Human proteins with target sites of multiple post-translational modification types are more prone to be involved in disease

Journal of Proteome Research

Volumn 13, Issue 6, 2014, Pages 2735-2748

  Huang, Qianli ^a   Chang, Jinhui ^a   Cheung, Man Kit ^a   Nong, Wenyan ^a   Li, Lei ^a   Lee, Ming Tsung ^a   Kwan, Hoi Shan ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

disease development; intrinsically disordered region; post translational modification; protein protein interaction; topological coefficient

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN; PROTEIN; PROTEIN BINDING; PROTEOME;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELLULAR DISTRIBUTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CORRELATION ANALYSIS; DNA PROTEIN COMPLEX; HUMAN; PATHOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; CHEMISTRY; DEGENERATIVE DISEASE; GENETIC PREDISPOSITION; GENETICS; METABOLISM; MOLECULAR GENETICS; NEOPLASM; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE;

GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR SEQUENCE ANNOTATION; NEOPLASMS; NEURODEGENERATIVE DISEASES; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEOME;

EID: 84902095889     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr401019d     Document Type: Article

References (129)

1. Choudhary, C.; Mann, M. Decoding signalling networks by mass spectrometry-based proteomics Nat. Rev. Mol. Cell Biol. 2010, 11, 427-439
2. Mann, M.; Jensen, O. N. Proteomic analysis of post-translational modifications Nat. Biotechnol. 2003, 21, 255-261
3. Tan, M.; Luo, H.; Lee, S.; Jin, F.; Yang, J. S.; Montellier, E.; Buchou, T.; Cheng, Z.; Rousseaux, S.; Rajagopal, N. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification Cell 2011, 146, 1016-1028
4. Young, N. L.; Plazas-Mayorca, M. D.; Garcia, B. A. Systems-wide proteomic characterization of combinatorial post-translational modification patterns Expert Rev. Proteomics 2010, 7, 79-92
5. Strahl, B. D.; Allis, C. D. The language of covalent histone modifications Nature 2000, 403, 41-45
6. Jenuwein, T.; Allis, C. D. Translating the histone code Science 2001, 293, 1074-1080
7. Rando, O. J. Combinatorial complexity in chromatin structure and function: revisiting the histone code Curr. Opin. Genet. Dev. 2012, 22, 148-155
8. Young, N. L.; Dimaggio, P. A.; Garcia, B. A. The significance, development and progress of high-throughput combinatorial histone code analysis Cell. Mol. Life Sci. 2010, 67, 3983-4000
9. Ruthenburg, A. J.; Li, H.; Milne, T. A.; Dewell, S.; McGinty, R. K.; Yuen, M.; Ueberheide, B.; Dou, Y.; Muir, T. W.; Patel, D. J. Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions Cell 2011, 145, 692-706
10. Benayoun, B. A.; Veitia, R. A. A post-translational modification code for transcription factors: sorting through a sea of signals Trends Cell Biol. 2009, 19, 189-197
11. Kowenz-Leutz, E.; Pless, O.; Dittmar, G.; Knoblich, M.; Leutz, A. Crosstalk between C/EBPbeta phosphorylation, arginine methylation, and SWI/SNF/Mediator implies an indexing transcription factor code EMBO J. 2010, 29, 1105-1115
12. Stark, G. R.; Wang, Y.; Lu, T. Lysine methylation of promoter-bound transcription factors and relevance to cancer Cell Res. 2011, 21, 375-380
13. Calnan, D. R.; Brunet, A. The FoxO code Oncogene 2008, 27, 2276-2288
14. Brenkman, A. B.; de Keizer, P. L.; van den Broek, N. J.; Jochemsen, A. G.; Burgering, B. M. Mdm2 induces mono-ubiquitination of FOXO4 PloS One 2008, 3, e2819
15. Esteve, P. O.; Chang, Y.; Samaranayake, M.; Upadhyay, A. K.; Horton, J. R.; Feehery, G. R.; Cheng, X.; Pradhan, S. A methylation and phosphorylation switch between an adjacent lysine and serine determines human DNMT1 stability Nat. Struct. Mol. Biol. 2011, 18, 42-48
16. Benkirane, M.; Sardet, C.; Coux, O. Lessons from interconnected ubiquitylation and acetylation of p53: think metastable networks Biochem. Soc. Trans. 2010, 38, 98-103
17. Ho, P. C.; Gupta, P.; Tsui, Y. C.; Ha, S. G.; Huq, M.; Wei, L. N. Modulation of lysine acetylation-stimulated repressive activity by Erk2-mediated phosphorylation of RIP140 in adipocyte differentiation Cell. Signalling 2008, 20, 1911-1919
18. Paolinelli, R.; Mendoza-Maldonado, R.; Cereseto, A.; Giacca, M. Acetylation by GCN5 regulates CDC6 phosphorylation in the S phase of the cell cycle Nat. Struct. Mol. Biol. 2009, 16, 412-420
19. Santonico, E.; Belleudi, F.; Panni, S.; Torrisi, M. R.; Cesareni, G.; Castagnoli, L. Multiple modification and protein interaction signals drive the Ring finger protein 11 (RNF11) E3 ligase to the endosomal compartment Oncogene 2010, 29, 5604-5618
20. Oldfield, C. J.; Meng, J.; Yang, J. Y.; Yang, M. Q.; Uversky, V. N.; Dunker, A. K. Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners BMC Genomics 2008, 9 (Suppl 1) S1
21. Dai, C.; Gu, W. p53 post-translational modification: deregulated in tumorigenesis Trends Mol. Med. 2010, 16, 528-536
22. Pennuto, M.; Palazzolo, I.; Poletti, A. Post-translational modifications of expanded polyglutamine proteins: impact on neurotoxicity Hum. Mol. Genet. 2009, 18, R40-R47
23. Karve, T. M.; Cheema, A. K. Small changes huge impact: the role of protein posttranslational modifications in cellular homeostasis and disease J. Amino Acids 2011, 2011, 207691
24. Wang, Y.; Lin, F.; Qin, Z. H. The role of post-translational modifications of huntingtin in the pathogenesis of Huntington's disease Neurosci. Bull. 2010, 26, 153-162
25. Liddy, K. A.; White, M. Y.; Cordwell, S. J. Functional decorations: post-translational modifications and heart disease delineated by targeted proteomics Genome Med. 2013, 5, 20
26. Martin, L.; Latypova, X.; Terro, F. Post-translational modifications of tau protein: implications for Alzheimer's disease Neurochem. Int. 2011, 58, 458-471
27. Fukushima, N.; Furuta, D.; Hidaka, Y.; Moriyama, R.; Tsujiuchi, T. Post-translational modifications of tubulin in the nervous system J. Neurochem. 2009, 109, 683-693
28. Kyrychenko, S.; Polakova, E.; Kang, C.; Pocsai, K.; Ullrich, N. D.; Niggli, E.; Shirokova, N. Hierarchical accumulation of RyR post-translational modifications drives disease progression in dystrophic cardiomyopathy Cardiovasc. Res. 2013, 97, 666-675
29. Pena-Altamira, L. E.; Polazzi, E.; Monti, B. Histone Post-translational Modifications in Huntington's and Parkinson's Diseases Curr. Pharm. Des. 2013, 19, 5085-5092
30. Anderson, J. P.; Walker, D. E.; Goldstein, J. M.; de Laat, R.; Banducci, K.; Caccavello, R. J.; Barbour, R.; Huang, J.; Kling, K.; Lee, M. Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease J. Biol. Chem. 2006, 281, 29739-29752
31. Goedert, M.; Spillantini, M. G.; Del Tredici, K.; Braak, H. 100 years of Lewy pathology Nat. Rev. Neurol. 2013, 9, 13-24
32. Zhao, J.; Xin, M.; Wang, T.; Zhang, Y.; Deng, X. Nicotine enhances the antiapoptotic function of Mcl-1 through phosphorylation Mol. Cancer Res. 2009, 7, 1954-1961
33. Liao, M.; Zhao, J.; Wang, T.; Duan, J.; Zhang, Y.; Deng, X. Role of bile salt in regulating Mcl-1 phosphorylation and chemoresistance in hepatocellular carcinoma cells Mol. Cancer 2011, 10, 44
34. Mattson, M. P. Acetylation unleashes protein demons of dementia Neuron 2010, 67, 900-902
35. Weaver, I. C. Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let's call the whole thing off Epigenetics 2007, 2, 22-28
36. Cho, H. S.; Shimazu, T.; Toyokawa, G.; Daigo, Y.; Maehara, Y.; Hayami, S.; Ito, A.; Masuda, K.; Ikawa, N.; Field, H. I. Enhanced HSP70 lysine methylation promotes proliferation of cancer cells through activation of Aurora kinase B Nat. Commun. 2012, 3, 1072
37. Zakrzewicz, D.; Zakrzewicz, A.; Preissner, K. T.; Markart, P.; Wygrecka, M. Protein Arginine Methyltransferases (PRMTs): Promising Targets for the Treatment of Pulmonary Disorders Int. J. Mol. Sci. 2012, 13, 12383-12400
38. Chen, F.; Fulton, D. J. An inhibitor of protein arginine methyltransferases, 7,7′-carbonylbis(azanediyl)bis(4-hydroxynaphthalene-2- sulfonic acid (AMI-1), is a potent scavenger of NADPH-oxidase-derived superoxide Mol. Pharm. 2010, 77, 280-287
39. Khoury, G. A.; Baliban, R. C.; Floudas, C. A. Proteome-wide post-translational modification statistics: frequency analysis and curation of the swiss-prot database Sci. Rep. 2011, 1, 90
40. Stenson, P. D.; Ball, E. V.; Mort, M.; Phillips, A. D.; Shaw, K.; Cooper, D. N. The Human Gene Mutation Database (HGMD) and Its Exploitation in the Fields of Personalized Genomics and Molecular Evolution. In Current Protocols in Bioinformatics, 2012; Chapter 1, Unit 13.
41. Prieto, C.; De Las Rivas, J. APID: Agile Protein Interaction DataAnalyzer Nucleic Acids Res. 2006, 34, W298-W302
42. Schaefer, M. H.; Fontaine, J. F.; Vinayagam, A.; Porras, P.; Wanker, E. E.; Andrade-Navarro, M. A. HIPPIE: Integrating protein interaction networks with experiment based quality scores PloS One 2012, 7, e31826
43. Patil, A.; Nakai, K.; Nakamura, H. HitPredict: a database of quality assessed protein-protein interactions in nine species Nucleic Acids Res. 2011, 39, D744-D749
44. Martin, A.; Ochagavia, M. E.; Rabasa, L. C.; Miranda, J.; Fernandez-de-Cossio, J.; Bringas, R. BisoGenet: a new tool for gene network building, visualization and analysis BMC Bioinf. 2010, 11, 91
45. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N. S.; Wang, J. T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13, 2498-2504
46. Assenov, Y.; Ramirez, F.; Schelhorn, S. E.; Lengauer, T.; Albrecht, M. Computing topological parameters of biological networks Bioinformatics 2008, 24, 282-284
47. Lu, X.; Jain, V. V.; Finn, P. W.; Perkins, D. L. Hubs in biological interaction networks exhibit low changes in expression in experimental asthma Molecular Syst. Biol. 2007, 3, 98
48. Huang da, W.; Sherman, B. T.; Lempicki, R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res. 2009, 37, 1-13
49. Briesemeister, S.; Rahnenfuhrer, J.; Kohlbacher, O. YLoc - an interpretable web server for predicting subcellular localization Nucleic Acids Res. 2010, 38, W497-W502
50. Rastogi, S.; Rost, B. LocDB: experimental annotations of localization for Homo sapiens and Arabidopsis thaliana Nucleic Acids Res. 2011, 39, D230-D234
51. Zhang, T.; Faraggi, E.; Xue, B.; Dunker, A. K.; Uversky, V. N.; Zhou, Y. SPINE-D: accurate prediction of short and long disordered regions by a single neural-network based method J. Biomol. Struct. Dyn. 2012, 29, 799-813
52. Schymkowitz, J.; Borg, J.; Stricher, F.; Nys, R.; Rousseau, F.; Serrano, L. The FoldX web server: an online force field Nucleic Acids Res. 2005, 33, W382-W388
53. Tan, M. S.; Yu, J. T.; Jiang, T.; Zhu, X. C.; Tan, L. The NLRP3 Inflammasome in Alzheimer's Disease Mol. Neurobiol. 2013, 48, 875-882
54. Xiong, H.; Wang, D.; Chen, L.; Choo, Y. S.; Ma, H.; Tang, C.; Xia, K.; Jiang, W.; Ronai, Z.; Zhuang, X. Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation J. Clin. Invest. 2009, 119, 650-660
55. Zhao, J.; Lee, S. H.; Huss, M.; Holme, P. The network organization of cancer-associated protein complexes in human tissues Sci. Rep. 2013, 3, 1583
56. Ruepp, A.; Waegele, B.; Lechner, M.; Brauner, B.; Dunger-Kaltenbach, I.; Fobo, G.; Frishman, G.; Montrone, C.; Mewes, H. W. CORUM: the comprehensive resource of mammalian protein complexes - 2009 Nucleic Acids Res. 2010, 38, D497-D501
57. Huls, D.; Storchova, Z.; Niessing, D. Post-translational modifications regulate assembly of early spindle orientation complex in yeast J. Biol. Chem. 2012, 287, 16238-16245
58. Seet, B. T.; Dikic, I.; Zhou, M. M.; Pawson, T. Reading protein modifications with interaction domains Nat. Rev. Mol. Cell Biol. 2006, 7, 473-483
59. Szumiel, I.; Foray, N. Chromatin acetylation, beta-amyloid precursor protein and its binding partner FE65 in DNA double strand break repair Acta Biochim. Pol. 2011, 58, 11-18
60. Dodson, C. A.; Bayliss, R. Activation of Aurora-A kinase by protein partner binding and phosphorylation are independent and synergistic J. Biol. Chem. 2012, 287, 1150-1157
61. Lee, C. W.; Ferreon, J. C.; Ferreon, A. C.; Arai, M.; Wright, P. E. Graded enhancement of p53 binding to CREB-binding protein (CBP) by multisite phosphorylation Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 19290-19295
62. Batchelor, E.; Loewer, A.; Mock, C.; Lahav, G. Stimulus-dependent dynamics of p53 in single cells Molecular Syst. Biol. 2011, 7, 488
63. Meek, D. W.; Anderson, C. W. Posttranslational modification of p53: cooperative integrators of function Cold Spring Harbor Perspect. Biol. 2009, 1, a000950
64. He, X.; Zhang, J. Why do hubs tend to be essential in protein networks? PLoS Genet. 2006, 2, e88
65. Sengupta, U.; Ukil, S.; Dimitrova, N.; Agrawal, S. Expression-based network biology identifies alteration in key regulatory pathways of type 2 diabetes and associated risk/complications PloS One 2009, 4, e8100
66. Ravasz, E.; Somera, A. L.; Mongru, D. A.; Oltvai, Z. N.; Barabasi, A. L. Hierarchical organization of modularity in metabolic networks Science 2002, 297, 1551-1555
67. Ryan, C. M.; Souda, P.; Bassilian, S.; Ujwal, R.; Zhang, J.; Abramson, J.; Ping, P.; Durazo, A.; Bowie, J. U.; Hasan, S. S. Post-translational modifications of integral membrane proteins resolved by top-down Fourier transform mass spectrometry with collisionally activated dissociation Mol. Cell. Proteomics 2010, 9, 791-803
68. Statsuk, A. V.; Shokat, K. M. Covalent cross-linking of kinases with their corresponding peptide substrates Methods Mol. Biol. 2012, 795, 179-190
69. Janke, C.; Bulinski, J. C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions Nat. Rev. Mol. Cell Biol. 2011, 12, 773-786
70. Wang, Y. T.; Yang, W. B.; Chang, W. C.; Hung, J. J. Interplay of posttranslational modifications in Sp1 mediates Sp1 stability during cell cycle progression J. Mol. Biol. 2011, 414, 1-14
71. Goulah, C. C.; Read, L. K. Differential effects of arginine methylation on RBP16 mRNA binding, guide RNA (gRNA) binding, and gRNA-containing ribonucleoprotein complex (gRNP) formation J. Biol. Chem. 2007, 282, 7181-7190
72. Burke, J. R.; Hura, G. L.; Rubin, S. M. Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control Genes Dev. 2012, 26, 1156-1166
73. Wang, Z.; Zang, C.; Rosenfeld, J. A.; Schones, D. E.; Barski, A.; Cuddapah, S.; Cui, K.; Roh, T. Y.; Peng, W.; Zhang, M. Q. Combinatorial patterns of histone acetylations and methylations in the human genome Nat. Genet. 2008, 40, 897-903
74. Huang, G.; Zhang, M.; Erdman, S. E. Posttranslational modifications required for cell surface localization and function of the fungal adhesin Aga1p Eukaryotic Cell 2003, 2, 1099-1114
75. Nowotny, P.; Gorski, S. M.; Han, S. W.; Philips, K.; Ray, W. J.; Nowotny, V.; Jones, C. J.; Clark, R. F.; Cagan, R. L.; Goate, A. M. Posttranslational modification and plasma membrane localization of the Drosophila melanogaster presenilin Mol. Cell. Neurosci. 2000, 15, 88-98
76. Kfoury, Y.; Nasr, R.; Journo, C.; Mahieux, R.; Pique, C.; Bazarbachi, A. The multifaceted oncoprotein Tax: subcellular localization, posttranslational modifications, and NF-kappaB activation Adv. Cancer Res. 2012, 113, 85-120
77. Roth, J. Protein N-glycosylation along the secretory pathway: Relationship to organelle topography and function, protein quality control, and cell interactions Chem. Rev. 2002, 102, 285-303
78. Chevallet, M.; Diemer, H.; Van Dorssealer, A.; Villiers, C.; Rabilloud, T. Toward a better analysis of secreted proteins: the example of the myeloid cells secretome Proteomics 2007, 7, 1757-1770
79. Pham, M. D.; Yu, S. S. F.; Han, C. C.; Chan, S. I. Improved Mass Spectrometric Analysis of Membrane Proteins Based on Rapid and Versatile Sample Preparation on Nanodiamond Particles Anal. Chem. 2013, 85, 6748-6755
80. Regeer, R. R.; Nicke, A.; Markovich, D. Quaternary structure and apical membrane sorting of the mammalian NaSi-1 sulfate transporter in renal cell lines Int. J. Biochem. Cell Biol. 2007, 39, 2240-2251
81. Mangravite, L. M.; Giacomini, K. M. Sorting of rat SPNT in renal epithelium is independent of N-glycosylation Pharm. Res. 2003, 20, 319-323
82. Maga, J. A.; Zhou, J. H.; Kambampati, R.; Peng, S.; Wang, X.; Bohnsack, R. N.; Thomm, A.; Golata, S.; Tom, P.; Dahms, N. M. Glycosylation-independent Lysosomal Targeting of Acid alpha-Glucosidase Enhances Muscle Glycogen Clearance in Pompe Mice J. Biol. Chem. 2013, 288, 1428-1438
83. Sehat, B.; Tofigh, A.; Lin, Y.; Trocme, E.; Liljedahl, U.; Lagergren, J.; Larsson, O. SUMOylation mediates the nuclear translocation and signaling of the IGF-1 receptor Sci. Signaling 2010, 3, ra10
84. Liu, G.; Xirodimas, D. P. NUB1 promotes cytoplasmic localization of p53 through cooperation of the NEDD8 and ubiquitin pathways Oncogene 2010, 29, 2252-2261
85. Navarro, M. N.; Goebel, J.; Feijoo-Carnero, C.; Morrice, N.; Cantrell, D. A. Phosphoproteomic analysis reveals an intrinsic pathway for the regulation of histone deacetylase 7 that controls the function of cytotoxic T lymphocytes Nat. Immunol. 2011, 12, 352-361
86. Westermann, S.; Weber, K. Post-translational modifications regulate microtubule function. Nature reviews Mol. Cell Biol. 2003, 4, 938-947
87. Cai, Q.; Robertson, E. S. Ubiquitin/SUMO modification regulates VHL protein stability and nucleocytoplasmic localization PloS One 210, 5, e12636
88. Herrero, E.; Davis, S. J. Time for a nuclear meeting: protein trafficking and chromatin dynamics intersect in the plant circadian system Mol. Plant 2012, 5, 554-565
89. Kondratov, R. V.; Chernov, M. V.; Kondratova, A. A.; Gorbacheva, V. Y.; Gudkov, A. V.; Antoch, M. P. BMAL1-dependent circadian oscillation of nuclear CLOCK: posttranslational events induced by dimerization of transcriptional activators of the mammalian clock system Genes Dev. 2003, 17, 1921-1932
90. Getty, A.; Kovacs, A. D.; Lengyel-Nelson, T.; Cardillo, A.; Hof, C.; Chan, C. H.; Pearce, D. A. Osmotic stress changes the expression and subcellular localization of the Batten disease protein CLN3 PloS One 2013, 8, e66203
91. Rosnoblet, C.; Legrand, D.; Demaegd, D.; Hacine-Gherbi, H.; de Bettignies, G.; Bammens, R.; Borrego, C.; Duvet, S.; Morsomme, P.; Matthijs, G. Impact of disease-causing mutations on TMEM165 subcellular localization, a recently identified protein involved in CDG-II Hum. Mol. Genet. 2013, 22, 2914-2928
92. Park, S.; Yang, J. S.; Shin, Y. E.; Park, J.; Jang, S. K.; Kim, S. Protein localization as a principal feature of the etiology and comorbidity of genetic diseases Mol. Syst. Biol. 2011, 7, 494
93. Iakoucheva, L. M.; Radivojac, P.; Brown, C. J.; O'Connor, T. R.; Sikes, J. G.; Obradovic, Z.; Dunker, A. K. The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 2004, 32, 1037-1049
94. Gao, J.; Thelen, J. J.; Dunker, A. K.; Xu, D. Musite, a tool for global prediction of general and kinase-specific phosphorylation sites Mol. Cell. Proteomics 2010, 9, 2586-2600
95. Xie, H.; Vucetic, S.; Iakoucheva, L. M.; Oldfield, C. J.; Dunker, A. K.; Obradovic, Z.; Uversky, V. N. Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins J. Proteome Res. 2007, 6, 1917-1932
96. Radivojac, P.; Vacic, V.; Haynes, C.; Cocklin, R. R.; Mohan, A.; Heyen, J. W.; Goebl, M. G.; Iakoucheva, L. M. Identification, analysis, and prediction of protein ubiquitination sites Proteins 2010, 78, 365-380
97. Hagai, T.; Azia, A.; Toth-Petroczy, A.; Levy, Y. Intrinsic disorder in ubiquitination substrates J. Mol. Biol. 2011, 412, 319-324
98. Hansen, J. C.; Lu, X.; Ross, E. D.; Woody, R. W. Intrinsic protein disorder, amino acid composition, and histone terminal domains J. Biol. Chem. 2006, 281, 1853-1856
99. Hon, W. C.; Wilson, M. I.; Harlos, K.; Claridge, T. D.; Schofield, C. J.; Pugh, C. W.; Maxwell, P. H.; Ratcliffe, P. J.; Stuart, D. I.; Jones, E. Y. Structural basis for the recognition of hydroxyproline in HIF-1 alpha by pVHL Nature 2002, 417, 975-978
100. Pang, C. N.; Hayen, A.; Wilkins, M. R. Surface accessibility of protein post-translational modifications J. Proteome Res. 2007, 6, 1833-1845
101. Sanchez, I. E.; Beltrao, P.; Stricher, F.; Schymkowitz, J.; Ferkinghoff-Borg, J.; Rousseau, F.; Serrano, L. Genome-wide prediction of SH2 domain targets using structural information and the FoldX algorithm PLoS Comput. Biol. 2008, 4, e1000052
102. Nishi, H.; Hashimoto, K.; Panchenko, A. R. Phosphorylation in protein-protein binding: effect on stability and function Structure 2011, 19, 1807-1815
103. Rose, P. W.; Bi, C.; Bluhm, W. F.; Christie, C. H.; Dimitropoulos, D.; Dutta, S.; Green, R. K.; Goodsell, D. S.; Prlic, A.; Quesada, M. The RCSB Protein Data Bank: new resources for research and education Nucleic Acids Res. 2013, 41, D475-D482
104. Yang, X. J. Multisite protein modification and intramolecular signaling Oncogene 2005, 24, 1653-1662
105. Bogan, A. A.; Thorn, K. S. Anatomy of hot spots in protein interfaces J. Mol. Biol. 1998, 280, 1-9
106. Tuncbag, N.; Gursoy, A.; Keskin, O. Identification of computational hot spots in protein interfaces: combining solvent accessibility and inter-residue potentials improves the accuracy Bioinformatics 2009, 25, 1513-1520
107. Brock, K.; Talley, K.; Coley, K.; Kundrotas, P.; Alexov, E. Optimization of electrostatic interactions in protein-protein complexes Biophys. J. 2007, 93, 3340-3352
108. Chakrabortee, S.; Meersman, F.; Kaminski Schierle, G. S.; Bertoncini, C. W.; McGee, B.; Kaminski, C. F.; Tunnacliffe, A. Catalytic and chaperone-like functions in an intrinsically disordered protein associated with desiccation tolerance Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 16084-16089
109. Shoemaker, B. A.; Portman, J. J.; Wolynes, P. G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 8868-8873
110. Zhou, H. X. Intrinsic disorder: signaling via highly specific but short-lived association Trends Biochem. Sci. 2012, 37, 43-48
111. Kruse, J. P.; Gu, W. SnapShot: p53 posttranslational modifications Cell 2008, 133, 930-930.e1
112. Beltrao, P.; Albanese, V.; Kenner, L. R.; Swaney, D. L.; Burlingame, A.; Villen, J.; Lim, W. A.; Fraser, J. S.; Frydman, J.; Krogan, N. J. Systematic functional prioritization of protein posttranslational modifications Cell 2012, 150, 413-425
113. Landry, C. R.; Levy, E. D.; Michnick, S. W. Weak functional constraints on phosphoproteomes Trends Genet. 2009, 25, 193-197
114. Lienhard, G. E. Non-functional phosphorylations? Trends Biochem. Sci. 2008, 33, 351-352
115. Martin, A. M.; Pouchnik, D. J.; Walker, J. L.; Wyrick, J. J. Redundant roles for histone H3 N-terminal lysine residues in subtelomeric gene repression in Saccharomyces cerevisiae Genetics 2004, 167, 1123-1132
116. Kornblihtt, A. R.; Schor, I. E.; Allo, M.; Dujardin, G.; Petrillo, E.; Munoz, M. J. Alternative splicing: a pivotal step between eukaryotic transcription and translation Nat. Rev. Mol. Cell Biol. 2013, 14, 153
117. Wang, E. T.; Sandberg, R.; Luo, S. J.; Khrebtukova, I.; Zhang, L.; Mayr, C.; Kingsmore, S. F.; Schroth, G. P.; Burge, C. B. Alternative isoform regulation in human tissue transcriptomes Nature 2008, 456, 470-476
118. Menon, R.; Im, H.; Zhang, E. Y.; Wu, S. L.; Chen, R.; Snyder, M.; Hancock, W. S.; Omenn, G. S. Distinct splice variants and pathway enrichment in the cell-line models of aggressive human breast cancer subtypes J. Proteome Res. 2014, 13, 212-227
119. Menon, R.; Omenn, G. S. Proteomic Characterization of Novel Alternative Splice Variant Proteins in Human Epidermal Growth Factor Receptor 2/neu-Induced Breast Cancers Cancer Res. 2010, 70, 3440-3449
120. Ellis, J. D.; Barrios-Rodiles, M.; Colak, R.; Irimia, M.; Kim, T.; Calarco, J. A.; Wang, X. C.; Pan, Q.; O'Hanlon, D.; Kim, P. M. Tissue-Specific Alternative Splicing Remodels Protein-Protein Interaction Networks Mol. Cell 2012, 46, 884-892
121. Buljan, M.; Chalancon, G.; Eustermann, S.; Wagner, G. P.; Fuxreiter, M.; Bateman, A.; Babu, M. M. Tissue-Specific Splicing of Disordered Segments that Embed Binding Motifs Rewires Protein Interaction Networks Mol. Cell 2012, 46, 871-883
122. Eksi, R.; Li, H. D.; Menon, R.; Wen, Y.; Omenn, G. S.; Kretzler, M.; Guan, Y. Systematically differentiating functions for alternatively spliced isoforms through integrating RNA-seq data PLoS Comput. Biol. 2013, 9, e1003314
123. Omenn, G. S.; Menon, R.; Zhang, Y. Innovations in proteomic profiling of cancers: alternative splice variants as a new class of cancer biomarker candidates and bridging of proteomics with structural biology J. Proteomics 2013, 90, 28-37
124. Menon, R.; Roy, A.; Mukherjee, S.; Belkin, S.; Zhang, Y.; Omenn, G. S. Functional implications of structural predictions for alternative splice proteins expressed in Her2/neu-induced breast cancers J. Proteome Res. 2011, 10, 5503-5511
125. Carroll, J.; Altman, M. C.; Fearnley, I. M.; Walker, J. E. Identification of membrane proteins by tandem mass spectrometry of protein ions Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 14330-14335
126. Arachea, B. T.; Sun, Z.; Potente, N.; Malik, R.; Isailovic, D.; Viola, R. E. Detergent selection for enhanced extraction of membrane proteins Protein Expression Purif. 2012, 86, 12-20
127. Mirza, S. P.; Halligan, B. D.; Greene, A. S.; Olivier, M. Improved method for the analysis of membrane proteins by mass spectrometry Physiol. Genomics 2007, 30, 89-94
128. Schwanhausser, B.; Busse, D.; Li, N.; Dittmar, G.; Schuchhardt, J.; Wolf, J.; Chen, W.; Selbach, M. Global quantification of mammalian gene expression control Nature 2011, 473, 337-342
129. Chammas, R.; Sonnenburg, J. L.; Watson, N. E.; Tai, T.; Farquhar, M. G.; Varki, N. M.; Varki, A. De-N-acetyl-gangliosides in humans: unusual subcellular distribution of a novel tumor antigen Cancer Res. 1999, 59, 1337-1346