{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T16:34:21Z","timestamp":1790440461398,"version":"4.1.0"},"reference-count":70,"publisher":"National Academy of Sciences","issue":"8","license":[{"start":{"date-parts":[[2020,2,11]],"date-time":"2020-02-11T00:00:00Z","timestamp":1581379200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2020,2,25]]},"abstract":"<jats:p>Mammalian cells present a fingerprint of their proteome to the adaptive immune system through the display of endogenous peptides on MHC-I complexes. MHC-I\u2212bound peptides originate from protein degradation by the proteasome, suggesting that stably folded, long-lived proteins could evade monitoring. Here, we investigate the role in antigen presentation of the ribosome-associated quality control (RQC) pathway for the degradation of nascent polypeptides that are encoded by defective messenger RNAs and undergo stalling at the ribosome during translation. We find that degradation of model proteins by RQC results in efficient MHC-I presentation, independent of their intrinsic folding properties. Quantitative profiling of MHC-I peptides in wild-type and RQC-deficient cells by mass spectrometry showed that RQC substantially contributes to the composition of the immunopeptidome. Our results also identify endogenous substrates of the RQC pathway in human cells and provide insight into common principles causing ribosome stalling under physiological conditions.<\/jats:p>","DOI":"10.1073\/pnas.1914401117","type":"journal-article","created":{"date-parts":[[2020,2,11]],"date-time":"2020-02-11T16:54:22Z","timestamp":1581440062000},"page":"4099-4108","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":43,"title":["Role for ribosome-associated quality control in sampling proteins for MHC class I-mediated antigen presentation"],"prefix":"10.1073","volume":"117","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2541-4707","authenticated-orcid":false,"given":"D\u00e9bora Broch","family":"Trentini","sequence":"first","affiliation":[{"name":"Department of Cellular Biochemistry, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matteo","family":"Pecoraro","sequence":"additional","affiliation":[{"name":"Department of Proteomics and Signal Transduction, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shivani","family":"Tiwary","sequence":"additional","affiliation":[{"name":"Computational Systems Biochemistry Research Group, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00fcrgen","family":"Cox","sequence":"additional","affiliation":[{"name":"Computational Systems Biochemistry Research Group, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany;"},{"name":"Department of Biological and Medical Psychology, University of Bergen, 5009 Bergen, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthias","family":"Mann","sequence":"additional","affiliation":[{"name":"Department of Proteomics and Signal Transduction, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0497-3016","authenticated-orcid":false,"given":"Mark S.","family":"Hipp","sequence":"additional","affiliation":[{"name":"Department of Cellular Biochemistry, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"F. Ulrich","family":"Hartl","sequence":"additional","affiliation":[{"name":"Department of Cellular Biochemistry, Max Planck Institute of Biochemistry, 82152 Martinsried, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2020,2,11]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1146\/annurev.immunol.17.1.739","article-title":"Degradation of cell proteins and the generation of MHC class I-presented peptides","volume":"17","author":"Rock K. L.","year":"1999","unstructured":"K. L. Rock, A. L. Goldberg, Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 17, 739\u2013779 (1999).","journal-title":"Annu. Rev. Immunol."},{"key":"e_1_3_4_2_2","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1016\/S0092-8674(94)90462-6","article-title":"Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules","volume":"78","author":"Rock K. L.","year":"1994","unstructured":"K. L. Rock ., Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78, 761\u2013771 (1994).","journal-title":"Cell"},{"key":"e_1_3_4_3_2","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/j.biocel.2016.07.019","article-title":"The ubiquitin-proteasome system and autophagy: Coordinated and independent activities","volume":"79","author":"Cohen-Kaplan V.","year":"2016","unstructured":"V. Cohen-Kaplan, I. Livneh, N. Avni, C. Cohen-Rosenzweig, A. Ciechanover, The ubiquitin-proteasome system and autophagy: Coordinated and independent activities. Int. J. Biochem. Cell Biol. 79, 403\u2013418 (2016).","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"e_1_3_4_4_2","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1146\/annurev-biochem-061516-044859","article-title":"The ubiquitin system, autophagy, and regulated protein degradation","volume":"86","author":"Varshavsky A.","year":"2017","unstructured":"A. Varshavsky, The ubiquitin system, autophagy, and regulated protein degradation. Annu. Rev. Biochem. 86, 123\u2013128 (2017).","journal-title":"Annu. Rev. Biochem."},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1084\/jem.175.1.163","article-title":"RMA\/S cells present endogenously synthesized cytosolic proteins to class I-restricted cytotoxic T lymphocytes","volume":"175","author":"Esquivel F.","year":"1992","unstructured":"F. Esquivel, J. Yewdell, J. Bennink, RMA\/S cells present endogenously synthesized cytosolic proteins to class I-restricted cytotoxic T lymphocytes. J. Exp. Med. 175, 163\u2013168 (1992).","journal-title":"J. Exp. Med."},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/j.it.2011.08.001","article-title":"DRiPs solidify: Progress in understanding endogenous MHC class I antigen processing","volume":"32","author":"Yewdell J. W.","year":"2011","unstructured":"J. W. Yewdell, DRiPs solidify: Progress in understanding endogenous MHC class I antigen processing. Trends Immunol. 32, 548\u2013558 (2011).","journal-title":"Trends Immunol."},{"key":"e_1_3_4_7_2","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.4049\/jimmunol.157.5.1823","article-title":"Defective ribosomal products (DRiPs): A major source of antigenic peptides for MHC class I molecules?","volume":"157","author":"Yewdell J. W.","year":"1996","unstructured":"J. W. Yewdell, L. C. Ant\u00f3n, J. R. Bennink, Defective ribosomal products (DRiPs): A major source of antigenic peptides for MHC class I molecules? J. Immunol. 157, 1823\u20131826 (1996).","journal-title":"J. Immunol."},{"key":"e_1_3_4_8_2","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/S0161-5890(02)00097-4","article-title":"To DRiP or not to DRiP: Generating peptide ligands for MHC class I molecules from biosynthesized proteins","volume":"39","author":"Yewdell J.","year":"2002","unstructured":"J. Yewdell, To DRiP or not to DRiP: Generating peptide ligands for MHC class I molecules from biosynthesized proteins. Mol. Immunol. 39, 139\u2013146 (2002).","journal-title":"Mol. Immunol."},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1038\/35008096","article-title":"Rapid degradation of a large fraction of newly synthesized proteins by proteasomes","volume":"404","author":"Schubert U.","year":"2000","unstructured":"U. Schubert ., Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404, 770\u2013774 (2000).","journal-title":"Nature"},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"1960","DOI":"10.1126\/science.1121925","article-title":"Protein synthesis upon acute nutrient restriction relies on proteasome function","volume":"310","author":"Vabulas R. M.","year":"2005","unstructured":"R. M. Vabulas, F. U. Hartl, Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310, 1960\u20131963 (2005).","journal-title":"Science"},{"key":"e_1_3_4_11_2","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.it.2014.01.002","article-title":"Re-examining class-I presentation and the DRiP hypothesis","volume":"35","author":"Rock K. L.","year":"2014","unstructured":"K. L. Rock, D. J. Farf\u00e1n-Arribas, J. D. Colbert, A. L. Goldberg, Re-examining class-I presentation and the DRiP hypothesis. Trends Immunol. 35, 144\u2013152 (2014).","journal-title":"Trends Immunol."},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1189\/jlb.1113599","article-title":"Translating DRiPs: MHC class I immunosurveillance of pathogens and tumors","volume":"95","author":"Ant\u00f3n L. C.","year":"2014","unstructured":"L. C. Ant\u00f3n, J. W. Yewdell, Translating DRiPs: MHC class I immunosurveillance of pathogens and tumors. J. Leukoc. Biol. 95, 551\u2013562 (2014).","journal-title":"J. Leukoc. Biol."},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/j.molcel.2013.03.010","article-title":"Principles of cotranslational ubiquitination and quality control at the ribosome","volume":"50","author":"Duttler S.","year":"2013","unstructured":"S. Duttler, S. Pechmann, J. Frydman, Principles of cotranslational ubiquitination and quality control at the ribosome. Mol. Cell 50, 379\u2013393 (2013).","journal-title":"Mol. Cell"},{"key":"e_1_3_4_14_2","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.1007\/s00018-011-0656-z","article-title":"Translating DRiPs: Progress in understanding viral and cellular sources of MHC class I peptide ligands","volume":"68","author":"Dolan B. P.","year":"2011","unstructured":"B. P. Dolan, J. R. Bennink, J. W. Yewdell, Translating DRiPs: Progress in understanding viral and cellular sources of MHC class I peptide ligands. Cell. Mol. Life Sci. 68, 1481\u20131489 (2011).","journal-title":"Cell. Mol. Life Sci."},{"key":"e_1_3_4_15_2","doi-asserted-by":"crossref","first-page":"227","DOI":"10.4049\/jimmunol.177.1.227","article-title":"Tight linkage between translation and MHC class I peptide ligand generation implies specialized antigen processing for defective ribosomal products","volume":"177","author":"Qian S.-B.","year":"2006","unstructured":"S.-B. Qian ., Tight linkage between translation and MHC class I peptide ligand generation implies specialized antigen processing for defective ribosomal products. J. Immunol. 177, 227\u2013233 (2006).","journal-title":"J. Immunol."},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"2065","DOI":"10.4049\/jimmunol.1003096","article-title":"Distinct pathways generate peptides from defective ribosomal products for CD8+ T cell immunosurveillance","volume":"186","author":"Dolan B. P.","year":"2011","unstructured":"B. P. Dolan ., Distinct pathways generate peptides from defective ribosomal products for CD8+ T cell immunosurveillance. J. Immunol. 186, 2065\u20132072 (2011).","journal-title":"J. Immunol."},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"3167","DOI":"10.1002\/eji.201242627","article-title":"Mature proteins derived from Epstein-Barr virus fail to feed into the MHC class I antigenic pool","volume":"42","author":"Fiebiger B. M.","year":"2012","unstructured":"B. M. Fiebiger, A. Moosmann, U. Behrends, J. Mautner, Mature proteins derived from Epstein-Barr virus fail to feed into the MHC class I antigenic pool. Eur. J. Immunol. 42, 3167\u20133173 (2012).","journal-title":"Eur. J. Immunol."},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"4801","DOI":"10.4049\/jimmunol.167.9.4801","article-title":"Cutting edge: Neosynthesis is required for the presentation of a T cell epitope from a long-lived viral protein","volume":"167","author":"Khan S.","year":"2001","unstructured":"S. Khan ., Cutting edge: Neosynthesis is required for the presentation of a T cell epitope from a long-lived viral protein. J. Immunol. 167, 4801\u20134804 (2001).","journal-title":"J. Immunol."},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"5410","DOI":"10.4049\/jimmunol.1300078","article-title":"Substrate-induced protein stabilization reveals a predominant contribution from mature proteins to peptides presented on MHC class I","volume":"191","author":"Colbert J. D.","year":"2013","unstructured":"J. D. Colbert, D. J. Farf\u00e1n-Arribas, K. L. Rock, Substrate-induced protein stabilization reveals a predominant contribution from mature proteins to peptides presented on MHC class I. J. Immunol. 191, 5410\u20135419 (2013).","journal-title":"J. Immunol."},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","first-page":"16998","DOI":"10.1073\/pnas.1210271109","article-title":"Using intein catalysis to probe the origin of major histocompatibility complex class I-presented peptides","volume":"109","author":"Farf\u00e1n-Arribas D. J.","year":"2012","unstructured":"D. J. Farf\u00e1n-Arribas, L. J. Stern, K. L. Rock, Using intein catalysis to probe the origin of major histocompatibility complex class I-presented peptides. Proc. Natl. Acad. Sci. U.S.A. 109, 16998\u201317003 (2012).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.1016\/j.cell.2012.10.044","article-title":"A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress","volume":"151","author":"Brandman O.","year":"2012","unstructured":"O. Brandman ., A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 151, 1042\u20131054 (2012).","journal-title":"Cell"},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1038\/nsmb.3147","article-title":"Ribosome-associated protein quality control","volume":"23","author":"Brandman O.","year":"2016","unstructured":"O. Brandman, R. S. Hegde, Ribosome-associated protein quality control. Nat. Struct. Mol. Biol. 23, 7\u201315 (2016).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"2097","DOI":"10.1073\/pnas.0812819106","article-title":"A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration","volume":"106","author":"Chu J.","year":"2009","unstructured":"J. Chu ., A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 106, 2097\u20132103 (2009).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_24_2","doi-asserted-by":"crossref","first-page":"5046","DOI":"10.1073\/pnas.1221724110","article-title":"Cdc48-associated complex bound to 60S particles is required for the clearance of aberrant translation products","volume":"110","author":"Defenouill\u00e8re Q.","year":"2013","unstructured":"Q. Defenouill\u00e8re ., Cdc48-associated complex bound to 60S particles is required for the clearance of aberrant translation products. Proc. Natl. Acad. Sci. U.S.A. 110, 5046\u20135051 (2013).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_25_2","doi-asserted-by":"crossref","first-page":"15981","DOI":"10.1073\/pnas.1413882111","article-title":"Structural basis for translational surveillance by the large ribosomal subunit-associated protein quality control complex","volume":"111","author":"Lyumkis D.","year":"2014","unstructured":"D. Lyumkis ., Structural basis for translational surveillance by the large ribosomal subunit-associated protein quality control complex. Proc. Natl. Acad. Sci. U.S.A. 111, 15981\u201315986 (2014).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_26_2","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1038\/nature09371","article-title":"Role of a ribosome-associated E3 ubiquitin ligase in protein quality control","volume":"467","author":"Bengtson M. H.","year":"2010","unstructured":"M. H. Bengtson, C. A. P. Joazeiro, Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467, 470\u2013473 (2010).","journal-title":"Nature"},{"key":"e_1_3_4_27_2","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1126\/science.aam7787","article-title":"CAT-tailing as a fail-safe mechanism for efficient degradation of stalled nascent polypeptides","volume":"357","author":"Kostova K. K.","year":"2017","unstructured":"K. K. Kostova ., CAT-tailing as a fail-safe mechanism for efficient degradation of stalled nascent polypeptides. Science 357, 414\u2013417 (2017).","journal-title":"Science"},{"key":"e_1_3_4_28_2","doi-asserted-by":"crossref","first-page":"2258","DOI":"10.1126\/science.1067338","article-title":"An mRNA surveillance mechanism that eliminates transcripts lacking termination codons","volume":"295","author":"Frischmeyer P. A.","year":"2002","unstructured":"P. A. Frischmeyer ., An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295, 2258\u20132261 (2002).","journal-title":"Science"},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1038\/nature04530","article-title":"Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation","volume":"440","author":"Doma M. K.","year":"2006","unstructured":"M. K. Doma, R. Parker, Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440, 561\u2013564 (2006).","journal-title":"Nature"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1016\/j.chembiol.2014.08.011","article-title":"Chemical biology strategies for posttranslational control of protein function","volume":"21","author":"Rakhit R.","year":"2014","unstructured":"R. Rakhit, R. Navarro, T. J. Wandless, Chemical biology strategies for posttranslational control of protein function. Chem. Biol. 21, 1238\u20131252 (2014).","journal-title":"Chem. Biol."},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"31328","DOI":"10.1074\/jbc.M111.264101","article-title":"Ligand-switchable substrates for a ubiquitin-proteasome system","volume":"286","author":"Egeler E. L.","year":"2011","unstructured":"E. L. Egeler, L. M. Urner, R. Rakhit, C. W. Liu, T. J. Wandless, Ligand-switchable substrates for a ubiquitin-proteasome system. J. Biol. Chem. 286, 31328\u201331336 (2011).","journal-title":"J. Biol. Chem."},{"key":"e_1_3_4_32_2","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1016\/j.cell.2006.07.025","article-title":"A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules","volume":"126","author":"Banaszynski L. A.","year":"2006","unstructured":"L. A. Banaszynski, L. C. Chen, L. A. Maynard-Smith, A. G. L. Ooi, T. J. Wandless, A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell 126, 995\u20131004 (2006).","journal-title":"Cell"},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1016\/j.chembiol.2010.07.009","article-title":"A general chemical method to regulate protein stability in the mammalian central nervous system","volume":"17","author":"Iwamoto M.","year":"2010","unstructured":"M. Iwamoto, T. Bj\u00f6rklund, C. Lundberg, D. Kirik, T. J. Wandless, A general chemical method to regulate protein stability in the mammalian central nervous system. Chem. Biol. 17, 981\u2013988 (2010).","journal-title":"Chem. Biol."},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1016\/S1074-7613(00)80447-1","article-title":"Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody","volume":"6","author":"Porgador A.","year":"1997","unstructured":"A. Porgador, J. W. Yewdell, Y. Deng, J. R. Bennink, R. N. Germain, Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6, 715\u2013726 (1997).","journal-title":"Immunity"},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"e1500154","DOI":"10.1126\/sciadv.1500154","article-title":"Translational control by lysine-encoding A-rich sequences","volume":"1","author":"Arthur L.","year":"2015","unstructured":"L. Arthur ., Translational control by lysine-encoding A-rich sequences. Sci. Adv. 1, e1500154 (2015).","journal-title":"Sci. Adv."},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1016\/j.molcel.2016.11.039","article-title":"Initiation of quality control during poly(A) translation requires site-specific ribosome ubiquitination","volume":"65","author":"Juszkiewicz S.","year":"2017","unstructured":"S. Juszkiewicz, R. S. Hegde, Initiation of quality control during poly(A) translation requires site-specific ribosome ubiquitination. Mol. Cell 65, 743\u2013750.e4 (2017).","journal-title":"Mol. Cell"},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1038\/ni860","article-title":"The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues","volume":"3","author":"York I. A.","year":"2002","unstructured":"I. A. York ., The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat. Immunol. 3, 1177\u20131184 (2002).","journal-title":"Nat. Immunol."},{"key":"e_1_3_4_38_2","doi-asserted-by":"crossref","first-page":"14189","DOI":"10.1074\/jbc.M413660200","article-title":"Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition","volume":"280","author":"Jiang H. Y.","year":"2005","unstructured":"H. Y. Jiang, R. C. Wek, Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J. Biol. Chem. 280, 14189\u201314202 (2005).","journal-title":"J. Biol. Chem."},{"key":"e_1_3_4_39_2","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1038\/s41594-019-0230-1","article-title":"CAT tails drive degradation of stalled polypeptides on and off the ribosome","volume":"26","author":"Sitron C. S.","year":"2019","unstructured":"C. S. Sitron, O. Brandman, CAT tails drive degradation of stalled polypeptides on and off the ribosome. Nat. Struct. Mol. Biol. 26, 450\u2013459 (2019).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"e_1_3_4_40_2","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/0022-1759(87)90175-X","article-title":"A simple method to eliminate the antigenicity of surface class I MHC molecules from the membrane of viable cells by acid treatment at pH 3","volume":"100","author":"Sugawara S.","year":"1987","unstructured":"S. Sugawara, T. Abo, K. Kumagai, A simple method to eliminate the antigenicity of surface class I MHC molecules from the membrane of viable cells by acid treatment at pH 3. J. Immunol. Methods 100, 83\u201390 (1987).","journal-title":"J. Immunol. Methods"},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"2262","DOI":"10.1126\/science.1067272","article-title":"Exosome-mediated recognition and degradation of mRNAs lacking a termination codon","volume":"295","author":"van Hoof A.","year":"2002","unstructured":"A. van Hoof, P. A. Frischmeyer, H. C. Dietz, R. Parker, Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295, 2262\u20132264 (2002).","journal-title":"Science"},{"key":"e_1_3_4_42_2","unstructured":"D. B. Trentini . Role for ribosomal quality control in sampling proteins for MHC class I-mediated antigen presentation. ProteomeXchange. http:\/\/www.ebi.ac.uk\/pride\/archive\/projects\/PXD014644. Deposited 17 July 2019."},{"key":"e_1_3_4_43_2","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1016\/j.cell.2016.09.015","article-title":"Kinetic analysis of protein stability reveals age-dependent degradation","volume":"167","author":"McShane E.","year":"2016","unstructured":"E. McShane ., Kinetic analysis of protein stability reveals age-dependent degradation. Cell 167, 803\u2013815.e21 (2016).","journal-title":"Cell"},{"key":"e_1_3_4_44_2","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1016\/j.molcel.2012.03.013","article-title":"Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3\u2032 end of aberrant mRNA","volume":"46","author":"Tsuboi T.","year":"2012","unstructured":"T. Tsuboi ., Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3\u2032 end of aberrant mRNA. Mol. Cell 46, 518\u2013529 (2012).","journal-title":"Mol. Cell"},{"key":"e_1_3_4_45_2","doi-asserted-by":"crossref","first-page":"1208","DOI":"10.1261\/rna.039446.113","article-title":"Translation of CGA codon repeats in yeast involves quality control components and ribosomal protein L1","volume":"19","author":"Letzring D. P.","year":"2013","unstructured":"D. P. Letzring, A. S. Wolf, C. E. Brule, E. J. Grayhack, Translation of CGA codon repeats in yeast involves quality control components and ribosomal protein L1. RNA 19, 1208\u20131217 (2013).","journal-title":"RNA"},{"key":"e_1_3_4_46_2","doi-asserted-by":"crossref","first-page":"28234","DOI":"10.1038\/srep28234","article-title":"Ribosome-associated Asc1\/RACK1 is required for endonucleolytic cleavage induced by stalled ribosome at the 3\u2032 end of nonstop mRNA","volume":"6","author":"Ikeuchi K.","year":"2016","unstructured":"K. Ikeuchi, T. Inada, Ribosome-associated Asc1\/RACK1 is required for endonucleolytic cleavage induced by stalled ribosome at the 3\u2032 end of nonstop mRNA. Sci. Rep. 6, 28234 (2016).","journal-title":"Sci. Rep."},{"key":"e_1_3_4_47_2","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1101\/gad.1490207","article-title":"Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast","volume":"21","author":"Ito-Harashima S.","year":"2007","unstructured":"S. Ito-Harashima, K. Kuroha, T. Tatematsu, T. Inada, Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev. 21, 519\u2013524 (2007).","journal-title":"Genes Dev."},{"key":"e_1_3_4_48_2","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1101\/gr.237826.118","article-title":"A compendium of conserved cleavage and polyadenylation events in mammalian genes","volume":"28","author":"Wang R.","year":"2018","unstructured":"R. Wang, D. Zheng, G. Yehia, B. Tian, A compendium of conserved cleavage and polyadenylation events in mammalian genes. Genome Res. 28, 1427\u20131441 (2018).","journal-title":"Genome Res."},{"key":"e_1_3_4_49_2","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.molcel.2018.08.037","article-title":"ZNF598 is a quality control sensor of collided ribosomes","volume":"72","author":"Juszkiewicz S.","year":"2018","unstructured":"S. Juszkiewicz ., ZNF598 is a quality control sensor of collided ribosomes. Mol. Cell 72, 469\u2013481.e7 (2018).","journal-title":"Mol. Cell"},{"key":"e_1_3_4_50_2","doi-asserted-by":"crossref","first-page":"1507","DOI":"10.1016\/j.cell.2018.10.009","article-title":"EMC is required to initiate accurate membrane protein topogenesis","volume":"175","author":"Chitwood P. J.","year":"2018","unstructured":"P. J. Chitwood, S. Juszkiewicz, A. Guna, S. Shao, R. S. Hegde, EMC is required to initiate accurate membrane protein topogenesis. Cell 175, 1507\u20131519.e16 (2018).","journal-title":"Cell"},{"key":"e_1_3_4_51_2","doi-asserted-by":"crossref","first-page":"e37018","DOI":"10.7554\/eLife.37018","article-title":"The ER membrane protein complex interacts cotranslationally to enable biogenesis of multipass membrane proteins","volume":"7","author":"Shurtleff M. J.","year":"2018","unstructured":"M. J. Shurtleff ., The ER membrane protein complex interacts cotranslationally to enable biogenesis of multipass membrane proteins. eLife 7, e37018 (2018).","journal-title":"eLife"},{"key":"e_1_3_4_52_2","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1126\/science.1257522","article-title":"Targeting and plasticity of mitochondrial proteins revealed by proximity-specific ribosome profiling","volume":"346","author":"Williams C. C.","year":"2014","unstructured":"C. C. Williams, C. H. Jan, J. S. Weissman, Targeting and plasticity of mitochondrial proteins revealed by proximity-specific ribosome profiling. Science 346, 748\u2013751 (2014).","journal-title":"Science"},{"key":"e_1_3_4_53_2","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.sbi.2015.07.013","article-title":"Mitochondrial machineries for insertion of membrane proteins","volume":"33","author":"Bohnert M.","year":"2015","unstructured":"M. Bohnert, N. Pfanner, M. van der Laan, Mitochondrial machineries for insertion of membrane proteins. Curr. Opin. Struct. Biol. 33, 92\u2013102 (2015).","journal-title":"Curr. Opin. Struct. Biol."},{"key":"e_1_3_4_54_2","doi-asserted-by":"crossref","first-page":"W429","DOI":"10.1093\/nar\/gkm256","article-title":"Advantages of combined transmembrane topology and signal peptide prediction\u2014The Phobius web server","volume":"35","author":"K\u00e4ll L.","year":"2007","unstructured":"L. K\u00e4ll, A. Krogh, E. L. L. Sonnhammer , Advantages of combined transmembrane topology and signal peptide prediction\u2014The Phobius web server. Nucleic Acids Res. 35 (suppl. 2), W429\u2013W432 (2007).","journal-title":"Nucleic Acids Res."},{"key":"e_1_3_4_55_2","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1016\/j.jmb.2004.03.016","article-title":"A combined transmembrane topology and signal peptide prediction method","volume":"338","author":"K\u00e4ll L.","year":"2004","unstructured":"L. K\u00e4ll, A. Krogh, E. L. L. Sonnhammer, A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 338, 1027\u20131036 (2004).","journal-title":"J. Mol. Biol."},{"key":"e_1_3_4_56_2","doi-asserted-by":"crossref","first-page":"27999","DOI":"10.1038\/srep27999","article-title":"Solute carrier 41A3 encodes for a mitochondrial Mg2+ efflux system","volume":"6","author":"Mastrototaro L.","year":"2016","unstructured":"L. Mastrototaro, A. Smorodchenko, J. R. Aschenbach, M. Kolisek, G. Sponder, Solute carrier 41A3 encodes for a mitochondrial Mg2+ efflux system. Sci. Rep. 6, 27999 (2016).","journal-title":"Sci. Rep."},{"key":"e_1_3_4_57_2","doi-asserted-by":"crossref","first-page":"aac4354","DOI":"10.1126\/science.aac4354","article-title":"In vivo aspects of protein folding and quality control","volume":"353","author":"Balchin D.","year":"2016","unstructured":"D. Balchin, M. Hayer-Hartl, F. U. Hartl, In vivo aspects of protein folding and quality control. Science 353, aac4354 (2016).","journal-title":"Science"},{"key":"e_1_3_4_58_2","doi-asserted-by":"crossref","first-page":"952","DOI":"10.1038\/nri1250","article-title":"Making sense of mass destruction: Quantitating MHC class I antigen presentation","volume":"3","author":"Yewdell J. W.","year":"2003","unstructured":"J. W. Yewdell, E. Reits, J. Neefjes, Making sense of mass destruction: Quantitating MHC class I antigen presentation. Nat. Rev. Immunol. 3, 952\u2013961 (2003).","journal-title":"Nat. Rev. Immunol."},{"key":"e_1_3_4_59_2","doi-asserted-by":"crossref","first-page":"16056","DOI":"10.1038\/ncomms16056","article-title":"The E3 ubiquitin ligase and RNA-binding protein ZNF598 orchestrates ribosome quality control of premature polyadenylated mRNAs","volume":"8","author":"Garzia A.","year":"2017","unstructured":"A. Garzia ., The E3 ubiquitin ligase and RNA-binding protein ZNF598 orchestrates ribosome quality control of premature polyadenylated mRNAs. Nat. Commun. 8, 16056 (2017).","journal-title":"Nat. Commun."},{"key":"e_1_3_4_60_2","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1146\/annurev-cellbio-111315-125249","article-title":"Ribosomal stalling during translation: Providing substrates for ribosome-associated protein quality control","volume":"33","author":"Joazeiro C. A. P.","year":"2017","unstructured":"C. A. P. Joazeiro, Ribosomal stalling during translation: Providing substrates for ribosome-associated protein quality control. Annu. Rev. Cell Dev. Biol. 33, 343\u2013368 (2017).","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"e_1_3_4_61_2","doi-asserted-by":"crossref","first-page":"2168","DOI":"10.1091\/mbc.E15-01-0040","article-title":"The ribosome quality control pathway can access nascent polypeptides stalled at the Sec61 translocon","volume":"26","author":"von der Malsburg K.","year":"2015","unstructured":"K. von der Malsburg, S. Shao, R. S. Hegde, The ribosome quality control pathway can access nascent polypeptides stalled at the Sec61 translocon. Mol. Biol. Cell 26, 2168\u20132180 (2015).","journal-title":"Mol. Biol. Cell"},{"key":"e_1_3_4_62_2","doi-asserted-by":"crossref","first-page":"30795","DOI":"10.1038\/srep30795","article-title":"Quality control of nonstop membrane proteins at the ER membrane and in the cytosol","volume":"6","author":"Arakawa S.","year":"2016","unstructured":"S. Arakawa ., Quality control of nonstop membrane proteins at the ER membrane and in the cytosol. Sci. Rep. 6, 30795 (2016).","journal-title":"Sci. Rep."},{"key":"e_1_3_4_63_2","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1083\/jcb.200903014","article-title":"Regulated Ire1-dependent decay of messenger RNAs in mammalian cells","volume":"186","author":"Hollien J.","year":"2009","unstructured":"J. Hollien ., Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186, 323\u2013331 (2009).","journal-title":"J. Cell Biol."},{"key":"e_1_3_4_64_2","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1126\/science.1129631","article-title":"Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response","volume":"313","author":"Hollien J.","year":"2006","unstructured":"J. Hollien, J. S. Weissman, Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104\u2013107 (2006).","journal-title":"Science"},{"key":"e_1_3_4_65_2","doi-asserted-by":"crossref","first-page":"e29216","DOI":"10.7554\/eLife.29216","article-title":"Regulated Ire1-dependent mRNA decay requires no-go mRNA degradation to maintain endoplasmic reticulum homeostasis in S. pombe","volume":"6","author":"Guydosh N. R.","year":"2017","unstructured":"N. R. Guydosh, P. Kimmig, P. Walter, R. Green, Regulated Ire1-dependent mRNA decay requires no-go mRNA degradation to maintain endoplasmic reticulum homeostasis in S. pombe. eLife 6, e29216 (2017).","journal-title":"eLife"},{"key":"e_1_3_4_66_2","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/s41594-017-0010-8","article-title":"Structural biology of Zika virus and other flaviviruses","volume":"25","author":"Hasan S. S.","year":"2018","unstructured":"S. S. Hasan, M. Sevvana, R. J. Kuhn, M. G. Rossmann, Structural biology of Zika virus and other flaviviruses. Nat. Struct. Mol. Biol. 25, 13\u201320 (2018).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"e_1_3_4_67_2","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1016\/j.celrep.2016.06.028","article-title":"Identification of Zika virus and Dengue virus dependency factors using functional genomics","volume":"16","author":"Savidis G.","year":"2016","unstructured":"G. Savidis ., Identification of Zika virus and Dengue virus dependency factors using functional genomics. Cell Rep. 16, 232\u2013246 (2016).","journal-title":"Cell Rep."},{"key":"e_1_3_4_68_2","doi-asserted-by":"crossref","first-page":"1666","DOI":"10.1016\/j.celrep.2019.04.051","article-title":"The ER membrane protein complex promotes biogenesis of Dengue and Zika virus non-structural multi-pass transmembrane proteins to support infection","volume":"27","author":"Lin D. L.","year":"2019","unstructured":"D. L. Lin ., The ER membrane protein complex promotes biogenesis of Dengue and Zika virus non-structural multi-pass transmembrane proteins to support infection. Cell Rep. 27, 1666\u20131674.e4 (2019).","journal-title":"Cell Rep."},{"key":"e_1_3_4_69_2","doi-asserted-by":"crossref","first-page":"658","DOI":"10.1074\/mcp.M114.042812","article-title":"Mass spectrometry of human leukocyte antigen class I peptidomes reveals strong effects of protein abundance and turnover on antigen presentation","volume":"14","author":"Bassani-Sternberg M.","year":"2015","unstructured":"M. Bassani-Sternberg, S. Pletscher-Frankild, L. J. Jensen, M. Mann, Mass spectrometry of human leukocyte antigen class I peptidomes reveals strong effects of protein abundance and turnover on antigen presentation. Mol. Cell. Proteomics 14, 658\u2013673 (2015).","journal-title":"Mol. Cell. Proteomics"},{"key":"e_1_3_4_70_2","doi-asserted-by":"crossref","first-page":"D442","DOI":"10.1093\/nar\/gky1106","article-title":"The PRIDE database and related tools and resources in 2019: Improving support for quantification data","volume":"47","author":"Perez-Riverol Y.","year":"2019","unstructured":"Y. Perez-Riverol ., The PRIDE database and related tools and resources in 2019: Improving support for quantification data. Nucleic Acids Res. 47, D442\u2013D450 (2019).","journal-title":"Nucleic Acids Res."}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.pnas.org\/syndication\/doi\/10.1073\/pnas.1914401117","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1914401117","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,26]],"date-time":"2023-09-26T14:20:36Z","timestamp":1695738036000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1914401117"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,11]]},"references-count":70,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2020,2,25]]}},"alternative-id":["10.1073\/pnas.1914401117"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1914401117","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.737354205.793571366","asserted-by":"object"}]},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,11]]},"assertion":[{"value":"2020-02-11","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}