The origins and evolution of functional modules: Lessons from protein complexes

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1467, 2006, Pages 507-517

  Pereira Leal, Jose B ^a   Levy, Emmanuel D ^a   Teichmann, Sarah A ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Duplication; Evolution; Functional module; Modularity; Protein complex; Protein interaction network

Indexed keywords

COMPLEXITY; PROTEIN;

MULTIPROTEIN COMPLEX; PROTEIN;

BIOLOGICAL MODEL; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; REVIEW;

EVOLUTION, MOLECULAR; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; PROTEINS;

EID: 33646347144     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2005.1807     Document Type: Article

References (96)

1. Aharoni, A., Gaidukov, L., Khersonsky, O., Mc, Q. G. S., Roodveldt, C. & Tawfik, D. S. 2005 The 'evolvability' of promiscuous protein functions. Nat. Genet. 37, 73-76.
2. Amoutzias, G. D., Robertson, D. L., Oliver, S. G. & Bornberg-Bauer, E. 2004 Convergent evolution of gene networks by single-gene duplications in higher eukaryotes. EMBO Rep. 5, 274-279. (doi:10.1038/sj.embor.7400096)
3. Amoutzias, G. D., Weiner, J. & Bornberg-Bauer, E. 2005 Phylogenetic profiling of protein interaction networks in eukaryotic transcription factors reveals focal proteins being ancestral to hubs. Gene 347, 247-253. (doi:10. 1016/j.gene.2004.12.031)
4. Andreeva, A., Howorth, D., Brenner, S. E., Hubbard, T. J., Chothia, C. & Murzin, A. G. 2004 SCOP database in 2004: refinements integrate structure and sequence family data. Nucleic Acids Res. 32, D226-D229. (doi:10.1093/nar/ gkh039)
5. Babu, M. M., Luscombe, N. M., Aravind, L., Gerstein, M. & Teichmann, S. A. 2004 Structure and evolution of transcriptional regulatory networks. Curr. Opin. Struct. Biol. 14, 283-291. (doi:10.1016/j.sbi.2004.05.004)
6. Bader, G. D. & Hogue, C. W. 2003 An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4, 2. (doi:10.1186/1471-2105-4-2)
7. Bahadur, R. P., Chakrabarti, P., Rodier, F. & Janin, J. 2003 Dissecting subunit interfaces in homodimeric proteins. Proteins 53, 708-719. (doi:10.1002/prot.10461)
8. Bahadur, R. P., Chakrabarti, P., Rodier, F. & Janin, J. 2004 A dissection of specific and non-specific protein-protein interfaces. J. Mol. Biol. 336, 943-955. (doi:10.1016/j.jmb. 2003.12.073)
9. Barabasi, A. L. & Albert, R. 1999 Emergence of scaling in random networks. Science 286, 509-512. (doi:10.1126/science.286.5439.509)
10. Barabasi, A. L. & Oltvai, Z. N. 2004 Network biology: understanding the cell's functional organization. Nat. Rev. Genet. 5, 101-113. (doi:10.1038/nrg1272)
11. Bell, S. D. & Jackson, S. P. 2001 Mechanism and regulation of transcription in archaea. Curr. Opin. Microbiol. 4, 208-213. (doi:10.1016/S1369-5274(00)00190-9)
12. Boehm, M. & Bonifacino, J. S. 2001 Adaptins: the final recount. Mol. Biol. Cell 12, 2907-2920.
13. Brazma, A. & Vilo, J. 2000 Gene expression data analysis. FEBS Lett. 480, 17-24. (doi:10.1016/S0014-5793(00) 01772-5)
14. Calabretta, R., Nolfi, S., Parisi, D. & Wagner, G. P. 1998 Emergence of Functional Modularity in robots. In From animals to animals, vol. 5 (ed. R. Pfeifer, B. Blumberg, J.-A. Meyer & S. W. Wilson), pp. 497-504. Cambridge, MA: MIT Press.
15. Calabretta, R., Nolfi, S., Parisi, D. & Wagner, G. P. 2000 Duplication of modules facilitates the evolution of functional specialization. Artif. Life 6, 69-84. (doi:10.1162/106454600568320)
16. Chakrabarti, P. & Janin, J. 2002 Dissecting protein-protein recognition sites. Proteins 47, 334-343. (doi:10.1002/prot.10085)
17. Chothia, C. 1992 One thousand families for the molecular biologist. Nature 357, 543-544. (doi:10.1038/357543a0)
18. Cohen, J. D. & Tong, F. 2001 Neuroscience. The face of controversy. Science 293, 2405-2407. (doi:10.1126/science.1066018)
19. Coulson, R. M. & Ouzounis, C. A. 2003 The phylogenetic diversity of eukaryotic transcription. Nucleic Acids Res. 31, 653-660. (doi:10.1093/nar/ gkg156)
20. Coulson, R. M., Enright, A. J. & Ouzounis, C. A. 2001 Transcription-associated protein families are primarily taxon-specific. Bioinformatics 17, 95-97. (doi:10.1093/bioinformatics/17.1.95)
21. Date, S. V. & Marcotte, E. M. 2003 Discovery of uncharacterized cellular systems by genome-wide analysis of functional linkages. Nat. Biotechnol. 21, 1055-1062. (doi:10.1038/nbt861)
22. de Lichtenberg, U., Jensen, L. J., Brunak, S. & Bork, P. 2005 Dynamic complex formation during the yeast cell cycle. Science 307, 724-727. (doi:10.1126/science.H05103)
23. Enright, A. J., Iliopoulos, I., Kyrpides, N. C. & Ouzounis, C. A. 1999 Protein interaction maps for complete genomes based on gene fusion events. Nature 402, 86-90. (doi:10.1038/47056)
24. Fell, D. A. & Wagner, A. 2000 The small world of metabolism. Nat. Biotechnol. 18, 1121-1122. (doi:10.1038/81025)
25. Fraser, H. B. 2005 Modularity and evolutionary constraint on proteins. Nat. Genet. 37, 351-352. (doi:10.1038/ng1530)
26. Gagneur, J., Krause, R., Bouwmeester, T. & Casari, G. 2004 Modular decomposition of protein-protein interaction networks. Genome Biol. 5, R57. (doi:10.1186/gb-2004-5-8-r57)
27. Gavin, A. C. et al. 2002 Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141-147. (doi:10.1038/415141a)
28. Goodsell, D. S. & Olson, A. J. 2000 Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29, 105-153. (doi:10.1146/annurev. biophys.29.1.105)
29. Guelzim, N., Bottani, S., Bourgine, P. & Kepes, F. 2002 Topological and causal structure of the yeast transcriptional regulatory network. Nat. Genet. 31, 60-63. (doi:10. 1038/ng873)
30. Han, J. D. et al. 2004 Evidence for dynamically organized modularity in the yeast protein-protein interaction network. Nature 430, 88-93. (doi:10.1038/nature02555)
31. Hansen, T. F. 2003 Is modularity necessary for evolvability? Remarks, on the relationship between pleiotropy and evolvability. Biosystems 69, 83-94. (doi:10.1016/S0303-2647(02)00132-6)
32. Hartwell, L. H., Hopfield, J. J., Leibler, S. & Murray, A. W. 1999 From molecular to modular cell biology. Nature 402, C47-C52. (doi:10.1038/35011540)
33. Henrick, K. & Thornton, J. M. 1998 PQS: a protein quaternary structure file server. Trends Biochem. Sci. 23, 358-361. (doi:10.1016/S0968- 0004(98)01253-5)
34. Ho, Y. et al. 2002 Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183. (doi:10.1038/415180a)
35. Huynen, M., Snel, B., Lathe 3rd, W. & Bork, P. 2000 Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome Res. 10, 1204-1210. (doi:10.1101/gr.10.8.1204)
36. Ihmels, J., Friedlander, G., Bergmann, S., Sarig, O., Ziv, Y. & Barkai, N. 2002 Revealing modular organization in the yeast transcriptional network. Nat. Genet. 31, 370-377.
37. James, L. C. & Tawfik, D. S. 2003 Conformational diversity and protein evolution-a 60-year-old hypothesis revisited. Trends Biochem. Sci. 28, 361-368. (doi:10.1016/S0968-0004(03)00135-X)
38. James, L. C., Roversi, P. & Tawfik, D. S. 2003 Antibody multispecificity mediated by conformational diversity. Science 299, 1362-1367. (doi:10.1126/science.1079731)
39. Janin, J. & Chothia, C. 1990 The structure of protein-protein recognition sites. J. Biol. Chem. 265, 16027-16030.
40. Janin, J., Miller, S. & Chothia, C. 1988 Surface, subunit interfaces and interior of oligomeric proteins. J. Mol. Biol. 204, 155-164. (doi:10.1016/0022-2836(88)90606-7)
41. Jeong, H., Tombor, B., Albert, R., Oltvai, Z. N. & Barabasi, A. L. 2000 The large-scale organization of metabolic networks. Nature 407, 651-654. (doi:10.1038/35036627)
42. King, A. D., Przulj, N. & Jurisica, I. 2004 Protein complex prediction via cost-based clustering. Bioinformatics 20, 3013-3020. (doi:10.1093/bioinformatics/bth351)
43. Kirschner, M. & Gerhart, J. 1998 Evolvability. Proc. Natl Acad. Sci. USA 95, 8420-8427. (doi:10.1073/pnas.95.15. 8420)
44. Kummerfeld, S. K. & Teichmann, S. A. 2005 Relative rates of gene fusion and fission in multi-domain proteins. Trends Genet. 21, 25-30. (doi:10.1016/j.tig.2004.11.007)
45. Kunin, V., Pereira-Leal, J. B. & Ouzounis, C. A. 2004 Functional evolution of the yeast protein interaction network. Mol. Biol. Evol. 21, 1171-1176. (doi:10.1093/molbev/msh085)
46. Kyrpides, N., Overbeek, R. & Ouzounis, C. 1999 Universal protein families and the functional content of the last universal common ancestor. J. Mol. Evol. 49, 413-423.
47. Langlois, R. 2002 Modularity in technology and organization. J. Econ. Behav. Organ. 49, 19-37. (doi:10.1016/S0167-2681(02)00056-2)
48. Levitt, M. & Chothia, C. 1976 Structural patterns in globular proteins. Nature 261, 552-558. (doi:10.1038/261552a0)
49. Lew, D. J. & Burke, D. J. 2003 The spindle assembly and spindle position checkpoints. Annu. Rev. Genet. 37, 251-282. (doi:10.1146/annurev.genet. 37.042203.120656)
50. Li, H., Pellegrini, M. & Eisenberg, D. 2005 Detection of parallel functional modules by comparative analysis of genome sequences. Nat. Biotechnol. 23, 253-260. (doi:10. 1038/nbt1065)
51. Liu, Y. & Eisenberg, D. 2002 3D domain swapping: as domains continue to swap. Protein Sci. 11, 1285-1299. (doi:10.1110/ps.0201402)
52. Liu, Y., Hart, P. J., Schlunegger, M. P. & Eisenberg, D. 1998 The crystal structure of a 3D domain-swapped dimer of RNase A at a 2.1-Å resolution. Proc. Natl. Acad. Sci. USA 95, 3437-3442. (doi:10.1073/pnas.95.7. 3437)
53. Lo Conte, L., Chothia, C. & Janin, J. 1999 The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285, 2177-2198. (doi:10.1006/jmbi.1998.2439)
54. Lynch, M. & Conery, J. S. 2000 The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155. (doi:10.1126/science.290.5494.1151)
55. Lynch, M. & Katju, V. 2004 The altered evolutionary trajectories of gene duplicates. Trends Genet. 20, 544-549. (doi:10.1016/j.tig.2004.09.001)
56. Makarova, K. S., Aravind, L., Galperin, M. Y., Grishin, N. V., Tatusov, R. L., Wolf, Y. I. & Koonin, E. V. 1999 Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell. Genome Res. 9, 608-628.
57. Marcotte, E. M., Pellegrini, M., Ng, H. L., Rice, D. W., Yeates, T. O. & Eisenberg, D. 1999 Detecting protein function and protein-protein interactions from genome sequences. Science 285, 751-753. (doi:10.1126/science. 285.5428.751)
58. Marianayagam, N. J., Sunde, M. & Matthews, J. M. 2004 The power of two: protein dimerization in biology. Trends Biochem. Sci. 29, 618-625. (doi:10.1016/j.tibs.2004.09.006)
59. Mewes, H. W. et al. 2002 MIPS: a database for genomes and protein sequences. Nucleic Acids Res. 30, 31-34. (doi:10. 1093/nar/30.1.31)
60. Murzin, A. G., Brenner, S. E., Hubbard, T. & Chothia, C. 1995 SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247, 536-540. (doi:10.1006/jmbi.1995. 0159)
61. Needham, J. 1933 On the dissociability of the fundamental processes in ontogenesis. Biol. Rev. 8, 180-233.
62. Pastor-Satorras, R., Smith, E. & Sole, R. V. 2003 Evolving protein interaction networks through gene duplication. J. Theor. Biol. 222, 199-210. (doi:10.1016/S0022-5193(03)00028-6)
63. Pellegrini, M., Marcotte, E. M., Thompson, M. J., Eisenberg, D. & Yeates, T. O. 1999 Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc. Natl Acad. Sci. USA 96, 4285-4288. (doi:10.1073/pnas.96.8.4285)
64. Pereira-Leal, J. B. & Teichmann, S. A. 2005 Novel specificities emerge by stepwise duplication of functional modules. Genome Res 15, 552-559. (doi:10.1101/gr. 3102105)
65. Pereira-Leal, J. B., Enright, A. J. & Ouzounis, C. A. 2004 Detection of functional modules from protein interaction networks. Proteins 54, 49-57. (doi:10.1002/prot.10505)
66. Pereira-Leal, J. B., Audit, B., Peregrin-Alvarez, J. M. & Ouzounis, C. A. 2005 An exponential core in the heart of the yeast protein interaction network. Mol. Biol. Evol. 22, 421-425. (doi:10.1093/molbev/msi024)
67. Prince, V. E. & Pickett, F. B. 2002 Splitting pairs: the diverging fates of duplicated genes. Nat. Rev. Genet. 3, 827-837. (doi:10.1038/nrg928)
68. Qin, H., Lu, H. H., Wu, W. B. & Li, W. H. 2003 Evolution of the yeast protein interaction network. Proc. Natl Acad. Sci. USA 100, 12 820-12 824. (doi:10.1073/pnas.2235584100)
69. Ravasz, E., Somera, A. L., Mongru, D. A., Oltvai, Z. N. & Barabasi, A. L. 2002 Hierarchical organization of modularity in metabolic networks. Science 297, 1551-1555. (doi:10.1126/science.1073374)
70. Rives, A. W. & Galitski, T. 2003 Modular organization of cellular networks. Proc. Natl Acad. Sci. USA 100, 1128-1133. (doi:10.1073/pnas. 0237338100)
71. Schlosser, G. 2004 The role of modules in development and evolution. In Modularity in development and evolution (ed. G. Schlosser & A. Wagner), pp. 519-582. Chicago: The Chicago University Press.
72. Schwartz, M. A. & Madhani, H. D. 2004 Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. Annu. Rev. Genet. 38, 725-748. (doi:10.1146/annurev. genet.39.073003.112634)
73. Segal, E., Shapira, M., Regev, A., Pe'er, D., Botstein, D., Koller, D. & Friedman, N. 2003 Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data. Nat. Genet. 34, 166-176.
74. Snel, B. & Huynen, M. A. 2004 Quantifying modularity in the evolution of biomolecular systems. Genome Res. 14, 391-397. (doi:10.1101/gr.1969504)
75. Snel, B., Bork, P. & Huynen, M. 2000 Genome evolution. Gene fusion versus gene fission. Trends Genet. 16, 9-11. (doi:10.1016/S0168-9525(99)01924-1)
76. Snel, B., Bork, P. & Huynen, M. A. 2002 The identification of functional modules from the genomic association of genes. Proc. Natl Acad. Sci. USA 99, 5890-5895. (doi:10.1073/pnas.092632599)
77. Soding, J. & Lupas, A. N. 2003 More than the sum of their parts: on the evolution of proteins from peptides. Bioessays 25, 837-846. (doi:10.1002/bies.10321)
78. Spirin, V. & Mirny, L. A. 2003 Protein complexes and functional modules in molecular networks. Proc. Natl Acad. Sci. USA 100, 12 123-12 128. (doi:10.1073/pnas. 2032324100)
79. Stock, D., Gibbons, C., Arechaga, I., Leslie, A. G. & Walker, J. E. 2000 The rotary mechanism of ATP synthase. Curr. Opin. Struct. Biol. 10, 672-679. (doi:10.1016/S0959-440X(00)00147-0)
80. Strogatz, S. H. 2001 Exploring complex networks. Nature 410, 268-276. (doi:10.1038/35065725)
81. Teichmann, S. A. 2002 The constraints protein-protein interactions place on sequence divergence. J. Mol. Biol. 324, 399-407. (doi:10.1016/S0022-2836(02) 01144-0)
82. Teichmann, S. A. & Babu, M. M. 2004 Gene regulatory network growth by duplication. Nat. Genet. 36, 492-496. (doi:10.1038/ng1340)
83. Teichmann, S. A., Park, J. & Chothia, C. 1998 Structural assignments to the Mycoplasma genitalium proteins show extensive gene duplications and domain rearrangements. Proc. Natl Acad. Sci. USA 95, 14658-14663. (doi:10.1073/pnas.95.25.14658)
84. Teichmann, S. A., Rison, S. C., Thornton, J. M., Riley, M., Gough, J. & Chothia, C. 2001 The evolution and structural anatomy of the small molecule metabolic pathways in Escherichia coli. J. Mol. Biol. 311, 693-708. (doi:10.1006/jmbi.2001.4912)
85. True, J. R. & Carroll, S. B. 2002 Gene co-option in physiological and morphological evolution. Annu. Rev. Cell Dev. Biol. 18, 53-80. (doi:10.1146/annurev.cellbio.18.020402.140619)
86. Vagnarelli, P. & Earnshaw, W. C. 2004 Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma 113, 211-222. (doi:10.1007/s00412-004-0307-3)
87. van Noort, V., Snel, B. & Huynen, M. A. 2004 The yeast coexpression network has a small-world, scale-free architecture and can be explained by a simple model. EMBO Rep. 5, 280-284. (doi:10.1038/sj.embor.7400090)
88. Vazquez, A., Flammini, A., Maritan, A. & Vespignani, A. 2003 Modeling of protein interaction networks. Complexus 1, 38-44. (doi:10.1159/000067642)
89. Vogel, C., Teichmann, S. A. & Pereira-Leal, J. 2005 The relationship between domain duplication and recombination. J. Mol. Biol. 346, 355-365. (doi:10.1016/j.jmb.2004. 11.050)
90. von Mering, C., Zdobnov, E. M., Tsoka, S., Ciccarelli, F. D., Pereira-Leal, J. B., Ouzounis, C. A. & Bork, P. 2003 Genome evolution reveals biochemical networks and functional modules. Proc. Natl Acad. Sci. USA 100, 15 428-15 433. (doi:10.1073/pnas.2136809100)
91. Wagner, G. (ed.) 1995 Adaptation and the modular design of organisms. London: Springer-Verlag.
92. Wagner, G. 1996 Homologues, natural kinds and the evolution of modularity. Am. Zool. 36, 36-43.
93. Wagner, A. 2005 Robustness, evolvability, and neutrality. FEBS Lett. 579, 1772-1778. (doi:10.1016/j.febslet.2005. 01.063)
94. Watts, D. J. & Strogatz, S. H. 1998 Collective dynamics of 'small-world' networks. Nature 393, 440-442. (doi:10. 1038/30918)
95. Winther, R. G. 2001 Varieties of modules: kinds, levels, origins, and behaviors. J. Exp. Zool. 291, 116-129. (doi:10.1002/jez.1064)
96. Woychik, N. & Reinberg, D. 2001 RNA polymerases: subunits and functional domains. In Nature encyclopedia of life sciences. Chichester: Wiley.