Premature Translational Termination Products Are Rapidly Degraded Substrates for MHC Class I Presentation

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Lacsina, Joshua R ^a   Marks, Odessa A ^b   Liu, Xiongfei ^a   Reid, David W ^a   Jagannathan, Sujatha ^a   Nicchitta, Christopher V ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; POLYPEPTIDE; PROTEASOME; PUROMYCIN;

ANTIGEN PRESENTATION; ARTICLE; CELL FATE; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR WEIGHT; PEPTIDE SYNTHESIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TARGETING; PROTEIN TRANSPORT; TIME; UBIQUITINATION;

ANTIGEN PRESENTATION; CELL LINE; HEK293 CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MONITORING, IMMUNOLOGIC; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; PUROMYCIN;

PROKARYOTA;

EID: 84871348710     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051968     Document Type: Article

References (44)

1. Schubert U, Antón LC, Gibbs J, Norbury CC, Yewdell JW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-4.
2. Princiotta MF, Finzi D, Qian S-B, Gibbs J, Schuchmann S, et al. (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18: 343-54.
3. Reits EA, Vos JC, Grommé M, Neefjes J, (2000) The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774-8.
4. Qian S-B, Reits E, Neefjes J, Deslich JM, Bennink JR, et al. (2006) Tight linkage between translation and MHC class I peptide ligand generation implies specialized antigen processing for defective ribosomal products. J Immunol 177: 227-33.
5. Yewdell JW, Nicchitta CV, (2006) The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol 27: 368-73.
6. Yewdell JW, (2007) Plumbing the sources of endogenous MHC class I peptide ligands. Curr Opin Immunol 19: 79-86.
7. Yewdell JW, Antón LC, Bennink JR, (1996) Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J Immunol 157: 1823-6.
8. Dolan BP, Bennink JR, Yewdell JW, (2011) Translating DRiPs: progress in understanding viral and cellular sources of MHC class I peptide ligands. Cell Mol Life Sci 68: 1481-9.
9. Manley JL, (1978) Synthesis and degradation of termination and premature-termination fragments of beta-galactosidase in vitro and in vivo. J Mol Biol 125: 407-32.
10. Tsung K, Inouye S, Inouye M, (1989) Factors affecting the efficiency of protein synthesis in Escherichia coli. Production of a polypeptide of more than 6000 amino acid residues. J Biol Chem 264: 4428-33.
11. Jørgensen F, Kurland CG, (1990) Processivity errors of gene expression in Escherichia coli. J Mol Biol 215: 511-21.
12. Menninger JR, (1976) Peptidyl transfer RNA dissociates during protein synthesis from ribosomes of Escherichia coli. J Biol Chem 251: 3392-8.
13. Menninger JR, (1979) Accumulation of peptidyl tRNA is lethal to Escherichia coli. J Bacteriol 137: 694-6.
14. Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, et al. (2003) Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 100: 3889-94.
15. Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS, (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-23.
16. Cardinaud S, Starck SR, Chandra P, Shastri N, (2010) The synthesis of truncated polypeptides for immune surveillance and viral evasion. PLoS ONE 5: e8692.
17. De Pereda JM, Waas WF, Jan Y, Ruoslahti E, Schimmel P, et al. (2004) Crystal structure of a human peptidyl-tRNA hydrolase reveals a new fold and suggests basis for a bifunctional activity. J Biol Chem 279: 8111-5.
18. Ishii T, Funakoshi M, Kobayashi H, (2006) Yeast Pth2 is a UBL domain-binding protein that participates in the ubiquitin-proteasome pathway. EMBO J 25: 5492-503.
19. Vázquez D (1979) Inhibitors of protein biosynthesis. Mol Biol Biochem Biophys 30: i-x, 1-312.
20. Goldberg AL, St John AC, (1976) Intracellular protein degradation in mammalian and bacterial cells: Part 2. Annu Rev Biochem 45: 747-803.
21. Qian S-B, Bennink JR, Yewdell JW, (2005) Quantitating defective ribosome products. Methods Mol Biol 301: 271-81.
22. McCallum CD, Do H, Johnson AE, Frydman J, (2000) The interaction of the chaperonin tailless complex polypeptide 1 (TCP1) ring complex (TRiC) with ribosome-bound nascent chains examined using photo-cross-linking. J Cell Biol 149: 591-602.
23. Lelouard H, Ferrand V, Marguet D, Bania J, Camosseto V, et al. (2004) Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins. J Cell Biol 164: 667-75.
24. Szeto J, Kaniuk NA, Canadien V, Nisman R, Mizushima N, et al. (2006) ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2: 189-99.
25. Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN, (1997) Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6: 715-26.
26. Qian S-B, Princiotta MF, Bennink JR, Yewdell JW, (2006) Characterization of rapidly degraded polypeptides in mammalian cells reveals a novel layer of nascent protein quality control. J Biol Chem 281: 392-400.
27. Schägger H, (2006) Tricine-SDS-PAGE. Nat Protoc 1: 16-22.
28. Sugawara S, Abo T, Kumagai K, (1987) 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: 83-90.
29. Qian S-B, Zhang X, Sun J, Bennink JR, Yewdell JW, et al. (2010) mTORC1 links protein quality and quantity control by sensing chaperone availability. J Biol Chem 285: 27385-95.
30. Leonhardt RM, Fiegl D, Rufer E, Karger A, Bettin B, et al. (2010) Post-endoplasmic reticulum rescue of unstable MHC class I requires proprotein convertase PC7. J Immunol 184: 2985-98.
31. Day PM, Yewdell JW, Porgador A, Germain RN, Bennink JR, (1997) Direct delivery of exogenous MHC class I molecule-binding oligopeptides to the endoplasmic reticulum of viable cells. Proc Natl Acad Sci U S A. 94: 8064-9.
32. Huang L, Kuhls MC, Eisenlohr LC, (2011) Hydrophobicity as a driver of MHC class I antigen processing. EMBO J 30: 1634-44.
33. Shoemaker CJ, Eyler DE, Green R, (2010) Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay. Science 330: 369-72.
34. Wherry EJ, Golovina TN, Morrison SE, Sinnathamby G, McElhaugh MJ, et al. (2006) Re-evaluating the generation of a "proteasome-independent" MHC class I-restricted CD8 T cell epitope. J Immunol 176: 2249-61.
35. van Endert P, (2011) Post-proteasomal and proteasome-independent generation of MHC class I ligands. Cell Mol Life Sci 68: 1553-67.
36. Marcilla M, Cragnolini JJ, López de Castro JA, (2007) Proteasome-independent HLA-B27 ligands arise mainly from small basic proteins. Mol Cell Proteomics 6: 923-38.
37. Gileadi U, Moins-Teisserenc HT, Correa I, Booth BL, Dunbar PR, et al. (1999) Generation of an immunodominant CTL epitope is affected by proteasome subunit composition and stability of the antigenic protein. J Immunol 163: 6045-52.
38. Golovina TN, Morrison SE, Eisenlohr LC, (2005) The impact of misfolding versus targeted degradation on the efficiency of the MHC class I-restricted antigen processing. J Immunol 174: 2763-9.
39. Dolan BP, Li L, Veltri CA, Ireland CM, Bennink JR, et al. (2011) Distinct pathways generate peptides from defective ribosomal products for CD8+ T cell immunosurveillance. J Immunol 186: 2065-72.
40. Gidalevitz T, Ben-Zvi A, Ho KH, Brignull HR, Morimoto RI, (2006) Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 311: 1471-4.
41. Reits E, Griekspoor A, Neijssen J, Groothuis T, Jalink K, et al. (2003) Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity. 18: 97-108.
42. Farfán-Arribas DJ, Stern LJ, Rock KL, (2012) Using intein catalysis to probe the origin of major histocompatibility complex class I-presented peptides. Proc Natl Acad Sci U S A. 109: 16998-7003.
43. Lev A, Princiotta MF, Zanker D, Takeda K, Gibbs JS, et al. (2010) Compartmentalized MHC class I antigen processing enhances immunosurveillance by circumventing the law of mass action. Proc Natl Acad Sci U S A 107: 6964-9.
44. Dolan BP, Knowlton JJ, David A, Bennink JR, Yewdell JW, (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: 6728-33.