Using the ubiquitin-modified proteome to monitor distinct and spatially restricted protein homeostasis dysfunction

Molecular and Cellular Proteomics

Volumn 15, Issue 8, 2016, Pages 2576-2593

  Gendron, Joshua M ^a,b   Webb, Kristofor ^a,c   Yang, Bing ^a   Rising, Lisa ^a   Zuzow, Nathan ^a   Bennett, Eric J ^a  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b YALE UNIVERSITY   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; PROTEOME; UBIQUITIN; ADENOSINE TRIPHOSPHATASE; CDC48 PROTEIN; CELL CYCLE PROTEIN; PROTEASOME INHIBITOR;

AGING; ARTICLE; CELL FRACTIONATION; DISEASE COURSE; HCT116 CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN QUALITY; PROTEOMICS; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; DRUG EFFECTS; HCT 116 CELL LINE; HOMEOSTASIS; LIQUID CHROMATOGRAPHY; METABOLISM; PROCEDURES; PROTEIN PROTEIN INTERACTION; TANDEM MASS SPECTROMETRY;

ADENOSINE TRIPHOSPHATASES; BINDING SITES; CELL CYCLE PROTEINS; CHROMATOGRAPHY, LIQUID; HCT116 CELLS; HOMEOSTASIS; HUMANS; PROTEASOME INHIBITORS; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY; UBIQUITINS;

EID: 84982797294     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M116.058420     Document Type: Article

References (62)

1. Rodrigo-Brenni, M. C., and Hegde, R. S. (2012) Design principles of protein biosynthesis-coupled quality control. Dev. Cell 23, 896-907
2. Wolff, S., Weissman, J. S., and Dillin, A. (2014) Differential scales of protein quality control. Cell 157, 52-64
3. Lykke-Andersen, J., and Bennett, E. J. (2014) Protecting the proteome: Eukaryotic cotranslational quality control pathways. J. Cell Biol. 204, 467-476
4. Comyn, S. A., Chan, G. T., and Mayor, T. (2014) False start: Cotranslational protein ubiquitination and cytosolic protein quality control. J. Proteomics 100, 92-101
5. Koga, H., Kaushik, S., and Cuervo, A. M. (2011) Protein homeostasis and aging: The importance of exquisite quality control. Ageing Res. Rev. 10, 205-215.
6. Labbadia, J., and Morimoto, R. I. (2015) The biology of proteostasis in aging and disease. Annu. Rev. Biochem. 84, 435-464.
7. Bence, N. F., Sampat, R. M., and Kopito, R. R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552-1555.
8. Bennett, E. J., Bence, N. F., Jayakumar, R., and Kopito, R. R. (2005) Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol. Cell 17, 351-365.
9. Chu, J., Hong, N. A., Masuda, C. A., Jenkins, B. V., Nelms, K. A., Goodnow, C. C., Glynne, R. J., Wu, H., Masliah, E., Joazeiro, C. A., and Kay, S. A. (2009) A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration. Proc. Natl. Acad. Sci. U S A 106, 2097-2103.
10. Das, I., Krzyzosiak, A., Schneider, K., Wrabetz, L., D'Antonio, M., Barry, N., Sigurdardottir, A., and Bertolotti, A. (2015) Preventing proteostasis diseases by selective inhibition of a phosphatase regulatory subunit. Science 348, 239-242
11. Lee, J. W., Beebe, K., Nangle, L. A., Jang, J., Longo-Guess, C. M., Cook, S. A., Davisson, M. T., Sundberg, J. P., Schimmel, P., and Ackerman, S. L. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443, 50-55
12. Ishimura, R., Nagy, G., Dotu, I., Zhou, H., Yang, X. L., Schimmel, P., Senju, S., Nishimura, Y., Chuang, J. H., and Ackerman, S. L. (2014) RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science 345, 455-459
13. Deshaies, R. J. (2014) Proteotoxic crisis, the ubiquitin-proteasome system, and cancer therapy. BMC Biol. 12, 94
14. Bhat, M., Robichaud, N., Hulea, L., Sonenberg, N., Pelletier, J., and Topisirovic, I. (2015) Targeting the translation machinery in cancer. Nat. Rev. Drug Discov. 14, 261-278
15. Silvera, D., Formenti, S. C., and Schneider, R. J. (2010) Translational control in cancer. Nat. Rev. Cancer 10, 254-266
16. Bence, N. F., Bennett, E. J., and Kopito, R. R. (2005) Application and analysis of the GFPu family of ubiquitin-proteasome system reporters. Methods Enzymol. 399, 481-490
17. Salomons, F. A., Acs, K., and Dantuma, N. P. (2010) Illuminating the ubiquitin/proteasome system. Exp. Cell. Res. 316, 1289-1295
18. Salomons, F. A., Verhoef, L. G., and Dantuma, N. P. (2005) Fluorescent reporters for the ubiquitin-proteasome system. Essays Biochem. 41, 113-128
19. Dantuma, N.,P., and Lindsten, K. (2010) Stressing the ubiquitin-proteasome system. Cardiovasc. Res. 85, 263-271
20. Dantuma, N. P., Lindsten, K., Glas, R., Jellne, M., and Masucci, M. G. (2000) Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome- dependent proteolysis in living cells. Nat. Biotechnol. 18, 538-543
21. Lindsten, K., Menendez-Benito, V., Masucci, M. G., and Dantuma, N. P. (2003) A transgenic mouse model of the ubiquitin/proteasome system. Nat. Biotechnol. 21, 897-902
22. Carrano, A. C., and Bennett, E. J. (2013) Using the ubiquitin-modified proteome to monitor protein homeostasis function. Mol. Cell Proteomics 12, 3521-3531
23. Kim, W., Bennett, E. J., Huttlin, E. L., Guo, A., Li, J., Possemato, A., Sowa, M. E., Rad, R., Rush, J., Comb M. J., Harper, J. W., and Gygi, S. P. (2011) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell, 44, 325-340
24. Elia, A. E., Boardman, A. P., Wang, D. C., Huttlin, E. L., Everley, R. A., Dephoure, N., Zhou, C., Koren, I., Gygi, S. P., and Elledge, S. J. (2015) Quantitative proteomic atlas of ubiquitination and acetylation in the DNA damage response. Mol. Cell 59, 867-881
25. Higgins, R., Gendron, J. M., Rising, L., Mak, R., Webb, K., Kaiser, S. E., Zuzow, N., Riviere, P., Yang, B., Fenech, E., Tang, X., Lindsay, S. A., Christianson, J. C., Hampton, R. Y., Wasserman, S. A., and Bennett, E. J. (2015) The unfolded protein response triggers site-specific regulatory ubiquitylation of 40S ribosomal proteins. Mol. Cell 59, 35-49
26. Povlsen, L. K., Beli, P., Wagner, S. A., Poulsen, S. L., Sylvestersen, K. B., Poulsen, J. W., Nielsen, M. L., Bekker-Jensen, S., Mailand, N., and Choudhary, C. (2012) Systems-wide analysis of ubiquitylation dynamics reveals a key role for PAF15 ubiquitylation in DNA-damage bypass. Nat. Cell Biol. 14, 1089-1098
27. Sarraf, S. A., Raman, M., Guarani-Pereira, V., Sowa, M. E., Huttlin, E. L., Gygi, S. P., and Harper, J. W. (2013) Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 496, 372-376
28. Udeshi, N. D., Mani, D. R., Eisenhaure, T., Mertins, P., Jaffe, J. D., Clauser, K. R., Hacohen, N., and Carr, S. A. (2012) Methods for quantification of in vivo changes in protein ubiquitination following proteasome and deubiquitinase inhibition. Mol. Cell. Proteomics 11, 148-159
29. Buckley, S. M., Aranda-Orgilles, B., Strikoudis, A., Apostolou, E., Loizou, E., Moran-Crusio, K., Farnsworth, C. L., Koller, A. A., Dasgupta, R., Silva, J. C., Stadtfeld, M., Hochedlinger, K., Chen, E. I., and Aifantis, I. (2012) Regulation of pluripotency and cellular reprogramming by the ubiquitinproteasome system. Cell Stem Cell 11, 783-798
30. Emanuele, M. J., Elia, A. E., Xu, Q., Thoma, C. R., Izhar, L., Leng, Y., Guo, A., Chen, Y. N., Rush, J., Hsu, P. W., Yen, H. C., and Elledge, S. J. (2011) Global identification of modular cullin-RING ligase substrates. Cell 147, 459-474
31. Kronke, J., Fink, E. C., Hollenbach, P. W., MacBeth, K. J., Hurst, S. N., Udeshi, N. D., Chamberlain, D. R., Mani, H. W., Man, A. K., Gandhi, T., Svinkina, R. K., Schneider, M., McConkey, P. P., Jaras, M., Griffiths, E., Wetzler, M., Bullinger, L., Cathers, B. E., Carr, S. A., Chopra, R., and Ebert, B. L. (2015) Lenalidomide induces ubiquitination and degradation of CK1alpha in del(5q) MDS. Nature 523, 183-188
32. Kronke, J., Udeshi, N. D., Narla, A., Grauman, P., Hurst, S. N., McConkey, M., Svinkina, T., Heckl, D., Comer, E., Li, X., Ciarlo, C., Hartman, E., Munshi, N., Schenone, M., Schreiber, S. A., Carr, S. L., and Ebert, B. L. (2014) Lenalidomide causes selective degradation of IKZF1 and IKZF3 in multiple myeloma cells. Science 343, 301-305
33. Theurillat, J. P., Udeshi, N. D., Errington, W. J., Svinkina, T., Baca, S. C., Pop, M., Wild, P. J., Blattner, M., Groner, A. C., Rubin, M. A., Moch, H., Prive, G. G., Carr, S. A., and Garraway, L. A. (2014) Prostate cancer. Ubiquitylome analysis identifies dysregulation of effector substrates in SPOP-mutant prostate cancer. Science 346, 85-89
34. Tong, Z., Kim, M. S., Pandey, A., and Espenshade, P. J. (2014) Identification of candidate substrates for the Golgi Tul1 E3 ligase using quantitative diGly proteomics in yeast. Mol. Cell. Proteomics 13, 2871-2882
35. Komander, D., and Rape, M. (2012) The ubiquitin code. Annu. Rev. Biochem. 81, 203-229
36. Williamson, A., Werner, A., and Rape, M. (2013) The Colossus of ubiquitylation: Decrypting a cellular code. Mol. Cell 49, 591-600
37. Sun, Z. W., and Allis, C. D. (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418, 104-108
38. Tanno, H., and Komada, M. (2013) The ubiquitin code and its decoding machinery in the endocytic pathway. J. Biochem. 153, 497-504
39. Anderson, D. J., Le Moigne, R., Djakovic, S., Kumar, B., Rice, J., Wong, S., Wang, J., Yao, B., Valle, E., Kiss von Soly, S., Madriaga, A., Soriano, F., Menon, M. K., Wu, Z. Y., Kampmann, M., Chen, Y., Weissman, J. S., Aftab, B. T., Yakes, F. M., Shawver, L., Zhou, H., Wustrow, D. J., and Rolfe, M. (2009) Targeting the AAA ATPase p97 as an approach to treat cancer through disruption of protein homeostasis. Cancer Cell 28, 653-665
40. Kisselev, A. F., and Goldberg, A. L. (2005) Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol. 398, 364-378
41. Tsirigos, K. D., Peters, C., Shu, N., Kall, L., and Elofsson, A. (2015) The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Res. 43, W401-W407
42. Schwartz, A.L., and Ciechanover, A. (2009) Targeting proteins for destruction by the ubiquitin system: Implications for human pathobiology. Annu. Rev. Pharmacol. Toxicol. 49,73-96
43. Menendez-Benito, V., Heessen, S., and Dantuma, N. P. (2005) Monitoring of ubiquitin-dependent proteolysis with green fluorescent protein substrates. Methods Enzymol. 399, 490-511
44. Xu, G., Paige, J. S., and Jaffrey, S. R. (2010) Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat. Biotechnol. 28, 868-873
45. Latres, E., Chiaur, D. S., and Pagano, M. (1999) The human F box protein beta-Trcp associates with the Cul1/Skp1 complex and regulates the stability of beta-catenin. Oncogene 18, 849-854
46. Mimnaugh, E. G., Chen, H. Y., Davie, J. R., Celis, J. E., and Neckers, L. (1997) Rapid deubiquitination of nucleosomal histones in human tumor cells caused by proteasome inhibitors and stress response inducers: Effects on replication, transcription, translation, and the cellular stress response. Biochemistry 36 14418-14429
47. Shcherbik, N., and Pestov, D. G. (2010) Ubiquitin and ubiquitin-like proteins in the nucleolus: Multitasking tools for a ribosome factory. Genes Cancer 1, 681-689
48. Bedford, L., Lowe, J., Dick, L. R., Mayer, R. J., and Brownell, J. E. (2011) Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat. Rev. Drug Discov. 10, 29-46
49. Meyer, H., and Weihl, C. C. (2014) The VCP/p97 system at a glance: Connecting cellular function to disease pathogenesis. J. Cell Sci. 127, 3877-3883
50. Christianson, J. C., and Ye, Y. (2014) Cleaning up in the endoplasmic reticulum: Ubiquitin in charge. Nat. Struct. Mol. Biol. 21, 325-335
51. Magnaghi, P., D'Alessio, R., Valsasina, B., Avanzi, N., Rizzi, S., Asa, D., Gasparri, F., Cozzi, L., Cucchi, U., Orrenius, C., Polucci, P., Ballinari, D., Perrera, C., Leone, A., Cervi, G., Casale, E., Xiao, Y., Wong, C., Anderson, D. J., Galvani, A., Donati, D., O'Brien, T., Jackson, P. K., and Isacchi, A. (2013) Covalent and allosteric inhibitors of the ATPase VCP/p97 induce cancer cell death. Nat. Chem. Biol. 9, 548-556
52. Chou, T. F., Brown, S. J., Minond, D., Nordin, B. E., Li, K., Jones, A. C., Chase, P., Porubsky, P. R., Stoltz, B. M., Schoenen, F. J., Patricelli, M. P., Hodder, P., Rosen, H., and Deshaies, R. J. (2011) Reversible inhibitor of p97, DBeQ, impairs both ubiquitin-dependent and autophagic protein clearance pathways. Proc. Natl. Acad. Sci. U S A 108, 4834-4839
53. Ying, Z., Wang, H., and Wang, G. (2013) The ubiquitin proteasome system as a potential target for the treatment of neurodegenerative diseases. Curr. Pharm. Des. 19, 3305-3314
54. Wilkinson, K. D. (2005) The discovery of ubiquitin-dependent proteolysis. Proc. Natl. Acad. Sci.U S A 102, 15280-15282
55. Qian, S. B., Princiotta, M. F. Bennink, J. R. and Yewdell, J. W. (2006) Characterization of rapidly degraded polypeptides in mammalian cells reveals a novel layer of nascent protein quality control. J. Biol. Chem. 281, 392-400
56. Schubert, U., Anton, L.C. Gibbs, J. Norbury, C.C. Yewdell, J.W. and Bennink, J.R. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404, 770-774
57. Wang, F., Durfee, L. A., and Huibregtse, J. M. (2013) A cotranslational ubiquitination pathway for quality control of misfolded proteins. Mol. Cell 50, 368-378
58. Lesur, A., and Domon, B. (2015) Advances in high-resolution accurate mass spectrometry application to targeted proteomics. Proteomics 15, 880-890
59. Garraway, L. A., and Lander, E. S. (2013) Lessons from the cancer genome. Cell 153, 17-37
60. Wang, M., Martin, T. Bensinger, W. Alsina, M. Siegel, D.S. Kavalerchik, E. Huang, M. Orlowski, R.Z. and Niesvizky, R. (2013) Phase 2 dose-expansion study (PX-171-006) of carfilzomib, lenalidomide, and low-dose dexamethasone in relapsed or progressive multiple myeloma. Blood 122, 3122-3128
61. Richardson, P.G., Sonneveld, P., Schuster, M. W., Irwin, D., Stadtmauer, E. A., Facon, T., Harousseau, J. L., Ben-Yehuda, D., Lonial, S., Goldschmidt, H., Reece, D., San-Miguel, J. F., Blade, J., Boccadoro, M., Cavenagh, J., Dalton, W. S., Boral, A. L., Esseltine, D. L., Porter, J. B., Schenkein, D., and Anderson, K. C., (2005) Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N. Engl. J. Med. 352, 2487-2498
62. Obeng, E. A., Carlson, L. M., Gutman, D. M., Harrington, W. J., Jr., Lee, K. P., and Boise, L. H. (2006) Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 107, 4907-4916