The structural and functional signatures of proteins that undergo multiple events of post-translational modification

Protein Science

Volumn 23, Issue 8, 2014, Pages 1077-1093

  Pejaver, Vikas ^a   Hsu, Wei Lun ^b   Xin, Fuxiao ^a,c   Dunker, A Keith ^b   Uversky, Vladimir N ^d,e   Radivojac, Predrag ^a  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GE GLOBAL RESEARCH   (United States)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

Crosstalk; Intrinsically disordered protein; Molecular recognition feature; MoRF; Post translational modification; Prediction; Protein; Protein interaction; Steric competition

Indexed keywords

PROTEIN;

CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; PROTEIN PROCESSING;

MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS;

EID: 84906854634     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2494     Document Type: Article

References (93)

1. Walsh C (2006) Posttranslational modification of proteins: expanding nature's inventory. Roberts and Company Publishers: Greenwood Village.
2. Deribe YL, Pawson T, Dikic I (2010) Post-translational modifications in signal integration. Nat Struct Mol Biol 17:666-672.
3. Nussinov R, Tsai C-J, Xin F, Radivojac P (2012) Allosteric post-translational modification codes. Trends Biochem Sci 37:447-455.
4. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41-45.
5. Yang X-J (2005) Multisite protein modification and intramolecular signaling. Oncogene 24:1653-1662.
6. Sims RJ III, Reinberg D (2008) Is there a code embedded in proteins that is based on post-translational modifications? Nat Rev Mol Cell Biol 9:815-820.
7. Benayoun BA, Veitia RA (2009) A post-translational modification code for transcription factors: sorting through a sea of signals. Trends Cell Biol 19:189-197.
8. Lothrop AP, Torres MP, Fuchs SM (2013) Deciphering post-translational modification codes. FEBS Lett 587: 1247-1257.
9. Heldin C-H, Westermark B (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79:1283-1316.
10. Gamble MJ, Freedman LP (2002) A coactivator code for transcription. Trends Biochem Sci 27:165-167.
11. Xu Y-X, Hirose Y, Zhou XZ, Lu KP, Manley JL (2003) Pin1 modulates the structure and function of human RNA polymerase II. Genes Dev 17:2765-2776.
12. Westermann S, Weber K (2003) Post-translational modifications regulate microtubule function. Nat Rev Mol Cell Biol 4:938-948.
13. Hutchins JR, Clarke PR (2004) Many fingers on the mitotic trigger: post-translational regulation of the Cdc25C phosphatase. Cell Cycle 3:41-45.
14. Calnan D, Brunet A (2008) The FoxO code. Oncogene 27:2276-2288.
15. Meek DW, Anderson CW (2009) Posttranslational modification of p53: cooperative integrators of function. Cold Spring Harb Perspect Biol 1. doi:10.1101/cshperspect.a000950.
16. Wang Z, Gucek M, Hart GW (2008) Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proc Natl Acad Sci USA 105:13793-13798.
17. van Noort, V, Seebacher J, Bader S, Mohammed S, Vonkova I, Betts MJ, Kühner S, Kumar R, Maier T, O'Flaherty M, Rybin V, Schmeisky A, Yus E, Stulke J, Serrano L, Russell RB, Heck AJR, Bork P, Gavin AC (2012) Cross-talk between phosphorylation and lysine acetylation in a genome-reduced bacterium. Mol Syst Biol 8:571.
18. Danielsen JM, Sylvestersen KB, Bekker-Jensen S, Szklarczyk D, Poulsen JW, Horn H, Jensen LJ, Mailand N, Nielsen ML (2011) Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol Cell Proteomics 10:M110.003590.
19. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, Mann M, Choudhary C (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10: M111.013284.
20. Swaney DL, Beltrao P, Starita L, Guo A, Rush J, Fields S, Krogan NJ, Villen J (2013) Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat Methods 10:676-682.
21. Pang CNI, Hayen A, Wilkins MR (2007) Surface accessibility of protein post-translational modifications. J Proteome Res 6:1833-1845.
22. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 3. Ligands, posttranslational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 6:1917-1932.
23. Gao J, Xu D (2012) Correlation between posttranslational modification and intrinsic disorder in protein. Pac Symp Biocomput 17:94-103.
24. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834-840.
25. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23:607-618.
26. Petrescu A-J, Milac A-L, Petrescu SM, Dwek RA, Wormald MR (2004) Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology 14:103-114.
27. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z (2001) Intrinsically disordered protein. J Mol Graph Model 19:26-59.
28. Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK (2007) Intrinsic disorder and functional proteomics. Biophys J 92:1439-1456.
29. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32:1037-1049.
30. Gsponer J, Futschik ME, Teichmann SA, Babu MM (2008) Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322:1365-1368.
31. Daily KM, Radivojac P, Dunker AK (2005) Intrinsic disorder and protein modifications: building an SVM predictor for methylation. In: IEEE Symp Comp Int in Bioinfo Comp Biol, CIBCB'05. IEEE, La Jolla, California, pp 475-481.
32. Radivojac P, Vacic V, Haynes C, Cocklin RR, Mohan A, Heyen JW, Goebl MG, Iakoucheva LM (2010) Identification, analysis, and prediction of protein ubiquitination sites. Proteins 78:365-380.
33. Johnson LN, Lewis RJ (2001) Structural basis for control by phosphorylation. Chem Rev 101:2209-2242.
34. Xin F, Radivojac P (2012) Post-translational modifications induce significant yet not extreme changes to protein structure. Bioinformatics 28:2905-2913.
35. Ma B, Nussinov R (2009) Regulating highly dynamic unstructured proteins and their coding mRNAs. Genome Biol 10:204.
36. Nishi H, Hashimoto K, Panchenko AR (2011) Phosphorylation in protein-protein binding: effect on stability and function. Structure 19:1807-1815.
37. Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362: 1043-1059.
38. Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, Uversky VN, Dunker AK (2007) Characterization of molecular recognition features, MoRFs, and their binding partners. J Proteome Res 6:2351-2366.
39. Hsu WL, Oldfield CJ, Xue B, Meng J, Huang F, Romero P, Uversky VN, Dunker AK (2013) Exploring the binding diversity of intrinsically disordered proteins involved in one-to-many binding. Protein Sci 22: 258-273.
40. Beltrao P, Albanese V, Kenner LR, Swaney DL, Burlingame A, Villen J, Lim WA, Fraser JS, Frydman J, Krogan NJ (2012) Systematic functional prioritization of protein posttranslational modifications. Cell 150:413-425.
41. Minguez P, Parca L, Diella F, Mende DR, Kumar R, Helmer-Citterich M, Gavin A-C, van Noort, V, Bork P (2012) Deciphering a global network of functionally associated post-translational modifications. Mol Syst Biol 8:599.
42. Woodsmith J, Kamburov A, Stelzl U (2013) Dual coordination of post translational modifications in human protein networks. PLoS Comput Biol 9:e1002933.
43. Peng M, Scholten A, Heck AJ, van Breukelen B (2014) Identification of enriched PTM crosstalk motifs from large-scale experimental data sets. J Proteome Res 13: 249-259.
44. Olsen JV, Mann M (2013) Status of large-scale analysis of post-translational modifications by mass spectrometry. Mol Cell Proteomics 12:3444-3452.
45. Eisenhaber B, Eisenhaber F (2010) Prediction of posttranslational modification of proteins from their amino acid sequence. Methods Mol Biol 609:365-384.
46. Xue Y, Liu Z, Cao J, Ren J, Computational prediction of post-translational modification sites in proteins. In: Yang N-S, Ed. (2011) Systems and computational biology: molecular and cellular experimental systems. InTech, pp 105-124.
47. Zhou F, Xue Y, Yao X, Xu Y (2006) A general user interface for prediction servers of proteins' post-translational modification sites. Nat Protoc 1:1318-1321.
48. Gao J, Thelen JJ, Dunker AK, Xu D (2010) Musite, a tool for global prediction of general and kinase-specific phosphorylation sites. Mol Cell Proteomics 9:2586-2600.
49. Costello J, Stolovitzky G (2013) Seeking the wisdom of crowds through challenge-based competitions in biomedical research. Clin Pharmacol Ther 93:396-398.
50. Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS, Tantos A, Szabo B, Tompa P, Chen J, Uversky VN, Obradovic Z, Dunker AK (2007) DisProt: The database of disordered proteins. Nucleic Acids Res 35:D786-D793.
51. Peng K, Radivojac P, Vucetic S, Dunker AK, Obradovic Z (2006) Length-dependent prediction of protein intrinsic disorder. BMC Bioinformatics 7:208.
52. The UniProt Consortium (2013) Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res 41:D43-D47.
53. Fisher RA (1922) On the interpretation of v2 from contingency tables, and the calculation of P. J R Stat Soc 85:87-94.
54. Liu J, Perumal NB, Oldfield CJ, Su EW, Uversky VN, Dunker AK (2006) Intrinsic disorder in transcription factors. Biochemistry 45:6873-6888.
55. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Uversky VN, Obradovic Z (2007) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 6:1882-1898.
56. Korneta I, Bujnicki JM (2012) Intrinsic disorder in the human spliceosomal proteome. PLoS Comput Biol 8: e1002641.
57. Romero PR, Zaidi S, Fang YY, Uversky VN, Radivojac P, Oldfield CJ, Cortese MS, Sickmeier M, LeGall T, Obradovic Z, Dunker AK (2006) Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc Natl Acad Sci USA 103:8390-8395.
58. Hirschey MD, Shimazu T, Huang JY, Verdin E (2009) Acetylation of mitochondrial proteins. Methods Enzymol 457:137-147.
59. Neutzner A, Benard G, Youle RJ, Karbowski M (2008) Role of the ubiquitin conjugation system in the maintenance of mitochondrial homeostasis. Ann N Y Acad Sci 1147:242-253.
60. Dinkel H, Chica C, Via A, Gould CM, Jensen LJ, Gibson TJ, Diella F (2011) Phospho.ELM: A database of phosphorylation sites-update 2011. Nucleic Acids Res 39:D261-D267.
61. Taverna SD, Ueberheide BM, Liu Y, Tackett AJ, Diaz RL, Shabanowitz J, Chait BT, Hunt DF, Allis CD (2007) Long-distance combinatorial linkage between methylation and acetylation on histone H3 N termini. Proc Natl Acad Sci USA 104:2086-2091.
62. Querfurth C, Diernfellner AC, Gin E, Malzahn E, Höfer T, Brunner M (2011) Circadian conformational change of the Neurospora clock protein FREQUENCY triggered by clustered hyperphosphorylation of a basic domain. Mol Cell 43:713-722.
63. Diella F, Haslam N, Chica C, Budd A, Michael S, Brown NP, Trave G, Gibson TJ (2008) Understanding eukaryotic linear motifs and their role in cell signaling and regulation. Front Biosci 13:6580-6603.
64. Davey NE, Edwards RJ, Shields DC (2010) Computational identification and analysis of protein short linear motifs. Front Biosci 15:801-825.
65. Uversky VN, Dunker AK (2010) Understanding protein non-folding. Biochim Biophys Acta 1804:1231- 1264.
66. Prabakaran S, Lippens G, Steen H, Gunawardena J (2012) Post-translational modification: nature's escape from genetic imprisonment and the basis for dynamic information encoding. Wiley Interdiscip Rev Syst Biol and Med 4:565-583.
67. Huang Q, Chang J, Cheung MK, Nong W, Li L, Lee Mt, Kwan HS (in press) Human proteins with target sites of multiple post-translational modification types are more prone to be involved in disease. J Proteome Res doi:10.1021/pr401019d.
68. Li W, Godzik A (2006) Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658-1659.
69. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat T, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235-242.
70. Prasad TK, Goel R, Kandasamy K, Keerthikumar S, Kumar S, Mathivanan S, Telikicherla D, Raju R, Shafreen B, Venugopal A, Balakrishnan L, Marimuthu A, Banerjee S, Somanathan DS, Sebastian A, Rani S, Ray S, Kishore CJH, Kanth S, Ahmed M, Kashyap MK, Mohmood R, Ramachandra YL, Krishna V, Rahiman BA, Mohan S, Ranganathan P, Ramabadran S, Chaerkady R, Pandey A (2009) Human protein reference database-2009 update. Nucleic Acids Res 37: D767-D772.
71. Gnad F, Gunawardena J, Mann M (2011) PHOSIDA 2011: The posttranslational modification database. Nucleic Acids Res 39:D253-D260.
72. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, Latham V, Sullivan M (2012) PhosphoSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40:D261-D270.
73. Daroczy Z (1970) Generalized information functions. Inform Control 16:36-51.
74. Uversky VN, Gillespie JR, Fink AL (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41:415-427.
75. Vucetic S, Brown CJ, Dunker AK, Obradovic Z (2003) Flavors of protein disorder. Proteins 52:573-584.
76. Vihinen M, Torkkila E, Riikonen P (1994) Accuracy of protein flexibility predictions. Proteins 19:141-149.
77. Eisenberg D, Weiss RM, Terwilliger TC (1984) The hydrophobic moment detects periodicity in protein hydrophobicity. Proc Natl Acad Sci USA 81:140-144.
78. Radivojac P, Obradovic Z, Smith DK, Zhu G, Vucetic S, Brown CJ, Lawson JD, Dunker AK (2004) Protein flexibility and intrinsic disorder. Protein Sci 13:71-80.
79. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389-3402.
80. Breiman L (1996) Bagging predictors. Mach Learn 24: 123-140.
81. Breiman L (2001) Random forests. Mach Learn 45: 5-32.
82. Vacic V, Iakoucheva LM, Radivojac P (2006) Two Sample Logo: A graphical representation of the differences between two sets of sequence alignments. Bioinformatics 22:1536-1537.
83. Sigrist CJ, De Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I (2013) New and continuing developments at PROSITE. Nucleic Acids Res 41:D344-D347.
84. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289-300.
85. Nie L, Sasaki M, Maki CG (2007) Regulation of p53 nuclear export through sequential changes in conformation and ubiquitination. J Biol Chem 282:14616-14625.
86. Saito Si, Yamaguchi H, Higashimoto Y, Chao C, Xu Y, Fornace AJ, Appella E, Anderson CW (2003) Phosphorylation site interdependence of human p53 posttranslational modifications in response to stress. J Biol Chem 278:37536-37544.
87. DeHart CJ, Chahal JS, Flint S, Perlman DH (2014) Extensive post-translational modification of active and inactivated forms of endogenous p53. Mol Cell Proteomics 13:1-17.
88. Kelley LA, Sutcliffe MJ (1997) OLDERADO: On-line database of ensemble representatives and domains. Protein Sci 6:2628-2630.
89. Zeng L, Zhang Q, Gerona-Navarro G, Moshkina N, Zhou M-M (2008) Structural basis of site-specific histone recognition by the bromodomains of human coactivators PCAF and CBP/p300. Structure 16:643-652.
90. Deng Z, Chen C-J, Chamberlin M, Lu F, Blobel GA, Speicher D, Cirillo LA, Zaret KS, Lieberman PM (2003) The CBP bromodomain and nucleosome targeting are required for Zta-directed nucleosome acetylation and transcription activation. Mol Cell Biol 23: 2633-2644.
91. Das C, Roy S, Namjoshi S, Malarkey CS, Jones DN, Kutateladze TG, Churchill ME, Tyler JK (2014) Binding of the histone chaperone ASF1 to the CBP bromodomain promotes histone acetylation. Proc Natl Acad Sci USA 111:E1072-E1081.
92. Chapman JR, Taylor MR, Boulton SJ (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47:497-510.
93. Zheng Y, Thomas PM, Kelleher NL (2013) Measurement of acetylation turnover at distinct lysines in human histones identifies long-lived acetylation sites. Nat Commun 4:2203.