Hsp90 inhibition induces both protein-specific and global changes in the ubiquitinome

Journal of Proteomics

Volumn 120, Issue , 2015, Pages 215-229

  Quadroni, Manfredo ^a   Potts, Alexandra ^a   Waridel, Patrice ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Chaperone; Hsp90; Mass spectrometry; Quantitation; Stress response; Ubiquitin

Indexed keywords

CELL PROTEIN; GLYCINE; POLYUBIQUITIN; PROTEASOME; STABLE ISOTOPE; HEAT SHOCK PROTEIN 90; PROTEOME; UBIQUITIN; UBIQUITINATED PROTEIN;

ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN SYNTHESIS; UBIQUITINATION; ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; JURKAT CELL LINE; METABOLISM; PHYSIOLOGY;

GENE EXPRESSION REGULATION, ENZYMOLOGIC; HSP90 HEAT-SHOCK PROTEINS; HUMANS; JURKAT CELLS; PROTEOME; UBIQUITIN; UBIQUITINATED PROTEINS; UBIQUITINATION;

EID: 84942048003     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.02.020     Document Type: Article

References (43)

1. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
2. Taipale M., Krykbaeva I., Koeva M., Kayatekin C., et al. Quantitative analysis of hsp90-client interactions reveals principles of substrate recognition. Cell 2012, 150:987-1001.
3. Makhnevych T., Houry W.a The role of Hsp90 in protein complex assembly. Biochim. Biophys. Acta 2011, 1823:674-682.
4. Travers J., Sharp S., Workman P. HSP90 inhibition: two-pronged exploitation of cancer dependencies. Drug Discov. Today 2012, 17:242-252.
5. Lawson B., Brewer J.W., Hendershot L.M. Geldanamycin, an hsp90/GRP94-binding drug, induces increased transcription of endoplasmic reticulum (ER) chaperones via the ER stress pathway. J. Cell. Physiol. 1998, 174:170-178.
6. Santagata S., Mendillo M.L., Tang Y., Subramanian A., et al. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science 2013, 341:1238303.
7. Maloney A., Clarke P.A., Naaby-Hansen S., Stein R., et al. Gene and protein expression profiling of human ovarian cancer cells treated with the heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Cancer Res. 2007, 67:3239-3253.
8. Sharma K., Vabulas R.M., Macek B., Pinkert S., et al. Quantitative proteomics reveals that Hsp90 inhibition preferentially targets kinases and the DNA damage response. Mol. Cell. Proteomics 2012, 11. (M111.014654).
9. Wu Z., Moghaddas Gholami A., Kuster B. Systematic identification of the HSP90 candidate regulated proteome. Mol. Cell. Proteomics 2012, 11. (M111.016675).
10. Qian S., McDonough H., Boellmann F., Cyr D.M., Patterson C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 2006, 440:551-555.
11. Hilt W. Targets of programmed destruction: a primer to regulatory proteolysis in yeast. Cell. Mol. Life Sci. 2004, 61:1615-1632.
12. Mayor T., Graumann J., Bryan J., MacCoss M.J., Deshaies R.J. Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol. Cell. Proteomics 2007, 6:1885-1895.
13. Argenzio E., Bange T., Oldrini B., Bianchi F., et al. Proteomic snapshot of the EGF-induced ubiquitin network. Mol. Syst. Biol. 2011, 7:462.
14. 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.
15. Carlson N., Rogers S., Rechsteiner M. Microinjection of ubiquitin: changes in protein degradation in HeLa cells subjected to heat-shock. J. Cell Biol. 1987, 104:547-555.
16. Dantuma N.P., Groothuis T.A.M., Salomons F.A., Neefjes J. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell Biol. 2006, 173:19-26.
17. Schubert U., Antón L.C., Gibbs J., Norbury C.C., et al. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000, 404:770-774.
18. Milner E., Gutter-Kapon L., Bassani-Strenberg M., Barnea E., et al. The effect of proteasome inhibition on the generation of the human leukocyte antigen (HLA) peptidome. Mol. Cell. Proteomics 2013, 12:1853-1864.
19. Vabulas R.M., Hartl F.U. Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 2005, 310:1960-1963.
20. Bourdetsky D., Schmelzer C.E.H., Admon A. The nature and extent of contributions by defective ribosome products to the HLA peptidome. Proc. Natl. Acad. Sci. U. S. A. 2014, 2014:1-9.
21. Yewdell J.W. DRiPs solidify: progress in understanding endogenous MHC class I antigen processing. Trends Immunol. 2011, 32:548-558.
22. Dolan B.P., Bennink J.R., Yewdell J.W. Translating DRiPs: progress in understanding viral and cellular sources of MHC class I peptide ligands. Cell. Mol. Life Sci. 2011, 68:1481-1489.
23. Duttler S., Pechmann S., Frydman J. Principles of cotranslational ubiquitination and quality control at the ribosome. Mol. Cell 2013, 50:379-393.
24. Wang F., Durfee L.a, Huibregtse J.M. A cotranslational ubiquitination pathway for quality control of misfolded proteins. Mol. Cell 2013, 50:368-378.
25. Fang N.N., Ng A.H.M., Measday V., Mayor T. Hul5 HECT ubiquitin ligase plays a major role in the ubiquitylation and turnover of cytosolic misfolded proteins. Nat. Cell Biol. 2011, 13:1344-1352.
26. Ng A.H.M., Fang N.N., Comyn S.a, Gsponer J., Mayor T. System-wide analysis reveals intrinsically disordered proteins are prone to ubiquitylation after misfolding stress. Mol. Cell. Proteomics 2013, 12:2456-2467.
27. Fierro-Monti I., Echeverria P., Racle J., Hernandez C., et al. Dynamic impacts of the inhibition of the molecular chaperone Hsp90 on the T-cell proteome have implications for anti-cancer therapy. PLoS One 2013, 8:e80425.
28. Fierro-Monti I., Racle J., Hernandez C., Waridel P., et al. A novel pulse-chase SILAC strategy measures changes in protein decay and synthesis rates induced by perturbation of proteostasis with an Hsp90 inhibitor. PLoS One 2013, 8:e80423.
29. Ong S.-E., Blagoev B., Kratchmarova I., Kristensen D.B., et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
30. Niedergang F., Dautry-Varsat A., Alcover A. Peptide antigen or superantigen-induced down-regulation of TCRs involves both stimulated and unstimulated receptors. J. Immunol. 1997, 159:1703-1710.
31. Niedergang F., San José E., Rubin B., Alarcón B., et al. Differential cytosolic tail dependence and intracellular fate of T-cell receptors internalized upon activation with superantigen or phorbol ester. Res. Immunol. 1997, 148:231-245.
32. Wiśniewski J.R., Zougman A., Mann M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J. Proteome Res. 2009, 8:5674-5678.
33. Vizcaíno J.a, Deutsch E.W., Wang R., Csordas A., et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 2014, 32:223-226.
34. Cox J., Neuhauser N., Michalski A., Scheltema R.A., et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 2011, 10:1794-1805.
35. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
36. Cox J., Mann M. 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high-throughput data. BMC Bioinform. 2012, 13(Suppl. 1):S12.
37. Udeshi N.D., Svinkina T., Mertins P., Kuhn E., et al. Refined preparation and use of anti-diglycine remnant (K-ε-GG) antibody enables routine quantification of 10,000s of ubiquitination sites in single proteomics experiments. Mol. Cell. Proteomics 2013, 12:825-831.
38. 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, 11:148-159.
39. Yorgin P.D., Hartson S.D., Fellah a M., Scroggins B.T., et al. Effects of geldanamycin, a heat-shock protein 90-binding agent, on T cell function and T cell nonreceptor protein tyrosine kinases. J. Immunol. 2000, 164:2915-2923.
40. Ohta K., Okoshi R., Wakabayashi M., Ishikawa A., et al. Geldanamycin, a heat-shock protein 90-binding agent, induces thymocyte apoptosis through destabilization of Lck in presence of 12-O-tetradecanoylphorbol 13-acetate. Biomed. Res. 2007, 28:33-42.
41. Smith J.R., Clarke P.a., de Billy E., Workman P. Silencing the cochaperone CDC37 destabilizes kinase clients and sensitizes cancer cells to HSP90 inhibitors. Oncogene 2009, 28:157-169.
42. Jane E.P., Pollack I.F. The heat shock protein antagonist 17-AAG potentiates the activity of enzastaurin against malignant human glioma cells. Cancer Lett. 2008, 268:46-55.
43. 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.