Translating DRiPs: MHC class I immunosurveillance of pathogens and tumors

Journal of Leukocyte Biology

Volumn 95, Issue 4, 2014, Pages 551-562

  Antón, Luis C ^a   Yewdell, Jonathan W ^b  

^a CSIC   (Spain)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Antigen processing; Compartmentalization; Cotranslational degradation; Nuclear translation; Ribosome; Translation

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OLIGOPEPTIDE;

CELL SURFACE; HOST RESISTANCE; HUMAN; IMMUNOSURVEILLANCE; NONHUMAN; PRIORITY JOURNAL; REVIEW; RIBOSOME; T LYMPHOCYTE; TUMOR IMMUNITY; TUMOR IMMUNOLOGY; VIRUS IMMUNITY; VIRUS REPLICATION;

ANTIGEN PROCESSING; COMPARTMENTALIZATION; COTRANSLATIONAL DEGRADATION; NUCLEAR TRANSLATION; RIBOSOME; TRANSLATION;

ANIMALS; ANTIGEN PRESENTATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MEDIATOR COMPLEX; MONITORING, IMMUNOLOGIC; NEOPLASMS; PROTEIN BIOSYNTHESIS; RIBOSOMES;

EID: 84899883247     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1113599     Document Type: Review

References (175)

1. Zinkernagel, R. M., Doherty, P. C. (1974) Restriction of in vitro T cellmediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 248, 701-702.
2. Yamazaki, K., Boyse, E. A., Mike, V., Thaler, H. T., Mathieson, B. J., Abbott, J., Boyse, J., Zayas, Z. A., Thomas, L. (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. J. Exp. Med. 144, 1324-1335.
3. Huh, G. S., Boulanger, L. M., Du, H., Riquelme, P. A., Brotz, T. M., Shatz, C. J. (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290, 2155-2159.
4. Cox, J. H., Yewdell, J. W., Eisenlohr, L. C., Johnson, P. R., Bennink, J. R. (1990) Antigen presentation requires transport of MHC class I molecules from the endoplasmic reticulum. Science 247, 715-718.
5. Restifo, N. P., Esquivel, F., Kawakami, Y., Yewdell, J. W., Mule, J. J., Rosenberg, S. A., Bennink, J. R. (1993) Identification of human cancers deficient in antigen processing. J. Exp. Med. 177, 265-272.
6. Townsend, A. R., Rothbard, J., Gotch, F. M., Bahadur, G., Wraith, D., McMichael, A. J. (1986) The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44, 959-968.
7. Babbitt, B. P., Allen, P. M., Matsueda, G. R., Haber, E., Unanue, E. R. (1985) Binding of immunogenic peptides to Ia histocompatibility molecules. Nature 317, 359-361.
8. Buus, S., Colon, S. M., Smith, C., Freed, J. H., Miles, C., Grey, H. M. (1986) Interaction between a "processed" ovalbumin peptide and Ia molecules. Proc. Natl. Acad. Sci. USA 83, 3968-3971.
9. Yewdell, J. W. (2011) DRiPs solidify: progress in understanding endogenous MHC class I antigen processing. Trends Immunol. 32, 548-558.
10. Starck, S. R., Shastri, N. (2011) Non-conventional sources of peptides presented by MHC class I. Cell. Mol. Life Sci. 68, 1471-1479.
11. Eisenlohr, L. C., Huang, L., Golovina, T. N. (2007) Rethinking peptide supply to MHC class I molecules. Nat. Rev. Immunol. 7, 403-410.
12. Yewdell, J. W., Anton, L. C., Bennink, J. R. (1996) Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J. Immunol. 157, 1823-1826.
13. Esquivel, F., Yewdell, J. W., Bennink, J. R. (1992) RMA/S cells present endogenously synthesized cytosolic proteins to class I-restricted cytotoxic T lymphocytes. J. Exp. Med. 175, 163-168.
14. Yewdell, J. W. (2003) Immunology. Hide and seek in the peptidome. Science 301, 1334-1335.
15. Shastri, N., Nguyen, V., Gonzalez, F. (1995) Major histocompatibility class I molecules can present cryptic translation products to T-cells. J. Biol. Chem. 270, 1088-1091.
16. Wang, R. F., Parkhurst, M. R., Kawakami, Y., Robbins, P. F., Rosenberg, S. A. (1996) Utilization of an alternative open reading frame of a normal gene in generating a novel human cancer antigen. J. Exp. Med. 183, 1131-1140.
17. Bullock, T. N. J., Eisenlohr, L. C. (1996) Ribosomal scanning past the primary initiation codon as a mechanism for expression of CTL epitopes encoded in alternative reading frames. J. Exp. Med. 184, 1319-1329.
18. Fetten, J. V., Roy, N., Giboa, E. (1991) A frameshift mutation at the NH2 terminus of the nucleoprotein gene does not affect generation of cytotoxic T lymphocyte epitopes. J. Immunol. 147, 2697-2705.
19. Berglund, P., Finzi, D., Bennink, J. R., Yewdell, J. W. (2007) Viral alteration of cellular translational machinery increases defective ribosomal products. J. Virol. 81, 7220-7229.
20. Netzer, N., Goodenbour, J. M., David, A., Dittmar, K. A., Jones, R. B., Schneider, J. R., Boone, D., Eves, E. M., Rosner, M. R., Gibbs, J. S., Embry, A., Dolan, B., Das, S., Hickman, H. D., Berglund, P., Bennink, J. R., Yewdell, J. W., Pan, T. (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462, 522-526.
21. Gout, J. F., Kelley Thomas, W., Smith, Z., Okamoto, K., Lynch, M. (2013) Large-scale detection of in vivo transcription errors. Proc. Natl. Acad. Sci. USA 110, 18584-18589.
22. Yewdell, J. (2002) To DRiP or not to DRiP: generating peptide ligands for MHC class I molecules from biosynthesized proteins. Mol. Immunol. 39, 139-146.
23. Yewdell, J. W., Nicchitta, C. V. (2006) The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol. 27, 368-373.
24. Istrail, S., Florea, L., Halldorsson, B. V., Kohlbacher, O., Schwartz, R. S., Yap, V. B., Yewdell, J. W., Hoffman, S. L. (2004) Comparative immunopeptidomics of humans and their pathogens. Proc. Natl. Acad. Sci. USA 101, 13268-13272.
25. Van Bleek, G. M., Nathenson, S. G. (1990) Isolation of an endogenously processed immunodominant viral peptide from the class I H-2K b molecule. Nature 348, 213-216.
26. Milner, E., Barnea, E., Beer, I., Admon, A. (2006) The turnover kinetics of major histocompatibility complex peptides of human cancer cells. Mol. Cell. Proteomics 5, 357-365.
27. Milner, E., Gutter-Kapon, L., Bassani-Strenberg, M., Barnea, E., Beer, I., Admon, A. (2013) The effect of proteasome inhibition on the generation of the human leukocyte antigen (HLA) peptidome. Mol. Cell. Proteomics 12, 1853-1864.
28. Hassan, C., Kester, M. G., de Ru, A. H., Hombrink, P., Drijfhout, J. W., Nijveen, H., Leunissen, J. A., Heemskerk, M. H., Falkenburg, J. H., van Veelen, P. A. (2013) The human leukocyte antigen-presented ligandome of B lymphocytes. Mol. Cell. Proteomics 12, 1829-1843.
29. Croft, N. P., Smith, S. A., Wong, Y. C., Tan, C. T., Dudek, N. L., Flesch, I. E., Lin, L. C., Tscharke, D. C., Purcell, A. W. (2013) Kinetics of antigen expression and epitope presentation during virus infection. PLoS Pathog. 9, e1003129.
30. Tscharke, D. C., Karupiah, G., Zhou, J., Palmore, T., Irvine, K. R., Haeryfar, S. M., Williams, S., Sidney, J., Sette, A., Bennink, J. R., Yewdell, J. W. (2005) Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J. Exp. Med. 201, 95-104.
31. Moutaftsi, M., Peters, B., Pasquetto, V., Tscharke, D. C., Sidney, J., Bui, H. H., Grey, H., Sette, A. (2006) A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus. Nat. Biotechnol. 24, 817-819.
32. Tan, C. T., Croft, N. P., Dudek, N. L., Williamson, N. A., Purcell, A. W. (2011) Direct quantitation of MHC-bound peptide epitopes by selected reaction monitoring. Proteomics 11, 2336-2340.
33. Yewdell, J. W., Bennink, J. R., Hosaka, Y. (1988) Cells process exogenous proteins for recognition by cytotoxic T lymphocytes. Science 239, 637-640.
34. Kurts, C. (2013) Molecular and cell-biological mechanisms of antigen cross-presentation. Front. Immunol. 4, 51.
35. De Verteuil, D., Granados, D. P., Thibault, P., Perreault, C. (2012) Origin and plasticity of MHC I-associated self peptides. Autoimmun. Rev. 11, 627-635.
36. Caron, E., Vincent, K., Fortier, M. H., Laverdure, J. P., Bramoulle, A., Hardy, M. P., Voisin, G., Roux, P. P., Lemieux, S., Thibault, P., Perreault, C. (2011) The MHC I immunopeptidome conveys to the cell surface an integrative view of cellular regulation. Mol. Syst. Biol. 7, 533.
37. Granados, D. P., Yahyaoui, W., Laumont, C. M., Daouda, T., Muratore-Schroeder, T. L., Cote, C., Laverdure, J. P., Lemieux, S., Thibault, P., Perreault, C. (2012) MHC I-associated peptides preferentially derive from transcripts bearing miRNA response elements. Blood 119, e181-e191.
38. Carthew, R. W., Sontheimer, E. J. (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655.
39. Orban, T. I., Izaurralde, E. (2005) Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 11, 459-469.
40. Gu, W. Y., Cochrane, M., Leggatt, G. R., Payne, E., Choyce, A., Zhou, F., Tindle, R., McMillan, N. A. J. (2009) Both treated and untreated tumors are eliminated by short hairpin RNA-based induction of targetspecific immune responses. Proc. Natl. Acad. Sci. USA 106, 8314-8319.
41. Zitvogel, L., Galluzzi, L., Smyth, M. J., Kroemer, G. (2013) Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 39, 74-88.
42. Senovilla, L., Vitale, I., Martins, I., Kepp, O., Galluzzi, L., Zitvogel, L., Castedo, M., Kroemer, G. (2013) An anticancer therapy-elicited immunosurveillance system that eliminates tetraploid cells. Oncoimmunology 2, e22409.
43. Hickman, H. D., Luis, A. D., Bardet, W., Buchli, R., Battson, C. L., Shearer, M. H., Jackson, K. W., Kennedy, R. C., Hildebrand, W. H. (2003) Cutting edge: class I presentation of host peptides following HIV infection. J. Immunol. 171, 22-26.
44. Wahl, A., Schafer, F., Bardet, W., Hildebrand, W. H. (2010) HLA class I molecules reflect an altered host proteome after influenza virus infection. Hum. Immunol. 71, 14-22.
45. Yewdell, J. W. (2001) Not such a dismal science: the economics of protein synthesis, folding, degradation and antigen processing. Trends Cell Biol. 11, 294-297.
46. Princiotta, M. F., Finzi, D., Qian, S-B., Gibbs, J., Schuchmann, S., Buttgereit, F., Bennink, J. R., Yewdell, J. W. (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18, 343-354.
47. Schubert, U., Antón, L. C., Gibbs, J., Norbury, C. C., Yewdell, J. W., Bennink, J. R. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404, 770-774.
48. Qian, S.-B., Princiotta, M. F., Bennink, J. R., 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.
49. Shaffer, A. L., Shapiro-Shelef, M., Iwakoshi, N. N., Lee, A. H., Qian, S. B., Zhao, H., Yu, X., Yang, L., Tan, B. K., Rosenwald, A., Hurt, E. M., Petroulakis, E., Sonenberg, N., Yewdell, J. W., Calame, K., Glimcher, L. H., Staudt, L. M. (2004) XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21, 81-93.
50. Oldfield, C. J., Cheng, Y., Cortese, M. S., Brown, C. J., Uversky, V. N., Dunker, A. K. (2005) Comparing and combining predictors of mostly disordered proteins. Biochemistry 44, 1989-2000.
51. Havugimana, P. C., Hart, G. T., Nepusz, T., Yang, H., Turinsky, A. L., Li, Z., Wang, P. I., Boutz, D. R., Fong, V., Phanse, S., Babu, M., Craig, S. A., Hu, P., Wan, C., Vlasblom, J., Dar, V. U., Bezginov, A., Clark, G. W., Wu, G. C., Wodak, S. J., Tillier, E. R., Paccanaro, A., Marcotte, E. M., Emili, A. (2012) A census of human soluble protein complexes. Cell 150, 1068-1081.
52. Siegel, J. J., Amon, A. (2012) New insights into the troubles of aneuploidy. Annu. Rev. Cell Dev. Biol. 28, 189-214.
53. Vabulas, R. M., Hartl, F. U. (2005) Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310, 1960-1963.
54. Wheatley, D. N., Giddings, M. R., Inglis, M. S. (1980) Kinetics of degradation of "short-" and "long-lived" proteins in cultured mammalian cells. Cell Biol. Int. Rep. 4, 1081-1090.
55. Cenci, S., Oliva, L., Cerruti, F., Milan, E., Bianchi, G., Raule, M., Mezghrani, A., Pasqualetto, E., Sitia, R., Cascio, P. (2012) Pivotal Advance: Protein synthesis modulates responsiveness of differentiating and malignant plasma cells to proteasome inhibitors. J. Leukoc. Biol. 92, 921-931.
56. Yewdell, J. W., Schubert, U., Bennink, J. R. (2001) At the crossroads of cell biology and immunology: DRiPs and other sources of peptide ligands for MHC class I molecules. J. Cell Sci. 114, 845-851.
57. Yewdell, J. W., Lacsina, J. R., Rechsteiner, M. C., Nicchitta, C. V. (2011) Out with the old, in with the new? Comparing methods for measuring protein degradation. Cell Biol. Int. 35, 457-462.
58. Ha, S. W., Ju, D., Xie, Y. (2014) Nuclear import factor Srp1 and its associated protein Sts1 couple ribosome-bound nascent polypeptides to proteasomes for cotranslational degradation. J. Biol. Chem. 289, 2701-2710.
59. Turner, G. C., Varshavsky, A. (2000) Detecting and measuring cotranslational protein degradation in vivo. Science 289, 2117-2120.
60. Wang, F., Durfee, L. A., Huibregtse, J. M. (2013) A cotranslational ubiquitination pathway for quality control of misfolded proteins. Mol. Cell 50, 368-378.
61. Garcia-Medel, N., Sanz-Bravo, A., Barnea, E., Admon, A., Lopez de Castro, A. (2012) The origin of proteasome-inhibitor resistant HLA class I peptidomes: a study with HLA-A*68:01. Mol. Cell. Proteomics 11, M111.011486.
62. Duttler, S., Pechmann, S., Frydman, J. (2013) Principles of cotranslational ubiquitination and quality control at the ribosome. Mol. Cell 50, 379-393.
63. Cox, J. H., Galardy, P., Bennink, J. R., Yewdell, J. W. (1995) Presentation of endogenous and exogenous antigens is not affected by inactivation of E1 ubiquitin-activating enzyme in temperature-sensitive cell lines. J. Immunol. 154, 511-519.
64. Huang, L., Marvin, J. M., Tatsis, N., Eisenlohr, L. C. (2011) Selective role of ubiquitin in MHC class I antigen presentation. J. Immunol. 186, 1904-1908.
65. Sha, Z., Brill, L. M., Cabrera, R., Kleifeld, O., Scheliga, J. S., Glickman, M. H., Chang, E. C., Wolf, D. A. (2009) The eIF3 interactome reveals the translasome, a supercomplex linking protein synthesis and degradation machineries. Mol. Cell 36, 141-152.
66. Pechmann, S., Willmund, F., Frydman, J. (2013) The ribosome as a hub for protein quality control. Mol. Cell 49, 411-421.
67. Bengtson, M. H., Joazeiro, C. A. (2010) Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467, 470-473.
68. Shao, S., von der Malsburg, K., Hegde, R. S. (2013) Listerin-dependent nascent protein ubiquitination relies on ribosome subunit dissociation. Mol. Cell 50, 637-648.
69. Liu, B., Han, Y., Qian, S. B. (2013) Cotranslational response to proteotoxic stress by elongation pausing of ribosomes. Mol. Cell 49, 453-463.
70. Hershko, A., Eytan, E., Ciechanover, A., Haas, A. L. (1982) Immunochemical analysis of the turnover of ubiquitin-protein conjugates in intact cells. Relationship to the breakdown of abnormal proteins. J. Biol. Chem. 257, 13964-13970.
71. 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. Mol. Cell 44, 325-340.
72. Carreau, A., El Hafny-Rahbi, B., Matejuk, A., Grillon, C., Kieda, C. (2011) Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J. Cell. Mol. Med. 15, 1239-1253.
73. Shoemaker, C. J., Green, R. (2012) Translation drives mRNA quality control. Nat. Struct. Mol. Biol. 19, 594-601.
74. Trcek, T., Sato, H., Singer, R. H., Maquat, L. E. (2013) Temporal and spatial characterization of nonsense-mediated mRNA decay. Genes Dev. 27, 541-551.
75. Varsally, W., Brogna, S. (2012) UPF1 involvement in nuclear functions. Biochem. Soc. Trans. 40, 778-783.
76. Iborra, F. J., Escargueil, A. E., Kwek, K. Y., Akoulitchev, A., Cook, P. R. (2004) Molecular cross-talk between the transcription, translation, and nonsense-mediated decay machineries. J. Cell Sci. 117, 899-906.
77. Hentze, M. W., Izaurralde, E. (2013) Making sense of nonsense. Nat. Struct. Mol. Biol. 20, 651-653.
78. Apcher, S., Daskalogianni, C., Lejeune, F., Manoury, B., Imhoos, G., Heslop, L., Fahraeus, R. (2011) Major source of antigenic peptides for the MHC class I pathway is produced during the pioneer round of mRNA translation. Proc. Natl. Acad. Sci. USA 108, 11572-11577.
79. Durand, S., Lykke-Andersen, J. (2013) Nonsense-mediated mRNA decay occurs during eIF4F-dependent translation in human cells. Nat. Struct. Mol. Biol. 20, 702-709.
80. Rufener, S. C., Muhlemann, O. (2013) eIF4E-bound mRNPs are substrates for nonsense-mediated mRNA decay in mammalian cells. Nat. Struct. Mol. Biol. 20, 710-717.
81. Mendell, J. T., Sharifi, N. A., Meyers, J. L., Martinez-Murillo, F., Dietz, H. C. (2004) Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36, 1073-1078.
82. Dolan, B. P., Knowlton, J. J., David, A., Bennink, J. R., Yewdell, J. W. (2010) RNA polymerase II inhibitors dissociate antigenic peptide generation from normal viral protein synthesis: a role for nuclear translation in defective ribosomal product synthesis? J. Immunol. 185, 6728-6733.
83. Pastor, F., Kolonias, D., Giangrande, P. H., Gilboa, E. (2010) Induction of tumour immunity by targeted inhibition of nonsense-mediated mRNA decay. Nature 465, 227-230.
84. Charneski, C. A., Hurst, L. D. (2013) Positively charged residues are the major determinants of ribosomal velocity. PLoS Biol. 11, e1001508.
85. Ingolia, Nicholas T., Lareau, Liana F., Weissman, Jonathan S. (2011) Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789-802.
86. Dimitrova, L. N., Kuroha, K., Tatematsu, T., Inada, T. (2009) Nascent peptide-dependent translation arrest leads to Not4p-mediated protein degradation by the proteasome. J. Biol. Chem. 284, 10343-10352.
87. Caron, E., Charbonneau, R., Huppé, G., Brochu, S., Perreault, C. (2005) The structure and location of SIMP/STT3B account for its prominent imprint on the MHC I immunopeptidome. Int. Immunol. 17, 1583-1596.
88. Cardinaud, S., Starck, S. R., Chandra, P., Shastri, N. (2010) The synthesis of truncated polypeptides for immune surveillance and viral evasion. PLoS One 5, e8692.
89. Brandman, O., Stewart-Ornstein, J., Wong, D., Larson, A., Williams, C. C., Li, G. W., Zhou, S., King, D., Shen, P. S., Weibezahn, J., Dunn, J. G., Rouskin, S., Inada, T., Frost, A., Weissman, J. S. (2012) A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 151, 1042-1054.
90. Meyer, H., Bug, M., Bremer, S. (2012) Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat. Cell Biol. 14, 117-123.
91. Stolz, A., Hilt, W., Buchberger, A., Wolf, D. H. (2011) Cdc48: a power machine in protein degradation. Trends Biochem. Sci. 36, 515-523.
92. Dolan, B. P., Li, L., Veltri, C. A., Ireland, C. M., Bennink, J. R., Yewdell, J. W. (2011) Distinct pathways generate peptides from defective ribosomal products for CD8+ T cell immunosurveillance. J. Immunol. 186, 2065-2072.
93. Palmer, A. L., Dolan, B. P. (2013) MHC class I antigen presentation of DRiP-derived peptides from a model antigen is not dependent on the AAA ATPase p97. PLoS One 8, e67796.
94. Kampinga, H. H., Craig, E. A. (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell. Biol. 11, 579-592.
95. Minami, R., Hayakawa, A., Kagawa, H., Yanagi, Y., Yokosawa, H., Kawahara, H. (2010) BAG-6 is essential for selective elimination of defective proteasomal substrates. J. Cell Biol. 190, 637-650.
96. Kawahara, H., Minami, R., Yokota, N. (2013) BAG6/BAT3: emerging roles in quality control for nascent polypeptides. J. Biochem. 153, 147-160.
97. Szeto, J., Kaniuk, N. A., Canadien, V., Nisman, R., Mizushima, N., Yoshimori, T., Bazett-Jones, D. P., Brumell, J. H. (2006) ALIS are stressinduced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2, 189-199.
98. Lelouard, H., Ferrand, V., Marguet, D., Bania, J., Camosseto, V., David, A., Gatti, E., Pierre, P. (2004) Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins 1. J. Cell Biol. 164, 667-675.
99. Lelouard, H., Gatti, E., Cappello, F., Gresser, O., Camosseto, V., Pierre, P. (2002) Transient aggregation of ubiquitinated proteins during dendritic cell maturation 3. Nature 417, 177-182.
100. Kamper, N., Franken, S., Temme, S., Koch, S., Bieber, T., Koch, N. (2012) γ-Interferon-regulated chaperone governs human lymphocyte antigen class II expression. FASEB J. 26, 104-116.
101. Wenger, T., Terawaki, S., Camosseto, V., Abdelrassoul, R., Mies, A., Catalan, N., Claudio, N., Clavarino, G., de Gassart, A., Rigotti Fde, A., Gatti, E., Pierre, P. (2012) Autophagy inhibition promotes defective neosynthesized proteins storage in ALIS, and induces redirection toward proteasome processing and MHCI-restricted presentation. Autophagy 8, 350-363.
102. Akahane, T., Sahara, K., Yashiroda, H., Tanaka, K., Murata, S. (2013) Involvement of Bag6 and the TRC pathway in proteasome assembly. Nat. Commun. 4, 2234.
103. Hotokezaka, Y., Tobben, U., Hotokezaka, H., Van Leyen, K., Beatrix, B., Smith, D. H., Nakamura, T., Wiedmann, M. (2002) Interaction of the eukaryotic elongation factor 1A with newly synthesized polypeptides. J. Biol. Chem. 277, 18545-18551.
104. Chuang, S. M., Chen, L., Lambertson, D., Anand, M., Kinzy, T. G., Madura, K. (2005) Proteasome-mediated degradation of cotranslationally damaged proteins involves translation elongation factor 1A. Mol. Cell. Biol. 25, 403-413.
105. Gandin, V., Gutierrez, G. J., Brill, L. M., Varsano, T., Feng, Y., Aza-Blanc, P., Au, Q., McLaughlan, S., Ferreira, T. A., Alain, T., Sonenberg, N., Topisirovic, I., Ronai, Z. A. (2013) Degradation of newly synthesized polypeptides by ribosome-associated RACK1/c-Jun N-terminal kinase/eukaryotic elongation factor 1A2 complex. Mol. Cell. Biol. 33, 2510-2526.
106. Meriin, A. B., Zaarur, N., Sherman, M. Y. (2012) Association of translation factor eEF1A with defective ribosomal products generates a signal for aggresome formation. J. Cell Sci. 125, 2665-2674.
107. Twitty, C. G., Jensen, S. M., Hu, H. M., Fox, B. A. (2011) Tumor-derived autophagosome vaccine: induction of cross-protective immune responses against short-lived proteins through a p62-dependent mechanism. Clin. Cancer Res. 17, 6467-6481.
108. Jeffery, W. R., Tomlinson, C. R., Brodeur, R. D. (1983) Localization of actin messenger RNA during early ascidian development. Dev. Biol. 99, 408-417.
109. Kislauskis, E. H., Zhu, X-c., Singer, R. H. (1997) β-Actin messenger RNA localization and protein synthesis augment cell motility. J. Cell Biol. 136, 1263-1270.
110. Cajigas, I. J., Will, T., Schuman, E. M. (2010) Protein homeostasis and synaptic plasticity. EMBO J. 29, 2746-2752.
111. Bingol, B., Sheng, M. (2011) Deconstruction for reconstruction: the role of proteolysis in Nneural plasticity and disease. Neuron 69, 22-32.
112. Larance, M., Ahmad, Y., Kirkwood, K. J., Ly, T., Lamond, A. I. (2013) Global subcellular characterization of protein degradation using quantitative proteomics. Mol. Cell. Proteomics 12, 638-650.
113. Pyhtila, B., Zheng, T., Lager, P. J., Keene, J. D., Reedy, M. C., Nicchitta, C. V. (2008) Signal sequence-and translation-independent mRNA localization to the endoplasmic reticulum. RNA 14, 445-453.
114. Reid, D. W., Nicchitta, C. V. (2012) Primary role for endoplasmic reticulum-bound ribosomes in cellular translation identified by ribosome profiling. J. Biol. Chem. 287, 5518-5527.
115. Schwab, S. R., Shugart, J. A., Horng, T., Malarkannan, S., Shastri, N. (2004) Unanticipated antigens: translation initiation at CUG with leucine. PLoS Biol. 2, 1774-1784.
116. Starck, S. R., Jiang, V., Pavon-Eternod, M., Prasad, S., McCarthy, B., Pan, T., Shastri, N. (2012) Leucine-tRNA initiates at CUG start codons for protein synthesis and presentation by MHC class I. Science 336, 1719-1723.
117. Brooks, P., Murray, R. Z., Mason, G. G., Hendil, K. B., Rivett, A. J. (2000) Association of immunoproteasomes with the endoplasmic reticulum. Biochem. J. 352, 611-615.
118. Brooks, P., Fuertes, G., Murray, R. Z., Bose, S., Knecht, E., Rechsteiner, M. C., Hendil, K. B., Tanaka, K., Dyson, J., Rivett, J. (2000) Subcellular localization of proteasomes and their regulatory complexes in mammalian cells. Biochem. J. 346, 155-161.
119. Reits, E. A., Vos, J. C., Gromme, M., Neefjes, J. (2000) The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404, 774-778.
120. Qian, S. B., Reits, E., Neefjes, J., Deslich, J. M., Bennink, J. R., Yewdell, J. W. (2006) Tight linkage between translation and MHC class I peptide ligand generation implies specialized antigen processing for defective ribosomal products. J. Immunol. 177, 227-233.
121. Lev, A., Princiotta, M. F., Zanker, D., Takeda, K., Gibbs, J. S., Kumagai, C., Waffarn, E., Dolan, B. P., Burgevin, A., Van Endert, P., Chen, W., Bennink, J. R., Yewdell, J. W. (2010) Compartmentalized MHC class I antigen processing enhances immunosurveillance by circumventing the law of mass action. Proc. Natl. Acad. Sci. USA 107, 6964-6969.
122. Lu, X., Gibbs, J. S., Hickman, H. D., David, A., Dolan, B. P., Jin, Y., Kranz, D. M., Bennink, J. R., Yewdell, J. W., Varma, R. (2012) Endogenous viral antigen processing generates peptide-specific MHC class I cell-surface clusters. Proc. Nat. Acad. Sci. USA 109, 15407-15412.
123. Ferez, M., Castro, M., Alarcon, B., van Santen, H. M. (2014) Cognate peptide-MHC complexes are expressed as tightly apposed nanoclusters in virus-infected cells to allow TCR crosslinking. J. Immunol. 192, 52-58.
124. Bosch, B., Heipertz, E. L., Drake, J. R., Roche, P. A. (2013) Major histocompatibility complex (MHC) class II-peptide complexes arrive at the plasma membrane in cholesterol-rich microclusters. J. Biol. Chem. 288, 13236-13242.
125. Noller, H. F. (2013) By ribosome possessed. J. Biol. Chem. 288, 24872-24885.
126. Mauro, V. P., Edelman, G. M. (2007) The ribosome filter redux. Cell Cycle 6, 2246-2251.
127. Mauro, V. P., Edelman, G. M. (2002) The ribosome filter hypothesis. Proc. Natl. Acad. Sci. USA 99, 12031-12036.
128. Bauer, J. W., Brandl, C., Haubenreisser, O., Wimmer, B., Weber, M., Karl, T., Klausegger, A., Breitenbach, M., Hintner, H., von der Haar, T., Tuite, M. F., Breitenbach-Koller, L. (2013) Specialized yeast ribosomes: a customized tool for selective mRNA translation. PLoS One 8, e67609.
129. Xue, S., Barna, M. (2012) Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell. Biol. 13, 355-369.
130. Kondrashov, N., Pusic, A., Stumpf, C. R., Shimizu, K., Hsieh, Andrew, C., Xue, S., Ishijima, J., Shiroishi, T., Barna, M. (2011) Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145, 383-397.
131. Vinckenbosch, N., Dupanloup, I., Kaessmann, H. (2006) Evolutionary fate of retroposed gene copies in the human genome. Proc. Natl. Acad. Sci. USA 103, 3220-3225.
132. Spence, J., Gali, R. R., Dittmar, G., Sherman, F., Karin, M., Finley, D. (2000) Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 102, 67-76.
133. Rezgui, V. A., Tyagi, K., Ranjan, N., Konevega, A. L., Mittelstaet, J., Rodnina, M. V., Peter, M., Pedrioli, P. G. (2013) tRNA tKUUU, tQUUG, and tEUUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding. Proc. Natl. Acad. Sci. USA 110, 12289-12294.
134. Hampel, A., Enger, M. D. (1973) Subcellular distribution of aminoacyltransfer RNA synthetases in Chinese hamster ovary cell culture. J. Mol. Biol. 79, 285-293.
135. Ussery, M. A., Tanaka, W. K., Hardesty, B. (1977) Subcellular distribution of aminoacyl-tRNA synthetases in various eukaryotic cells. Eur. J. Biochem. 72, 491-500.
136. Kaminska, M., Havrylenko, S., Decottignies, P., Le Marechal, P., Negrutskii, B., Mirande, M. (2009) Dynamic organization of aminoacyltRNA synthetase complexes in the cytoplasm of human cells. J. Biol. Chem. 284, 13746-13754.
137. David, A., Netzer, N., Strader, M. B., Das, S. R., Chen, C. Y., Gibbs, J., Pierre, P., Bennink, J. R., Yewdell, J. W. (2011) RNA-binding targets aminoacyl-tRNA-synthetases to translating ribosomes. J. Biol. Chem. 286, 20688-20700.
138. Pan, T. (2013) Adaptive translation as a mechanism of stress response and adaptation. Annu. Rev. Genet. 47, 121-137.
139. Kyriacou, S. V., Deutscher, M. P. (2008) An important role for the multienzyme aminoacyl-tRNA synthetase complex in mammalian translation and cell growth. Mol. Cell 29, 419-427.
140. Stapulionis, R., Deutscher, M. P. (1995) A channeled tRNA cycle during mammalian protein synthesis. Proc. Natl. Acad. Sci. USA 92, 7158-7161.
141. Santagata, S., Mendillo, M. L., Tang, Y-c., Subramanian, A., Perley, C. C., Roche, S. P., Wong, B., Narayan, R., Kwon, H., Koeva, M., Amon, A., Golub, T. R., Porco, J. A., Whitesell, L., Lindquist, S. (2013) Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state. Science 341, 1238303.
142. Birnstiel, M. L., Hyde, B. B. (1963) Protein synthesis by isolated pea nucleoli. J. Cell Biol. 18, 41-50.
143. Carneiro, J., Leblond, C. P. (1959) Continuous protein synthesis in nuclei, shown by radioautography with H3-labeled amino acids. Science 129, 391-392.
144. Allfrey, V. G., Mirsky, A. E., Osawa, S. (1957) Protein synthesis in isolated cell nuclei. J. Gen. Physiol. 40, 451-490.
145. Zimmerman, E. F., Hackney, J., Nelson, P., Arias, I. M. (1969) Protein synthesis in isolated nuclei and nucleoli of HeLa cells. Biochemistry 8, 2636-2644.
146. Wu, R. S., Warner, J. R. (1971) Cytoplasmic synthesis of nuclear proteins: kinetics of accumulation of radioactive proteins in various cell fractions after brief pulses. J. Cell Biol. 51, 643-652.
147. Iborra, F. J., Jackson, D. A., Cook, P. R. (2004) The case for nuclear translation 1. J. Cell Sci. 117, 5713-5720.
148. Dahlberg, J. E., Lund, E., Goodwin, E. B. (2003) Nuclear translation: what is the evidence? RNA 9, 1-8.
149. Nathanson, L., Xia, T., Deutscher, M. P. (2003) Nuclear protein synthesis: a re-evaluation. RNA 9, 9-13.
150. David, A., Dolan, B. P., Hickman, H. D., Knowlton, J. J., Clavarino, G., Pierre, P., Bennink, J. R., Yewdell, J. W. (2012) Nuclear translation visualized by ribosome-bound nascent chain puromycylation. J. Cell Biol. 197, 45-57.
151. Pederson, T. (2013) The persistent plausibility of protein synthesis in the nucleus: process, palimpsest or pitfall? Curr. Opin. Cell Biol. 25, 520-521.
152. Dahlberg, J., Lund, E. (2012) Nuclear translation or nuclear peptidyl transferase? Nucleus 3, 320-321.
153. Brogna, S., Sato, T. A., Rosbash, M. (2002) Ribosome components are associated with sites of transcription. Mol. Cell 10, 93-104.
154. Al-Jubran, K., Wen, J., Abdullahi, A., Roy Chaudhury, S., Li, M., Ramanathan, P., Matina, A., De, S., Piechocki, K., Rugjee, K. N., Brogna, S. (2013) Visualization of the joining of ribosomal subunits reveals the presence of 80S ribosomes in the nucleus. RNA 19, 1669-1683.
155. Apcher, S., Millot, G., Daskalogianni, C., Scherl, A., Manoury, B., Fahraeus, R. (2013) Translation of pre-spliced RNAs in the nuclear compartment generates peptides for the MHC class I pathway. Proc. Natl. Acad. Sci. USA 110, 17951-17956.
156. Klein, J. (1986) Natural History of the Major Histocompatibility Complex. Wiley, New York, NY, USA.
157. Lee, C., Yen, K., Cohen, P. (2013) Humanin: a harbinger of mitochondrial-derived peptides? Trends Endocrinol. Metab. 24, 222-228.
158. Calvo, S. E., Pagliarini, D. J., Mootha, V. K. (2009) Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc. Natl. Acad. Sci. USA 106, 7507-7512.
159. Menschaert, G., Van Criekinge, W., Notelaers, T., Koch, A., Crappé, J., Gevaert, K., Van Damme, P. (2013) Deep proteome coverage based on ribosome profiling aids mass spectrometry-based protein and peptide discovery and provides evidence of alternative translation products and near-cognate translation initiation events. Mol. Cell. Proteomics 12, 1780-1790.
160. Slavoff, S. A., Mitchell, A. J., Schwaid, A. G., Cabili, M. N., Ma, J., Levin, J. Z., Karger, A. D., Budnik, B. A., Rinn, J. L., Saghatelian, A. (2013) Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nat. Chem. Biol. 9, 59-64.
161. Vanderperre, B., Lucier, J.-F., Bissonnette, C., Motard, J., Tremblay, G., Vanderperre, S., Wisztorski, M., Salzet, M., Boisvert, F-M., Roucou, X. (2013) Direct detection of alternative open reading frames translation products in human significantly expands the proteome. PLoS One 8, e70698.
162. Malarkannan, S., Horng, T., Shih, P. P., Schwab, S., Shastri, N. (1999) Presentation of out-of-frame peptide/MHC class I complexes by a novel translation initiation mechanism. Immunity 10, 681-690.
163. Farfán-Arribas, D. J., Stern, L. J., Rock, K. L. (2012) Using intein catalysis to probe the origin of major histocompatibility complex class I-presented peptides. Proc. Natl. Acad. Sci. USA 109, 16998-17003.
164. Carbone, F. R., Moore, M. W., Sheil, J. M., Bevan, M. J. (1988) Induction of cytotoxic T lymphocytes by primary in vitro stimulation with peptides. J. Exp. Med. 167, 1767-1779.
165. Bassani-Sternberg, M., Barnea, E., Beer, I., Avivi, I., Katz, T., Admon, A. (2010) Soluble plasma HLA peptidome as a potential source for cancer biomarkers. Proc. Natl. Acad. Sci. USA 107, 18769-18776.
166. Reits, E. A., Hodge, J. W., Herberts, C. A., Groothuis, T. A., Chakraborty, M., Wansley, E. K., Camphausen, K., Luiten, R. M., de Ru, A. H., Neijssen, J., Griekspoor, A., Mesman, E., Verreck, F. A., Spits, H., Schlom, J., van Veelen, P., Neefjes, J. J. (2006) Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J. Exp. Med. 203, 1259-1271.
167. Banaszynski, L. A., Chen, L. C., Maynard-Smith, L. A., Ooi, A. G., Wandless, T. J. (2006) A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell 126, 995-1004.
168. Barondeau, D. P., Kassmann, C. J., Tainer, J. A., Getzoff, E. D. (2006) Understanding GFP posttranslational chemistry: structures of designed variants that achieve backbone fragmentation, hydrolysis, and decarboxylation. J. Am. Chem. Soc. 128, 4685-4693.
169. Yewdell, J. W., Reits, E., Neefjes, J. (2003) Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat. Rev. Immunol. 3, 952-961.
170. Dolan, B. P., Sharma, A. A., Gibbs, J. S., Cunningham, T. J., Bennink, J. R., Yewdell, J. W. (2012) MHC class I antigen processing distinguishes endogenous antigens based on their translation from cellular vs. viral mRNA. Proc. Natl. Acad. Sci. USA 109, 7025-7030.
171. Villanueva, M. S., Fischer, P., Feen, K., Pamer, E. G. (1994) Efficiency of MHC class I antigen processing: a quantitative analysis. Immunity 1, 479-489.
172. Villanueva, M. S., Sijts, A. J., Pamer, E. G. (1995) Listeriolysin is processed efficiently into an MHC class I-associated epitope in Listeria monocytogenes-infected cells. J. Immunol. 155, 5227-5233.
173. Boon, T., Coulie, P. G., Van den Eynde, B. J., van der Bruggen, P. (2006) Human T cell responses against melanoma. Annu. Rev. Immunol. 24, 175-208.
174. Mathis, D., Benoist, C. (2009) Aire. Annu. Rev. Immunol. 27, 287-312.
175. Murata, S., Sasaki, K., Kishimoto, T., Niwa, S-I., Hayashi, H., Takahama, Y., Tanaka, K. (2007) Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 316, 1349-1353.