Unraveling the ubiquitin-regulated signaling networks by mass spectrometry-based proteomics

Proteomics

Volumn 13, Issue 3-4, 2013, Pages 526-537

  Low, Teck Yew ^a,b   Magliozzi, Roberto ^c   Guardavaccaro, Daniele ^c   Heck, Albert J R ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Cell biology; Deubiquitylating; Diglycine; Post translational modification; Proteasome; Ubiquitin

Indexed keywords

LYSINE; PEPTIDE; POLYUBIQUITIN; PROTEASOME; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3;

BINDING AFFINITY; CONJUGATION; DNA REPAIR; GENETIC ENGINEERING; HUMAN; MASS SPECTROMETRY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; ENDOPEPTIDASES; HUMANS; MASS SPECTROMETRY; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATED PROTEINS; UBIQUITINATION;

EID: 84874001045     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201200244     Document Type: Review

References (107)

1. Hershko, A., Ciechanover, A., The ubiquitin system. Annu. Rev. Biochem. 1998, 67, 425-479.
2. Haglund, K., Dikic, I., Ubiquitylation and cell signaling. EMBO J. 2005, 24, 3353-3359.
3. Mukhopadhyay, D., Riezman, H., Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007, 315, 201-205.
4. Pickart, C. M., Eddins, M. J., Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 2004, 1695, 55-72.
5. Semple, C. A. M., The comparative proteomics of ubiquitination in mouse. Genome Res. 2003, 13, 1389-1394.
6. Pickart, C. M., Fushman, D., Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 2004, 8, 610-616.
7. Love, K. R., Catic, A., Schlieker, C., Ploegh, H. L., Mechanisms, biology and inhibitors of deubiquitinating enzymes. Nat. Chem. Biol. 2007, 3, 697-705.
8. Dikic, I., Wakatsuki, S., Walters, K. J., Ubiquitin-binding domains - from structures to functions. Nat. Rev. Mol. Cell Biol. 2009, 10, 659-671.
9. Garavelli, J. S., The RESID Database of Protein Modifications as a resource and annotation tool. Proteomics 2004, 4, 1527-1533.
10. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C. et al., Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal 2010, 3, ra3.
11. Mischerikow, N., Heck, A. J. R., Targeted large-scale analysis of protein acetylation. Proteomics 2011, 11, 571-589.
12. Zielinska, D. F., Gnad, F., Wiśniewski, J. R., Mann, M., Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 2010, 141, 897-907.
13. Peng, J., Schwartz, D., Elias, J. E., Thoreen, C. C. et al., A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 2003, 21, 921-926.
14. Xu, P., Peng, J., Dissecting the ubiquitin pathway by mass spectrometry. Biochim. Biophys. Acta 2006, 1764, 1940-1947.
15. Jeon, H. B., Choi, E. S., Yoon, J. H., Hwang, J. H. et al., A proteomics approach to identify the ubiquitinated proteins in mouse heart. Biochem. Biophys. Res. Commun. 2007, 357, 731-736.
16. Peng, J., Evaluation of proteomic strategies for analyzing ubiquitinated proteins. BMB Rep. 2008, 41, 177-183.
17. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M. et al., A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17, 1030-1032.
18. Tagwerker, C., Flick, K., Cui, M., Guerrero, C. et al., A tandem affinity tag for two-step purification under fully denaturing conditions: application in ubiquitin profiling and protein complex identification combined with in vivocross-linking. Mol. Cell Proteomics 2006, 5, 737-748.
19. Danielsen, J. M. R., Sylvestersen, K. B., Bekker-Jensen, S., Szklarczyk, D. et al., Mass spectrometric analysis of lysine ubiquitylation reveals promiscuity at site level. Mol. Cell Proteomics 2011, 10, M110.003590.
20. Oshikawa, K., Matsumoto, M., Oyamada, K., Nakayama, K. I., Proteome-wide identification of ubiquitylation sites by conjugation of engineered lysine-less ubiquitin. J. Proteome Res. 2012, 11, 796-807.
21. Shi, Y., Xu, P., Qin, J., Ubiquitinated proteome: ready for global? Mol. Cell Proteomics 2011, 10, R110.006882.
22. Fujimuro, M., Sawada, H., Yokosawa, H., Production and characterization of monoclonal antibodies specific to multi-ubiquitin chains of polyubiquitinated proteins. FEBS Lett. 1994, 349, 173-180.
23. Hatakeyama, S., Matsumoto, M., Nakayama, K. I., in: Deshaies, R. J. (Ed.), Ubiquitin and Protein Degradation, Part B, vol. 399, Academic Press, New York 2005, pp. 277-286.
24. Matsumoto, M., Hatakeyama, S., Oyamada, K., Oda, Y. et al., Large-scale analysis of the human ubiquitin-related proteome. PROTEOMICS 2005, 5, 4145-4151.
25. Matsumoto, M. L., Wickliffe, K. E., Dong, K. C., Yu, C. et al., K11-linked polyubiquitination in cell cycle control revealed by a K11 linkage-specific antibody. Mol. Cell 2010, 39, 477-484.
26. Matsumoto, M. L., Dong, K. C., Yu, C., Phu, L. et al., Engineering and structural characterization of a linear polyubiquitin-specific antibody. J. Mol. Biol. 2012, 418, 134-144.
27. Newton, K., Matsumoto, M. L., Ferrando, R. E., Wickliffe, K. E. et al., Using linkage-specific monoclonal antibodies to analyze cellular ubiquitylation. Methods Mol. Biol. 2012, 832, 185-196.
28. Hicke, L., Schubert, H. L., Hill, C. P., Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 2005, 6, 610-621.
29. Hjerpe, R., Aillet, F., Lopitz-Otsoa, F., Lang, V. et al., Efficient protection and isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. EMBO Rep. 2009, 10, 1250-1258.
30. Lopitz-Otsoa, F., Rodriguez-Suarez, E., Aillet, F., Casado-Vela, J. et al., Integrative analysis of the ubiquitin proteome isolated using tandem ubiquitin binding entities (TUBEs). J. Proteome. 2011, 75, 2998-3014.
31. Shi, Y., Chan, D. W., Jung, S. Y., Malovannaya, A. et al., A data set of human endogenous protein ubiquitination sites. Mol. Cell Proteomics 2011, 10, M110.002089.
32. Akimov, V., Rigbolt, K. T. G., Nielsen, M. M., Blagoev, B., Characterization of ubiquitination dependent dynamics in growth factor receptor signaling by quantitative proteomics. Mol. Biosyst. 2011, 7, 3223-3233.
33. Xu, G., Paige, J. S., Jaffrey, S. R., Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat. Biotech. 2010, 28, 868-873.
34. Wagner, S. A., Beli, P., Weinert, B. T., Nielsen, M. L. et al., A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell Proteomics 2011, 10, M111.013284.
35. Kim, W., Bennett, E. J., Huttlin, E. L., Guo, A. et al., Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44, 325-340.
36. Wagner, S. A., Beli, P., Weinert, B. T., Scholz, C. et al., Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol. Cell Proteomics 2012, M112.017905. [Epub ahead of print].
37. Udeshi, N. D., Mani, D. R., Eisenhaure, T., Mertins, P. et al., Methods for quantification of in vivo changes in protein ubiquitination following proteasome and deubiquitinase inhibition. Mol. Cell Proteomics 2012, 11, M111.016857.
38. de Bettignies, G., Coux, O., Proteasome inhibitors: dozens of molecules and still counting. Biochimie 2010, 92, 1530-1545.
39. Altun, M., Kramer, H. B., Willems, L. I., McDermott, J. L. et al., Activity-based chemical proteomics accelerates inhibitor development for deubiquitylating enzymes. Chem. Biol. 2011, 18, 1401-1412.
40. Warren, M. R. E., Parker, C. E., Mocanu, V., Klapper, D. et al., Electrospray ionization tandem mass spectrometry of model peptides reveals diagnostic fragment ions for protein ubiquitination. Rapid Commun. Mass Spectrom. 2005, 19, 429-437.
41. Seyfried, N. T., Xu, P., Duong, D. M., Cheng, D. et al., Systematic approach for validating the ubiquitinated proteome. Anal. Chem. 2008, 80, 4161-4169.
42. Wang, M., Cheng, D., Peng, J., Pickart, C. M., Molecular determinants of polyubiquitin linkage selection by an HECT ubiquitin ligase. EMBO J. 2006, 25, 1710-1719.
43. Xu, P., Peng, J., Characterization of polyubiquitin chain structure by middle-down mass spectrometry. Anal. Chem. 2008, 80, 3438-3444.
44. Denis, N. J., Vasilescu, J., Lambert, J.-P., Smith, J. C. et al., Tryptic digestion of ubiquitin standards reveals an improved strategy for identifying ubiquitinated proteins by mass spectrometry. Proteomics 2007, 7, 868-874.
45. Syka, J. E. P., Coon, J. J., Schroeder, M. J., Shabanowitz, J. et al., Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 2004, 101, 9528-9533.
46. Nielsen, M. L., Vermeulen, M., Bonaldi, T., Cox, J. et al., Iodoacetamide-induced artifact mimics ubiquitination in mass spectrometry. Nat. Methods 2008, 5, 459-460.
47. Elias, J. E., Gygi, S. P., Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 2007, 4, 207-214.
48. Käll, L., Canterbury, J. D., Weston, J., Noble, W. S. et al., Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 2007, 4, 923-925.
49. Chalkley, R. J., Clauser, K. R., Modification site localization scoring: strategies and performance. Mol. Cell Proteomics 2012, 11, 3-14.
50. Ikeda, F., Dikic, I., Atypical ubiquitin chains: new molecular signals. "Protein Modifications: Beyond the Usual Suspects" review series. EMBO Rep. 2008, 9, 536-542.
51. Hicke, L., Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2001, 2, 195-201.
52. Thrower, J. S., Hoffman, L., Rechsteiner, M., Pickart, C. M., Recognition of the polyubiquitin proteolytic signal. EMBO J. 2000, 19, 94-102.
53. Saeki, Y., Kudo, T., Sone, T., Kikuchi, Y. et al., Lysine 63-linked polyubiquitin chain may serve as a targeting signal for the 26S proteasome. EMBO J. 2009, 28, 359-371.
54. Koegl, M., Hoppe, T., Schlenker, S., Ulrich, H. D. et al., A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell 1999, 96, 635-644.
55. Kirisako, T., Kamei, K., Murata, S., Kato, M. et al., A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 2006, 25, 4877-4887.
56. Tokunaga, F., Sakata, S., Saeki, Y., Satomi, Y. et al., Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat. Cell Biol. 2009, 11, 123-132.
57. Rahighi, S., Ikeda, F., Kawasaki, M., Akutsu, M. et al., Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 2009, 136, 1098-1109.
58. Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W. et al., Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. USA 2003, 100, 6940-6945.
59. Kirkpatrick, D. S., Hathaway, N. A., Hanna, J., Elsasser, S. et al., Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nat. Cell Biol. 2006, 8, 700-710.
60. Havlis, J., Shevchenko, A., Absolute quantification of proteins in solutions and in polyacrylamide gels by mass spectrometry. Anal. Chem. 2004, 76, 3029-3036.
61. Xu, P., Cheng, D., Duong, D. M., Rush, J. et al., A proteomic strategy for quantifying polyubiquitin chain topologies. Israel J. Chem. 2010, 46, 171-182.
62. Phu, L., Izrael-Tomasevic, A., Matsumoto, M. L., Bustos, D. et al., Improved quantitative mass spectrometry methods for characterizing complex ubiquitin signals. Mol. Cell. Proteomics 2011, 10, M110.003756.
63. Xu, P., Duong, D. M., Seyfried, N. T., Cheng, D. et al., Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009, 137, 133-145.
64. Huang, F., Kirkpatrick, D., Jiang, X., Gygi, S. et al., Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 2006, 21, 737-748.
65. Kaiser, S. E., Riley, B. E., Shaler, T. A., Trevino, R. S. et al., Protein standard absolute quantification (PSAQ) method for the measurement of cellular ubiquitin pools. Nat. Methods 2011, 8, 691-696.
66. Brun, V., Dupuis, A., Adrait, A., Marcellin, M. et al., Isotope-labeled protein standards toward absolute quantitative proteomics. Mol. Cell. Proteomics 2007, 6, 2139-2149.
67. Nakayama, K. I., Nakayama, K., Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 2006, 6, 369-381.
68. Cardozo, T., Pagano, M., The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 2004, 5, 739-751.
69. Fukunaga, R., Hunter, T., MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. The EMBO J. 1997, 16, 1921-1933.
70. Burande, C. F., Heuzé, M. L., Lamsoul, I., Monsarrat, B. et al., A label-free quantitative proteomics strategy to identify E3 ubiquitin ligase substrates targeted to proteasome degradation. Mol. Cell. Proteomics 2009, 8, 1719-1727.
71. Koo, B. K., Spit, M., Jordens, I., Low, T. Y. et al., Tumour suppressor RNF43 is a stem cell E3 ligase that induces endocytosis of Wnt receptors. Nature 2012, 488, 665-669.
72. Bennett, E. J., Rush, J., Gygi, S. P., Harper, J. W., Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 2010, 143, 951-965.
73. Duda, D. M., Borg, L. A., Scott, D. C., Hunt, H. W. et al., Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 2008, 134, 995-1006.
74. Lee, K. A., Hammerle, L. P., Andrews, P. S., Stokes, M. P. et al., Ubiquitin ligase substrate identification through quantitative proteomics at both the protein and peptide levels. J. Biol. Chem. 2011, 286, 41530-41538.
75. Yaron, A., Hatzubai, A., Davis, M., Lavon, I. et al., Identification of the receptor component of the IkappaBalpha-ubiquitin ligase. Nature 1998, 396, 590-594.
76. Dorrello, N. V., Peschiaroli, A., Guardavaccaro, D., Colburn, N. H. et al., S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 2006, 314, 467-471.
77. Peschiaroli, A., Dorrello, N. V., Guardavaccaro, D., Venere, M. et al., SCFbetaTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol. Cell 2006, 23, 319-329.
78. Guardavaccaro, D., Frescas, D., Dorrello, N. V., Peschiaroli, A. et al., Control of chromosome stability by the beta-TrCP-REST-Mad2 axis. Nature 2008, 452, 365-369.
79. Kruiswijk, F., Yuniati, L., Magliozzi, R., Low, T. Y. et al., Coupled activation and degradation of eEF2K regulates protein synthesis in response to genotoxic stress. Sci. Signal 2012, 5, ra40.
80. D'Angiolella, V., Donato, V., Vijayakumar, S., Saraf, A. et al., SCF(cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 2010, 466, 138-142.
81. D'Angiolella, V., Donato, V., Forrester, F. M., Jeong, Y.-T. et al., Cyclin F-mediated degradation of ribonucleotide reductase M2 controls genome integrity and DNA repair. Cell 2012, 149, 1023-1034.
82. Busino, L., Millman, S. E., Scotto, L., Kyratsous, C. A. et al., Fbxw7α- and GSK3-mediated degradation of p100 is a pro-survival mechanism in multiple myeloma. Nat. Cell Biol. 2012, 14, 375-385.
83. Liu, B., Zheng, Y., Wang, T.-D., Xu, H.-Z. et al., Proteomic identification of common SCF ubiquitin ligase FBXO6-interacting glycoproteins in three kinds of cells. J. Proteome Res. 2012, 11, 1773-1781.
84. Teixeira, F. R., Yokoo, S., Gartner, C. A., Manfiolli, A. O. et al., Identification of FBXO25-interacting proteins using an integrated proteomics approach. Proteomics 2010, 10, 2746-2757.
85. Yumimoto, K., Matsumoto, M., Oyamada, K., Moroishi, T. et al., Comprehensive identification of substrates for F-box proteins by differential proteomics analysis. J. Proteome Res. 2012, 11, 3175-3185.
86. Paul, F. E., Hosp, F., Selbach, M., Analyzing protein-protein interactions by quantitative mass spectrometry. Methods 2011, 54, 387-395.
87. Wu, G., Xu, G., Schulman, B. A., Jeffrey, P. D. et al., Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol. Cell 2003, 11, 1445-1456.
88. Reyes-Turcu, F. E., Ventii, K. H., Wilkinson, K. D., Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 2009, 78, 363-397.
89. Nijman, S. M. B., Luna-Vargas, M. P. A., Velds, A., Brummelkamp, T. R. et al., A genomic and functional inventory of deubiquitinating enzymes. Cell 2005, 123, 773-786.
90. Hemelaar, J., Galardy, P. J., Borodovsky, A., Kessler, B. M. et al., Chemistry-based functional proteomics: mechanism-based activity-profiling tools for ubiquitin and ubiquitin-like specific proteases. J. Proteome Res. 2004, 3, 268-276.
91. Borodovsky, A., Ovaa, H., Kolli, N., Gan-Erdene, T. et al., Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem. Biol. 2002, 9, 1149-1159.
92. Ventii, K. H., Wilkinson, K. D., Protein partners of deubiquitinating enzymes. Biochem. J. 2008, 414, 161-175.
93. Sowa, M. E., Bennett, E. J., Gygi, S. P., Harper, J. W., Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138, 389-403.
94. Kouranti, I., McLean, J. R., Feoktistova, A., Liang, P. et al., A global census of fission yeast deubiquitinating enzyme localization and interaction networks reveals distinct compartmentalization profiles and overlapping functions in endocytosis and polarity. PLoS Biol. 2010, 8, e1000471.
95. Poulsen, J. W., Madsen, C. T., Young, C., Kelstrup, C. D. et al., Comprehensive profiling of proteome changes upon sequential deletion of deubiquitylating enzymes. J. Proteomics 2012, 75, 3886-3897.
96. Farriol-Mathis, N., Garavelli, J. S., Boeckmann, B., Duvaud, S. et al., Annotation of post-translational modifications in the Swiss-Prot knowledge base. Proteomics 2004, 4, 1537-1550.
97. 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.
98. Hornbeck, P. V., Kornhauser, J. M., Tkachev, S., Zhang, B. et al., PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 2012, 40, D261-D270.
99. Han, Y., Lee, H., Park, J. C., Yi, G.-S., E3Net: a system for exploring E3-mediated regulatory networks of cellular functions. Mol. Cell Proteomics 2012, 11, O111.014076.
100. Lee, W.-C., Lee, M., Jung, J. W., Kim, K. P. et al., Kim, D., SCUD: Saccharomyces cerevisiae ubiquitination database. BMC Genomics 2008, 9, 440.
101. Du, Z., Zhou, X., Li, L., Su, Z., plantsUPS: a database of plants' Ubiquitin Proteasome System. BMC Genomics 2009, 10, 227.
102. Lee, H., Yi, G.-S., Park, J. C., E3Miner: a text mining tool for ubiquitin-protein ligases. Nucleic Acids Res. 2008, 36, W416-W422.
103. Tung, C.-W., Ho, S.-Y., Computational identification of ubiquitylation sites from protein sequences. BMC Bioinformatics 2008, 9, 310.
104. Radivojac, P., Vacic, V., Haynes, C., Cocklin, R. R. et al., Identification, analysis, and prediction of protein ubiquitination sites. Proteins 2010, 78, 365-380.
105. Hunter, T., The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 2007, 28, 730-738.
106. Grabbe, C., Husnjak, K., Dikic, I., The spatial and temporal organization of ubiquitin networks. Nat. Rev. Mol. Cell Biol. 2011, 12, 295-307.
107. Lamond, A. I., Uhlen, M., Horning, S., Makarov, A. et al., Advancing cell biology through proteomics in space and time (PROSPECTS). Mol. Cell Proteomics 2012, 11, O112.017731.