Titration DB: Storage and analysis of NMR-monitored protein pH titration curves

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 4, 2010, Pages 843-857

  Farrell, Damien ^a   Miranda, Emanuel Sá ^a   Webb, Helen ^a   Georgi, Nikolaj ^a   Crowley, Peter B ^b   McIntosh, Lawrence P ^c,d   Nielsen, Jens Erik ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Chemical shift; Database; NMR pH titration; Protein pKa values; Protonation; Titration

Indexed keywords

PLASTOCYANIN; PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; LIGAND BINDING; NITROGEN NUCLEAR MAGNETIC RESONANCE; PH MEASUREMENT; PKA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STABILITY; PROTON TRANSPORT; ALGORITHM; CHEMISTRY; KINETICS; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH;

ALGORITHMS; HYDROGEN-ION CONCENTRATION; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN STABILITY; PROTEINS;

EID: 77949311905     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22611     Document Type: Article

References (95)

1. Tanford C. Protein denaturation. C Theoretical models for the mechanism of denaturation. Adv Protein Chem 1970; 24: 1-95.
2. Søndergaard CR, Mcintosh LP, Pollastri G, Nielsen JE. Determination of electrostatic interaction energies and protonation state populations in enzyme active sites. J Mol Biol 2008; 376: 269-287.
3. Nielsen JE. Analyzing enzymatic pH activity profiles and protein, titration, curves using structure-based pKa calculations and titration curve fitting. Methods Enzymol 2009; 454: 233-258.
4. Yamazaki T, Lee W, Revington M, Mattiello DL, Dahlquist FW, Arrowsmith CH, Kay LE. An HNCA pulse scheme for the backbone assignment of 15N, 13C, 2H-labeled proteins: application to a 37-kDa Trp repressor-DNA. complex. J Am Chem Soc 2002; 116: 6464-6465.
5. Toseland CP, McSparron H, Davies MN, Flower DR. PPD v1.0-an integrated, web-accessible database of experimentally determined protein pKa values. Nucleic Acids Res 2006; 34(database issue): D199-D203.
6. Pace CN, Alston RW, Shaw KL. Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci 2000; 9: 1395-1398.
7. Garcia-Moreno B, Chen LX, March KL, Gurd RS, Gurd FR. Electrostatic interactions in sperm whale myoglobin. Site specificity, roles in structural elements, and external electrostatic potential distributions. J Biol Chem 1985; 260: 14070-14082.
8. Fersht A. Enzyme structure and mechanism, Vol.21. New York: W.H. Freeman; 1985. 475 p.
9. Joshi MD, Sidhu G, Nielsen JE, Brayer GD, Withers SG, Mcintosh LP. Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidase. Biochemistry 2001; 40: 10115-10139. (Pubitemid 32800119)
10. Nielsen JE, McCammon JA. Calculating pKa values in enzyme active sites. Protein Sci 2003; 12: 1894-1901.
11. Sakurai K, Goto Y. Principal component analysis of the pH-dependent conformational transitions of bovine beta-lactoglobulin monitored by heteronuclear NMR. Proc Natl Acad Sci USA 2007; 104: 15346-15351. (Pubitemid 47502920)
12. Warshel A, Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites. J Biol Chem 1998; 273: 27035-27038. (Pubitemid 28500403)
13. Yang AS, Gunner MR, Sampogna R, Sharp K, Honig B. On the calculation of pKas in proteins. Proteins 1993; 15: 252-265.
14. Nielsen JE, Vriend G. Optimizing the hydrogen-bond network in Poisson-Boltzmami equation-based pK(a) calculations. Proteins 2001; 43: 403-412.
15. Antosiewicz J, McCammon JA, Gilson MK. Prediction of pH-dependent properties of proteins. J Mol Biol 1994; 238: 415-436.
16. Mehler EL, Guarnieri F. A self-consistent, microenvironment modulated screened coulomb potential approximation to calculate pHdependent electrostatic effects in proteins. Biophys J 1999; 77: 3-22.
17. van Vlijmen HW, Schaefer M, Karplus M. Improving the accuracy of protein pKa calculations: conformational averaging versus the average structure. Proteins 1998; 33: 145-158.
18. Li H, Robertson AD, Jensen JH. Very fast empirical prediction and rationalization of protein pKa values. Proteins 2005; 61: 704-721. (Pubitemid 41753142)
19. Alexov EG, Gunner MR. Incorporating protein conformational flexibility into the calculation of pH-depeudent protein properties. Biophys J 1997; 72: 2075-2093.
20. Warshel A, Sharma PK, Kato M, Parson WW. Modeling electrostatic effects in proteins. Biochim Biophys Acta 2006; 1764: 1647-1676.
21. Berman H, Henrick K, Nakamura H. Announcing the worldwide protein data bank. Nat Struct Biol 2003; 10: 980. (Pubitemid 37500485)
22. Popov K, Rönkkömäki H, Lajunen LHJ. Guidelines for NMR measurements for determination of high and low pKa values (IUPAC technical report). Pure Appl Chem 2006; 78: 663-675.
23. Yu L, Fesik SW. pH titration of the histidine residues of cyclophilin and FK506 binding protein in the absence and presence of immunosuppressant ligands. Biochim Biophys Acta 1994; 1209: 24-32.
24. Schubert M, Poon DK, Wicki J, Tarling CA, Kwan EM, Nielsen JE, Withers SG, McIntosh LP. Probing electrostatic interactions along the reaction pathway of a glycoside hydrolase: histidine characterization by NMR spectroscopy. Biochemistry 2007; 46: 7383-7395.
25. Pelton JG, Torchia DA, Meadow ND, Roseman S. Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci 1993; 2: 543-558.
26. Yamazaki T, Yoshida M, Nagayama K. Complete assignments of magnetic resonances of ribonuclease H from Escherichia coli by double- and triple-resonance 2D and 3D NMR spectroscopies. Biochemistry 1993; 32: 5656-5669.
27. Oda Y, Yamazaki T, Nagayama K, Kanaya S, Kuroda Y, Nakamura H. Individual ionization constants of all the carboxyl groups in ribonuciease HI from Escherichia coli determined by NMR. Biochemistry 1994; 33: 5275-5284.
28. 13C NMR spectroscopy: application to apo calmodulin. J Am Chem Soc 2007; 129: 15805-15813.
29. Joshi MD, Hedberg A, Mcintosh LP. Complete measurement of the pKa values of the carboxyl and imidazole groups in Bacillus circulars xylanase. Protein Sci 1997; 6: 2667-2670.
30. 15N heteronuclear correlation spectroscopy. J Am Chem Soc 2006; 128: 15388-15389.
31. Buckingham. AD. Chemical shift in the nuclear magnetic resonance spectra of molecules containing polar groups. Can J Chem 1960; 38: 300-307.
32. Hass MA, Jensen MR, Led JJ. Probing electric fields in proteins in solution by NMR spectroscopy. Proteins 2008; 72: 333-343.
33. Kukic P, Farrell D, Sendergaard C, Bjarnadottir U, Bradley J, Pollastri G, Nielsen JE. Improving the analysis of NMR spectra tracking pH-induced conformational changes: Removing artefacts of the electric field on the NMR chemical shift. Proteins (in press).
34. 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 1995; 6: 135-140.
35. Tomlinson JH, Uliah S, Hansen PE, Williamson MP. Characterization of salt bridges to lysines in the protein G B1 domain. J Am. Chem Soc 2009; 131: 4674-4684.
36. How the F test works to compare models. GraphPad Software, Inc. http://www.graphpad.com/help/prism5/prism5help.htrnl?howtheftestworks.htm
37. Joshi MD, Sidhu G, Pot I, Brayer GD, Withers SG, Mcintosh LP. Hydrogen bonding and catalysis: a novel explanation for how a single amino acid substitution can change the pH optimum of a glycosidase. J Mol Biol 2000; 299: 255-279.
38. Shrager RI, Cohen JS, Heller SR, Sachs DH, Schechter AN. Mathematical models for interacting groups in nuclear magnetic resonance titration curves. Biochemistry 1972; 11: 541-547.
39. Mossner E, Iwai H, Glockshuber R. Influence of the pK(a) value of the buried, active-site cysteine on the redox properties of thioredoxin-like oxidoreductases. FEBS Lett 2000; 477: 21-26.
40. Alexandrescu AT, Mills DA, Ulrich EL, Chinami M, Markley JL. NMR assignments of the four histidines of staphylococcal nuclease in native and denatured states. Biochemistry 1988; 27: 2158-2165.
41. 1H NMR. Biochemistry 1995; 34: 16186-16193.
42. Baker WR, Kintanar A. Characterization of the pH titration shifts of ribonuclease A by one- and two-dimensional nuclear magnetic resonance spectroscopy. Arch Biochem Biophys 1996; 327: 189-199. (Pubitemid 26063749)
43. Betz M, Lohr F, Wienk H, Ruterjans H. Long-range nature of the interactions between titratable groups in Bacillus agaradhaerens family 11 xylanase: pH titration of B, agaradhaerens xylanase. Biochemistry 2004; 43: 5820-5831.
44. 1H NMR characterization of the urokinase kringle module. Structural, but not functional, relatedness to homologous domains. J Biol Chem 1993; 268: 13858-13868.
45. 2+. J Mol Biol 2001; 310: 659-672.
46. Cocco MJ, Kao YH, Phillips AT, Lecomte JT. Structural comparison of apomyoglobin and metaquomyoglobin: pH titration of histidines by NMR spectroscopy. Biochemistry 1992; 31: 6481-6491.
47. Cohen JS, Griffin JH, Schechter AN. Nuclear magnetic resonance titration curves of histidine ring protons. IV. The effects of phosphate and sulfate on ribonuclease. J Biol Chem 1973; 248: 4305-4310.
48. Consonni R, Arosio I, Belloni B, Fogolari F, Fusi P, Shehi E, Zetta L. Investigations of Sso7d catalytic residues by NMR titration shifts and electrostatic calculations. Biochemistry 2003; 42: 1421-1429.
49. 1H NMR spectroscopy pH titration of the catalytic histidine residue in the 109 kDa Leuconostoc mesenteroides enzyme. Biochemistry 2002; 41: 6939-6945.
50. Day RM, Thalhauser CJ, Sudmeier JL, Vincent MP, Torchilin EV, Sanford DG, Bachovchin CW, Bachovchin WW. Tautomerism, acidbase equilibria, and H-bonding of the six histidines in subtilisin BPN' by NMR. Protein Sci 2003; 12: 794-810.
51. Geierstanger B, Jamin M, Volkman BF, Baldwin RL. Protonation behavior of histidine 24 and histidine 119 in forming the pH 4 folding intermediate of apomyoglobin. Biochemistry 1998; 37: 4254-4265.
52. Gooley PR, Keniry MA, Dimitrov RA, Marsh DE, Keizer DW, Gayler KR, Grant BR. The NMR solution structure and characterization of pH dependent chemical shifts of the beta-elicitin, cryptogein. J Biomol NMR 1998; 12: 523-534.
53. Kern G, Pelton J, Marqusee S, Kern D. Structural properties of the histidine-containing loop in HIV-1 RNase H. Biophys Chem 2002; 96: 285-291.
54. Kesvatera T, Jonsson B, Thulin E, Linse S. Measurement and modelling of sequence-specific pKa values of lysine residues in calbindin D9k. J Mol Biol 1996; 259: 828-839.
55. Koide A, Jordan MR, Horner SR, Batori V, Koide S. Stabilization of a fibronectin type III domain by the removal of unfavorable electrostatic interactions on the protein surface. Biochemistry 2001; 40: 10326-10333.
56. Kuhlman B, Luisi DL, Young P, Raleigh DP. pKa values and the pH dependent stability of the N-terminal domain of L9 as probes of electrostatic interactions in the denatured state. Differentiation between local and nonlocal interactions. Biochemistry 1999; 38: 4896-4903.
57. Laurents DV, Huyghues-Dcspointes BM, Bruix M, Thurlkill RL, Schell D, Newsom. S, Grimsley GR, Shaw KL, Trevino S, Rico M, Briggs JM, Antosiewicz JM, Scholtz JM., Pace CN. Charge-charge interactions are key determinants of the pK values of ionizabie groups in ribonuclease Sa (pI = 3.5) and a basic variant (pI = 10.2). J Mol Biol 2003; 325: 1077-1092.
58. Lee KK, Fitch CA, Lecomte JT, Garcia-Moreno EB. Electrostatic effects in highly charged proteins: salt sensitivity of pKa values of histidines in staphylococcal nuclease. Biochemistry 2002; 41: 5656-5667.
59. Legler PM, Massiah MA, Mildvan AS. Mutational, kinetic, and NMR studies of the mechanism of E. coli GDP-mannose mannosyl hydrolase, an unusual Nudix enzyme. Biochemistry 2002; 41: 10834-10848.
60. Lund-KatzS,WehrliS,ZaiouM,NewhouseY,WeisgraberKH,PhillipsMC, Effectsofpolymorphism,onthemicroenvironmentoftheLDLreceptor- bindingregionofhumanapoE.JLipidRes2001;42:894-901.(Pubitemid32545844)
61. Marti DN, Bosshard HR. Electrostatic interactions in leucine zippers: thermodynamic analysis of the contributions of Glu and His residues and the effect of mutating salt bridges. J Mol Biol. 2003; 330: 621-637.
62. Schmidt L, Christensen HE, Harris P. Structure of plastocyanin from the cyanobacterium Anabaena variabilis. Acta Crystallogr D Biol Crystallogr 2006; 62(Pt 9): 1022-1029.
63. Marti DN, Jelesarov I, Bosshard HR. Interhelical ion pairing in coiled coils: solution structure of a heterodimeric leucine zipper and determination of pKa values of Glu side chains. Biochemistry 2000; 39: 12804-12818.
64. Oliveberg M, Arcus VL, Fersht AR. pKA values of carboxyl groups in the native and denatured states of barnase: the pKA values of the denatured state are on average 0.4 units lower than those of model compounds. Biochemistry 1995; 34: 9424-9433.
65. Perez-Canadillas JM, Campos-Olivas R, Lacadena J, Martinez del Pozo A, Gavilanes JG, Santoro J, Rico M, Bruix M. Characterization of pKa values and titration shifts in the cytotoxic ribonuclease alphasarcin by NMR. Relationship between electrostatic interactions, structure, and catalytic function. Biochemistry 1998; 37: 15865-15876.
66. 13C nuclear magnetic resonance studies at 90.5 MHz of the basic pancreatic trypsin inhibitor. Biochemistry 1978; 17: 2263-2269.
67. Sato K, Dennison C. Effect of histidine 6 protonation on the active site structure and electron-transfer capabilities of pseudoazurin from Achromobacter cycloclastes. Biochemistry 2002; 41: 120-130.
68. Schaller W, Robertson AD. pH, ionic strength, and temperature dependences of ionization equilibria for the carboxyl groups in turkey ovomucoid third domain. Biochemistry 1995; 34: 4714-4723.
69. Song J, Laskowski M, Jr, Qasim MA, Markley JL. Two conformational states of Turkey ovomucoid third domain at low pH: threedimensional structures, internal dynamics, and interconversion kinetics and thermodynamics. Biochemistry 2003; 42: 6380-6391.
70. Sun X, Sun H, Ge R, Richter M, Woodworth RC, Mason AB, He QY. The low pKa value of iron-binding ligand Tyr188 and its implication in iron release and anion binding of human transferrin. FEBS Lett 2004; 573: 181-185.
71. Sundd M, Iverson N, Ibarra-Molero B, Sanchez-Ruiz JM, Robertson AD. Electrostatic interactions in ubiquitin; stabilization of carboxylates by lysine amino groups. Biochemistry 2002; 41: 7586-7596.
72. Sundd M, Robertson AD. Rearrangement of charge-charge interactions in variant ubiquitins as detected by double-mutant cycles and NMR. J Mol Biol 2003; 332: 927-936.
73. Szyperski T, Antuch W, Schick M, Betz A, Stone SR, Wuthrich K. Transient hydrogen bonds identified on the surface of the NMR solution structure of Hirudin. Biochemistry 1994; 33: 9303-9310.
74. Tan YJ, Oliveberg M, Davis B, Fersht AR. Perturbed pKA-values in the denatured states of proteins. J Mol Biol 1995; 254: 980-992.
75. Thomas CL, McKinnon E, Granger BL, Harms E, van Etten RL. Kinetic and spectroscopic studies of tritrichomonas foetus low-molecular weight phosphotyrosyl phosphatase. Hydrogen bond networks and electrostatic effects. Biochemistry 2002; 41: 15601-15609.
76. Tishmack PA, Bashford D, Harms E, van Etten RL. Use of 1H NMR spectroscopy and computer simulations to analyze histidine pKa changes in a protein tyrosine phosphatase: experimental and theoretical determination of electrostatic properties in a small protein. Biochemistry 1997; 36: 11984-11994. (Pubitemid 27424128)
77. Wolff N, Deniau C, Letoffe S, Simenel C, Kumar V, Stojiljkovic I, Wandersman C, Delepierre M, Lecroisey A. Histidine pK(a) shifts and changes of tautomeric states induced by the binding of gallium-protoporphyrin IX in the hemophore HasA(SM). Protein Sci 2002; 11: 757-765.
78. Zhou Z, Swenson RP. Evaluation of the electrostatic effect of the 5′-phosphate of the flavin mononudeotide cofactor on the oxidation-reduction potentials of the flavodoxin from desulfovibrio vulgaris (Hildenborough). Biochemistry 1996; 35: 12443-12454.
79. Thurlkill RL, Grimsley GR, Scholtz JM, Pace CN. pK values of the ionizable groups of proteins. Protein Sci 2006; 15: 1214-1218.
80. Fogolari F, Ragona L, Licciardi S, Romagnoli S, Michelutti R, Ugolini R, Molinari H. Electrostatic properties of bovine beta-lactoglobulin. Proteins 2000; 39: 317-330.
81. Nozaki Y, Tanford C. Examination of titration behavior. Methods Enzymol 1967; 11: 715-734.
82. Gurd FR, Keim P, Glushko VG, Lawson PJ, Marshall RC, Nigen AM, Vigna RA. Carbon-13 nuclear magnetic resonance of some pentapeptides. Ann Arbor Science Publishers: Ann Arbor, MI; 1972. pp 45-49.
83. 1H NMR. Biophys J 1994; 66: 1180-1184.
84. Grimsley GR, Scholtz JM, Pace CN. A summary of the measured pK values of the ionizable groups in folded proteins. Protein Sci 2009; 18: 247-251.
85. Crowley PB. Ph.D. Thesis: Transient Protein Interactions of Photosynthetic Redox Partners. Leiden University; 2002.
86. Guss JM, Harrowell PR, Murata M, Norris VA, Freeman HC. Crystal structure analyses of reduced (CuI) poplar plastocyanin at six pH values. J Mol Biol 1986; 192: 361-387.
87. Yanagisawa S, Crowley PB, Firbank SJ, Lawler AT, Hunter DM, McFarlane W, Li C, Kohzuma T, Banfield MJ, Dennison C. Pi-interaction tuning of the active site properties of metalloproteins. J Am Chem Soc 2008; 130: 15420-15428.
88. Schumann FH, Riepl H, Maurer T, Gronwald W, Neidig KP, Kalbitzer HR. Combined chemical shift changes and amino acid specific chemical shift mapping of protein-protein interactions. J Biomol. NMR 2007; 39: 275-289..
89. Frantz J. g3data. http://www.frantz.fi/software/g3data.php[accessed March 2007].
90. Tigris.org. Subversion, http://subve.rsion.tigris.org/; 2002 [accessed on March 2007].
91. Vriend G. WHAT IF: a molecular modeling and drug design program. J Mol Graph 1990; 8: 52-56.
92. Levenberg K, Method for the solution of certain non-linear problems in least squares. Q Appl Math 1944; 2: 164-168.
93. Motuisky HJ, Ransnas LA. Fitting curves to data using nonlinear regression: a practical and nonmathematical review. FASEB J 1987; 1: 365-374.
94. Tynan-Connolly BM, Nielsen JE. pKD: re-designing protein pKa values. Nucleic Acids Res 2006; 34(web server issue): W48-W51.
95. Nielsen JE. Analysing the pH-dependent properties of proteins using pKa calculations. J Mol Graph Model 2007; 25: 691-699.