Home LiteratureArticle Details
PMID: 17468399 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Specificity in protein interactions and its relationship with sequence diversity and coevolution.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 104 ·No. 19 ·2007-05-08 ·Pages 7999-8004

Hakes L, Lovell SC, Oliver SG, Robertson DL

Abstract

Studies of interacting proteins have found correlated evolution of the sequences of binding partners, apparently as a result of compensating mutations to maintain specificity (i.e., molecular coevolution). Here, we analyze the coevolution of interacting proteins in yeast and demonstrate correlated evolution of binding partners in eukaryotes. Detailed investigation of this apparent coevolution, focusing on the proteins' surface and binding interface, surprisingly leads to no improvement in the correlation. We conclude that true coevolution, as characterized by compensatory mutations between binding partners, is unlikely to be chiefly responsible for the apparent correlated evolution. We postulate that the correlation between sequence alignments is simply due to interacting proteins being subject to similar constraints on their evolutionary rate. Because gene expression has a strong influence on evolutionary rate, and interacting proteins will tend to have similar levels of expression, we investigated this particular constraint. We found that the absolute expression level outperformed correlated evolution for predicting interacting protein partners. A correlation between sequence alignments could also be identified not only between pairs of proteins that physically interact but also between those that are merely functionally related (i.e., within the same protein complex). This indicates that the observed correlated evolution of interacting proteins is due to similar constraints on evolutionary rate and not coevolution.

MeSH Terms
Amino Acid Sequence Evolution, Molecular Gene Expression Proteins/chemistry ROC Curve Sequence Alignment
Chemicals
Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Hakes Luke
Faculty of Life Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester, M13 9PT, United Kingdom.
Lovell Simon C
Oliver Stephen G
Robertson David L
References (53)
53 references, click to expand
  1. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae.
    Nature. 2004 Apr 8;428(6983):617-24 PMID: 15004568
  2. The coordinated evolution of yeast proteins is constrained by functional modularity.
    Trends Genet. 2006 Aug;22(8):416-9 PMID: 16797778
  3. Large-scale co-evolution analysis of protein structural interlogues using the global protein structural interactome map (PSIMAP).
    Bioinformatics. 2004 May 1;20(7):1138-50 PMID: 14764552
  4. Evolutionary genomics: yeasts accelerate beyond BLAST.
    Curr Biol. 2004 May 25;14(10):R392-4 PMID: 15186766
  5. Protein interaction networks from yeast to human.
    Curr Opin Struct Biol. 2004 Jun;14(3):292-9 PMID: 15193308
  6. Coevolution of gene expression among interacting proteins.
    Proc Natl Acad Sci U S A. 2004 Jun 15;101(24):9033-8 PMID: 15175431
  7. ADVICE: Automated Detection and Validation of Interaction by Co-Evolution.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W69-72 PMID: 15215353
  8. Genome evolution in yeasts.
    Nature. 2004 Jul 1;430(6995):35-44 PMID: 15229592
  9. A scale of functional divergence for yeast duplicated genes revealed from analysis of the protein-protein interaction network.
    Genome Biol. 2004;5(10):R76 PMID: 15461795
  10. Principles of protein-protein recognition.
    Nature. 1975 Aug 28;256(5520):705-8 PMID: 1153006
  11. Solvent-accessible surfaces of proteins and nucleic acids.
    Science. 1983 Aug 19;221(4612):709-13 PMID: 6879170
  12. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach.
    Biometrics. 1988 Sep;44(3):837-45 PMID: 3203132
  13. Surface, subunit interfaces and interior of oligomeric proteins.
    J Mol Biol. 1988 Nov 5;204(1):155-64 PMID: 3216390
  14. An investigation of protein subunit and domain interfaces.
    Protein Eng. 1988 Jul;2(2):101-13 PMID: 3244692
  15. The structure of protein-protein recognition sites.
    J Biol Chem. 1990 Sep 25;265(27):16027-30 PMID: 2204619
  16. Protein-protein interactions: a review of protein dimer structures.
    Prog Biophys Mol Biol. 1995;63(1):31-65 PMID: 7746868
  17. Principles of protein-protein interactions.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):13-20 PMID: 8552589
  18. Molecular evidence for an ancient duplication of the entire yeast genome.
    Nature. 1997 Jun 12;387(6634):708-13 PMID: 9192896
  19. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  20. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  21. PQS: a protein quaternary structure file server.
    Trends Biochem Sci. 1998 Sep;23(9):358-61 PMID: 9787643
  22. Dissecting the regulatory circuitry of a eukaryotic genome.
    Cell. 1998 Nov 25;95(5):717-28 PMID: 9845373
  23. Comparative analysis of the Saccharomyces cerevisiae and Caenorhabditis elegans protein interaction networks.
    BMC Evol Biol. 2005;5:23 PMID: 15777474
  24. Mutual information in protein multiple sequence alignments reveals two classes of coevolving positions.
    Biochemistry. 2005 May 17;44(19):7156-65 PMID: 15882054
  25. PSIbase: a database of Protein Structural Interactome map (PSIMAP).
    Bioinformatics. 2005 May 15;21(10):2541-3 PMID: 15749693
  26. Structure, function, and evolution of transient and obligate protein-protein interactions.
    Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):10930-5 PMID: 16043700
  27. The inference of protein-protein interactions by co-evolutionary analysis is improved by excluding the information about the phylogenetic relationships.
    Bioinformatics. 2005 Sep 1;21(17):3482-9 PMID: 15994190
  28. Assessing protein co-evolution in the context of the tree of life assists in the prediction of the interactome.
    J Mol Biol. 2005 Sep 30;352(4):1002-15 PMID: 16139301
  29. The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species.
    Genome Res. 2005 Oct;15(10):1456-61 PMID: 16169922
  30. Why highly expressed proteins evolve slowly.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14338-43 PMID: 16176987
  31. BioGRID: a general repository for interaction datasets.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D535-9 PMID: 16381927
  32. A single determinant dominates the rate of yeast protein evolution.
    Mol Biol Evol. 2006 Feb;23(2):327-37 PMID: 16237209
  33. The origins and evolution of functional modules: lessons from protein complexes.
    Philos Trans R Soc Lond B Biol Sci. 2006 Mar 29;361(1467):507-17 PMID: 16524839
  34. Proteome survey reveals modularity of the yeast cell machinery.
    Nature. 2006 Mar 30;440(7084):631-6 PMID: 16429126
  35. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae.
    Nature. 2006 Mar 30;440(7084):637-43 PMID: 16554755
  36. An integrated view of protein evolution.
    Nat Rev Genet. 2006 May;7(5):337-48 PMID: 16619049
  37. From molecular to modular cell biology.
    Nature. 1999 Dec 2;402(6761 Suppl):C47-52 PMID: 10591225
  38. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.
    Mol Biol Evol. 2000 Jan;17(1):32-43 PMID: 10666704
  39. Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate.
    Mol Biol Evol. 2000 Jan;17(1):68-74 PMID: 10666707
  40. Co-evolution of proteins with their interaction partners.
    J Mol Biol. 2000 Jun 2;299(2):283-93 PMID: 10860738
  41. Highly expressed genes in yeast evolve slowly.
    Genetics. 2001 Jun;158(2):927-31 PMID: 11430355
  42. Similarity of phylogenetic trees as indicator of protein-protein interaction.
    Protein Eng. 2001 Sep;14(9):609-14 PMID: 11707606
  43. In silico two-hybrid system for the selection of physically interacting protein pairs.
    Proteins. 2002 May 1;47(2):219-27 PMID: 11933068
  44. Comparative assessment of large-scale data sets of protein-protein interactions.
    Nature. 2002 May 23;417(6887):399-403 PMID: 12000970
  45. Co-evolutionary analysis reveals insights into protein-protein interactions.
    J Mol Biol. 2002 Nov 15;324(1):177-92 PMID: 12421567
  46. Exploiting the co-evolution of interacting proteins to discover interaction specificity.
    J Mol Biol. 2003 Mar 14;327(1):273-84 PMID: 12614624
  47. Dosage sensitivity and the evolution of gene families in yeast.
    Nature. 2003 Jul 10;424(6945):194-7 PMID: 12853957
  48. On the number of protein-protein interactions in the yeast proteome.
    Nucleic Acids Res. 2003 Jul 15;31(14):4157-61 PMID: 12853633
  49. Protein complexes and functional modules in molecular networks.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12123-8 PMID: 14517352
  50. MUSCLE: multiple sequence alignment with high accuracy and high throughput.
    Nucleic Acids Res. 2004;32(5):1792-7 PMID: 15034147
  51. An algorithm for predicting protein-protein interaction sites: Abnormally exposed amino acid residues and secondary structure elements.
    Protein Sci. 2006 May;15(5):1017-29 PMID: 16641487
  52. A novel method for detecting intramolecular coevolution: adding a further dimension to selective constraints analyses.
    Genetics. 2006 May;173(1):9-23 PMID: 16547113
  53. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome.
    Science. 2004 Apr 9;304(5668):304-7 PMID: 15001715
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.0609962104
Published
2007-05-08
Epub
2007-00-27
Pages
7999-8004
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1876561
Subset
IM
External Links
PubMed source DOI: 10.1073/pnas.0609962104 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2