Experimental detection of short regulatory motifs in eukaryotic proteins: Tips for good practice as well as for bad

Cell Communication and Signaling

Volumn 13, Issue 1, 2015, Pages

  Gibson, Toby J ^a   Dinkel, Holger ^a   Van Roey, Kim ^a,b   Diella, Francesca ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

Author keywords

Bioinformatics; Cell regulation; Experimental design; Linear motifs; Molecular switches; Protein complexes

Indexed keywords

PROTEOME; PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; CLINICAL DATA REPOSITORY; EUKARYOTE; EXPERIMENTAL DESIGN; GOOD CLINICAL PRACTICE; HUMAN; IN VITRO STUDY; MOLECULAR SWITCH; MOLECULE; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DATABASE; PROTEIN MOTIF; PROTEIN PROCESSING; SCORING SYSTEM; SEQUENCE ALIGNMENT; SHORT REGULATORY MOTIF; VALIDATION STUDY; WORKFLOW; ANIMAL; BIOLOGY; CHEMISTRY; GENETIC SCREENING; GENETICS; METABOLISM;

AMINO ACID MOTIFS; ANIMALS; COMPUTATIONAL BIOLOGY; EUKARYOTA; GENETIC TESTING; HUMANS; PROTEINS;

EID: 84958125950     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/s12964-015-0121-y     Document Type: Article

References (118)

1. Czernilofsky AP, Levinson AD, Varmus HE, Bishop JM, Tischer E, Goodman HM. Nucleotide sequence of an avian sarcoma virus oncogene (src) and proposed amino acid sequence for gene product. Nature. 1980;287:198-203.
2. de Klein A, van Kessel AG, Grosveld G, Bartram CR, Hagemeijer A, Bootsma D, et al. A cellular oncogene is translocated to the Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1982;300:765-7.
3. Papp B, Pal C, Hurst LD. Dosage sensitivity and the evolution of gene families in yeast. Nature. 2003;424:194-7.
4. Kaizu K, Moriya H, Kitano H. Fragilities caused by dosage imbalance in regulation of the budding yeast cell cycle. PLoS Genet. 2010;6:e1000919.
5. Veitia RA, Potier MC. Gene dosage imbalances: Action, reaction, and models. Trends Biochem Sci. 2015;40:309-17.
6. Gibson TJ, Seiler M, Veitia RA. The transience of transient overexpression. Nat Methods. 2013;10:715-21.
7. Scott JD, Pawson T. Cell signaling in space and time: where proteins come together and when they're apart. Science. 2009;326:1220-4.
8. Gibson TJ. Cell regulation: Determined to signal discrete cooperation. Trends Biochem Sci. 2009;34:471-82.
9. Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V, Larsen B, et al. A global protein kinase and phosphatase interaction network in yeast. Science. 2010;328:1043-6.
10. Clancy T, Hovig E. From proteomes to complexomes in the era of systems biology. Proteomics. 2014;14:24-41.
11. Bienz M. Signalosome assembly by domains undergoing dynamic head-to-tail polymerization. Trends Biochem Sci. 2014;39:487-95.
12. Khalil AM, Rinn JL. RNA-protein interactions in human health and disease. Semin Cell Dev Biol. 2011;22:359-65.
13. Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell. 2012;149:1192-205.
14. Boja ES, Rodriguez H. Proteogenomic convergence for understanding cancer pathways and networks. Clin Proteomics. 2014;11:22.
15. Good MC, Zalatan JG, Lim WA. Scaffold proteins: hubs for controlling the flow of cellular information. Science. 2011;332:680-6.
16. Beck M, Topf M, Frazier Z, Tjong H, Xu M, Zhang S, et al. Exploring the spatial and temporal organization of a cell's proteome. J Struct Biol. 2011;173:483-96.
17. Van Roey K, Gibson TJ, Davey NE. Motif switches: Decision-making in cell regulation. Curr Opin Struct Biol. 2012;22:378-85.
18. Lavoie H, Li JJ, Thevakumaran N, Therrien M, Sicheri F. Dimerization-induced allostery in protein kinase regulation. Trends Biochem Sci. 2014;39:475-86.
19. Chang L, Barford D. Insights into the anaphase-promoting complex: A molecular machine that regulates mitosis. Curr Opin Struct Biol. 2014;29:1-9.
20. Balagopalan L, Coussens NP, Sherman E, Samelson LE, Sommers CL. The LAT story: A tale of cooperativity, coordination, and choreography. Cold Spring Harb Perspect Biol. 2010;2:a005512.
21. Aragon E, Goerner N, Zaromytidou AI, Xi Q, Escobedo A, Massague J, et al. A Smad action turnover switch operated by WW domain readers of a phosphoserine code. Genes Dev. 2011;25:1275-88.
22. Motlagh HN, Wrabl JO, Li J, Hilser VJ. The ensemble nature of allostery. Nature. 2014;508:331-9.
23. Choudhary C, Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol. 2010;11:427-39.
24. Akiva E, Friedlander G, Itzhaki Z, Margalit H. A dynamic view of domain-motif interactions. PLoS Comput Biol. 2012;8:e1002341.
25. Kortum RL, Rouquette-Jazdanian AK, Samelson LE. Ras and extracellular signal-regulated kinase signaling in thymocytes and T cells. Trends Immunol. 2013;34:259-68.
26. Dinkel H, Van Roey K, Michael S, Davey NE, Weatheritt RJ, Born D, et al. The eukaryotic linear motif resource ELM: 10 years and counting. Nucleic Acids Res. 2014;42:D259-66.
27. Tompa P, Davey NE, Gibson TJ, Babu MM. A million peptide motifs for the molecular biologist. Mol Cell. 2014;55:161-9.
28. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, et al. Intrinsically disordered protein. J Mol Graph Model. 2001;19:26-59.
29. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol. 2004;337:635-45.
30. Fuxreiter M, Tompa P, Simon I. Local structural disorder imparts plasticity on linear motifs. Bioinformatics. 2007;23:950-6.
31. Pancsa R, Fuxreiter M. Interactions via intrinsically disordered regions: what kind of motifs? IUBMB Life. 2012;64:513-20.
32. Van Roey K, Uyar B, Weatheritt RJ, Dinkel H, Seiler M, Budd A, et al. Short linear motifs: ubiquitous and functionally diverse protein interaction modules directing cell regulation. Chem Rev. 2014;114:6733-78.
33. Bandyra KJ, Bouvier M, Carpousis AJ, Luisi BF. The social fabric of the RNA degradosome. Biochim Biophys Acta. 1829;2013:515-22.
34. Waddington CH. The strategy of the genes. London: George Allen & Unwin; 1957.
35. Masel J, Siegal ML. Robustness: Mechanisms and consequences. Trends Genet. 2009;25:395-403.
36. Kitano H. Biological robustness. Nat Rev Genet. 2004;5:826-37.
37. Van Roey K, Dinkel H, Weatheritt RJ, Gibson TJ, Davey NE. The switches.ELM resource: A compendium of conditional regulatory interaction interfaces. Sci Signal. 2013;6:rs7.
38. Davey NE, Van Roey K, Weatheritt RJ, Toedt G, Uyar B, Altenberg B, et al. Attributes of short linear motifs. Mol Biosyst. 2012;8:268-81.
39. Neduva V, Russell RB. DILIMOT: Discovery of linear motifs in proteins. Nucleic Acids Res. 2006;34:W350-5.
40. Di Fiore B, Davey NE, Hagting A, Izawa D, Mansfeld J, Gibson TJ, et al. The ABBA motif binds APC/C activators and is shared by APC/C substrates and regulators. Dev Cell. 2015;32:358-72.
41. Davey NE, Cowan JL, Shields DC, Gibson TJ, Coldwell MJ, Edwards RJ. SLiMPrints: conservation-based discovery of functional motif fingerprints in intrinsically disordered protein regions. Nucleic Acids Res. 2012;40:10628-41.
42. McConnachie G, Langeberg LK, Scott JD. AKAP signaling complexes: getting to the heart of the matter. Trends Mol Med. 2006;12:317-23.
43. Suck D, Kabsch W, Mannherz HG. Three-dimensional structure of the complex of skeletal muscle actin and bovine pancreatic DNAse I at 6-A resolution. Proc Natl Acad Sci U S A. 1981;78:4319-23.
44. Xu D, Farmer A, Collett G, Grishin NV, Chook YM. Sequence and structural analyses of nuclear export signals in the NESdb database. Mol Biol Cell. 2012;23:3677-93.
45. Chakrabarti O, Rane NS, Hegde RS. Cytosolic aggregates perturb the degradation of nontranslocated secretory and membrane proteins. Mol Biol Cell. 2011;22:1625-37.
46. Diella F, Haslam N, Chica C, Budd A, Michael S, Brown NP, et al. Understanding eukaryotic linear motifs and their role in cell signaling and regulation. Front Biosci. 2008;13:6580-603.
47. Li W, Cowley A, Uludag M, Gur T, McWilliam H, Squizzato S, et al. The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res. 2015;43:W580-4.
48. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2 - A multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009;25:1189-91.
49. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7:539.
50. Drozdetskiy A, Cole C, Procter J, Barton GJ. JPred4: A protein secondary structure prediction server. Nucleic Acids Res. 2015;43:W389-94.
51. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: The protein families database. Nucleic Acids Res. 2014;42:D222-30.
52. Letunic I, Doerks T, Bork P. SMART: Recent updates, new developments and status in 2015. Nucleic Acids Res. 2015;43:D257-60.
53. Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S, Lopez R, et al. The InterPro protein families database: The classification resource after 15 years. Nucleic Acids Res. 2015;43:D213-21.
54. Dosztanyi Z, Csizmok V, Tompa P, Simon I. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics. 2005;21:3433-4.
55. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, et al. The protein data bank. Nucleic Acids Res. 2000;28:235-42.
56. Ruepp A, Waegele B, Lechner M, Brauner B, Dunger-Kaltenbach I, Fobo G, et al. CORUM: The comprehensive resource of mammalian protein complexes - 2009. Nucleic Acids Res. 2010;38:D497-501.
57. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, et al. STRING v9.1: Protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 2013;41:D808-15.
58. Ponten F, Jirstrom K, Uhlen M. The human protein atlas - A tool for pathology. J Pathol. 2008;216:387-93.
59. Yu CS, Cheng CW, Su WC, Chang KC, Huang SW, Hwang JK, et al. CELLO2GO: A web server for protein subCELlular LOcalization prediction with functional gene ontology annotation. PLoS ONE. 2014;9:e99368.
60. Bjorling E, Uhlen M. Antibodypedia, a portal for sharing antibody and antigen validation data. Mol Cell Proteomics. 2008;7:2028-37.
61. Genomes Pages - Eukaryota. http://www.ebi.ac.uk/genomes/eukaryota.html. Accessed 4 November 2015.
62. Nagy A, Patthy L. MisPred: A resource for identification of erroneous protein sequences in public databases. Database. 2013;2013:bat053.
63. Chica C, Labarga A, Gould CM, Lopez R, Gibson TJ. A tree-based conservation scoring method for short linear motifs in multiple alignments of protein sequences. BMC Bioinformatics. 2008;9:229.
64. Do CB, Katoh K. Protein multiple sequence alignment. Methods Mol Biol. 2008;484:379-413.
65. Weatheritt RJ, Gibson TJ. Linear motifs: lost in (pre)translation. Trends Biochem Sci. 2012;37:333-41.
66. Buljan M, Chalancon G, Eustermann S, Wagner GP, Fuxreiter M, Bateman A, et al. Tissue-specific splicing of disordered segments that embed binding motifs rewires protein interaction networks. Mol Cell. 2012;46:871-83.
67. Ellis JD, Barrios-Rodiles M, Colak R, Irimia M, Kim T, Calarco JA, et al. Tissue-specific alternative splicing remodels protein-protein interaction networks. Mol Cell. 2012;46:884-92.
68. Rubin SM, Gall AL, Zheng N, Pavletich NP. Structure of the Rb C-terminal domain bound to E2F1-DP1: A mechanism for phosphorylation-induced E2F release. Cell. 2005;123:1093-106.
69. Dias J, Van Nguyen N, Georgiev P, Gaub A, Brettschneider J, Cusack S, et al. Structural analysis of the KANSL1/WDR5/KANSL2 complex reveals that WDR5 is required for efficient assembly and chromatin targeting of the NSL complex. Genes Dev. 2014;28:929-42.
70. Schuch B, Feigenbutz M, Makino DL, Falk S, Basquin C, Mitchell P, et al. The exosome-binding factors Rrp6 and Rrp47 form a composite surface for recruiting the Mtr4 helicase. EMBO J. 2014;33:2829-46.
71. Davey NE, Haslam NJ, Shields DC, Edwards RJ. SLiMSearch 2.0: Biological context for short linear motifs in proteins. Nucleic Acids Res. 2011;39:W56-60.
72. Loewen CJ, Roy A, Levine TP. A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 2003;22:2025-35.
73. Herzog F, Kahraman A, Boehringer D, Mak R, Bracher A, Walzthoeni T, et al. Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science. 2012;337:1348-52.
74. Liu F, Rijkers DT, Post H, Heck AJ. Proteome-wide profiling of protein assemblies by cross-linking mass spectrometry. Nat Methods. 2015. doi: 10.1038/nmeth.3603.
75. Combe CW, Fischer L, Rappsilber J. xiNET: cross-link network maps with residue resolution. Mol Cell Proteomics. 2015;14:1137-47.
76. Roux KJ, Kim DI, Raida M, Burke B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol. 2012;196:801-10.
77. Coyaud E, Mis M, Laurent EM, Dunham WH, Couzens AL, Robitaille M, et al. BioID-based Identification of Skp Cullin F-box (SCF)beta-TrCP1/2 E3 Ligase Substrates. Mol Cell Proteomics. 2015;14:1781-95.
78. Kerrien S, Orchard S, Montecchi-Palazzi L, Aranda B, Quinn AF, Vinod N, et al. Broadening the horizon - level 2.5 of the HUPO-PSI format for molecular interactions. BMC Biol. 2007;5:44.
79. Cho S, Velikovsky CA, Swaminathan CP, Houtman JC, Samelson LE, Mariuzza RA. Structural basis for differential recognition of tyrosine-phosphorylated sites in the linker for activation of T cells (LAT) by the adaptor Gads. EMBO J. 2004;23:1441-51.
80. Dimasi N. Crystal structure of the C-terminal SH3 domain of the adaptor protein GADS in complex with SLP-76 motif peptide reveals a unique SH3-SH3 interaction. Int J Biochem Cell Biol. 2007;39:109-23.
81. Deng L, Velikovsky CA, Swaminathan CP, Cho S, Mariuzza RA. Structural basis for recognition of the T cell adaptor protein SLP-76 by the SH3 domain of phospholipase Cgamma1. J Mol Biol. 2005;352:1-10.
82. Pletneva EV, Sundd M, Fulton DB, Andreotti AH. Molecular details of Itk activation by prolyl isomerization and phospholigand binding: The NMR structure of the Itk SH2 domain bound to a phosphopeptide. J Mol Biol. 2006;357:550-61.
83. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: Back to metabolism in KEGG. Nucleic Acids Res. 2014;42:D199-205.
84. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498-504.
85. Nishida K, Ono K, Kanaya S, Takahashi K. KEGGscape: A Cytoscape app for pathway data integration. F1000Res. 2014;3:144.
86. Dinkel H, Chica C, Via A, Gould CM, Jensen LJ, Gibson TJ, et al. Phospho.ELM: A database of phosphorylation sites - update 2011. Nucleic Acids Res. 2011;39:D261-7.
87. Linding R, Russell RB, Neduva V, Gibson TJ. GlobPlot: Exploring protein sequences for globularity and disorder. Nucleic Acids Res. 2003;31:3701-8.
88. Rajasekaran S, Balla S, Gradie P, Gryk MR, Kadaveru K, Kundeti V, et al. Minimotif miner 2nd release: A database and web system for motif search. Nucleic Acids Res. 2009;37:D185-90.
89. Obenauer JC, Cantley LC, Yaffe MB. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 2003;31:3635-41.
90. Trabuco LG, Lise S, Petsalaki E, Russell RB. PepSite: Prediction of peptide-binding sites from protein surfaces. Nucleic Acids Res. 2012;40:W423-7.
91. Davey NE, Haslam NJ, Shields DC, Edwards RJ. SLiMFinder: A web server to find novel, significantly over-represented, short protein motifs. Nucleic Acids Res. 2010;38:W534-9.
92. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10.
93. Smedley D, Haider S, Durinck S, Pandini L, Provero P, Allen J, et al. The BioMart community portal: An innovative alternative to large, centralized data repositories. Nucleic Acids Res. 2015;43:W589-98.
94. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, et al. Analysis Tool Web Services from the EMBL-EBI. Nucleic Acids Res. 2013;41:W597-600.
95. Katoh K, Standley DM. MAFFT: Iterative refinement and additional methods. Methods Mol Biol. 2014;1079:131-46.
96. Schreiber F, Patricio M, Muffato M, Pignatelli M, Bateman A. TreeFam v9: A new website, more species and orthology-on-the-fly. Nucleic Acids Res. 2014;42:D922-5.
97. Powell S, Forslund K, Szklarczyk D, Trachana K, Roth A, Huerta-Cepas J, et al. eggNOG v4.0: Nested orthology inference across 3686 organisms. Nucleic Acids Res. 2014;42:D231-9.
98. Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science. 1997;278:631-7.
99. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 2010;38:W529-33.
100. Laskowski RA. PDBsum: summaries and analyses of PDB structures. Nucleic Acids Res. 2001;29:221-2.
101. Oates ME, Romero P, Ishida T, Ghalwash M, Mizianty MJ, Xue B, et al. D(2)P(2): Database of disordered protein predictions. Nucleic Acids Res. 2013;41:D508-16.
102. Potenza E, Di Domenico T, Walsh I, Tosatto SC. MobiDB 2.0: An improved database of intrinsically disordered and mobile proteins. Nucleic Acids Res. 2015;43:D315-20.
103. Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS, Tantos A, et al. DisProt: The Database of Disordered Proteins. Nucleic Acids Res. 2007;35:D786-93.
104. Chatr-Aryamontri A, Breitkreutz BJ, Oughtred R, Boucher L, Heinicke S, Chen D, et al. The BioGRID interaction database: 2015 update. Nucleic Acids Res. 2015;43:D470-8.
105. Orchard S, Ammari M, Aranda B, Breuza L, Briganti L, Broackes-Carter F, et al. The MIntAct project - IntAct as a common curation platform for 11 molecular interaction databases. Nucleic Acids Res. 2014;42:D358-63.
106. Higurashi M, Ishida T, Kinoshita K. PiSite: A database of protein interaction sites using multiple binding states in the PDB. Nucleic Acids Res. 2009;37:D360-4.
107. Ceol A, Chatr-aryamontri A, Santonico E, Sacco R, Castagnoli L, Cesareni G. DOMINO: A database of domain-peptide interactions. Nucleic Acids Res. 2007;35:D557-60.
108. Veres DV, Gyurko DM, Thaler B, Szalay KZ, Fazekas D, Korcsmaros T, et al. ComPPI: A cellular compartment-specific database for protein-protein interaction network analysis. Nucleic Acids Res. 2015;43:D485-93.
109. Weatheritt RJ, Jehl P, Dinkel H, Gibson TJ. iELM - A web server to explore short linear motif-mediated interactions. Nucleic Acids Res. 2012;40:W364-9.
110. Tanabe M, Kanehisa M. Using the KEGG database resource. Curr Protoc Bioinformatics. 2012. doi: 10.1002/0471250953.bi0112s38.
111. Rastogi S, Rost B. LocDB: Experimental annotations of localization for Homo sapiens and Arabidopsis thaliana. Nucleic Acids Res. 2011;39:D230-4.
112. Gene-Ontology-Consortium. The Gene Ontology project in 2008. Nucleic Acids Res. 2008;36:D440-4.
113. Binder JX, Pletscher-Frankild S, Tsafou K, Stolte C, O'Donoghue SI, Schneider R, et al. COMPARTMENTS: unification and visualization of protein subcellular localization evidence. Database. 2014;2014:bau012.
114. Sprenger J, Lynn Fink J, Karunaratne S, Hanson K, Hamilton NA, Teasdale RD. LOCATE: A mammalian protein subcellular localization database. Nucleic Acids Res. 2008;36:D230-3.
115. Santos A, Tsafou K, Stolte C, Pletscher-Frankild S, O'Donoghue SI, Jensen LJ. Comprehensive comparison of large-scale tissue expression datasets. PeerJ. 2015;3:e1054.
116. UniProt-Consortium. UniProt: A hub for protein information. Nucleic Acids Res. 2015;43:D204-12.
117. Alm T, von Feilitzen K, Lundberg E, Sivertsson A, Uhlen M. A chromosome-centric analysis of antibodies directed toward the human proteome using Antibodypedia. J Proteome Res. 2014;13:1669-76.
118. IUPAC publications. http://www.iupac.org/home/publications.html. Accessed 4 November 2015.