Cis–trans isomerization of omega dihedrals in proteins

Peptide bonds in protein structures are mainly found in trans conformation with a torsion angle ω close to 180°. Only a very low proportion is observed in cis conformation with ω angle around 0°. Cis–trans isomerization leads to local conformation changes which play an important role in many biological processes. In this paper, we reviewed the recent discoveries and research achievements in this field. First, we presented some interesting cases of biological processes in which cis–trans isomerization is directly implicated. It is involved in protein folding and various aspect of protein function like dimerization interfaces, autoinhibition control, channel gating, membrane binding. Then we reviewed conservation studies of cis peptide bonds which emphasized evolution constraints in term of sequence and local conformation. Finally we made an overview of the numerous molecular dynamics studies and prediction methodologies already developed to take into account this structural feature in the research area of protein modeling. Many cis peptide bonds have not been recognized as such due to the limited resolution of the data and to the refinement protocol used. Cis–trans proline isomerization reactions represents a vast and promising research area that still needs to be further explored for a better understanding of isomerization mechanism and improvement of cis peptide bond predictions.

[1]  C. Deber,et al.  Hypothesis about the function of membrane-buried proline residues in transport proteins. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Dimitrios I. Fotiadis,et al.  PBOND: Web Server for the Prediction of Proline and Non-Proline cis/trans Isomerization , 2009, Genom. Proteom. Bioinform..

[3]  A. Ryo,et al.  Pin1 Regulates Centrosome Duplication, and Its Overexpression Induces Centrosome Amplification, Chromosome Instability, and Oncogenesis , 2006, Molecular and Cellular Biology.

[4]  Y. Kang.  Conformational preferences of non-prolyl and prolyl residues. , 2006, The journal of physical chemistry. B.

[5]  T. Darden,et al.  Trans-cis isomerization of proline 22 in bovine prothrombin fragment 1: a surprising result of structural characterization. , 1998, Biochemistry.

[6]  A. Miranker,et al.  A native to amyloidogenic transition regulated by a backbone trigger , 2006, Nature Structural &Molecular Biology.

[7]  A T Brünger,et al.  Proline cis‐trans isomerization in staphylococcal nuclease: Multi‐substate free energy perturbation calculations , 1995, Protein science : a publication of the Protein Society.

[8]  K. Gunasekaran,et al.  Disallowed Ramachandran conformations of amino acid residues in protein structures. , 1996, Journal of molecular biology.

[9]  R. Birge,et al.  Proline cis-trans isomerization controls autoinhibition of a signaling protein. , 2007, Molecular cell.

[10]  G. N. Ramachandran,et al.  Conformation of polypeptides and proteins. , 1968, Advances in protein chemistry.

[11]  D. Raleigh,et al.  Local control of peptide conformation: stabilization of cis proline peptide bonds by aromatic proline interactions. , 1998, Biopolymers.

[12]  M-L Wang,et al.  Support vector machines for prediction of peptidyl prolyl cis/trans isomerization. , 2008, The journal of peptide research : official journal of the American Peptide Society.

[13]  A. Jabs,et al.  Non-proline cis peptide bonds in proteins. , 1999, Journal of molecular biology.

[14]  W. Steigemann,et al.  Two cis‐prolines in the Bence‐Jones protein Rei and the cis‐pro‐bend , 1974, FEBS letters.

[15]  Paramita Sarkar,et al.  Structural basis for regulation of the Crk signaling protein by a proline switch , 2010, Nature chemical biology.

[16]  A. Toro‐Labbé,et al.  How does Pin1 catalyze the cis-trans prolyl peptide bond isomerization? A QM/MM and mean reaction force study. , 2012, The journal of physical chemistry. B.

[17]  Henry A. Lester,et al.  Cis–trans isomerization at a proline opens the pore of a neurotransmitter-gated ion channel , 2005, Nature.

[18]  G J Williams,et al.  The Protein Data Bank: a computer-based archival file for macromolecular structures. , 1978, Archives of biochemistry and biophysics.

[19]  The mean reaction force: a method to study the influence of the environment on reaction mechanisms. , 2011, The Journal of chemical physics.

[20]  R. L. Baldwin,et al.  Acid catalysis of the formation of the slow-folding species of RNase A: evidence that the reaction is proline isomerization. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Avijit Chakrabartty,et al.  Autoinhibition of the Kit Receptor Tyrosine Kinase by the Cytosolic Juxtamembrane Region , 2003, Molecular and Cellular Biology.

[22]  C. Etchebest,et al.  Bayesian probabilistic approach for predicting backbone structures in terms of protein blocks , 2000, Proteins.

[23]  Eric Darve,et al.  Adaptive biasing force method for scalar and vector free energy calculations. , 2008, The Journal of chemical physics.

[24]  J E Wampler,et al.  Occurrence and role of cis peptide bonds in protein structures. , 1990, Journal of molecular biology.

[25]  Bohdan Schneider,et al.  A short survey on protein blocks , 2010, Biophysical Reviews.

[26]  Alexandre G de Brevern,et al.  αIIbβ3 integrin: new allelic variants in Glanzmann thrombasthenia, effects on ITGA2B and ITGB3 mRNA splicing, expression, and structure–function , 2010, Human mutation.

[27]  A G Murzin,et al.  SCOP: a structural classification of proteins database for the investigation of sequences and structures. , 1995, Journal of molecular biology.

[28]  P. Y. Chou,et al.  Conformational parameters for amino acids in helical, beta-sheet, and random coil regions calculated from proteins. , 1974, Biochemistry.

[29]  J. Thornton,et al.  Deviations from planarity of the peptide bond in peptides and proteins. , 1996, Journal of molecular biology.

[30]  D T Jones,et al.  Protein secondary structure prediction based on position-specific scoring matrices. , 1999, Journal of molecular biology.

[31]  Jiangning Song,et al.  Prediction of cis/trans isomerization in proteins using PSI-BLAST profiles and secondary structure information , 2006, BMC Bioinformatics.

[32]  Andreas Christmann,et al.  Support vector machines , 2008, Data Mining and Knowledge Discovery Handbook.

[33]  L. Nicholson,et al.  Prolyl cis-trans isomerization as a molecular timer. , 2007, Nature chemical biology.

[34]  Alessandra Corazza,et al.  Molecular dynamics simulation of β2‐microglobulin in denaturing and stabilizing conditions , 2011, Proteins.

[35]  K. Wüthrich,et al.  The X‐Pro peptide bond as an nmr probe for conformational studies of flexible linear peptides , 1976, Biopolymers.

[36]  L. Nicholson,et al.  The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-β production , 2006, Nature.

[37]  Dimitrios I. Fotiadis,et al.  Prediction of cis/trans isomerization using feature selection and support vector machines , 2009, J. Biomed. Informatics.

[38]  C. Dobson,et al.  A peptide model for proline isomerism in the unfolded state of staphylococcal nuclease. , 1992, Journal of molecular biology.

[39]  Christopher J. Nelson,et al.  Proline Isomerization of Histone H3 Regulates Lysine Methylation and Gene Expression , 2006, Cell.

[40]  D. Pal,et al.  Cis peptide bonds in proteins: residues involved, their conformations, interactions and locations. , 1999, Journal of molecular biology.

[41]  Dirk Labudde,et al.  2Statistically significant dependence of the Xaa-Pro peptide bond conformation on secondary structure and amino acid sequence , 2004, BMC Structural Biology.

[42]  J. R. Somoza,et al.  Coupling between trans/cis proline isomerization and protein stability in staphylococcal nuclease , 1996, Protein science : a publication of the Protein Society.

[43]  Dirk Labudde,et al.  COPS - Cis/trans peptide bond conformation prediction of amino acids on the basis of secondary structure information , 2005, Bioinform..

[44]  C. Etchebest,et al.  A structural alphabet for local protein structures: Improved prediction methods , 2005, Proteins.

[45]  M. Levitt.  Effect of proline residues on protein folding. , 1981, Journal of molecular biology.

[46]  H. Scheraga,et al.  Proline cis-trans isomerization and protein folding. , 2002, Biochemistry.

[47]  L. Nicholson,et al.  The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-β production , 2007, Nature.

[48]  A. Jabs,et al.  Peptide bonds revisited , 1998, Nature Structural &Molecular Biology.

[49]  Ann M Stock,et al.  Structure of a cholesterol-binding protein deficient in Niemann–Pick type C2 disease , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  H. Halvorson,et al.  Consideration of the Possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. , 1975, Biochemistry.

[51]  A. D. de Brevern,et al.  Modeling and Molecular Dynamics of HPA-1a and -1b Polymorphisms: Effects on the Structure of the β3 Subunit of the αIIbβ3 Integrin , 2012, PloS one.

[52]  Mark S.P. Sansom,et al.  Hinges, swivels and switches: the role of prolines in signalling via transmembrane α-helices , 2000 .

[53]  Vladimir Vapnik,et al.  An overview of statistical learning theory , 1999, IEEE Trans. Neural Networks.

[54]  John P. Overington,et al.  Derivation of rules for comparative protein modeling from a database of protein structure alignments , 1994, Protein science : a publication of the Protein Society.

[55]  S. Gåseidnes,et al.  Structural insights into the catalytic mechanism of a family 18 exo-chitinase , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Yaoqi Zhou,et al.  Improving protein fold recognition and template-based modeling by employing probabilistic-based matching between predicted one-dimensional structural properties of query and corresponding native properties of templates , 2011, Bioinform..

[57]  K. Lu,et al.  Phosphorylation-specific prolyl isomerization: is there an underlying theme? , 2005, Nature Cell Biology.

[58]  F. Gräter,et al.  On the cis to trans isomerization of prolyl-peptide bonds under tension. , 2012, The journal of physical chemistry. B.

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

[60]  G. Bussi,et al.  Trans−cis Switching Mechanisms in Proline Analogues and Their Relevance for the Gating of the 5-HT3 Receptor , 2009, The journal of physical chemistry. B.

[61]  Haruki Nakamura,et al.  Intra- and intermolecular interaction inducing pyramidalization on both sides of a proline dipeptide during isomerization: an ab initio QM/MM molecular dynamics simulation study in explicit water. , 2009, Journal of the American Chemical Society.

[62]  N. Srinivasan,et al.  Cis–trans peptide variations in structurally similar proteins , 2012, Amino Acids.

[63]  M. Weiss,et al.  Two non‐proline cis peptide bonds may be important for factor XIII function , 1998, FEBS letters.

[64]  H. Weinstein,et al.  Hinges, swivels and switches: the role of prolines in signalling via transmembrane alpha-helices. , 2000, Trends in pharmacological sciences.

[65]  G. Nelsestuen,et al.  Importance of cis-proline 22 in the membrane-binding conformation of bovine prothrombin. , 1996, Biochemistry.

[66]  U. Hahn,et al.  Replacement of a cis proline simplifies the mechanism of ribonuclease T1 folding. , 1990, Biochemistry.

[67]  Robert Preissner,et al.  Conservation of cis prolyl bonds in proteins during evolution , 2004, Proteins.

[68]  Robert Preissner,et al.  Prediction of prolyl residues in cis‐conformation in protein structures on the basis of the amino acid sequence , 1990, FEBS letters.

[69]  B. Matthews.  Comparison of the predicted and observed secondary structure of T4 phage lysozyme. , 1975, Biochimica et biophysica acta.