Coevolution in defining the functional specificity

Covariation between sites can arise due to a common evolutionary history. At the same time, structure and function of proteins play significant role in evolvability of different sites that are not directly connected with the common ancestry. The nature of forces which cause residues to coevolve is still not thoroughly understood, it is especially not clear how coevolutionary processes are related to functional diversification within protein families. We analyzed both functional and structural factors that might cause covariation of specificity determinants and showed that they more often participate in coevolutionary relationships with each other and other sites compared with functional sites and those sites that are not under strong functional constraints. We also found that protein sites with higher number of coevolutionary connections with other sites have a tendency to evolve slower. Our results indicate that in some cases coevolutionary connections exist between specificity sites that are located far away in space but are under similar functional constraints. Such correlated changes and compensations can be realized through the stepwise coevolutionary processes which in turn can shed light on the mechanisms of functional diversification. Proteins 2009. Published 2008 Wiley‐Liss, Inc.

[1]  C. Markert,et al.  Evolution of the Gene , 1948, Nature.

[2]  C. Yanofsky,et al.  Protein Structure Relationships Revealed by Mutational Analysis , 1964, Science.

[3]  Dr. Susumu Ohno.  Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[4]  R. Doolittle.  Similar amino acid sequences: chance or common ancestry? , 1981, Science.

[5]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[6]  A. Lapedes,et al.  Covariation of mutations in the V3 loop of human immunodeficiency virus type 1 envelope protein: an information theoretic analysis. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[7]  C. Sander,et al.  Correlated mutations and residue contacts in proteins , 1994, Proteins.

[8]  C. Sander,et al.  Can three-dimensional contacts in protein structures be predicted by analysis of correlated mutations? , 1994, Protein engineering.

[9]  E. Neher.  How frequent are correlated changes in families of protein sequences? , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[10]  K. Hatrick,et al.  Compensating changes in protein multiple sequence alignments. , 1994, Protein engineering.

[11]  A. Valencia,et al.  Correlated mutations contain information about protein-protein interaction. , 1997, Journal of molecular biology.

[12]  W. Taylor,et al.  Effectiveness of correlation analysis in identifying protein residues undergoing correlated evolution. , 1997, Protein engineering.

[13]  G. Chelvanayagam,et al.  An analysis of simultaneous variation in protein structures. , 1997, Protein engineering.

[14]  H. Kagamiyama,et al.  Directed evolution of an aspartate aminotransferase with new substrate specificities. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  B. Rost,et al.  Effective use of sequence correlation and conservation in fold recognition. , 1999, Journal of molecular biology.

[16]  W R Taylor,et al.  Coevolving protein residues: maximum likelihood identification and relationship to structure. , 1999, Journal of molecular biology.

[17]  X. Gu,et al.  Statistical methods for testing functional divergence after gene duplication. , 1999, Molecular biology and evolution.

[18]  Stefan M. Larson,et al.  Analysis of covariation in an SH3 domain sequence alignment: applications in tertiary contact prediction and the design of compensating hydrophobic core substitutions. , 2000, Journal of molecular biology.

[19]  W. Atchley,et al.  Separation of phylogenetic and functional associations in biological sequences by using the parametric bootstrap. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Russell,et al.  Analysis and prediction of functional sub-types from protein sequence alignments. , 2000, Journal of molecular biology.

[21]  W. Atchley,et al.  Correlations among amino acid sites in bHLH protein domains: an information theoretic analysis. , 2000, Molecular biology and evolution.

[22]  F. Cohen,et al.  Co-evolution of proteins with their interaction partners. , 2000, Journal of molecular biology.

[23]  P. Tuff,et al.  Exploring a phylogenetic approach for the detection of correlated substitutions in proteins. , 2000, Molecular biology and evolution.

[24]  A. Valencia,et al.  Similarity of phylogenetic trees as indicator of protein-protein interaction. , 2001, Protein engineering.

[25]  Georgios G. Gkoutos,et al.  Lipid-facing correlated mutations and dimerization in G-protein coupled receptors. , 2001, Protein engineering.

[26]  L Pritchard,et al.  Evaluation of a novel method for the identification of coevolving protein residues. , 2001, Protein engineering.

[27]  Jimin Pei,et al.  AL2CO: calculation of positional conservation in a protein sequence alignment , 2001, Bioinform..

[28]  Itay Mayrose,et al.  Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues , 2002, ISMB.

[29]  G Vriend,et al.  Correlated Mutation Analyses on Very Large Sequence Families , 2002, Chembiochem : a European journal of chemical biology.

[30]  L. Mirny,et al.  Using orthologous and paralogous proteins to identify specificity determining residues , 2002, Genome Biology.

[31]  Tal Pupko,et al.  A branch-and-bound algorithm for the inference of ancestral amino-acid sequences when the replacement rate varies among sites: Application to the evolution of five gene families , 2002, Bioinform..

[32]  A. Valencia,et al.  Computational methods for the prediction of protein interactions. , 2002, Current opinion in structural biology.

[33]  S A Benner,et al.  Detecting compensatory covariation signals in protein evolution using reconstructed ancestral sequences. , 2002, Journal of molecular biology.

[34]  A. Horovitz,et al.  Mapping pathways of allosteric communication in GroEL by analysis of correlated mutations , 2002, Proteins.

[35]  Jianpeng Ma,et al.  Allosteric transition pathways in the lactose repressor protein core domains: Asymmetric motions in a homodimer , 2003, Protein science : a publication of the Protein Society.

[36]  Rama Ranganathan,et al.  Allosteric determinants in guanine nucleotide-binding proteins , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Thomas W. H. Lui,et al.  Using multiple interdependency to separate functional from phylogenetic correlations in protein alignments , 2003, Bioinform..

[38]  Gürol M. Süel,et al.  Evolutionarily conserved networks of residues mediate allosteric communication in proteins , 2003, Nature Structural Biology.

[39]  Claes Gustafsson,et al.  Systematic variation of amino acid substitutions for stringent assessment of pairwise covariation. , 2003, Journal of molecular biology.

[40]  John A. Katzenellenbogen,et al.  Allosteric Control of Ligand Selectivity between Estrogen Receptors α and β - Implications for Other Nuclear Receptors , 2004 .

[41]  Thomas Madej,et al.  Analysis of protein homology by assessing the (dis)similarity in protein loop regions , 2004, Proteins.

[42]  Rama Ranganathan,et al.  Structural Determinants of Allosteric Ligand Activation in RXR Heterodimers , 2004, Cell.

[43]  B. Katzenellenbogen,et al.  Allosteric control of ligand selectivity between estrogen receptors alpha and beta: implications for other nuclear receptors. , 2004, Molecular cell.

[44]  R. Aldrich,et al.  Influence of conservation on calculations of amino acid covariance in multiple sequence alignments , 2004, Proteins.

[45]  Mikhail S. Gelfand,et al.  SDPpred: a tool for prediction of amino acid residues that determine differences in functional specificity of homologous proteins , 2004, Nucleic Acids Res..

[46]  G. Gloor,et al.  Mutual information in protein multiple sequence alignments reveals two classes of coevolving positions. , 2005, Biochemistry.

[47]  W. Atchley,et al.  Networks of coevolving sites in structural and functional domains of serpin proteins. , 2005, Molecular biology and evolution.

[48]  L. C. Martin,et al.  Using information theory to search for co-evolving residues in proteins , 2005, Bioinform..

[49]  A. Jean-Marie,et al.  A model-based approach for detecting coevolving positions in a molecule. , 2005, Molecular biology and evolution.

[50]  Zhilei Chen,et al.  Rapid creation of a novel protein function by in vitro coevolution. , 2005, Journal of molecular biology.

[51]  J. Heringa,et al.  Sequence comparison by sequence harmony identifies subtype-specific functional sites , 2006, Nucleic acids research.

[52]  Emil Alexov,et al.  Predicting residue contacts using pragmatic correlated mutations method: reducing the false positives , 2006, BMC Bioinformatics.

[53]  H. Wolfson,et al.  Correlated mutations: Advances and limitations. A study on fusion proteins and on the Cohesin‐Dockerin families , 2006, Proteins.

[54]  Raja Jothi,et al.  Co-evolutionary analysis of domains in interacting proteins reveals insights into domain-domain interactions mediating protein-protein interactions. , 2006, Journal of molecular biology.

[55]  Wei Cai,et al.  Prediction of functional specificity determinants from protein sequences using log-likelihood ratios , 2006, Bioinform..

[56]  J. Clark Lagarias,et al.  Flexible mapping of homology onto structure with Homolmapper , 2007, BMC Bioinformatics.

[57]  John Kuriyan,et al.  The origin of protein interactions and allostery in colocalization , 2007, Nature.

[58]  David Haussler,et al.  Detecting Coevolution in and among Protein Domains , 2007, PLoS Comput. Biol..

[59]  C. Sander,et al.  Determinants of protein function revealed by combinatorial entropy optimization , 2007, Genome Biology.

[60]  Anna R Panchenko,et al.  Functional specificity lies within the properties and evolutionary changes of amino acids. , 2007, Journal of molecular biology.

[61]  Narmada Thanki,et al.  CDD: a conserved domain database for interactive domain family analysis , 2006, Nucleic Acids Res..

[62]  Gregory B. Gloor,et al.  Mutual information without the influence of phylogeny or entropy dramatically improves residue contact prediction , 2008, Bioinform..

[63]  Haruki Nakamura,et al.  Remediation of the protein data bank archive , 2007, Nucleic Acids Res..

[64]  Jeffrey J. Gray,et al.  Contact rearrangements form coupled networks from local motions in allosteric proteins , 2008, Proteins.

[65]  J. Trewhella,et al.  Ligand-induced conformational changes and conformational dynamics in the solution structure of the lactose repressor protein. , 2008, Journal of molecular biology.

[66]  Tord Snäll,et al.  Reassessing a sparse energetic network within a single protein domain , 2008, Proceedings of the National Academy of Sciences.

[67]  Mona Singh,et al.  Characterization and prediction of residues determining protein functional specificity , 2008, Bioinform..