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Mass spectrometry: a technique of many faces

Published online by Cambridge University Press:  28 November 2016

Maya A. Olshina
Affiliation:
Department of Biomolecular Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel
Michal Sharon*
Affiliation:
Department of Biomolecular Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel
*
*Author for correspondence: Prof. M. Sharon, Department of Biomolecular Sciences, Weizmann Institute of Science, 234 Herzl St, Rehovot 7610001, Israel. Tel.: +972-8-934-3947; Fax: +972-8-934-6010; Email: [email protected]

Abstract

Protein complexes form the critical foundation for a wide range of biological process, however understanding the intricate details of their activities is often challenging. In this review we describe how mass spectrometry (MS) plays a key role in the analysis of protein assemblies and the cellular pathways which they are involved in. Specifically, we discuss how the versatility of mass spectrometric approaches provides unprecedented information on multiple levels. We demonstrate this on the ubiquitin-proteasome proteolytic pathway, a process that is responsible for protein turnover. We follow the various steps of this degradation route and illustrate the different MS workflows that were applied for elucidating molecular information. Overall, this review aims to stimulate the integrated use of multiple mass spectrometry approaches for analyzing complex biological systems.

Type
Review
Copyright
Copyright © Cambridge University Press 2016 

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References

Aebersold, R. & Mann, M. (2003). Mass spectrometry-based proteomics. Nature 422, 198207.CrossRefGoogle ScholarPubMed
Aiken, C. T., Kaake, R. M., Wang, X. & Huang, L. (2011). Oxidative stress-mediated regulation of proteasome complexes. Molecular & Cellular Proteomics 10, R110·006924.CrossRefGoogle ScholarPubMed
Asher, G. (2005). A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73. Genes & Development 19, 316321.CrossRefGoogle ScholarPubMed
Asher, G., Dym, O., Tsvetkov, P., Adler, J. & Shaul, Y. (2006). The crystal structure of NAD(P)H Quinone Oxidoreductase 1 in complex with its potent inhibitor dicoumarol. Biochemistry 45, 63726378.Google Scholar
Bar-Nun, S. & Glickman, M. H. (2011). Proteasomal AAA-ATPases: structure and function. Biochimica et Biophysica Acta 1823, 6782.CrossRefGoogle ScholarPubMed
Baugh, J. M., Viktorova, E. G. & Pilipenko, E. V. (2009). Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitination. Journal of Molecular Biology 386, 814827.Google Scholar
Benesch, J. L. P. (2009). Collisional activation of protein complexes: picking up the pieces. Journal of the American Society for Mass Spectrometry 20, 341348.Google Scholar
Ben-Nissan, G., Chotiner, A., Tarnavsky, M. & Sharon, M. (2016). Structural characterization of missense mutations using high resolution mass spectrometry: a case study of the Parkinson's-related protein, DJ-1. Journal of the American Society for Mass Spectrometry 27, 10621070.Google Scholar
Ben-Nissan, G. & Sharon, M. (2014). Regulating the 20S proteasome ubiquitin-independent degradation pathway. Biomolecules 4, 862884.Google Scholar
Benesch, J. L. P., Ruotolo, B. T., Simmons, D. A. & Robinson, C. V. (2007). Protein complexes in the gas phase: technology for structural genomics and proteomics. Chemical Reviews 107, 35443567.Google Scholar
Bennett, E. J., Rush, J., Gygi, S. P. & Harper, J. W. (2010). Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 143, 951965.CrossRefGoogle ScholarPubMed
Bohn, S., Beck, F., Sakata, E., Walzthoeni, T., Beck, M., Aebersold, R., Förster, F., Baumeister, W. & Nickell, S. (2010). Structure of the 26S proteasome from Schizosaccharomyces pombe at subnanometer resolution. Proceedings of the National Academy of Sciences 107, 2099220997.Google Scholar
Boname, J. M., Thomas, M., Stagg, H. R., Xu, P., Peng, J. & Lehner, P. J. (2010). Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic 11, 210220.Google Scholar
Brodbelt, J. S. (2014). Photodissociation mass spectrometry: new tools for characterization of biological molecules. Chemical Society Reviews 43, 27572783.Google Scholar
Calabrese, A. N. & Pukala, T. L. (2013). Chemical cross-linking and mass spectrometry for the structural analysis of protein assemblies. Australian Journal of Chemistry 66, 749759.Google Scholar
Chait, B. T., Cadene, M., Olinares, P. D., Rout, M. P. & Shi, Y. (2016). Revealing higher order protein structure using mass spectrometry. Journal of the American Society for Mass Spectrometry 27, 952965.CrossRefGoogle ScholarPubMed
Chorev, D. S., Ben-Nissan, G. & Sharon, M. (2015). Exposing the subunit diversity and modularity of protein complexes by structural mass spectrometry approaches. Proteomics 15, 27772791.CrossRefGoogle ScholarPubMed
Chu-Ping, M., Slaughter, C. A. & Demartino, G. N. (1992). Purification and characterization of a protein inhibitor of the 20S proteasome (macropain). Biochimica et Biophysica Acta 1119, 303311.CrossRefGoogle ScholarPubMed
Cooks, R. G., Terwilliger, D. T., Ast, T., Beynon, J. H. & Keough, T. (1975). Surface modified mass spectrometry. Journal of the American Chemical Society 97, 15831585.Google Scholar
Dayon, L., Hainard, A., Licker, V., Turck, N., Kuhn, K., Hochstrasser, D. F., Burkhard, P. R. & Sanchez, J.-C. (2008). Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-Plex isobaric tags. Analytical Chemistry 80, 29212931.Google Scholar
Dick, T. P., Nussbaum, A. K., Deeg, M., Heinemeyer, W., Groll, M., Schirle, M., Keilholz, W., Stevanović, S., Wolf, D. H., Huber, R., Rammensee, H.-G. & Schild, H. (1998). Contribution of proteasomal β-subunits to the cleavage of peptide substrates analyzed with yeast mutants. Journal of Biological Chemistry 273, 2563725646.CrossRefGoogle Scholar
Domon, B. & Aebersold, R. (2006). Mass spectrometry and protein analysis. Science 312, 212217.Google Scholar
Fabre, B., Lambour, T., Bouyssié, D., Menneteau, T., Monsarrat, B., Burlet-Schiltz, O. & Bousquet-Dubouch, M.-P. (2014a). Comparison of label-free quantification methods for the determination of protein complexes subunits stoichiometry. EuPA Open Proteomics 4, 8286.CrossRefGoogle Scholar
Fabre, B., Lambour, T., Delobel, J., Amalric, F., Monsarrat, B., Burlet-Schiltz, O. & Bousquet-Dubouch, M.-P. (2013). Subcellular distribution and dynamics of active proteasome complexes unraveled by a workflow combining in vivo complex cross-linking and quantitative proteomics. Molecular & Cellular Proteomics 12, 687699.Google Scholar
Fabre, B., Lambour, T., Garrigues, L., Amalric, F., Vigneron, N., Menneteau, T., Stella, A., Monsarrat, B., Van Den Eynde, B., Burlet-Schiltz, O. & Bousquet-Dubouch, M. P. (2015). Deciphering preferential interactions within supramolecular protein complexes: the proteasome case. Molecular Systems Biology 11, 771771.Google Scholar
Fabre, B., Lambour, T., Garrigues, L., Ducoux-Petit, M., Amalric, F., Monsarrat, B., Burlet-Schiltz, O. & Bousquet-Dubouch, M.-P. (2014b). Label-free quantitative proteomics reveals the dynamics of proteasome complexes composition and stoichiometry in a wide range of human cell lines. Journal of Proteome Research 13, 30273037.Google Scholar
Fang, S. & Weissman, A. M. (2004). A field guide to ubiquitylation. Cellular and Molecular Life Sciences 61, 15461561.Google Scholar
Fenn, J. B., Mann, M., Meng, C. K., Wong, S. F. & Whitehouse, C. M. (1989). Electrospray ionization for mass spectrometry of large biomolecules. Science 246, 6471.Google Scholar
Finley, D. (2009). Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annual Review of Biochemistry 78, 477513.Google Scholar
Finley, D., Chen, X. & Walters, K. J. (2016). Gates, channels, and switches: elements of the proteasome machine. Trends in Biochemical Sciences 41, 7793.Google Scholar
Finley, D., Ulrich, H. D., Sommer, T. & Kaiser, P. (2012). The ubiquitin-proteasome system of Saccharomyces cerevisiae. Genetics 192, 319360.Google Scholar
Funakoshi, M., Tomko, R. J. Jr., Kobayashi, H. & Hochstrasser, M. (2009). Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 137, 887899.Google Scholar
Gaskell, S. J. (1997). Electrospray: principles and practice. Journal of Mass Spectrometry 32, 677688.Google Scholar
Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W. & Gygi, S. P. (2003). Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proceedings of the National Academy of Sciences 100, 69406945.Google Scholar
Gillet, L. C., Leitner, A. & Aebersold, R. (2016). Mass spectrometry applied to bottom-up proteomics: entering the high-throughput era for hypothesis testing. Annual Review of Analytical Chemistry 9, 449472.Google Scholar
Glickman, M. H. & Ciechanover, A. (2002). The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiological Reviews 82, 373428.Google Scholar
Goldberg, A. L. (2003). Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895899.Google Scholar
Grice, G. L., Lobb, I. T., Weekes, M. P., Gygi, S. P., Antrobus, R. & Nathan, J. A. (2015). The proteasome distinguishes between heterotypic and homotypic lysine-11-linked polyubiquitin chains. Cell Reports 12, 545553.CrossRefGoogle ScholarPubMed
Groll, M., Ditzel, L., Löwe, J., Stock, D., Bochtler, M., Bartunik, H. D. & Huber, R. (1997). Structure of 20S proteasome from yeast at 2·4 Å resolution. Nature 386, 463471.Google Scholar
Guillaume, B., Chapiro, J., Stroobant, V., Colau, D., Van Holle, B., Parvizi, G., Bousquet-Dubouch, M.-P., Théate, I., Parmentier, N. & Van Den Eynde, B. J. (2010). Two abundant proteasome subtypes that uniquely process some antigens presented by HLA class I molecules. Proceedings of the National Academy of Sciences 107, 1859918604.Google Scholar
Heck, A. J. R. (2008). Native mass spectrometry: a bridge between interactomics and structural biology. Nature Methods 5, 927933.Google Scholar
Hendil, K. B., Kriegenburg, F., Tanaka, K., Murata, S., Lauridsen, A.-M. B., Johnsen, A. H. & Hartmann-Petersen, R. (2009). The 20S proteasome as an assembly platform for the 19S regulatory complex. Journal of Molecular Biology 394, 320328.Google Scholar
Hwang, J., Winkler, L. & Kalejta, R. F. (2011). Ubiquitin-independent proteasomal degradation during oncogenic viral infections. Biochimica et Biophysica Acta 1816, 147157.Google Scholar
Isasa, M., Rose, C. M., Elsasser, S., Navarrete-Perea, J., Paulo, J. A., Finley, D. J. & Gygi, S. P. (2015). Multiplexed, proteome-wide protein expression profiling: yeast deubiquitylating enzyme knockout strains. Journal of Proteome Research 14, 53065317.Google Scholar
Juraschek, R., Dülcks, T. & Karas, M. (1999). Nanoelectrospray—More than just a minimized-flow electrospray ionization source. Journal of the American Society for Mass Spectrometry 10, 300308.CrossRefGoogle ScholarPubMed
Kaneko, T., Hamazaki, J., Iemura, S.-I., Sasaki, K., Furuyama, K., Natsume, T., Tanaka, K. & Murata, S. (2009). Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137, 914925.CrossRefGoogle ScholarPubMed
Karas, M. & Hillenkamp, F. (1988). Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Analytical Chemistry 60, 23012303.Google Scholar
Kao, A., Chiu, C.-L., Vellucci, D., Yang, Y., Patel, V. R., Guan, S., Randall, A., Baldi, P., Rychnovsky, S. D. & Huang, L. (2011). Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes. Molecular & Cellular Proteomics 10, M110·002212.CrossRefGoogle ScholarPubMed
Kao, A., Randall, A., Yang, Y., Patel, V. R., Kandur, W., Guan, S., Rychnovsky, S. D., Baldi, P. & Huang, L. (2012). Mapping the structural topology of the yeast 19S proteasomal regulatory particle using chemical cross-linking and probabilistic modeling. Molecular & Cellular Proteomics 11, 15661577.Google Scholar
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. & Gygi, S. P. (2011). Systematic and quantitative assessment of the ubiquitin-modified proteome. Molecular Cell 44, 325340.Google Scholar
Kirkpatrick, D. S., Gerber, S. A. & Gygi, S. P. (2005). The absolute quantification strategy: a general procedure for the quantification of proteins and post-translational modifications. Methods 35, 265273.Google Scholar
Kirkpatrick, D. S., Hathaway, N. A., Hanna, J., Elsasser, S., Rush, J., Finley, D., King, R. W. & Gygi, S. P. (2006). Quantitative analysis of in vitro ubiquitinated cyclin B1 reveals complex chain topology. Nature Cell Biology 8, 700710.CrossRefGoogle ScholarPubMed
Konijnenberg, A., Butterer, A. & Sobott, F. (2013). Native ion mobility-mass spectrometry and related methods in structural biology. Biochimica et Biophysica Acta 1834, 1239.Google Scholar
Kostova, Z. & Wolf, D. H. (2003). For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin–proteasome connection. EMBO Journal 22, 23092317.CrossRefGoogle ScholarPubMed
Krüger, E. & Kloetzel, P.-M. (2012). Immunoproteasomes at the interface of innate and adaptive immune responses: two faces of one enzyme. Current Opinion in Immunology 24, 7783.CrossRefGoogle ScholarPubMed
Kunjappu, M. J. & Hochstrasser, M. (2014). Assembly of the 20S proteasome. Biochimica et Biophysica Acta 1843, 212.Google Scholar
Lander, G. C., Estrin, E., Matyskiela, M. E., Bashore, C., Nogales, E. & Martin, A. (2012). Complete subunit architecture of the proteasome regulatory particle. Nature 482, 186191.CrossRefGoogle ScholarPubMed
Lasker, K., Förster, F., Bohn, S., Walzthoeni, T., Villa, E., Unverdorben, P., Beck, F., Aebersold, R., Sali, A. & Baumeister, W. (2012). Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proceedings of the National Academy of Sciences 109, 13801387.Google Scholar
Leitner, A., Faini, M., Stengel, F. & Aebersold, R. (2016). Crosslinking and mass spectrometry: an integrated technology to understand the structure and function of molecular machines. Trends in Biochemical Sciences 41, 2032.Google Scholar
Leitner, A., Joachimiak, L. A., Unverdorben, P., Walzthoeni, T., Frydman, J., Förster, F. & Aebersold, R. (2014). Chemical cross-linking/mass spectrometry targeting acidic residues in proteins and protein complexes. Proceedings of the National Academy of Sciences 111, 94559460.Google Scholar
Leitner, A., Walzthoeni, T., Walzthoeni, T., Kahraman, A., Herzog, F., Kahraman, A., Rinner, O., Herzog, F., Beck, M. & Aebersold, R. (2010). Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics. Molecular & Cellular Proteomics 9, 16341649.Google Scholar
Loo, J. A. (1997). Studying noncovalent protein complexes by electrospray ionization mass spectrometry. Mass Spectrometry Reviews 16, 123.Google Scholar
Lowe, J., Stock, D., Jap, B., Zwickl, P., Baumeister, W. & Huber, R. (1995). Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3·4 Å resolution. Science 268, 533539.Google Scholar
Luan, B., Huang, X., Wu, J., Mei, Z., Wang, Y., Xue, X., Yan, C., Wang, J., Finley, D. J., Shi, Y. & Wang, F. (2016). Structure of an endogenous yeast 26S proteasome reveals two major conformational states. Proceedings of the National Academy of Sciences 113, 26422647.CrossRefGoogle ScholarPubMed
Mehmood, S., Allison, T. M. & Robinson, C. V. (2015). Mass spectrometry of protein complexes: from origins to applications. Annual Review of Physical Chemistry 66, 453474.Google Scholar
Moscovitz, O., Ben-Nissan, G., Fainer, I., Pollack, D., Mizrachi, L. & Sharon, M. (2015). The Parkinson's-associated protein DJ-1 regulates the 20S proteasome. Nature Communications 6, 6609 1–13.Google Scholar
Moscovitz, O., Tsvetkov, P., Hazan, N., Michaelevski, I., Keisar, H., Ben-Nissan, G., Shaul, Y. & Sharon, M. (2012). A mutually inhibitory feedback loop between the 20S proteasome and its regulator, NQO1. Molecular Cell 47, 7686.Google Scholar
Park, S., Roelofs, J., Kim, W., Robert, J., Schmidt, M., Gygi, S. P. & Finley, D. (2009). Hexameric assembly of the proteasomal ATPases is templated through their C termini. Nature 459, 866870.CrossRefGoogle ScholarPubMed
Peters, J.-M. (2002). The anaphase-promoting complex: proteolysis in mitosis and beyond. Molecular Cell 9, 931943.CrossRefGoogle ScholarPubMed
Pickart, C. M. & Fushman, D. (2004). Polyubiquitin chains: polymeric protein signals. Current Opinion in Chemical Biology 8, 610616.Google Scholar
Pickering, A. M. & Davies, K. J. A. (2012). Degradation of damaged proteins: the main function of the 20S proteasome. Progress in Molecular Biology and Translational Science 109, 227248.CrossRefGoogle Scholar
Rappsilber, J. (2011). The beginning of a beautiful friendship: cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. Journal of Structural Biology 173, 530540.Google Scholar
Rappsilber, J., Siniossoglou, S., Hurt, E. C. & Mann, M. (2000). A generic strategy to analyze the spatial organization of multi-protein complexes by cross-linking and mass spectrometry. Analytical Chemistry 72, 267275.Google Scholar
Reyes-Turcu, F. E., Ventii, K. H. & Wilkinson, K. D. (2009). Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annual review of Biochemistry 78, 363397.Google Scholar
Roelofs, J., Park, S., Haas, W., Tian, G., Mcallister, F. E., Huo, Y., Lee, B.-H., Zhang, F., Shi, Y., Gygi, S. P. & Finley, D. (2009). Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459, 861865.Google Scholar
Rose, R. J., Damoc, E., Denisov, E., Makarov, A. & Heck, A. J. R. (2012). High-sensitivity Orbitrap mass analysis of intact macromolecular assemblies. Nature Methods 9, 10841086.Google Scholar
Saeki, Y., Toh-E, A., Kudo, T., Kawamura, H. & Tanaka, K. (2009). Multiple proteasome-interacting proteins assist the assembly of the yeast 19S regulatory particle. Cell 137, 900913.Google Scholar
Sakata, E., Stengel, F., Fukunaga, K., Zhou, M., Saeki, Y., Förster, F., Baumeister, W., Tanaka, K. & Robinson, C. V. (2011). The catalytic activity of Ubp6 enhances maturation of the proteasomal regulatory particle. Molecular Cell 42, 637649.Google Scholar
Schmidt, M., Haas, W., Crosas, B., Santamaria, P. G., Gygi, S. P., Walz, T. & Finley, D. (2005). The HEAT repeat protein Blm10 regulates the yeast proteasome by capping the core particle. Nature Structural & Molecular Biology 12, 294303.Google Scholar
Schwartz, A. L. & Ciechanover, A. (2009). Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annual Review of Pharmacology and Toxicology 49, 7396.Google Scholar
Seifert, U., Bialy, L. P., Ebstein, F., Bech-Otschir, D., Voigt, A., Schröter, F., Prozorovski, T., Lange, N., Steffen, J., Rieger, M., Kuckelkorn, U., Aktas, O., Kloetzel, P.-M. & Krüger, E. (2010). Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 142, 613624.Google Scholar
Sharon, M. (2013). Structural MS pulls its weight. Science 340, 10591060.Google Scholar
Sharon, M. & Robinson, C. V. (2007). The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annual Review of Biochemistry 76, 167193.Google Scholar
Sharon, M., Taverner, T., Ambroggio, X. I., Deshaies, R. J. & Robinson, C. V. (2006). Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biology 4, 13141323.Google Scholar
Shibatani, T., Carlson, E. J., Larabee, F., Mccormack, A. L., Früh, K. & Skach, W. R. (2006). Global organization and function of mammalian cytosolic proteasome pools: implications for PA28 and 19S regulatory complexes. Molecular Biology of the Cell 17, 49624971.Google Scholar
Silva, J. C., Gorenstein, M. V., Li, G.-Z., Vissers, J. P. C. & Geromanos, S. J. (2006). Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Molecular & Cellular Proteomics 5, 144156.Google Scholar
Sinz, A., Sharon, M., Chorev, D. & Arlt, C. (2015). Chemical cross-linking and native mass spectrometry: a fruitful combination for structural biology. Protein Science 24, 11931209.Google Scholar
Snijder, J. & Heck, A. J. R. (2014). Analytical approaches for size and mass analysis of large protein assemblies. Annual Review of Analytical Chemistry 7, 4364.Google Scholar
Stefl, S., Nishi, H., Petukh, M., Panchenko, A. R. & Alexov, E. (2013). Molecular mechanisms of disease-causing missense mutations. Journal of Molecular Biology 425, 39193936.Google Scholar
Sutherland, B. W., Toews, J. & Kast, J. (2008). Utility of formaldehyde cross-linking and mass spectrometry in the study of protein–protein interactions. Journal of Mass Spectrometry 43, 699715.Google Scholar
Syka, J. E. P., Coon, J. J., Schroeder, M. J., Shabanowitz, J. & Hunt, D. F. (2004). Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proceedings of the National Academy of Sciences 101, 95289533.CrossRefGoogle ScholarPubMed
Tomko, R. J., Funakoshi, M., Schneider, K., Wang, J. & Hochstrasser, M. (2010). Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: implications for proteasome structure and assembly. Molecular Cell 38, 393403.CrossRefGoogle ScholarPubMed
Tomko, R. J. & Hochstrasser, M. (2011). Incorporation of the Rpn12 subunit couples completion of proteasome regulatory particle lid assembly to lid-base joining. Molecular Cell 44, 907917.Google Scholar
Tomko, R. J., Taylor, D. W., Chen, Z. A., Wang, H.-W., Rappsilber, J. & Hochstrasser, M. (2015). A single α helix drives extensive remodeling of the proteasome lid and completion of regulatory particle assembly. Cell 163, 432444.Google Scholar
Unno, M., Mizushima, T., Morimoto, Y., Tomisugi, Y., Tanaka, K., Yasuoka, N. & Tsukihara, T. (2002). The structure of the mammalian 20S proteasome at 2·75 Å resolution. Structure 10, 609618.Google Scholar
Ustrell, V., Hoffman, L., Pratt, G. & Rechsteiner, M. (2002). PA200, a nuclear proteasome activator involved in DNA repair. EMBO Journal 21, 35163525.Google Scholar
Vandermarliere, E., Mueller, M. & Martens, L. (2013). Getting intimate with trypsin, the leading protease in proteomics. Mass Spectrometry Reviews 32, 453465.CrossRefGoogle ScholarPubMed
Verma, R., Aravind, L., Oania, R., Mcdonald, W. H., Yates, J. R., Koonin, E. V., Deshaies, R. J. (2002). Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611615.Google Scholar
Verma, R., Oania, R., Graumann, J. & Deshaies, R. J. (2004). Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118, 99110.Google Scholar
Wilm, M. & Mann, M. (1996). Analytical properties of the nanoelectrospray ion source. Analytical Chemistry 68, 18.Google Scholar
Xu, P., Duong, D. M., Seyfried, N. T., Cheng, D., Xie, Y., Robert, J., Rush, J., Hochstrasser, M., Finley, D. & Peng, J. (2009). Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137, 133145.Google Scholar
Yu, C., Yang, Y., Wang, X., Guan, S., Fang, L., Liu, F., Walters, K. J., Kaiser, P. & Huang, L. (2016). Characterization of dynamic UbR-proteasome subcomplexes by in vivo cross-linking (X) assisted bimolecular tandem affinity purification (XBAP) and label-free quantitation. Molecular & Cellular Proteomics 15, 22792292.Google Scholar
Yu, Z., Livnat-Levanon, N., Kleifeld, O., Mansour, W., Nakasone, M. A., Castañeda, C. A., Dixon, E. K., Fushman, D., Reis, N., Pick, E. & Glickman, M. H. (2015). Base-CP proteasome can serve as a platform for stepwise lid formation. Bioscience Reports 35, 114.Google Scholar
Zenobi, R. & Knochenmuss, R. (1998). Ion formation in MALDI mass spectrometry. Mass Spectrometry Reviews 17, 337366.Google Scholar
Zhou, M. & Wysocki, V. H. (2014). Surface induced dissociation: dissecting noncovalent protein complexes in the gas phase. Accounts of Chemical Research 47, 10101018.CrossRefGoogle ScholarPubMed
Zubarev, R. A. & Kelleher, N. L. (1998). Electron capture dissociation of multiply charged protein cations. A nonergodic process. Journal of the American Chemical Society 120, 32653266.Google Scholar