Detection and characterization of serine and threonine hydroxyl protons in Bacillus circulans xylanase by NMR spectroscopy

Journal of Biomolecular NMR

Volumn 58, Issue 1, 2014, Pages 17-25

  Brockerman, Jacob A ^a   Okon, Mark ^a   McIntosh, Lawrence P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Glycoside hydrolase; Hydroxyl amino acid; NMR spectroscopy; Protein structure and dynamics

Indexed keywords

BACILLUS; ENDO-1,4-BETA XYLANASES; HYDROGEN-ION CONCENTRATION; HYDROXYLATION; KINETICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTONS; SERINE; THREONINE;

EID: 84895192404     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-013-9799-6     Document Type: Article

References (41)

1. Agarwal V, Linser R, Fink U, Faelber K, Reif B (2010) Identification of hydroxyl protons, determination of their exchange dynamics, and characterization of hydrogen bonding in a microcrystallin protein. J Am Chem Soc 132:3187-3195
2. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006
3. Baturin SJ, Okon M, McIntosh LP (2011) Structure, dynamics, and ionization equilibria of the tyrosine residues in Bacillus circulans xylanase. J Biomol NMR 51:379-394
4. 199Hg J-couplings in metal-substituted rubredoxin from Pyrococcus furiosus. J Biomol NMR 2:527-533
5. 1H) coupling constants of intramolecularly hydrogen-bonded compounds. Magn Reson Chem 36:S104-S110
6. Breeze AL (2000) Isotope-filtered NMR methods for the study of biomolecular structure and interactions. Prog Nucl Magn Reson Spectrosc 36(4):323-372
7. Clark AJ (1963) Genetic analysis of a "double male" strain of Escherichia coli K-12. Genetics 48:105-120
8. Connelly GP, Withers SG, McIntosh LP (2000) Analysis of the dynamic properties of Bacillus circulans xylanase upon formation of a covalent glycosyl-enzyme intermediate. Protein Sci 9:512-5242
9. Creighton TE (2010) The biophysical chemistry of nuclei acids and proteins. Helvetian Press, NY
10. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NNMpipe - a multidimensional spectral processing system based on Unix pipes. J Biomol NMR 6(3):277-293
11. Goddard TD, Kneeler DG (1999) Sparky 3, 3rd edn. University of California, San Francisco, CA
12. 2O in protein NMR - application to sensitivity enhancement and NOE measurements. J Am Chem Soc 115:12593-12594
13. Hansen PE (1981) Carbon-hydrogen spin-spin coupling constants. Prog Nucl Magn Reson Spectrosc 14:175-295
14. 15N NMR spectroscopy: use of the INEPT experiment to follow individual amides in detergent-solubilized M13 coat protein. Biochemistry 29:6303-6313
15. Ho BK, Agard DA (2008) Identification of new, well-populated amino-acid sidechain rotamers involving hydroxyl-hydrogen atoms and sulfhydryl-hydrogen atoms. BMC Struct Biol 8:41
16. Hwang TL, Mori S, Shaka AJ, vanZijl PCM (1997) Application of phase-modulated CLEAN chemical EXchange spectroscopy (CLEANEX-PM) to detect water-protein proton exchange and intermolecular NOEs. J Am Chem Soc 119:6203-6204
17. Ikura M, Bax A (1992) Isotope-filtered 2D NMR of a protein peptide complex - study of a skeletal-muscle myosin light chain kinase fragment bound to calmodulin. J Am Chem Soc 114:2433-2440
18. Iwahara J, Wojciak JM, Clubb RT (2001) Improved NMR spectra of a protein-DNA complex through rational mutagenesis and the application of a sensitivity optimized isotope-filtered NOESY experiment. J Biomol NMR 19:231-241
19. Joshi MD, Hedberg A, McIntosh LP (1997) Complete measurement of the pKa values of the carboxyl and imidazole groups in Bacillus circulans xylanase. Protein Sci 6:2667-2670
20. Joshi MD, Sidhu G, Nielsen JE, Brayer GD, Withers SG, McIntosh LP (2001) Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidase. Biochemistry 40:10115-10139
21. Knauf MA, Lohr F, Curley GP, O'Farrell P, Mayhew SG, Muller F, Ruterjans H (1993) Homonuclear and heteronuclear NMR studies of oxidized Desulfovibrio vulgaris flavodoxin. Sequential assignments and identification of secondary structure elements. Eur J Biochem 213:167-184
22. Kossiakoff AA, Shpungin J, Sintchak MD (1990) Hydroxyl hydrogen conformations in trypsin determined by the neutron-diffraction solvent difference map method - relative importance of steric and electrostatic factors in defining hydrogen-bonding geometries. Proc Natl Acad Sci USA 87:4468-4472
23. Liepinsh E, Otting G (1996) Proton exchange rates from amino acid side chains - implications for image contrast. Magn Reson Med 35:30-42
24. Liepinsh E, Otting G, Wuthrich K (1992) NMR spectroscopy of hydroxyl protons in aqueous solutions of peptides and proteins. J Biomol NMR 2:447-465
25. Lohr F, Mayhew SG, Ruterjans H (2000) Detection of scalar couplings across NH···OP and OH···OP hydrogen bonds in a flavoprotein. J Am Chem Soc 122:9289-9295
26. McIntosh LP, Naito D, Baturin SJ, Okon M, Joshi MD, Nielsen JE (2011) Dissecting electrostatic interactions in Bacillus circulans xylanase through NMR-monitored pH titrations. J Biomol NMR 51:5-19
27. 15N NMR. Methods Enzymol 177:44-73
28. Ogura K, Terasawa H, Inagaki F (1996) An improved double-tuned and isotope-filtered pulse scheme based on a pulsed field gradient and a wide-band inversion shaped pulse. J Biomol NMR 8:492-498
29. Peelen S, Vervoort J (1994) Two-dimensional NMR studies of the flavin binding site of Desulfovibrio vulgaris flavodoxin in its three redox states. Arch Biochem Biophys 314:291-300
30. Piotto M, Saudek V, Sklenar V (1992) Gradient-tailored excitation for single-quantum NMR-spectroscopy of aqueous solutions. J Biomol NMR 2:661-665
31. Plesniak LA, Connelly GP, Wakarchuk WW, McIntosh LP (1996a) Characterization of a buried neutral histidine residue in Bacillus circulans xylanase: NMR assignments, pH titration, and hydrogen exchange. Protein Sci 5(11):2319-2328
32. Plesniak LA, Wakarchuk WW, McIntosh LP (1996b) Secondary structure and NMR assignments of Bacillus circulans xylanase. Protein Sci 5(6):1118-1135
33. Plevin MJ, Hayashi I, Ikura M (2008) 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 130:14918-14919
34. Segawa T, Kateb F, Duna L, Bodnhausen G, Pelupessy P (2008) Exchange rate constants of invisible proteins in proteins determined by NMR spectroscopy. ChemBioChem 9:537-542
35. Sung WL, Luk CK, Zahab DM, Wakarchuk W (1993) Overexpression and purification of the Bacillus subtilis and Bacillus circulans xylanases in Escherichia coli. Protein Expr Purif 4:200-216
36. Takeda M, Jee J, Ono AM, Terauchi T, Kainosho M (2011) 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 133:17420-17427
37. Ulrich EL, Akutsu H, Doreleijers JF, Harano Y, Ioannidis YE, Lin J, Livny M, Mading S, Maziuk D, Miller Z, Nakatani E, Schulte CF, Tolmie DE, Wenger RK, Yao HY, Markley JL (2008) BioMagResBank. Nucleic Acids Res 36:D402-D408
38. 3-threonine for solution NMR studies of large protein complexes: application to the 670 kDa proteasome. PLoS ONE 7(9):e43725
39. 15N-amino acids. J Biomol NMR 8:184-192
40. Word JM, Lovell SC, Richardson JS, Richardson DC (1999) Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation. J Mol Biol 285:1735-1747
41. Zwahlen C, Legault P, Vincent SJF, Greenblatt J, Konrat R, Kay LE (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage lambda N-peptide/boxB RNA complex. J Am Chem Soc 119:6711-6721