An evaluation review of the prediction of protonation states in proteins versus crystallographic experiment

Crystallography Reviews

Volumn 15, Issue 4, 2009, Pages 231-259

  Fisher, Stuart J ^a,b   Wilkinson, James ^a   Henchman, Richard H ^a   Helliwell, John R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b INSTITUT LAUE LANGEVIN   (France)

Author keywords

Amino acids; Neutron crystallography; NMR; Protein pKa predictions; Protonation states; X ray crystallography

Indexed keywords

CALCULATION TOOLS; CRYSTALLOGRAPHIC DATA; HISTIDINE RESIDUES; NEUTRON CRYSTALLOGRAPHY; PROTEIN CRYSTAL; PROTONATION STATE; PROTONATION STATES;

AMINO ACIDS; FORECASTING; MINERALOGY; NEUTRONS; NUCLEAR MAGNETIC RESONANCE; ORGANIC ACIDS; PHOSPHATASES; PROTEINS; PROTONATION; SELF ASSEMBLY;

X RAY CRYSTALLOGRAPHY;

EID: 77951431536     PISSN: 0889311X     EISSN: 14763508     Source Type: Journal    
DOI: 10.1080/08893110903213700     Document Type: Article

References (65)

1. Bon, C.; Lehmann, M.S.; Wilkinson, C. Quasi-Laue Neutron-Diffraction Study of the Water Arrangement in Crystals of Triclinic Hen Egg-Ehite Lysozyme. Acta Crystallogr. D 1999, 55, 978-987. (Pubitemid 29235595)
2. Kossiakoff, A.A.; Spencer, S.A. Neutron Diffraction Identifies His 57 as the Catalytic Base in Trypsin. Nature 1980, 288, 414-416.
3. Vriend, G. WHAT IF: A Molecular Modeling and Drug Design Program. J. Mol. Graph. Model. 1990, 8, 52-56. (Pubitemid 20717037)
4. Nielsen, J.E.; Andersen, K.V.; Honig, B.; Hooft, R.W.W.; Klebe, G.; Vriend, G.; Wade, R.C. Improving Macromolecular Electrostatics Calculations. Protein Eng. 1999, 12, 657-662. (Pubitemid 29425550)
5. Blakeley, M.P. Neutron Macromolecular Crystallography. Crystallogr. Rev. 2009, 15, 157-218.
6. Liljas, A.; Liljas, L.; Piskur, J.; Lindblom, G.; Nissen, P.; Kjeldgaard, M. Textbook of Structural Biology; Singapore: World Scientific, 2009; p. 14.
7. Li, H.; Robertson, A.D.; Jensen, J.H. Very Fast Empirical Prediction and Rationalization of Protein pKa Values. Proteins: Structure, Function, Bioinform. 2005, 61, 704-721. (Pubitemid 41753142)
8. Steitz, T.A.; Shulman, R.G. Crystallographic and NMR Studies of the Serine Proteases. Ann. Rev. Biophys. Bioeng. 1982, 11, 419-444.
9. Szyperski, T.; Antuch, W.; Schick, M.; Betz, A.; Stone, S.R.; Wuthrich, K. Transient Hydrogen Bonds Identified on the Surface of the NMR Solution Structure of Hirudin. Biochemistry 1994, 33, 9303-9310. (Pubitemid 24272882)
10. Šdergaard, C.R.; McIntosh, L.P.; Pollastri, G.; Nielsen, J.E. Determination of Electrostatic Interaction Energies and Protonation State Populations in Enzyme Active Sites. J. Mol. Biol. 2008, 376, 269-287.
11. Powers, N.; Jensen, J.H. Chemically Accurate Protein Structures: Validation of Protein NMR Structures by Comparison of Measured and Predicted pKa Values. J. Biomol. NMR 2006, 35, 39-51. (Pubitemid 43947777)
12. Gordon, J.C.; Myers, J.B.; Folta, T.; Shoja, V.; Heath, L.S.; Onufriev, A. H++: A Server for Estimating pKa's and Adding Missing Hydrogens to Macromolecules. Nucl. Acids Res. 2005, 33, W368-371. (Pubitemid 44529945)
13. Georgescu, R.E.; Alexov, E.G.; Gunner, M.R. Combining Conformational Flexibility and Continuum Electrostatics for Calculating pKa's in Proteins. Biophys. J. 2002, 83, 1731-1748.
14. Mongan, J.; Case, D.A. Biomolecular Simulations at Constant pH. Curr. Opin. Struct. Biol. 2005, 15, 157-163. (Pubitemid 40503335)
15. Li, X.; Jacobson, M.P.; Zhu, K.; Zhao, S.; Friesner, R.A. Assignment of Polar States for Protein Amino Acid Residues using an Interaction Cluster Decomposition Algorithm and its Application to High Resolution Protein Structure Modeling. Proteins 2007, 66, 824-837. (Pubitemid 46273068)
16. Bashford, D. Macroscopic Electrostatic Models for Protonation States in Proteins. Front. Biosci. 2004, 9, 1082-1099. (Pubitemid 39060831)
17. Kuhn, B.; Kollman, P.A.; Stahl, M. Prediction of pKa Shifts in Proteins Using a Combination of Molecular Mechanical and Continuum Solvent Calculations. J. Comput. Chem. 2004, 25, 1865-1872.
18. Liptak, M.D.; Shields, G.C. Accurate pKa Calculations for Carboxylic Acids Using Complete Basis Set and Gaussian-n Models Combined with CPCM Continuum Solvation Methods. J. Am. Chem. Soc. 2001, 123, 7314-7319. (Pubitemid 32879445)
19. Nielsen, J.E. Analysing the pH-Dependent Properties of Proteins Using pKa Calculations. J. Mol. Graph. Modell. 2007, 25, 691-699.
20. Simonson, T.; Carlsson, J.; Case, D.A. Proton Binding to Proteins: pKa Calculations with Explicit and Implicit Solvent Models. J. Am. Chem. Soc. 2004, 126, 4167-4180. (Pubitemid 38453876)
21. Shurki, A.; Warshel, A. Structure/Function Correlations of Proteins using MM, QM/MM, and Related Approaches: Methods, Concepts, Pitfalls, and Current Progress. Adv. Prot. Chem. 2003, 66, 249-313. (Pubitemid 37392318)
22. Ivanov, I.; Chen., B.; Raugei, S.; Klein, M.L. Relative pKa Values from First-Principles Molecular Dynamics: The Case of Histidine Deprotonation. J. Phys. Chem. B 2006, 110, 6365-6371.
23. Warwicker, J. Improved pKa Calculations through Flexibility Based Sampling of a Water- Dominated Interaction Scheme. Prot. Sci. 2004, 13, 2793-2805. (Pubitemid 39274646)
24. Alexov, E.G.; Gunner, M.R. Incorporating Protein Conformational Flexibility into the Calculation of pH-Dependent Protein Properties. Biophys. J. 1997, 72, 2075-2093.
25. Davies, M.N.; Toseland, C.P.; Moss, D.S.; Flower, D.R. Benchmarking pKa Prediction. BMC Biochemistry 2006, 7, 18.
26. Hasselbalch, K.A. Die Berechnung der Wassersroffzahl des Blutes ous der freien und gebunden Kohlensaure desselben, und die Sauerstoffbindung des Blutes als Funktion der Wasserstoffzahl. Biochem. Z. 1917, 78, 112-144.
27. Kalb (Gilboa), A.J.; Helliwell, J.R. Concanavalin A. In Handbook of Metalloproteins; Messerschmidt, A., Huber, R., Poulos, T., Weghardt, K., Eds.; New York: John Wiley, 2001; pp. 963-1372
28. Weis, W.I.; Drickamer, K. Structural Basis of Lectin-Carbohydrate Recognition. Ann. Rev. Biochem. 1996, 65, 441-473. (Pubitemid 26250616)
29. Deacon, A.; Gleichmann, T.; Kalb (Gilboa), A.J.; Price, H.; Raftery, J.; Bradbrook, G.; Yariv, J.; Helliwell, J.R. The Structure of Concanavalin A and its Bound Solvent Determined with Small-Molecule Accuracy at 0.94A-Resolution. J. Chem. Soc., Faraday Trans. 1997, 93, 4305-4312. (Pubitemid 127820971)
30. Sumner, J.B. The Globulins of the Jack Bean, Canavalia ensiformis. J. Biol. Chem. 1919, 37, 137-141.
31. Carrell, H.L.; Rubin, B.H.; Hurley, T.J.; Glusker, J.P. X-ray Crystal Structure of D-Xylose Isomerase at 4A - Resolution. J. Biol. Chem. 1984, 259, 3230-3236. (Pubitemid 14159449)
32. Katz, A.K.; Li, X.; Carrell, H.L.; Hanson, B.L.; Langan, P.; Coates, L.; Schoenborn, B.P.; Glusker, J.P.; Bunick, G.J. Locating Active-Site Hydrogen Atoms in D-Xylose Isomerase: Time-of-Flight Neutron Diffraction. Proc. Natl Acad. Sci. 2006, 103, 8342-8347. (Pubitemid 43838457)
33. Ostermann, A.; Tanaka, I.; Engler, N.; Niimura, N.; Parak, F.G. Hydrogen and Deuterium in Myoglobin as seen by a Neutron Structure Determination at 1.5A - Resolution. Biophys. Chem. 2002, 95, 183-193. (Pubitemid 34327273)
34. Ahmed, H.U.; Blakeley, M.P.; Cianci, M.; Hubbard, J.A.; Helliwell, J.R.; Cruickshank, D.W.J. The Determination of Protonation States in Proteins. Acta Crystallogr. D 2007, 63, 906-922. (Pubitemid 47094573)
35. Parkin, S.; Rupp, B.; Hope, H. Atomic Resolution Structure of Concanavalin A at 120 K. Acta Crystallogr. D 1996, 52, 1161-1168. (Pubitemid 27093820)
36. Collaborative Computational Project 4 The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr. D 1994, 50, 760-763.
37. Carrell, H.L.; Hoier, H.; Glusker, J.P. Modes of Binding Substrates and their Analogues to the Enzyme D-Xylose Isomerase. Acta Crystallogr. D 1994, 50, 113-123. (Pubitemid 2054261)
38. Wang, J.; Dauter, M.; Alkire, R.; Joachimiak, A.; Dauter, Z. Triclinic lysozyme at 0.65A - Resolution. Acta Crystallogr. D 2007, 63, 1254-1268.
39. Walsh, M.A.; Schneider, T.R.; Sieker, L.C.; Dauter, Z.; Lamzin, V.S.; Wilson, K.S. Refinement of Triclinic Hen Egg-White Lysozyme at Atomic Resolution. Acta Crystallogr. D 1998, 54, 522-546. (Pubitemid 28343795)
40. Bartik, K.; Redfield, C.; Dobson, C.M. Measurement of the Individual pKa Values of Acidic Residues of Hen and Turkey Lysozymes by Two-Dimensional 1H NMR. Biophys. J. 1994, 66, 1180-1184. (Pubitemid 24106364)
41. Arcovito, A.; Benfatto, M.; Cianci, M.; Hasnain, S.S.; Nienhaus, K.; Nienhaus, G.U.; Savino, C.; Strange, R.W.; Vallone, B.; Della Longa, S. X-ray Structure Analysis of a Metalloprotein with Enhanced Active-site Resolution Using in situ X-Ray Absorption near Edge Structure Spectroscopy. Proc. Natl Acad. Sci. 2007, 104, 6211-6216.
42. Vojtchovsky̌, J.; Chu, K.; Berendzen, J.; Sweet, R.M.; Schlichting, I. Crystal Structures of Myoglobin-Ligand Complexes at Near-Atomic Resolution. Biophys J. 1999, 77, 2153-2174.
43. Dalvit, C.; Wright, P.E. Assignment of Resonances in the 1H Nuclear Magnetic Resonance Spectrum of the Carbon Monoxide Complex of Sperm Whale Myoglobin by Phase-Sensitive Two-Dimensional Techniques. J. Mol. Biol. 1987, 194, 313-327.
44. O?sapay, K.; Theriault, Y.; Wright, P.E.; Case, D.A. Solution Structure of Carbonmonoxy Myoglobin Determined from Nuclear Magnetic Resonance Distance and Chemical Shift Constraints. J. Mol. Biol. 1994, 244, 183-197.
45. Cocco, M.J.; Kao, Y.H.; Phillips, A.T.; Lecomte, J.T.J. Structural Comparison of Apomyoglobin and Metaquomyoglobin: pH Titration of Histidines by NMR Spectroscopy. Biochemistry 1992, 31, 6481-6491.
46. Fisher, S.J.; Helliwell, J.R. An Investigation into Structural Changes due to Deuteration. Acta Crystallogr. A 2008, 64, 359-367.
47. Berisio, R.; Sica, F.; Lamzin, V.S.; Wilson, K.S.; Zagari, A.; Mazzarella, L. Atomic resolution structures of ribonuclease A at six pH values. Acta Crystallogr. D - Biol. Crystallogr. 2002, 58, 441-450.
48. Wlodawer, A.; Sjolin, L. Structure of Ribonuclease-A - Results of Joint Neutron and X-Ray Refinement at 2.0A - Resolution. Biochemistry 1983, 22, 2720-2728.
49. Berisio, R.; Lamzin, V.S.; Sica, F.; Wilson, K.S.; Zagari, A.; Mazzarella, L. Protein Titration in the Crystal State. J. Mol. Biol. 1999, 292, 845-854.
50. Tilton, R.F.; Dewan, J.C.; Petsko, G.A. Effects of Temperature on Protein-Structure and Dynamics - X-Ray Crystallographic Studies of the Protein Ribonuclease-A at 9 Different Temperatures from 98-K to 320-K. Biochemistry 1992, 31, 2469-2481.
51. Cuchillo, C.M.; Vilanova, M.; Nogues, M.V. Pancreatic ribonucleases. Pancreatic Ribonucleases in Ribonucleases: Structures and Functions; Academic Press: New York, 1997; pp. 271-300.
52. Quirk, D.J.; Raines, R.T. His . . . Asp Catalytic Dyad of Ribonuclease A: Histidine pKa Values in the Wild-Type, D121N, and D121A Enzymes. Biophys. J. 1999, 76, 1571-1579.
53. Wlodawer, A.; Borkakoti, N.; Moss, D.S.; Howlin, B. Comparison of Two Independently Refined Models of Ribonuclease-A. Acta Crystallogr. B 1986, 42, 379-387.
54. Varnai, P.; Warshel, A. Computer Simulation Studies of the Catalytic Mechanism of Human Aldose Reductase. J. Am. Chem. Soc. 2000, 122, 3849-3860.
55. Ruiz, F.; Hazemann, I.; Mitschler, A.; Joachimiak, A.; Schneider, T.; Karplus, M.; Podjarny, A. The Crystallographic Structure of the Aldose Reductase-IDD552 Complex Shows Direct Proton Donation from Tyrosine 48. Acta Crystallogr. D - Biol. Crystallogr. 2004, 60, 1347-1354.
56. Ondrechen, M.J.; Clifton, J.G.; Ringe, D. THEMATICS: A Simple Computational Predictor of Enzyme Function from Structure. Proc. Natl Acad. Sci. USA 2001, 98, 12473-12478.
57. Quarmby, R.; Nordens, D.A.; Zagalsky, P.F.; Ceccaldi, H.J.; Daumas, R. Studies on the Quaternary Structure of the Lobster Exoskeleton Carotenoprotein, Crustacyanin. Comparative Biochem. Physiol. B: Biochem. Mol. Biol. 1977, 56, 55-61.
58. Cianci, M.; Rizkallah, P.J.; Olczak, A.; Raftery, J.; Chayen, N.E.; Zagalsky, P.F.; Helliwell, J.R. The Molecular Basis of the Coloration Mechanism in Lobster Shell: Beta-Crustacyanin at 3.2A-Resolution. Proc. Natl Acad. Sci. 2002, 99, 9795-9800.
59. DeLano, W.L. The PyMOL Molecular Graphics System. http://www.pymol.org 2002.
60. Wijk, A.A.C.; Spaans, A.; Uzunbajakava, N.; Otto, C.; deGroot, H.J.M.; Lugtenburg, J.; Buda, F. Spectroscopy and Quantum Chemical Modeling Reveal a Predominant Contribution of Excitonic Interactions to the Bathochromic Shift in-Crustacyanin, the Blue Carotenoprotein in the Carapace of the Lobster Homarus gammarus. J. Am. Chem. Soc. 2005, 127, 1438-1445.
61. Durbeej, B.; Eriksson, L.A. Protein-Bound Chromophores Astaxanthin and Phytochromoblilin: Excited State Quantum Chemical Studies. Phys. Chem. Chem. Phys. 2006, 8, 4053.
62. Gordon, E.J.; Leonard, G.A.; McSweeney, S.; Zagalsky, P.F. The C1 Subunit of [alpha]- Crustacyanin: The de novo Phasing of the Crystal Structure of a 40 kDa Homodimeric Protein Using the Anomalous Scattering from S Atoms Combined with direct Methods. Acta Crystallogr. D 2001, 57, 1230-1237.
63. Cianci, M.; Rizkallah, P.J.; Olczak, A.; Raftery, J.; Chayen, N.E.; Zagalsky, P.F.; Helliwell, J.R. Structure of Lobster Apocrustacyanin A1 Using Softer X-Rays. Acta Crystallogr. D 2001, 57, 1219-1229.
64. Habash, J.; Helliwell, J.R.; Raftery, J.; Cianci, M.; Rizkallah, P.J.; Chayen, N.E.; Nneji, G.A.; Zagalsky, P.F. The Structure and Refinement of Apocrustacyanin C2 to 1.3A -Resolution and the Search for Differences between this Protein and the Homologous Apoproteins A1 and C1. Acta Crystallogr. D 2004, 60, 493-498.
65. Habash, J.; Boggon, T.J.; Raftery, J.; Chayen, N.E.; Zagalsky, P.F.; Helliwell, J.R. Apocrustacyanin C1 Crystals Grown in Space and on Earth Using Vapour-Diffusion Geometry: Protein Structure Refinements and Electron-Density Map Comparisons. Acta Crystallogr. D 2003, 59, 1117-1123