The ultrahigh resolution crystal structure of ribonuclease A containing an isoaspartyl residue: Hydration and sterochemical analysis(679 views) Esposito L, Vitagliano L, Sica F, Sorrentino G, Zagari A, Mazzarella L
Affiliations: Centro Di Studio Di Biocristallografia, CNR, Università Di Napoli Federico II, Via Mezzocannone 4, I-80134, Napoli, Italy
References: Allen, F.H., Bellard, S., Brice, M.D., Cartwright, B.A., Doubleday, A., Higgs, H., Hummelink, T., Watson, D.G., The Cambridge Crystallographic Data Centre: Computer-based search, retrieval, analysis and display of information (1979) Acta Crystallog. Sect. B, 35, pp. 2331-233
Ashida, T., Tsunogae, Y., Tanaka, I., Yamane, T., Peptide chain structure parameters, bond angles and conformational angles from the Cambridge Structural Database (1987) Acta Crystallog. Sect. B, 43, pp. 212-218
Beintema, J.J., Schuller, C., Irie, M., Carsana, A., Molecular evolution of the ribonuclease superfamily (1988) Prog. Biophys. Mol. Biol., 51, pp. 165-192
Berisio, R., Lamzin, V.S., Sica, F., Wilson, K.S., Zagari, A., Mazzarella, L., Protein titration in the crystal state (1999) J. Mol. Biol., 292, pp. 845-854
Blokzijl, W.B., Engberts, J.B.F.N., Hydrophobic effects. Opinions and facts (1993) Angew. Chem. Int. Ed. Engl., 32, pp. 1545-1579
Brunger, A.T., Free R-value: A novel statistical quantity for assessing the accuracy of crystal structures (1992) Nature, 355, pp. 472-475
Brunger, A.T., (1993), X-PLOR version 3.1 Manual, Yale University Press, New Haven, USA, CTBurling, F.T., Weis, W.I., Flaherty, K.M., Brunger, A.T., Direct observation of protein solvation and discrete disorder with experimental crystallographic phases (1996) Science, 271, pp. 72-77
Capasso, S., Mazzarella, L., Sica, F., Zagari, A., Salvadori, S., Spontaneous cyclization of the aspartic acid side-chain to the succinimide derivative (1992) J. Chem. Soc. Chem. Commun., 12, pp. 919-921
Capasso, S., Di Donato, A., Esposito, L., Sica, F., Sorrentino, G., Vitagliano, L., Zagari, A., Mazzarella, L., Deamidation in proteins: The crystal structure of bovine pancreatic ribonuclease with an isoaspartyl residue at position 67 (1996) J. Mol. Biol., 257, pp. 492-496
Catanzano, F., Graziano, G., Capasso, S., Barone, G., Thermodynamic analysis of the effect of selective monodeamidation at asparagine 67 in ribonuclease A (1997) Protein Sci, 6, pp. 1682-1693
Clore, G.M., Bax, A., Omichinski, J.G., Gronenborn, A.M., Localization of bound water in the solution structure of a complex of the erythroid transcription factor GATA-1 with DNA (1994) Structure, 2, pp. 89-94
Dauter, Z., Lamzin, V.S., Wilson, K.S., The benefits of atomic resolution (1997) Curr. Opin. Struct. Biol., 7, pp. 681-688
DeMel, V.S.J., Martin, P.D., Dosher, M.S., Edwards, B.F.P., Structural changes that accompany the reduced catalytic efficiency of two semisynthetic ribonuclease analogs (1992) J. Biol. Chem., 267, pp. 247-256
DeMel, V.S.J., Dosher, M.S., Glinn, M.A., Martin, P.D., Ram, M.L., Edwards, B.F.P., Structural investigation of catalytically modified F120L and F120Y semisynthetic ribonucleases (1994) Protein Sci, 3, pp. 39-50
Derewenda, Z.S., Lee, L., Derewenda, V., The occurrence of C - H···O hydrogen bonds in proteins (1995) J. Mol. Biol., 252, pp. 248-262
Di Donato, A., Ciardiello, M.A., De Nigris, M., Piccoli, R., Mazzarella, L., D'Alessio, G., Selective deamidation of ribonuclease A (1993) J. Biol. Chem., 268, pp. 4745-4751
Engh, R.A., Huber, R., Accurate bond and angle parameters for X-ray protein structure refinement (1991) Acta Crystallog. Sect. A, 47, pp. 392-400
Esnouf, R.M., An extensively modified version of MolScript that includes greatly enhanced coloring capabilities (1997) J. Mol. Graph., 15, pp. 132-134
Wilson, K.S., Butterworth, S., Dauter, Z., Lamzin, V.S., Walsh, M., Wodak, S., Pontius, J., MacArthur, M.W., Who checks the checkers? (1998) J. Mol. Biol., 276, pp. 417-436
Fabiola, G.F., Krishnaswamy, S., Nagarajan, V., Pattabhi, V., C - H···O hydrogen bonds in β-sheets (1997) Acta Crystallog. Sect. D, 53, pp. 316-320
Fedorov, A.A., Joseph-McCarthy, D., Fedorov, E., Sirakova, D., Graf, I., Almo, S.C., Ionic interactions in crystalline bovine pancreatic ribonuclease A (1996) Biochemistry, 35, pp. 15962-15979
Fisher, B.M., Ha, J.-H., Raines, R.T., Coulombic forces in protein-RNA interactions: Binding and cleavage by ribonuclease A and variants at Lys7, Arg10, and Lys66 (1998) Biochemistry, 37, pp. 12121-12132
Fisher, B.M., Schultz, L.W., Raines, R.T., Coulombic effects of remote subsites on the active site of ribonuclease A (1998) Biochemistry, 37, pp. 17386-17401
Flocco, M.M., Mowbray, S.L., Strange bedfellows: Interactions between acidic side-chains in proteins (1995) J. Mol. Biol., 254, pp. 96-105
Garman, E.F., Schneider, T.R., Macromolecular cryocrystallography (1997) J. Appl. Crystallog., 30, pp. 211-237
Genick, U.K., Soltis, S.M., Kuhn, P., Canestrelli, I.L., Getzoff, E.D., Structure at 0.85 Å resolution of an early protein photocycle intermediate (1998) Nature, 392, pp. 206-209
Gilliland, G.L., Crystallographic studies of ribonuclease complexes (1997), pp. 305-341. , Ribonucleases: Structure and Functions (D'Alessio, G. and Riordan, J. F., eds), Academic Press, New YorkHerzberg, O., Moult, J., Analysis of the steric strain in the polypeptide backbone of protein molecules (1991) Proteins: Struct. Funct. Genet., 11, pp. 223-229
Hooft, R.W.W., Vriend, G., Sander, C., Abola, E.E., Errors in protein structures (1996) Nature, 381, p. 272
Jiang, X., Cao, M., Teppen, B., Newton, S., Schafer, L., Predictions of protein backbone structural parameters from first principles: Systematic comparisons of calculated N-Calpha-C' angles with high-resolution protein crystallographic results (1995) J. Phys. Chem., 99, pp. 10521-10525
Jones, T.A., Zou, J.Y., Cowan, S.W., Kjeldgaard, M., Improved methods for binding protein models in electron density maps and the location of errors in these models (1991) Acta Crystallog. Sect. A, 47, pp. 109-110
Kabsch, W., Sander, C., Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features (1983) Biopolymers, 22, pp. 2577-2637
Karplus, P.A., Experimentally observed conformation-dependent geometry and hidden strain in proteins (1996) Protein Sci, 5, pp. 1406-1420
Karplus, P.A., Schultz, G.E., Refined structure of glutathione reductase at 1.54 A resolution (1987) J. Mol. Biol., 195, pp. 701-729
Kraulis, P.J., MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures (1991) J. Appl. Crystallog., 24, pp. 946-950
Kuhn, P., Knapp, M., Soltis, S.M., Ganshaw, G., Thoene, M., Bott, R., The 0.78 Å structure of a serine protease: Bacillus lentus subtilisin (1998) Biochemistry, 37, pp. 13446-13452
Kumaraswamy, V.S., Lindley, P.F., Slingsby, C., Glover, I.D., An eye lens protein-water structure: 1.2 A resolution structure of γB-crystallin at 150 K (1996) Acta Crystallog. Sect. D, 52, pp. 611-622
Lamzin, V., Dauter, Z., Wilson, K.S., Dictionary of protein stereochemistry (1995) J. Appl. Crystallog., 28, pp. 338-340
Laskowski, R.A., MacArthur, M.W., Moss, D.S., Thornton, J.M., PROCHECK: A program to check the stereochemical quality of protein structures (1993) J. Appl. Crystallog., 26, pp. 283-291
Longhi, S., Czjzek, M., Cambillau, C., Messages from ultrahigh resolution crystal structures (1998) Curr. Opin. Struct. Biol., 8, pp. 730-737
MacArthur, M.W., Thornton, J.M., Deviations from planarity of the peptide bond in peptides and proteins (1996) J. Mol. Biol., 264, pp. 1180-1195
Martin, P.D., Doscher, M.S., Edwards, B.F.P., The refined crystal structure of a fully active semi-synthetic ribonuclease at 1.8 A resolution (1987) J. Biol. Chem., 262, pp. 15930-15938
Merrit, E.A., Murphy, M.E.P., RASTER3D version 2.0: A program for photorealistic molecular graphics (1994) Acta Crystallog. Sect. D, 50, pp. 869-879
Merritt, E.A., Kuhn, P., Sarfaty, S., Erbe, J.L., Holmes, R.K., Hol, W.G.J., The 1.25 A resolution refinement of the cholera toxin B-pentamer: Evidence of peptide backbone strain at the receptor-binding site (1998) J. Mol. Biol., 282, pp. 1043-1059
Morris, A.L., MacArthur, M.W., Hutchinson, E.G., Thornton, J.M., Stereochemical quality of protein structure coordinates (1992) Proteins: Struct. Funct. Genet., 12, pp. 345-364
Neidle, S., Berman, H.M., Shieh, H.S., Highly structured water network in crystals of a deoxydi-nucleoside-drug complex (1980) Nature, 288, pp. 129-133
Noguchi, S., Satow, Y., Uchida, T., Sasaki, C., Matsuzaki, T., Crystal structure of Ustilago sphaerogena ribonuclease U2 at 1.8 Å resolution (1995) Biochemistry, 34, pp. 15583-15591
Noguchi, S., Miyawaki, K., Satow, Y., Succinimide and isoaspartate residues in the crystal structures of hen gg-white lysozyme complexed with tri-N-acetylchitotriose (1998) J. Mol. Biol., 278, pp. 231-238
Otwinowski, Z., Minor, W., Processing of X-ray diffraction data collected in oscillation mode (1997) Methods Enzymol, 276, pp. 307-326
Raines, R.T., Ribonuclease A (1998) Chem. Rev., 98, pp. 1045-1065
Ramachandran, G.N., Sasisekharan, V., Conformation of polypeptides and proteins (1968) Advan. Protein Chem., 23, pp. 283-437
Richardson, R.M., Pares, X., Cuchillo, C.M., Chemical modification by pyridoxal 5'-phosphate and cyclohexane-1,2-dione indicates that Lys-7 and Arg-10 are involved in the p2 phosphate binding subsite of bovine pancreatic ribonuclease A (1990) Biochem. J., 267, pp. 593-599
Ridder, I.S., Rozeboom, H.J., Dijkstra, B.W., Haloalkane dehalogenase from Xanthobacter autotrophicus GJ10 refined at 1.15 A resolution (1999) Acta Crystallog. Sect. D, 55, pp. 1273-1290
Sandalova, T., Schneider, G., Kack, H., Lindqvist, Y., Structure of dethiobiotin synthetase at 0.97 Å resolution (1999) Acta Crystallog. Sect. D, 55, pp. 610-624
Santoro, J., Gonzales, C., Druix, M., Neira, J.L., Nieto, J.L., Herranz, J., Rico, M., High-resolution three-dimensional structure of ribonuclease A in solution by nuclear magnetic resonance spectroscopy (1993) J. Mol. Biol., 229, pp. 722-734
Schultz, L.W., Quirk, D.J., Raines, R.T., His···Asp catalytic dyad of ribonuclease A: Structure and function of the wild-type, D121N, and D121A enzymes (1998) Biochemistry, 37, pp. 8886-8898
Sevcik, J., Dauter, Z., Lamzin, V.S., Wilson, K.S., Ribonuclease from Streptomyces aureofaciens at atomic resolution (1996) Acta Crystallog. Sect. D, 52, pp. 327-344
Sheldrick, G.M., Phase annealing in SHELX-90: Direct methods for larger structures (1990) Acta Crystallog. Sect. A, 46, pp. 467-473
Teeter, M.M., Water structure of a hydrophobic protein at atomic resolution: Pentagon rings of a water molecules in crystals of crambin (1984) Proc. Natl. Acad. Sci. USA, 81, pp. 6014-6018
Teeter, M.M., Roe, S.M., Heo, N.H., Atomic resolution (0.83 A) crystal structure of the hydrophobic protein crambin at 130 K (1993) J. Mol. Biol., 230, pp. 292-311
Thanki, N., Thornton, J.M., Goodfellow, J.M., Distribution of water around amino acids in proteins (1988) J. Mol. Biol., 202, pp. 637-657
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 (1999) Acta Crystallog. Sect. D, 54, pp. 522-546
Wilson, A.J.C., Determination of absolute from relative X-ray data intensities (1942) Nature, 150, pp. 151-152
Wlodawer, A., Anders, L.A., Sjolin, L., Gilliland, G.L., Structure of phosphate-free ribonuclease A refined at 1.26 Å (1988) Biochemistry, 2, pp. 2705-2717
Allen, F. H., Bellard, S., Brice, M. D., Cartwright, B. A., Doubleday, A., Higgs, H., Hummelink, T., Watson, D. G., The Cambridge Crystallographic Data Centre: Computer-based search, retrieval, analysis and display of information (1979) Acta Crystallog. Sect. B, 35, pp. 2331-233
Beintema, J. J., Schuller, C., Irie, M., Carsana, A., Molecular evolution of the ribonuclease superfamily (1988) Prog. Biophys. Mol. Biol., 51, pp. 165-192
Blokzijl, W. B., Engberts, J. B. F. N., Hydrophobic effects. Opinions and facts (1993) Angew. Chem. Int. Ed. Engl., 32, pp. 1545-1579
Brunger, A. T., Free R-value: A novel statistical quantity for assessing the accuracy of crystal structures (1992) Nature, 355, pp. 472-475
Brunger, A. T., (1993), X-PLOR version 3. 1 Manual, Yale University Press, New Haven, USA, CTBurling, F. T., Weis, W. I., Flaherty, K. M., Brunger, A. T., Direct observation of protein solvation and discrete disorder with experimental crystallographic phases (1996) Science, 271, pp. 72-77
Clore, G. M., Bax, A., Omichinski, J. G., Gronenborn, A. M., Localization of bound water in the solution structure of a complex of the erythroid transcription factor GATA-1 with DNA (1994) Structure, 2, pp. 89-94
DeMel, V. S. J., Martin, P. D., Dosher, M. S., Edwards, B. F. P., Structural changes that accompany the reduced catalytic efficiency of two semisynthetic ribonuclease analogs (1992) J. Biol. Chem., 267, pp. 247-256
DeMel, V. S. J., Dosher, M. S., Glinn, M. A., Martin, P. D., Ram, M. L., Edwards, B. F. P., Structural investigation of catalytically modified F120L and F120Y semisynthetic ribonucleases (1994) Protein Sci, 3, pp. 39-50
Derewenda, Z. S., Lee, L., Derewenda, V., The occurrence of C - H O hydrogen bonds in proteins (1995) J. Mol. Biol., 252, pp. 248-262
Engh, R. A., Huber, R., Accurate bond and angle parameters for X-ray protein structure refinement (1991) Acta Crystallog. Sect. A, 47, pp. 392-400
Esnouf, R. M., An extensively modified version of MolScript that includes greatly enhanced coloring capabilities (1997) J. Mol. Graph., 15, pp. 132-134
Wilson, K. S., Butterworth, S., Dauter, Z., Lamzin, V. S., Walsh, M., Wodak, S., Pontius, J., MacArthur, M. W., Who checks the checkers? (1998) J. Mol. Biol., 276, pp. 417-436
Fabiola, G. F., Krishnaswamy, S., Nagarajan, V., Pattabhi, V., C - H O hydrogen bonds in -sheets (1997) Acta Crystallog. Sect. D, 53, pp. 316-320
Fedorov, A. A., Joseph-McCarthy, D., Fedorov, E., Sirakova, D., Graf, I., Almo, S. C., Ionic interactions in crystalline bovine pancreatic ribonuclease A (1996) Biochemistry, 35, pp. 15962-15979
Fisher, B. M., Ha, J. -H., Raines, R. T., Coulombic forces in protein-RNA interactions: Binding and cleavage by ribonuclease A and variants at Lys7, Arg10, and Lys66 (1998) Biochemistry, 37, pp. 12121-12132
Fisher, B. M., Schultz, L. W., Raines, R. T., Coulombic effects of remote subsites on the active site of ribonuclease A (1998) Biochemistry, 37, pp. 17386-17401
Flocco, M. M., Mowbray, S. L., Strange bedfellows: Interactions between acidic side-chains in proteins (1995) J. Mol. Biol., 254, pp. 96-105
Garman, E. F., Schneider, T. R., Macromolecular cryocrystallography (1997) J. Appl. Crystallog., 30, pp. 211-237
Genick, U. K., Soltis, S. M., Kuhn, P., Canestrelli, I. L., Getzoff, E. D., Structure at 0. 85 resolution of an early protein photocycle intermediate (1998) Nature, 392, pp. 206-209
Gilliland, G. L., Crystallographic studies of ribonuclease complexes (1997), pp. 305-341. , Ribonucleases: Structure and Functions (D'Alessio, G. and Riordan, J. F., eds), Academic Press, New YorkHerzberg, O., Moult, J., Analysis of the steric strain in the polypeptide backbone of protein molecules (1991) Proteins: Struct. Funct. Genet., 11, pp. 223-229
Hooft, R. W. W., Vriend, G., Sander, C., Abola, E. E., Errors in protein structures (1996) Nature, 381, p. 272
Jones, T. A., Zou, J. Y., Cowan, S. W., Kjeldgaard, M., Improved methods for binding protein models in electron density maps and the location of errors in these models (1991) Acta Crystallog. Sect. A, 47, pp. 109-110
Karplus, P. A., Experimentally observed conformation-dependent geometry and hidden strain in proteins (1996) Protein Sci, 5, pp. 1406-1420
Karplus, P. A., Schultz, G. E., Refined structure of glutathione reductase at 1. 54 A resolution (1987) J. Mol. Biol., 195, pp. 701-729
Kleywegt, G. J., Jones, T. A., Phi/Psi-chology: Ramachandran revisited (1996) Structure, 4, pp. 1395-1400
Kraulis, P. J., MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures (1991) J. Appl. Crystallog., 24, pp. 946-950
Kumaraswamy, V. S., Lindley, P. F., Slingsby, C., Glover, I. D., An eye lens protein-water structure: 1. 2 A resolution structure of B-crystallin at 150 K (1996) Acta Crystallog. Sect. D, 52, pp. 611-622
Laskowski, R. A., MacArthur, M. W., Moss, D. S., Thornton, J. M., PROCHECK: A program to check the stereochemical quality of protein structures (1993) J. Appl. Crystallog., 26, pp. 283-291
MacArthur, M. W., Thornton, J. M., Deviations from planarity of the peptide bond in peptides and proteins (1996) J. Mol. Biol., 264, pp. 1180-1195
Martin, P. D., Doscher, M. S., Edwards, B. F. P., The refined crystal structure of a fully active semi-synthetic ribonuclease at 1. 8 A resolution (1987) J. Biol. Chem., 262, pp. 15930-15938
Merrit, E. A., Murphy, M. E. P., RASTER3D version 2. 0: A program for photorealistic molecular graphics (1994) Acta Crystallog. Sect. D, 50, pp. 869-879
Merritt, E. A., Kuhn, P., Sarfaty, S., Erbe, J. L., Holmes, R. K., Hol, W. G. J., The 1. 25 A resolution refinement of the cholera toxin B-pentamer: Evidence of peptide backbone strain at the receptor-binding site (1998) J. Mol. Biol., 282, pp. 1043-1059
Morris, A. L., MacArthur, M. W., Hutchinson, E. G., Thornton, J. M., Stereochemical quality of protein structure coordinates (1992) Proteins: Struct. Funct. Genet., 12, pp. 345-364
Raines, R. T., Ribonuclease A (1998) Chem. Rev., 98, pp. 1045-1065
Ramachandran, G. N., Sasisekharan, V., Conformation of polypeptides and proteins (1968) Advan. Protein Chem., 23, pp. 283-437
Richardson, R. M., Pares, X., Cuchillo, C. M., Chemical modification by pyridoxal 5'-phosphate and cyclohexane-1, 2-dione indicates that Lys-7 and Arg-10 are involved in the p2 phosphate binding subsite of bovine pancreatic ribonuclease A (1990) Biochem. J., 267, pp. 593-599
Ridder, I. S., Rozeboom, H. J., Dijkstra, B. W., Haloalkane dehalogenase from Xanthobacter autotrophicus GJ10 refined at 1. 15 A resolution (1999) Acta Crystallog. Sect. D, 55, pp. 1273-1290
Schultz, L. W., Quirk, D. J., Raines, R. T., His Asp catalytic dyad of ribonuclease A: Structure and function of the wild-type, D121N, and D121A enzymes (1998) Biochemistry, 37, pp. 8886-8898
Sheldrick, G. M., Phase annealing in SHELX-90: Direct methods for larger structures (1990) Acta Crystallog. Sect. A, 46, pp. 467-473
Sheldrick, G. M., Schneider, T. R., SHELXL: High-resolution refinement (1997) Methods Enzymol., 277, pp. 319-343
Teeter, M. M., Water structure of a hydrophobic protein at atomic resolution: Pentagon rings of a water molecules in crystals of crambin (1984) Proc. Natl. Acad. Sci. USA, 81, pp. 6014-6018
Teeter, M. M., Roe, S. M., Heo, N. H., Atomic resolution (0. 83 A) crystal structure of the hydrophobic protein crambin at 130 K (1993) J. Mol. Biol., 230, pp. 292-311
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 (1999) Acta Crystallog. Sect. D, 54, pp. 522-546
Wilson, A. J. C., Determination of absolute from relative X-ray data intensities (1942) Nature, 150, pp. 151-152
The ultrahigh resolution crystal structure of ribonuclease A containing an isoaspartyl residue: Hydration and sterochemical analysis
Crystals of the deamidated form of bovine pancreatic ribonuclease which contains an isoaspartyl residue in position 67 diffract to 0.87 Angstrom at 100 K. We have refined the crystallographic model using anisotropic displacement parameters for all atoms to a conventional crystallographic residual R = 0.101 for all observed reflections in the resolution range 61.0-0.87 Angstrom. The ratio observations /parameters is 7.2 for the final model. This structure represents one of the highest resolution protein structures to date and interestingly, it is the only example containing more than one molecule in the asymmetric unit with a resolution better than 1.0 Angstrom. The non-crystallographic symmetry has been used as a validation check of the geometrical parameters and it has allowed an estimate for an upper limit of errors associated with this high resolution model. In the present structure it was possible to obtain a more accurate picture of the active site whose electron density was not clearly interpretable in the previous 1.9 Angstrom resolution structure. In particular, the P1 site is alternatively occupied either by a sulphate anion or by a water molecule network. Most of hydrogen atoms were visible in the electron density maps, including those involved in C-alpha-H-alpha ... O interactions. Analysis of protein-solvent interactions has revealed the occurrence of an extensive cluster of water molecules, predominantly arranged in pentagonal fused rings and surrounding hydrophobic moiety of side-chains. Finally, in spite of the limited sample of residues, we have detected a clear dependence of backbone N-C-alpha-C angle on residue conformation. This correlation can be fruitfully used as a valuable tool in protein structure validation. (C) 2000 Academic Press.
The ultrahigh resolution crystal structure of ribonuclease A containing an isoaspartyl residue: Hydration and sterochemical analysis