Versatility and Invariance in the Evolution of Homologous Heteromeric Interfaces

PLoS Computational Biology

Volumn 8, Issue 8, 2012, Pages

  Andreani, Jessica ^a,b,c   Faure, Guilhem ^a,b,c   Guerois, Raphaël ^a,b,c  

^a DIF   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PARTNERS; COMPLEX INTERFACE; DESCRIPTORS; ELEMENTARY INTERACTIONS; GEOMETRIC PROPERTIES; HOMOLOGOUS COMPLEXES; INTERACTION PREDICTION; MULTIPLE SEQUENCE ALIGNMENTS; PROTEIN COMPLEXES; PROTEIN-PROTEIN INTERACTIONS;

PROTEINS;

ARTICLE; COMPLEX FORMATION; EVOLUTION; PREDICTION; PROTEIN BINDING; PROTEIN DATABASE; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; SEQUENCE ALIGNMENT;

EID: 84866108547     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002677     Document Type: Article

References (66)

1. Stein A, Mosca R, Aloy P, (2011) Three-dimensional modeling of protein interactions and complexes is going'omics. Curr Opin Struct Biol 21: 200-208.
2. Schreiber G, Keating AE, (2011) Protein binding specificity versus promiscuity. Curr Opin Struct Biol 21: 50-61.
3. Mayrose I, Graur D, Ben-Tal N, Pupko T, (2004) Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior. Mol Biol Evol 21: 1781-1791.
4. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
5. Teichmann SA, (2002) The constraints protein-protein interactions place on sequence divergence. J Mol Biol 324: 399-407.
6. Caffrey DR, Somaroo S, Hughes JD, Mintseris J, Huang ES, (2004) Are protein-protein interfaces more conserved in sequence than the rest of the protein surface? Protein Sci 13: 190-202.
7. Kim PM, Lu LJ, Xia Y, Gerstein MB, (2006) Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314: 1938-1941.
8. Levy ED, Boeri Erba E, Robinson CV, Teichmann SA, (2008) Assembly reflects evolution of protein complexes. Nature 453: 1262-1265.
9. Aloy P, Ceulemans H, Stark A, Russell RB, (2003) The relationship between sequence and interaction divergence in proteins. J Mol Biol 332: 989-998.
10. Levy ED, Pereira-Leal JB, (2008) Evolution and dynamics of protein interactions and networks. Curr Opin Struct Biol 18: 349-357.
11. Eames M, Kortemme T, (2007) Structural mapping of protein interactions reveals differences in evolutionary pressures correlated to mRNA level and protein abundance. Structure 15: 1442-1451.
12. Franzosa EA, Xia Y, (2009) Structural determinants of protein evolution are context-sensitive at the residue level. Mol Biol Evol 26: 2387-2395.
13. Guharoy M, Chakrabarti P, (2005) Conservation and relative importance of residues across protein-protein interfaces. Proc Natl Acad Sci U S A 102: 15447-15452.
14. Guharoy M, Chakrabarti P, (2010) Conserved residue clusters at protein-protein interfaces and their use in binding site identification. BMC Bioinformatics 11: 286.
15. Mintseris J, Weng Z, (2005) Structure, function, and evolution of transient and obligate protein-protein interactions. Proc Natl Acad Sci U S A 102: 10930-10935.
16. Halperin I, Wolfson H, Nussinov R, (2006) Correlated mutations: advances and limitations. A study on fusion proteins and on the Cohesin-Dockerin families. Proteins 63: 832-845.
17. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T, (2009) Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci U S A 106: 67-72.
18. Procaccini A, Lunt B, Szurmant H, Hwa T, Weigt M, (2011) Dissecting the specificity of protein-protein interaction in bacterial two-component signaling: orphans and crosstalks. PLoS One 6: e19729.
19. Capra EJ, Perchuk BS, Lubin EA, Ashenberg O, Skerker JM, et al. (2010) Systematic dissection and trajectory-scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways. PLoS Genet 6: e1001220.
20. Reichmann D, Rahat O, Cohen M, Neuvirth H, Schreiber G, (2007) The molecular architecture of protein-protein binding sites. Curr Opin Struct Biol 17: 67-76.
21. Rahat O, Yitzhaky A, Schreiber G, (2008) Cluster conservation as a novel tool for studying protein-protein interactions evolution. Proteins 71: 621-630.
22. Madaoui H, Guerois R, (2008) Coevolution at protein complex interfaces can be detected by the complementarity trace with important impact for predictive docking. Proc Natl Acad Sci U S A 105: 7708-7713.
23. Levin KB, Dym O, Albeck S, Magdassi S, Keeble AH, et al. (2009) Following evolutionary paths to protein-protein interactions with high affinity and selectivity. Nat Struct Mol Biol 16: 1049-1055.
24. Ortlund EA, Bridgham JT, Redinbo MR, Thornton JW, (2007) Crystal structure of an ancient protein: evolution by conformational epistasis. Science 317: 1544-1548.
25. Keskin O, Nussinov R, (2007) Similar binding sites and different partners: implications to shared proteins in cellular pathways. Structure 15: 341-354.
26. Tuncbag N, Gursoy A, Guney E, Nussinov R, Keskin O, (2008) Architectures and functional coverage of protein-protein interfaces. J Mol Biol 381: 785-802.
27. Gao M, Skolnick J, (2010) Structural space of protein-protein interfaces is degenerate, close to complete, and highly connected. Proc Natl Acad Sci U S A 107: 22517-22522.
28. Chakrabarti P, Janin J, (2002) Dissecting protein-protein recognition sites. Proteins 47: 334-343.
29. Bahadur RP, Chakrabarti P, Rodier F, Janin J, (2004) A dissection of specific and non-specific protein-protein interfaces. J Mol Biol 336: 943-955.
30. Ofran Y, Rost B, (2003) Analysing six types of protein-protein interfaces. J Mol Biol 325: 377-387.
31. Albeck S, Schreiber G, (1999) Biophysical characterization of the interaction of the beta-lactamase TEM-1 with its protein inhibitor BLIP. Biochemistry 38: 11-21.
32. Albeck S, Unger R, Schreiber G, (2000) Evaluation of direct and cooperative contributions towards the strength of buried hydrogen bonds and salt bridges. J Mol Biol 298: 503-520.
33. Shen YF, Chen YH, Chu SY, Lin MI, Hsu HT, et al. (2011) E339...R416 salt bridge of nucleoprotein as a feasible target for influenza virus inhibitors. Proc Natl Acad Sci U S A 108: 16515-16520.
34. De S, Krishnadev O, Srinivasan N, Rekha N, (2005) Interaction preferences across protein-protein interfaces of obligatory and non-obligatory components are different. BMC Struct Biol 5: 15.
35. Hu Z, Ma B, Wolfson H, Nussinov R, (2000) Conservation of polar residues as hot spots at protein interfaces. Proteins 39: 331-342.
36. Faure G, Andreani J, Guerois R, (2012) InterEvol database: exploring the structure and evolution of protein complex interfaces. Nucleic Acids Res 40: D847-856.
37. Walhout AJ, Sordella R, Lu X, Hartley JL, Temple GF, et al. (2000) Protein interaction mapping in C. elegans using proteins involved in vulval development. Science 287: 116-122.
38. Perica T, Chothia C, (2010) Ubiquitin-molecular mechanisms for recognition of different structures. Curr Opin Struct Biol 20: 367-376.
39. Levy ED, (2010) A simple definition of structural regions in proteins and its use in analyzing interface evolution. J Mol Biol 403: 660-670.
40. Aloy P, Russell RB, (2002) Interrogating protein interaction networks through structural biology. Proc Natl Acad Sci U S A 99: 5896-5901.
41. Kadota Y, Amigues B, Ducassou L, Madaoui H, Ochsenbein F, et al. (2008) Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Rep 9: 1209-1215.
42. Winkler GS, Albert TK, Dominguez C, Legtenberg YI, Boelens R, et al. (2004) An altered-specificity ubiquitin-conjugating enzyme/ubiquitin-protein ligase pair. J Mol Biol 337: 157-165.
43. Lijnzaad P, Berendsen HJ, Argos P, (1996) A method for detecting hydrophobic patches on protein surfaces. Proteins 26: 192-203.
44. Lijnzaad P, Argos P, (1997) Hydrophobic patches on protein subunit interfaces: characteristics and prediction. Proteins 28: 333-343.
45. Jacak R, Leaver-Fay A, Kuhlman B, (2012) Computational protein design with explicit consideration of surface hydrophobic patches. Proteins 80: 825-838.
46. Rajamani D, Thiel S, Vajda S, Camacho CJ, (2004) Anchor residues in protein-protein interactions. Proc Natl Acad Sci U S A 101: 11287-11292.
47. Karanicolas J, Corn JE, Chen I, Joachimiak LA, Dym O, et al. (2011) A de novo protein binding pair by computational design and directed evolution. Mol Cell 42: 250-260.
48. Lewis SM, Kuhlman BA, (2011) Anchored design of protein-protein interfaces. PLoS One 6: e20872.
49. Friedland GD, Lakomek NA, Griesinger C, Meiler J, Kortemme T, (2009) A correspondence between solution-state dynamics of an individual protein and the sequence and conformational diversity of its family. PLoS Comput Biol 5: e1000393.
50. Zhu H, Domingues FS, Sommer I, Lengauer T, (2006) NOXclass: prediction of protein-protein interaction types. BMC Bioinformatics 7: 27.
51. Zhao N, Pang B, Shyu CR, Korkin D, (2011) Charged residues at protein interaction interfaces: unexpected conservation and orchestrated divergence. Protein Sci 20: 1275-1284.
52. Andre I, Strauss CE, Kaplan DB, Bradley P, Baker D, (2008) Emergence of symmetry in homooligomeric biological assemblies. Proc Natl Acad Sci U S A 105: 16148-16152.
53. Lukatsky DB, Shakhnovich BE, Mintseris J, Shakhnovich EI, (2007) Structural similarity enhances interaction propensity of proteins. J Mol Biol 365: 1596-1606.
54. Grueninger D, Treiber N, Ziegler MO, Koetter JW, Schulze MS, et al. (2008) Designed protein-protein association. Science 319: 206-209.
55. Hashimoto K, Panchenko AR, (2010) Mechanisms of protein oligomerization, the critical role of insertions and deletions in maintaining different oligomeric states. Proc Natl Acad Sci U S A 107: 20352-20357.
56. Meenan NA, Sharma A, Fleishman SJ, Macdonald CJ, Morel B, et al. (2010) The structural and energetic basis for high selectivity in a high-affinity protein-protein interaction. Proc Natl Acad Sci U S A 107: 10080-10085.
57. Tuncbag N, Gursoy A, Nussinov R, Keskin O, (2011) Predicting protein-protein interactions on a proteome scale by matching evolutionary and structural similarities at interfaces using PRISM. Nat Protoc 6: 1341-1354.
58. Janin J, Chothia C, (1990) The structure of protein-protein recognition sites. J Biol Chem 265: 16027-16030.
59. Jones S, Thornton JM, (1996) Principles of protein-protein interactions. Proc Natl Acad Sci U S A 93: 13-20.
60. Lo Conte L, Chothia C, Janin J, (1999) The atomic structure of protein-protein recognition sites. J Mol Biol 285: 2177-2198.
61. Kortemme T, Kim DE, Baker D, (2004) Computational alanine scanning of protein-protein interfaces. Sci STKE 2004: pl2.
62. Kawabata T, (2003) MATRAS: A program for protein 3D structure comparison. Nucleic Acids Res 31: 3367-3369.
63. Poupon A, (2004) Voronoi and Voronoi-related tessellations in studies of protein structure and interaction. Curr Opin Struct Biol 14: 233-241.
64. Lindauer K, Bendic C, Suhnel J, (1996) HBexplore-a new tool for identifying and analysing hydrogen bonding patterns in biological macromolecules. Comput Appl Biosci 12: 281-289.
65. Hubbard SJ, Thornton JM (1993) NACCESS Computer Program. Department of Biochemistry and Molecular Biology, University College London.
66. Ihaka R, Gentleman R, (1996) R: A language for data analysis and graphics. Journal of Computational and Graphical Statistics 5: 299-314.