Experimental evidence for the correlation of bond distances in peptide groups detected in ultrahigh-resolution protein structures.

The structural analysis of a deamidated derivative of ribonuclease A, determined at 0.87 A resolution, reveals a highly significant negative correlation between CN and CO bond distances in peptide groups. This trend, i.e. the CO bond lengthens when the CN bond shortens, is also found in seven out of eight protein structures, determined at ultrahigh resolution (<0.95 A). In five of them the linear correlation is statistically significant at the 95% confidence level. The present findings are consistent with the traditional view of amide resonance and, although already found in small peptide structures, they represent a new and important result. In fact, in a protein structure the fine details of the peptide geometry are only marginally affected by the crystal field and they are mostly produced by intramolecular and solvent interactions. The analysis of very high-resolution protein structures can reveal subtle information about local electronic features of proteins which may be critical to folding, function or ligand binding.

[1]  L. Vitagliano,et al.  The ultrahigh resolution crystal structure of ribonuclease A containing an isoaspartyl residue: hydration and sterochemical analysis. , 2000, Journal of molecular biology.

[2]  A. Cieplak.  Regression and principal component analyses of internal coordinates for the carboxamide and carboxylate groups. Diversity of amide bonding in primary carboxamides, oligopeptides, and lactams , 1994 .

[3]  R. Stein,et al.  Mechanistic studies of enzymic and nonenzymic prolyl cis-trans isomerization , 1992 .

[4]  P. Chakrabarti,et al.  Structural Characteristics of the Carboxylic Amide Group , 1982 .

[5]  R. Raines,et al.  Solvent Effects on the Energetics of Prolyl Peptide Bond Isomerization. , 1992, Journal of the American Chemical Society.

[6]  G J Williams,et al.  The Protein Data Bank: a computer-based archival file for macromolecular structures. , 1977, Journal of molecular biology.

[7]  R F Standaert,et al.  Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex , 1991, Science.

[8]  V. Lamzin,et al.  Crystal structure of the EF‐hand parvalbumin at atomic resolution (0.91 Å) and at low temperature (100 K). Evidence for conformational multistates within the hydrophobic core , 1999, Protein science : a publication of the Protein Society.

[9]  M. Wall,et al.  High-resolution macromolecular structure determination using CCD detectors and synchrotron radiation. , 1995, Structure.

[10]  Herman J. Geise,et al.  An ab initio study of crystal field effects, part 3: Solid- and gas-phase geometry of formamide, modeling the changes in a peptide group due to hydrogen bonds , 1991 .

[11]  F. Allen,et al.  The Cambridge Crystallographic Data Centre: computer-based search, retrieval, analysis and display of information , 1979 .

[12]  K S Wilson,et al.  Atomic resolution (0.94 A) structure of Clostridium acidurici ferredoxin. Detailed geometry of [4Fe-4S] clusters in a protein. , 1997, Biochemistry.

[13]  V S Lamzin,et al.  Refinement of triclinic hen egg-white lysozyme at atomic resolution. , 1998, Acta crystallographica. Section D, Biological crystallography.

[14]  Z. Dauter,et al.  Refinement of rubredoxin from Desulfovibrio vulgaris at 1.0 A with and without restraints. , 1992, Acta crystallographica. Section B, Structural science.

[15]  Z. Dauter,et al.  Experimental Observation of Bonding Electrons in Proteins* , 1999, The Journal of Biological Chemistry.

[16]  Péter G. Szalay,et al.  High-level electron correlation calculations on formamide and the resonance model , 1997 .

[17]  G. Sheldrick,et al.  SHELXL: high-resolution refinement. , 1997, Methods in enzymology.

[18]  C. Cambillau,et al.  Messages from ultrahigh resolution crystal structures. , 1998, Current opinion in structural biology.

[19]  Elizabeth D. Getzoff,et al.  Structure at 0.85 Å resolution of an early protein photocycle intermediate , 1998, Nature.

[20]  G. A. Jeffrey,et al.  Pyramidalization of carbonyl carbons in asymmetric environments: carboxylates, amides, and amino acids , 1985 .

[21]  Z. Ren,et al.  Synchrotron radiation applications to macromolecular crystallography. , 1997, Current opinion in structural biology.

[22]  Z. Dauter,et al.  The benefits of atomic resolution. , 1997, Current opinion in structural biology.

[23]  C. Robinson,et al.  Removal of the N‐terminal hexapeptide from human β2‐microglobulin facilitates protein aggregation and fibril formation , 2000, Protein science : a publication of the Protein Society.

[24]  V Lamzin,et al.  Ab initio solution and refinement of two high-potential iron protein structures at atomic resolution. , 1999, Acta crystallographica. Section D, Biological crystallography.

[25]  Macromolecular crystallography with a third-generation synchrotron source. , 1999, Acta crystallographica. Section D, Biological crystallography.

[26]  C. Breneman,et al.  Resonance interactions in acyclic systems. 3. Formamide internal rotation revisited. Charge and energy redistribution along the C-N bond rotational pathway , 1992 .

[27]  James Raftery,et al.  The structure of concanavalin A and its bound solvent determined with small-molecule accuracy at 0.94 [Aring ]resolution , 1997 .

[28]  V Lamzin,et al.  Accurate protein crystallography at ultra-high resolution: valence electron distribution in crambin. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  P. Kuhn,et al.  The 0.78 A structure of a serine protease: Bacillus lentus subtilisin. , 1998, Biochemistry.