Protein Flexibility Facilitates Quaternary Structure Assembly and Evolution

PLoS Biology

Volumn 12, Issue 5, 2014, Pages

  Marsh, Joseph A ^a,c   Teichmann, Sarah A ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Italy)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; PROTEIN; PROTEIN SUBUNIT;

ARTICLE; EUKARYOTE; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN QUATERNARY STRUCTURE; PROTEIN SUBUNIT; STRUCTURE ANALYSIS; ANIMAL; APICOMPLEXA; ARABIDOPSIS; BACTERIUM; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; FUNGUS; PROTEIN MULTIMERIZATION;

ANIMALS; APICOMPLEXA; ARABIDOPSIS; BACTERIA; EVOLUTION, MOLECULAR; FUNGI; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; PROTEINS;

EID: 84901445186     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001870     Document Type: Article

References (62)

1. Robinson CV, Sali A, Baumeister W, (2007) The molecular sociology of the cell. Nature 450: 973-982 doi:10.1038/nature06523.
2. Tarassov K, Messier V, Landry CR, Radinovic S, Serna Molina MM, et al. (2008) An in vivo map of the yeast protein interactome. Science 320: 1465-1470 doi:10.1126/science.1153878.
3. Havugimana PC, Hart GT, Nepusz T, Yang H, Turinsky AL, et al. (2012) A census of human soluble protein complexes. Cell 150: 1068-1081 doi:10.1016/j.cell.2012.08.011.
4. Monod J, Wyman J, Changeux J-P, (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88-118.
5. Perica T, Marsh JA, Sousa FL, Natan E, Colwell LJ, et al. (2012) The emergence of protein complexes: quaternary structure, dynamics and allostery. Biochem Soc Trans 40: 475-491.
6. Bershtein S, Mu W, Wu W, Shakhnovich EI, (2012) Soluble oligomerization provides a beneficial fitness effect on destabilizing mutations. Proc Natl Acad Sci USA 109: 4857-4862 doi:10.1073/pnas.1118157109.
7. Lynch M, (2013) Evolutionary diversification of the multimeric states of proteins. Proc Natl Acad Sci USA 110: E2821-E2828 doi:10.1073/pnas.1310980110.
8. Blundell TL, Srinivasan N, (1996) Symmetry, stability, and dynamics of multidomain and multicomponent protein systems. Proc Natl Acad Sci U S A 93: 14243-14248.
9. Goodsell DS, Olson AJ, (2000) Structural symmetry and protein function. Annu Rev Biophys Biomol Struct 29: 105-153 doi:10.1146/annurev.biophys.29.1.105.
10. Levy ED, Pereira-Leal JB, Chothia C, Teichmann SA, (2006) 3D complex: a structural classification of protein complexes. PLoS Comput Biol 2: e155 doi:10.1371/journal.pcbi.0020155.
11. Janin J, Bahadur RP, Chakrabarti P, (2008) Protein-protein interaction and quaternary structure. Q Rev Biophys 41: 133-180 doi:10.1017/S0033583508004708.
12. Levy ED, Erba EB, Robinson CV, Teichmann SA, (2008) Assembly reflects evolution of protein complexes. Nature 453: 1262-1265 doi:10.1038/nature06942.
13. Marsh JA, Hernández H, Hall Z, Ahnert S, Perica T, et al. (2013) Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 153: 461-470.
14. Boehr DD, Nussinov R, Wright PE, (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5: 789-796 doi:10.1038/nchembio.232.
15. Dobbins SE, Lesk VI, Sternberg MJE, (2008) Insights into protein flexibility: the relationship between normal modes and conformational change upon protein-protein docking. Proc Natl Acad Sci USA 105: 10390-10395 doi:10.1073/pnas.0802496105.
16. Marsh JA, Teichmann SA, (2011) Relative solvent accessible surface area predicts protein conformational changes upon binding. Structure 19: 859-867 doi:10.1016/j.str.2011.03.010.
17. Marsh JA, Teichmann SA, (2014) Parallel dynamics and evolution: protein conformational fluctuations and assembly reflect evolutionary changes in sequence and structure. BioEssays 36: 209-218.
18. Namba K, (2001) Roles of partly unfolded conformations in macromolecular self-assembly. Genes Cells 6: 1-12.
19. Hegyi H, Schad E, Tompa P, (2007) Structural disorder promotes assembly of protein complexes. BMC Struct Biol 7: 65 doi:10.1186/1472-6807-7-65.
20. Tóth-Petróczy Á, Oldfield CJ, Simon I, Takagi Y, Dunker AK, et al. (2008) Malleable machines in transcription regulation: the mediator complex. PLoS Comput Biol 4: e1000243 doi:10.1371/journal.pcbi.1000243.
21. Chothia C, (1975) Structural invariants in protein folding. Nature 254: 304-308.
22. Marsh JA, (2013) Buried and accessible surface area control intrinsic protein flexibility. J Mol Biol 425: 3250-3263.
23. Hall Z, Hernández H, Marsh JA, Teichmann SA, Robinson CV, (2013) The role of salt bridges, charge density, and subunit flexibility in determining disassembly routes of protein complexes. Structure 21: 1325-1337 doi:10.1016/j.str.2013.06.004.
24. Gunasekaran K, Tsai C-J, Nussinov R, (2004) Analysis of ordered and disordered protein complexes reveals structural features discriminating between stable and unstable monomers. J Mol Biol 341: 1327-1341 doi:10.1016/j.jmb.2004.07.002.
25. Marsh JA, Teichmann SA, Forman-Kay JD, (2012) Probing the diverse landscape of protein flexibility and binding. Curr Opin Struct Biol 22: 643-650 doi:10.1016/j.sbi.2012.08.008.
26. Lukatsky DB, Shakhnovich BE, Mintseris J, Shakhnovich EI, (2007) Structural similarity enhances interaction propensity of proteins. J Mol Biol 365: 1596-1606 doi:10.1016/j.jmb.2006.11.020.
27. André I, Strauss CEM, Kaplan DB, Bradley P, Baker D, (2008) Emergence of symmetry in homooligomeric biological assemblies. Proc Natl Acad Sci USA 105: 16148-16152 doi:10.1073/pnas.0807576105.
28. Lo Conte L, Chothia C, Janin J, (1999) The atomic structure of protein-protein recognition sites. J Mol Biol 285: 2177-2198.
29. Gunasekaran K, Tsai C-J, Kumar S, Zanuy D, Nussinov R, (2003) Extended disordered proteins: targeting function with less scaffold. Trends Biochem Sci 28: 81-85.
30. Perica T, Chothia C, Teichmann SA, (2012) Evolution of oligomeric state through geometric coupling of protein interfaces. Proc Natl Acad Sci USA 109: 8127-8132 doi:10.1073/pnas.1120028109.
31. Dayhoff JE, Shoemaker BA, Bryant SH, Panchenko AR, (2010) Evolution of protein binding modes in homooligomers. J Mol Biol 395: 860 doi:10.1016/j.jmb.2009.10.052.
32. Kim WK, Henschel A, Winter C, Schroeder M, (2006) The many faces of protein-protein interactions: a compendium of interface geometry. PLoS Comput Biol 2: e124 doi:10.1371/journal.pcbi.0020124.
33. Matthews LR, Vaglio P, Reboul J, Ge H, Davis BP, et al. (2001) Identification of potential interaction networks using sequence-based searches for conserved protein-protein interactions or "interologs.". Genome Res 11: 2120-2126 doi:10.1101/gr.205301.
34. Aloy P, Ceulemans H, Stark A, Russell RB, (2003) The relationship between sequence and interaction divergence in proteins. J Mol Biol 332: 989-998.
35. Yu H, Luscombe NM, Lu HX, Zhu X, Xia Y, et al. (2004) Annotation transfer between genomes: protein-protein interologs and protein-DNA regulogs. Genome Res 14: 1107-1118 doi:10.1101/gr.1774904.
36. Beltrao P, Serrano L, (2007) Specificity and evolvability in eukaryotic protein interaction networks. PLoS Comput Biol 3: e25 doi:10.1371/journal.pcbi.0030025.
37. Lewis ACF, Jones NS, Porter MA, Deane CM, (2012) What evidence is there for the homology of protein-protein interactions? PLoS Comput Biol 8: e1002645 doi:10.1371/journal.pcbi.1002645.
38. Andreani J, Faure G, Guerois R, (2012) Versatility and invariance in the evolution of homologous heteromeric interfaces. PLoS Comput Biol 8: e1002677 doi:10.1371/journal.pcbi.1002677.
39. Van Dam TJP, Snel B, (2008) Protein complex evolution does not involve extensive network rewiring. PLoS Comput Biol 4: e1000132 doi:10.1371/journal.pcbi.1000132.
40. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, et al. (2009) EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19: 327-335 doi:10.1101/gr.073585.107.
41. Altenhoff AM, Schneider A, Gonnet GH, Dessimoz C, (2011) OMA 2011: orthology inference among 1000 complete genomes. Nucl Acids Res 39: D289-D294 doi:10.1093/nar/gkq1238.
42. Albà MM, Castresana J, (2005) Inverse relationship between evolutionary rate and age of mammalian genes. Mol Biol Evol 22: 598-606 doi:10.1093/molbev/msi045.
43. Domazet-Loso T, Tautz D, (2003) An evolutionary analysis of orphan genes in Drosophila. Genome Res 13: 2213-2219 doi:10.1101/gr.1311003.
44. Lynch M, (2012) The evolution of multimeric protein assemblages. Mol Biol Evol 29: 1353-1366 doi:10.1093/molbev/msr300.
45. Pereira-Leal JB, Levy ED, Kamp C, Teichmann SA, (2007) Evolution of protein complexes by duplication of homomeric interactions. Genome Biol 8: R51 doi:10.1186/gb-2007-8-4-r51.
46. Wainright PO, Hinkle G, Sogin ML, Stickel SK, (1993) Monophyletic origins of the metazoa: an evolutionary link with fungi. Science 260: 340-342.
47. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN, (2005) Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J 272: 5129-5148 doi:10.1111/j.1742-4658.2005.04948.x.
48. Patil A, Nakamura H, (2006) Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett 580: 2041-2045 doi:10.1016/j.febslet.2006.03.003.
49. Ekman D, Light S, Björklund ÅK, Elofsson A, (2006) What properties characterize the hub proteins of the protein-protein interaction network of Saccharomyces cerevisiae? Genome Biology 7: R45 doi:10.1186/gb-2006-7-6-r45.
50. Miller S, Lesk AM, Janin J, Chothia C, (1987) The accessible surface area and stability of oligomeric proteins. Nature 328: 834-836 doi:10.1038/328834a0.
51. Kim PM, Sboner A, Xia Y, Gerstein M, (2008) The role of disorder in interaction networks: a structural analysis. Mol Syst Biol 4: 179-179 doi:10.1038/msb.2008.16.
52. Hsu W-L, Oldfield CJ, Xue B, Meng J, Huang F, et al. (2013) Exploring the binding diversity of intrinsically disordered proteins involved in one-to-many binding. Protein Sci 22: 258-273 doi:10.1002/pro.2207.
53. Fernández A, Lynch M, (2011) Non-adaptive origins of interactome complexity. Nature 474: 502-505 doi:10.1038/nature09992.
54. Janin J, Sternberg MJE, (2013) Protein flexibility, not disorder, is intrinsic to molecular recognition. F1000 Biol Rep 5: 2 doi:10.3410/B5-2.
55. Levy ED, (2007) PiQSi: protein quaternary structure investigation. Structure 15: 1364-1367 doi:10.1016/j.str.2007.09.019.
56. Gough J, Karplus K, Hughey R, Chothia C, (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313: 903-919 doi:10.1006/jmbi.2001.5080.
57. Frishman D, Argos P, (1995) Knowledge-based protein secondary structure assignment. Proteins 23: 566-579 doi:10.1002/prot.340230412.
58. Dosztányi Z, Csizmók V, Tompa P, Simon I, (2005) The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J Mol Biol 347: 827-839 doi:10.1016/j.jmb.2005.01.071.
59. Wilson D, Pethica R, Zhou Y, Talbot C, Vogel C, et al. (2009) SUPERFAMILY-sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res 37: D380-D386 doi:10.1093/nar/gkn762.
60. Chakravarty D, Guharoy M, Robert CH, Chakrabarti P, Janin J, (2013) Reassessing buried surface areas in protein-protein complexes. Protein Sci 22: 1453-1457 doi:10.1002/pro.2330.
61. Huang Y, Cao H, Liu Z, (2012) Three-dimensional domain swapping in the protein structure space. Proteins 80: 1610-1619 doi:10.1002/prot.24055.
62. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39: D561-D568 doi:10.1093/nar/gkq973.