Proteome-wide discovery of evolutionary conserved sequences in disordered regions

Science Signaling

Volumn 5, Issue 215, 2012, Pages

  Nguyen Ba, Alex N ^a,b   Yeh, Brian J ^b   Van Dyk, Dewald ^a,d   Davidson, Alan R ^d   Andrews, Brenda J ^a,d   Weiss, Eric L ^c   Moses, Alan M ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYCLIN DEPENDENT KINASE 1; KARYOPHERIN; PROTEIN KINASE; PROTEOME; FUNGAL PROTEIN;

ARTICLE; BIOINFORMATICS; ENZYME SUBSTRATE; HIDDEN MARKOV MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PROBABILITY; PROTEIN TERTIARY STRUCTURE; YEAST;

PHYLO;

AMINO ACID MOTIFS; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; HUMANS; MARKOV CHAINS; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; PROTEOME; YEASTS;

EID: 84858267844     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002515     Document Type: Article

References (106)

1. J. J. Ward, J. S. Sodhi, L. J. McGuffin, B. F. Buxton, D. T. Jones, Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337, 635-645 (2004).
2. M. Wells, H. Tidow, T. J. Rutherford, P. Markwick, M. R. Jensen, E. Mylonas, D. I. Svergun, M. Blackledge, A. R. Fersht, Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain. Proc. Natl. Acad. Sci. U.S.A. 105, 5762-5767 (2008).
3. V. N. Uversky, C. J. Oldfield, A. K. Dunker, Intrinsically disordered proteins in human diseases: Introducing the D2 concept. Annu. Rev. Biophys. 37, 215-246 (2008).
4. L. S. Ostedgaard, O. Baldursson, D. W. Vermeer, M. J. Welsh, A. D. Robertson, A functional R domain from cystic fibrosis transmembrane conductance regulator is predominantly unstructured in solution. Proc. Natl. Acad. Sci. U.S.A. 97, 5657-5662 (2000).
5. P. E. Wright, H. J. Dyson, Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm. J. Mol. Biol. 293, 321-331 (1999).
6. J. H. Fong, B. A. Shoemaker, S. O. Garbuzynskiy, M. Y. Lobanov, O. V. Galzitskaya, A. R. Panchenko, Intrinsic disorder in protein interactions: Insights from a comprehensive structural analysis. PLoS Comput. Biol. 5, e1000316 (2009).
7. A. B. Sigalov, A. V. Zhuravleva, V. Y. Orekhov, Binding of intrinsically disordered proteins is not necessarily accompanied by a structural transition to a folded form. Biochimie 89, 419-421 (2007).
8. A. K. Dunker, J. D. Lawson, C. J. Brown, R. M. Williams, P. Romero, J. S. Oh, C. J. Oldfield, A. M. Campen, C. M. Ratliff, K. W. Hipps, J. Ausio, M. S. Nissen, R. Reeves, C. Kang, C. R. Kissinger, R. W. Bailey, M. D. Griswold, W. Chiu, E. C. Garner, Z. Obradovic, Intrinsically disordered protein. J. Mol. Graph. Model. 19, 26-59 (2001).
9. S. Brocca, M. Samalíková, V. N. Uversky, M. Lotti, M. Vanoni, L. Alberghina, R. Grandori, Order propensity of an intrinsically disordered protein, the cyclin-dependentkinase inhibitor Sic1. Proteins 76, 731-746 (2009).
10. A. K. Dunker, C. J. Brown, J. D. Lawson, L. M. Iakoucheva, Z. Obradović, Intrinsic disorder and protein function. Biochemistry 41, 6573-6582 (2002).
11. A. K. Dunker, M. S. Cortese, P. Romero, L. M. Iakoucheva, V. N. Uversky, Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J. 272, 5129-5148 (2005).
12. L. M. Iakoucheva, P. Radivojac, C. J. Brown, T. R. O'Connor, J. G. Sikes, Z. Obradovic, A. K. Dunker, The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 32, 1037-1049 (2004).
13. H. J. Dyson, P. E. Wright, Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208 (2005).
14. C. M. Gould, F. Diella, A. Via, P. Puntervoll, C. Gemünd, S. Chabanis-Davidson, S. Michael, A. Sayadi, J. C. Bryne, C. Chica, M. Seiler, N. E. Davey, N. Haslam, R. J. Weatheritt, A. Budd, T. Hughes, J. Pas, L. Rychlewski, G. Travé, R. Aasland, M. Helmer-Citterich, R. Linding, T. J. Gibson, ELM: The status of the 2010 eukaryotic linear motif resource. Nucleic Acids Res. 38, D167-D180 (2010).
15. A. Ureta-Vidal, L. Ettwiller, E. Birney, Comparative genomics: Genome-wide analysis in metazoan eukaryotes. Nat. Rev. Genet. 4, 251-262 (2003).
16. P. Beltrao, L. Serrano, Comparative genomics and disorder prediction identify biologically relevant SH3 protein interactions. PLoS Comput. Biol. 1, e26 (2005).
17. J. Mok, P. M. Kim, H. Y. K. Lam, S. Piccirillo, X. Zhou, G. R. Jeschke, D. L. Sheridan, S. A. Parker, V. Desai, M. Jwa, E. Cameroni, H. Niu, M. Good, A. Remenyi, J. L. N. Ma, Y. J. Sheu, H. E. Sassi, R. Sopko, C. S. M. Chan, C. De Virgilio, N. M. Hollingsworth, W. A. Lim, D. F. Stern, B. Stillman, B. J. Andrews, M. B. Gerstein, M. Snyder, B. E. Turk, Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Sci. Signal. 3, ra12 (2010).
18. R. Linding, L. J. Jensen, G. J. Ostheimer, M. A. T. M. van Vugt, C. Jørgensen, I. M. Miron, F. Diella, K. Colwill, L. Taylor, K. Elder, P. Metalnikov, V. Nguyen, A. Pasculescu, J. Jin, J. G. Park, L. D. Samson, J. R. Woodgett, R. B. Russell, P. Bork, M. B. Yaffe, T. Pawson, Systematic discovery of in vivo phosphorylation networks. Cell 129, 1415-1426 (2007).
19. R. Tonikian, X. Xin, C. P. Toret, D. Gfeller, C. Landgraf, S. Panni, S. Paoluzi, L. Castagnoli, B. Currell, S. Seshagiri, H. Yu, B. Winsor, M. Vidal, M. B. Gerstein, G. D. Bader, R. Volkmer, G. Cesareni, D. G. Drubin, P. M. Kim, S. S. Sidhu, C. Boone, Bayesian modeling of the yeast SH3 domain interactome predicts spatiotemporal dynamics of endocytosis proteins. PLoS Biol. 7, e1000218 (2009).
20. D. S. Lieber, O. Elemento, S. Tavazoie, Large-scale discovery and characterization of protein regulatory motifs in eukaryotes. PLoS One 5, e14444 (2010).
21. V. Neduva, R. Linding, I. Su-Angrand, A. Stark, F. de Masi, T. J. Gibson, J. Lewis, L. Serrano, R. B. Russell, Systematic discovery of new recognition peptides mediating protein interaction networks. PLoS Biol. 3, e405 (2005).
22. A. Siepel, G. Bejerano, J. S. Pedersen, A. S. Hinrichs, M. Hou, K. Rosenbloom, H. Clawson, J. Spieth, L. W. Hillier, S. Richards, G. M. Weinstock, R. K. Wilson, R. A. Gibbs, W. J. Kent, W. Miller, D. Haussler, Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050 (2005).
23. R. Linding, L. J. Jensen, F. Diella, P. Bork, T. J. Gibson, R. B. Russell, Protein disorder prediction: Implications for structural proteomics. Structure 11, 1453-1459 (2003).
24. A. N. Nguyen Ba, A. M. Moses, Evolution of characterized phosphorylation sites in budding yeast. Mol. Biol. Evol. 27, 2027-2037 (2010).
25. C. Chica, A. Labarga, C. M. Gould, R. López, T. J. Gibson, A tree-based conservation scoring method for short linear motifs in multiple alignments of protein sequences. BMC Bioinformatics 9, 229 (2008).
26. J. L. Gordon, K. P. Byrne, K. H. Wolfe, Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet. 5, e1000485 (2009).
27. S. Ren, V. N. Uversky, Z. Chen, A. K. Dunker, Z. Obradovic, Short linear motifs recognized by SH2, SH3 and Ser/Thr kinase domains are conserved in disordered protein regions. BMC Genomics 9 (Suppl. 2), S26 (2008).
28. P. Nash, X. Tang, S. Orlicky, Q. Chen, F. B. Gertler, M. D. Mendenhall, F. Sicheri, T. Pawson, M. Tyers, Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414, 514-521 (2001).
29. T. Mittag, S. Orlicky, W. Y. Choy, X. Tang, H. Lin, F. Sicheri, L. E. Kay, M. Tyers, J. D. Forman-Kay, Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor. Proc. Natl. Acad. Sci. U.S.A. 105, 17772-17777 (2008).
30. J. A. Ubersax, E. L. Woodbury, P. N. Quang, M. Paraz, J. D. Blethrow, K. Shah, K. M. Shokat, D. O. Morgan, Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864 (2003).
31. S. L. Jaspersen, D. O. Morgan, Cdc14 activates cdc15 to promote mitotic exit in budding yeast. Curr. Biol. 10, 615-618 (2000).
32. V. Wanke, I. Pedruzzi, E. Cameroni, F. Dubouloz, C. De Virgilio, Regulation of G0 entry by the Pho80-Pho85 cyclin-CDK complex. EMBO J. 24, 4271-4278 (2005).
33. C. A. Ydenberg, M. D. Rose, Antagonistic regulation of Fus2p nuclear localization by pheromone signaling and the cell cycle. J. Cell Biol. 184, 409-422 (2009).
34. D. P. Denning, S. S. Patel, V. Uversky, A. L. Fink, M. Rexach, Disorder in the nuclear pore complex: The FG repeat regions of nucleoporins are natively unfolded. Proc. Natl. Acad. Sci. U.S.A. 100, 2450-2455 (2003).
35. C. K. Lau, T. H. Giddings Jr., M. Winey, A novel allele of Saccharomyces cerevisiae NDC1 reveals a potential role for the spindle pole body component Ndc1p in nuclear pore assembly. Eukaryot. Cell 3, 447-458 (2004).
36. H. J. Chial, M. P. Rout, T. H. Giddings, M.Winey, Saccharomyces cerevisiae Ndc1p is a shared component of nuclear pore complexes and spindle pole bodies. J. Cell Biol. 143, 1789-1800 (1998).
37. D. T. Warren, P. D. Andrews, C. W. Gourlay, K. R. Ayscough, Sla1p couples the yeast endocytic machinery to proteins regulating actin dynamics. J. Cell Sci. 115, 1703-1715 (2002).
38. B. A. Buschhorn, J. M. Peters, How APC/C orders destruction. Nat. Cell Biol. 8, 209-211 (2006).
39. E. Choi, J. M. Dial, D. E. Jeong, M. C. Hall, Unique D box and KEN box sequences limit ubiquitination of Acm1 and promote pseudosubstrate inhibition of the anaphase-promoting complex. J. Biol. Chem. 283, 23701-23710 (2008).
40. E. M. J. King, S. J. A. van der Sar, K. G. Hardwick, Mad3 KEN boxes mediate both Cdc20 and Mad3 turnover, and are critical for the spindle checkpoint. PLoS One 2, e342 (2007).
41. O. Cohen-Fix, J. M. Peters, M. W. Kirschner, D. Koshland, Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10, 3081-3093 (1996).
42. Y. L. Juang, J. Huang, J. M. Peters, M. E. McLaughlin, C. Y. Tai, D. Pellman, APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle. Science 275, 1311-1314 (1997).
43. C. Hendrickson, M. A. Meyn III, L. Morabito, S. L. Holloway, The KEN box regulates Clb2 proteolysis in G1 and at the metaphase-to-anaphase transition. Curr. Biol. 11, 1781-1787 (2001).
44. O. Feine, A. Zur, H. Mahbubani, M. Brandeis, Human Kid is degraded by the APC/C(Cdh1) but not by the APC/C(Cdc20). Cell Cycle 6, 2516-2523 (2007).
45. J. S. Chang, F. Winston, Spt10 and Spt21 are required for transcriptional silencing in Saccharomyces cerevisiae. Eukaryot. Cell 10, 118-129 (2011).
46. P. T. Spellman, G. Sherlock, M. Q. Zhang, V. R. Iyer, K. Anders, M. B. Eisen, P. O. Brown, D. Botstein, B. Futcher, Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9, 3273-3297 (1998).
47. R. Sopko, D. Huang, N. Preston, G. Chua, B. Papp, K. Kafadar, M. Snyder, S. G. Oliver, M. Cyert, T. R. Hughes, C. Boone, B. Andrews, Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21, 319-330 (2006).
48. D. Kressler, J. de la Cruz, M. Rojo, P. Linder, Dbp6p is an essential putative ATP-dependent RNA helicase required for 60S-ribosomal-subunit assembly in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 1855-1865 (1998).
49. J. M. Charette, S. J. Baserga, The DEAD-box RNA helicase-like Utp25 is an SSU processome component. RNA 16, 2156-2169 (2010).
50. G. D. Bader, C. W. V. Hogue, An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4, 2 (2003).
51. T. de Beer, A. N. Hoofnagle, J. L. Enmon, R. C. Bowers, M. Yamabhai, B. K. Kay, M. Overduin, Molecular mechanism of NPF recognition by EH domains. Nat. Struct. Biol. 7, 1018-1022 (2000).
52. A. N. Nguyen Ba, A. Pogoutse, N. Provart, A. M. Moses, NLStradamus: A simple hidden Markov model for nuclear localization signal prediction. BMC Bioinformatics 10, 202 (2009).
53. A. Lange, R. E. Mills, C. J. Lange, M. Stewart, S. E. Devine, A. H. Corbett, Classical nuclear localization signals: Definition, function, and interaction with importin a. J. Biol. Chem. 282, 5101-5105 (2007).
54. M. J. Macias, S. Wiesner, M. Sudol, WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett. 513, 30-37 (2002).
55. A. A. Rodal, A. L. Manning, B. L. Goode, D. G. Drubin, Negative regulation of yeast WASp by two SH3 domain-containing proteins. Curr. Biol. 13, 1000-1008 (2003).
56. A. F. Roth, J. Wan, A. O. Bailey, B. Sun, J. A. Kuchar, W. N. Green, B. S. Phinney, J. R. Yates III, N. G. Davis, Global analysis of protein palmitoylation in yeast. Cell 125, 1003-1013 (2006).
57. Y. Ho, A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S. L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, L. Yang, C.Wolting, I. Donaldson, S. Schandorff, J. Shewnarane, M. Vo, J. Taggart, M. Goudreault, B. Muskat, C. Alfarano, D. Dewar, Z. Lin, K. Michalickova, A. R. Willems, H. Sassi, P. A. Nielsen, K. J. Rasmussen, J. R. Andersen, L. E. Johansen, L. H. Hansen, H. Jespersen, A. Podtelejnikov, E. Nielsen, J. Crawford, V. Poulsen, B. D. Sørensen, J. Matthiesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. V. Hogue, D. Figeys, M. Tyers, Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183 (2002).
58. A. Breitkreutz, H. Choi, J. R. Sharom, L. Boucher, V. Neduva, B. Larsen, Z. Y. Lin, B. J. Breitkreutz, C. Stark, G. Liu, J. Ahn, D. Dewar-Darch, T. Reguly, X. Tang, R. Almeida, Z. S. Qin, T. Pawson, A. C. Gingras, A. I. Nesvizhskii, M. Tyers, A global protein kinase and phosphatase interaction network in yeast. Science 328, 1043-1046 (2010).
59. J. M. Jansen, A. G. Wanless, C. W. Seidel, E. L. Weiss, Cbk1 regulation of the RNA-binding protein Ssd1 integrates cell fate with translational control. Curr. Biol. 19, 2114-2120 (2009).
60. E. Mazanka, J. Alexander, B. J. Yeh, P. Charoenpong, D. M. Lowery, M. Yaffe, E. L. Weiss, The NDR/LATS family kinase Cbk1 directly controls transcriptional asymmetry. PLoS Biol. 6, e203 (2008).
61. D. Jacobs, D. Glossip, H. Xing, A. J. Muslin, K. Kornfeld, Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev. 13, 163-175 (1999).
62. A. Reményi, M. C. Good, W. A. Lim, Docking interactions in protein kinase and phosphatase networks. Curr. Opin. Struct. Biol. 16, 676-685 (2006).
63. P. Uetz, L. Giot, G. Cagney, T. A. Mansfield, R. S. Judson, J. R. Knight, D. Lockshon, V. Narayan, M. Srinivasan, P. Pochart, A. Qureshi-Emili, Y. Li, B. Godwin, D. Conover, T. Kalbfleisch, G. Vijayadamodar, M. Yang, M. Johnston, S. Fields, J. M. Rothberg, A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403, 623-627 (2000).
64. T. Ito, T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, Y. Sakaki, A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. U.S.A. 98, 4569-4574 (2001).
65. H. Jeong, S. P. Mason, A. L. Barabási, Z. N. Oltvai, Lethality and centrality in protein networks. Nature 411, 41-42 (2001).
66. N. Bertin, N. Simonis, D. Dupuy, M. E. Cusick, J. D. J. Han, H. B. Fraser, F. P. Roth, M. Vidal, Confirmation of organized modularity in the yeast interactome. PLoS Biol. 5, e153 (2007).
67. C. Haynes, C. J. Oldfield, F. Ji, N. Klitgord, M. E. Cusick, P. Radivojac, V. N. Uversky, M. Vidal, L. M. Iakoucheva, Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput. Biol. 2, e100 (2006).
68. N. E. Davey, R. J. Edwards, D. C. Shields, Computational identification and analysis of protein short linear motifs. Front. Biosci. 15, 801-825 (2010).
69. J. C. Obenauer, L. C. Cantley, M. B. Yaffe, Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641 (2003).
70. T. L. Bailey, C. Elkan, Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28-36 (1994).
71. N. E. Davey, D. C. Shields, R. J. Edwards, SLiMDisc: Short, linear motif discovery, correcting for common evolutionary descent. Nucleic Acids Res. 34, 3546-3554 (2006).
72. R. J. Edwards, N. E. Davey, D. C. Shields, SLiMFinder: A probabilistic method for identifying over-represented, convergently evolved, short linear motifs in proteins. PLoS One 2, e967 (2007).
73. V. Neduva, R. B. Russell, DILIMOT: Discovery of linear motifs in proteins. Nucleic Acids Res. 34, W350-W355 (2006).
74. B. Mészáros, I. Simon, Z. Dosztányi, Prediction of protein binding regions in disordered proteins. PLoS Comput. Biol. 5, e1000376 (2009).
75. D. A. Tagle, B. F. Koop, M. Goodman, J. L. Slightom, D. L. Hess, R. T. Jones, Embryonic ε and γ globin genes of a prosimian primate (Galago crassicaudatus). Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. J. Mol. Biol. 203, 439-455 (1988).
76. P. Cliften, P. Sudarsanam, A. Desikan, L. Fulton, B. Fulton, J. Majors, R. Waterston, B. A. Cohen, M. Johnston, Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301, 71-76 (2003).
77. W. J. Kent, C. W. Sugnet, T. S. Furey, K. M. Roskin, T. H. Pringle, A. M. Zahler, D. Haussler, The human genome browser at UCSC. Genome Res. 12, 996-1006 (2002).
78. P. Flicek, M. R. Amode, D. Barrell, K. Beal, S. Brent, Y. Chen, P. Clapham, G. Coates, S. Fairley, S. Fitzgerald, L. Gordon, M. Hendrix, T. Hourlier, N. Johnson, A. Kähäri, D. Keefe, S. Keenan, R. Kinsella, F. Kokocinski, E. Kulesha, P. Larsson, I. Longden, W. McLaren, B. Overduin, B. Pritchard, H. S. Riat, D. Rios, G. R. S. Ritchie, M. Ruffier, M. Schuster, D. Sobral, G. Spudich, Y. A. Tang, S. Trevanion, J. Vandrovcova, A. J. Vilella, S. White, S. P. Wilder, A. Zadissa, J. Zamora, B. L. Aken, E. Birney, F. Cunningham, I. Dunham, R. Durbin, X. M. Fernández-Suarez, J. Herrero, T. J. P. Hubbard, A. Parker, G. Proctor, J. Vogel, S. M. J. Searle, Ensembl 2011. Nucleic Acids Res. 39, D800-D806 (2011).
79. J. S. Bonifacino, L. M. Traub, Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447 (2003).
80. T. Darsow, C. G. Burd, S. D. Emr, Acidic di-leucine motif essential for AP-3-dependent sorting and restriction of the functional specificity of the Vam3p vacuolar t-SNARE. J. Cell Biol. 142, 913-922 (1998).
81. A. M. Moses, C. R. Landry, Moving from transcriptional to phospho-evolution: Generalizing regulatory evolution? Trends Genet. 26, 462-467 (2010).
82. L. J. Jensen, T. S. Jensen, U. de Lichtenberg, S. Brunak, P. Bork, Co-evolution of transcriptional and post-translational cell-cycle regulation. Nature 443, 594-597 (2006).
83. SGD Project, Saccharomyces Genome Database; http://www.yeastgenome.org/.
84. K. Katoh, K. Misawa, K. Kuma, T. Miyata, MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066 (2002).
85. Z. Yang, PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).
86. I. Wapinski, A. Pfeffer, N. Friedman, A. Regev, Natural history and evolutionary principles of gene duplication in fungi. Nature 449, 54-61 (2007).
87. S. Heinicke, M. S. Livstone, C. Lu, R. Oughtred, F. Kang, S. V. Angiuoli, O. White, D. Botstein, K. Dolinski, The Princeton Protein Orthology Database (P-POD): A comparative genomics analysis tool for biologists. PLoS One 2, e766 (2007).
88. S. F. Altschul, T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang,W. Miller, D. J. Lipman, Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997).
89. B. E. Suzek, H. Huang, P. McGarvey, R. Mazumder, C. H. Wu, UniRef: Comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23, 1282-1288 (2007).
90. R. Durbin, S. R. Eddy, A. Krogh, G. Mitchison, Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids (Cambridge University Press, Cambridge, UK, 1998).
91. J. Felsenstein, Evolutionary trees from DNA sequences: A maximum likelihood approach. J. Mol. Evol. 17, 368-376 (1981).
92. E. Rivas, S. R. Eddy, Probabilistic phylogenetic inference with insertions and deletions. PLoS Comput. Biol. 4, e1000172 (2008).
93. R. A. Cartwright, Logarithmic gap costs decrease alignment accuracy. BMC Bioinformatics 7, 527 (2006).
94. A. M. Waterhouse, J. B. Procter, D. M. A. Martin, M. Clamp, G. J. Barton, Jalview Version 2 - A multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).
95. J. J. Ward, L. J. McGuffin, K. Bryson, B. F. Buxton, D. T. Jones, The DISOPRED server for the prediction of protein disorder. Bioinformatics 20, 2138-2139 (2004).
96. D. T. Jones, W. R. Taylor, J. M. Thornton, A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33, 3038-3049 (1994).
97. J. C. Wootton, S. Federhen, Statistics of local complexity in amino acid sequences and sequence databases. Comput. Chem. 17, 149-163 (1993).
98. T. F. Smith, M. S. Waterman, Identification of common molecular subsequences. J. Mol. Biol. 147, 195-197 (1981).
99. P. Shannon, A. Markiel, O. Ozier, N. S. Baliga, J. T. Wang, D. Ramage, N. Amin, B. Schwikowski, T. Ideker, Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).
100. M. D. Robinson, J. Grigull, N. Mohammad, T. R. Hughes, FunSpec: A web-based cluster interpreter for yeast. BMC Bioinformatics 3, 35 (2002).
101. G. E. Crooks, G. Hon, J. M. Chandonia, S. E. Brenner, WebLogo: A sequence logo generator. Genome Res. 14, 1188-1190 (2004).
102. T. D. Schneider, R. M. Stephens, Sequence logos: A new way to display consensus sequences. Nucleic Acids Res. 18, 6097-6100 (1990).
103. S. Ghaemmaghami, W. K. Huh, K. Bower, R. W. Howson, A. Belle, N. Dephoure, E. K. O'Shea, J. S. Weissman, Global analysis of protein expression in yeast. Nature 425, 737-741 (2003).
104. D.M. Gelperin, M. A. White, M. L. Wilkinson, Y. Kon, L. A. Kung, K. J. Wise, N. Lopez-Hoyo, L. Jiang, S. Piccirillo, H. Yu, M. Gerstein, M. E. Dumont, E. M. Phizicky, M. Snyder, E. J. Grayhack, Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev. 19, 2816-2826 (2005).
105. H. Zhu, M. Bilgin, R. Bangham, D. Hall, A. Casamayor, P. Bertone, N. Lan, R. Jansen, S. Bidlingmaier, T. Houfek, T. Mitchell, P. Miller, R. A. Dean, M. Gerstein, M. Snyder, Global analysis of protein activities using proteome chips. Science 293, 2101-2105 (2001).
106. M. D. Abramoff, P. J. Magalhaes, S. J. Ram, Image processing with ImageJ. Biophotonics Int. 11, 36-42 (2004).