination of backbone nitrogen-nitrogen J correlations in proteins. J Biomol NMR 10:403–408. https://doi.org/10.1023/A:1018373601391

Article  Google Scholar 

Tripler TN, Maciejewski MW, Teschke CM, Alexandrescu AT (2015) NMR assignments for the insertion domain of bacteriophage CUS-3 coat protein. Biomol NMR Assign. https://doi.org/10.1007/s12104-015-9604-4

Article  Google Scholar 

Tripler TN, Kaplan AR, Alexandrescu AT, Teschke CM (2019) Conservation and divergence of the I-domain inserted into the ubiquitous HK97 coat protein fold in P22-like bacteriophages. J Virol. https://doi.org/10.1128/JVI.00007-19

Article  Google Scholar 

Tuchsen E, Hansen PE (1988) Carbonyl 13C NMR spectrum of basic pancreatic trypsin inhibitor: resonance assignments by selective amide hydrogen isotope labeling and detection of isotope effects on 13C nuclear shielding. Biochemistry 27:8568–8576. https://doi.org/10.1021/bi00423a010

Article  Google Scholar 

Tuchsen E, Hansen PE (1991) Hydrogen bonding monitored by deuterium isotope effects on carbonyl 13C chemical shift in BPTI: intra-residue hydrogen bonds in antiparallel beta-sheet. Int J Biol Macromol 13:2–8. https://doi.org/10.1016/0141-8130(91)90002-c

Article  Google Scholar 

Tugarinov V (2013) Four-bond deuterium isotope effects on the chemical shifts of amide nitrogens in proteins. Magn Reson Chem 51:722–728. https://doi.org/10.1002/mrc.4007

Article  Google Scholar 

Uchida K, Markley JL, Kainosho M (2005) 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 44:11811–11820. https://doi.org/10.1021/bi050467s

Article  Google Scholar 

Venters RA, Farmer BT 2nd, Fierke CA, Spicer LD (1996) Characterizing the use of perdeuteration in NMR studies of large proteins: 13C, 15N and 1H assignments of human carbonic anhydr