Initiation codon scanthrough versus termination codon readthrough demonstrates strong potential for major histocompatibility complex class I- restricted cryptic epitope expression

Journal of Experimental Medicine

Volumn 186, Issue 7, 1997, Pages 1051-1058

  Bullock, Timothy N J ^a   Patterson, Anthony E ^a   Franlin, Laura L ^a   Notidis, Evangelia ^a   Eisenlohr, Laurence C ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR;

ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CODON; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; IMMUNE RESPONSE; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MOUSE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TISSUE CULTURE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CODON, INITIATOR; CODON, TERMINATOR; EPITOPES; FEMALE; GENE EXPRESSION REGULATION; GENES, MHC CLASS I; MICE; MICE, INBRED STRAINS; MUTAGENESIS, INSERTIONAL; PROTEIN BIOSYNTHESIS; RIBOSOMES; VIRAL CORE PROTEINS;

EID: 0030763646     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.7.1051     Document Type: Article

References (41)

1. Bjorkman, P.J., M.A. Saper, B. Samraoui, W.S. Bennett, J.L. Strominger, and D.C. Wiley. 1987. Structure of the human class I histocompatibility antigen, HLA-A2. Nature (Lond.). 329:506-512.
2. Townsend, A., and H. Bodmer. 1989. Antigen recognition by class I-restricted T lymphocytes. Annu. Rev. Immunol. 7:601-624.
3. Yewdell, J.W., and J.R. Bennink. 1992. Cell biology of antigen processing and presentation to major histocompatibility complex class I molecule-restricted T lymphocytes. Adv. Immunol. 52:1-123.
4. Heemels, M.-T., and H. Ploegh. 1995. Generation, translocation, and presentation of MHC class I-restricted peptides. Annu. Rev. Biochem. 64:463-491.
5. York, I.A., and K.L. Rock. 1996. Antigen processing and presentation by the class I major histocompatibility complex. Annu. Rev. Immunol. 14:369-396.
6. Townsend, A.R.M., F.M. Gotch, and J. Davey. 1985. Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell. 42:457-467.
7. Sweetser, M.T., L. Morrison, V.L. Braciale, and T.J. Braciale. 1989. Recognition of pre-processed endogenous antigen by class I but not class II MHC-restricted T cells. Nature (Lond.). 342:180-182.
8. Eisenlohr, L.C., J.W. Yewdell, and J.R. Bennink. 1992. Flanking sequences influence the presentation of an endogenously synthesized peptide to cytotoxic T lymphocytes. J. Exp. Med. 175:481-487.
9. Uenaka, A., T. Ono, T. Akisawa, H. Wada, T. Yasuda, and E. Nakayama. 1994. Identification of a unique antigen peptide pRL1 on BALB/c RL♂1 leukemia recognized by cytotoxic t lymphocytes and its relation to the Akt oncogene. J. Exp. Med. 180:1599-1607.
10. Guilloux, Y., S. Lucas, V.G. Brichard, A. Van Pel, C. Viret, E.D. De Plaen, F. Brasseur, B. Lethé, F. Jotereau, and T. Boon. 1996. A peptide recognized by human cytolytic T lymphocytes on HLA-A2 melanoma is encoded by an intron sequence of the N-acetylglucosaminyltransferase V gene. J. Exp. Med. 183:1173-1183.
11. Gooding, L.R., K.A. O'Connell, R. Geib, and J.M. Pipas. 1988. Cytotoxic T cell recognition of the SV40 tumor antigen: a note of caution. In Processing and Presentation of Antigens. B. Pernis, S. Silverstein, and H. Vogel, editors. Academic Press, New York. 87-95.
12. Fetten, J.V., N. Roy, and E. Gilboa. 1991. A frameshift mutation at the NH2 terminus ot the nucleoprotein gene does not affect generation of cytotoxic T lymphocyte epitopes. J. Immunol. 147:2697-2705.
13. b complex to T cells. J. Immunol. 150:2724-2736.
14. Hahn, Y.S., V.L. Braciale, and T.J. Braciale. 1991. Presentation of viral antigen to class I major histocompatibility complex-restricted cytotoxic T lymphocytes. Recognition of an immunodominant influenza hemagglutinin site by cytotoxic T lymphocytes is independent of the position of the site in the hemagglutinin translation product. J. Exp. Med. 174:733-736.
15. Wang, R.-F., M.R. Parkhurst, Y. Kawakami, P.F. Robbins, and S.A. Rosenberg. 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.
16. Kozak, M. 1978. How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell. 15:1109-1123.
17. Kozak, M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
18. Kozak, M. 1992. A consideration of alternative models for the initiation of translation in eukaryotes. Crit. Rev. Biochem. Mol. Biol. 27:385-402.
19. Kozak, M. 1984. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucl. Acids Res. 12:857-872.
20. Kozak, M. 1987. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucl. Acids Res. 15:8125-8148.
21. Kozak, M. 1989. Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol. Cell. Biol. 9:5073-5080.
22. Morlé, F., B. Lopez, T. Henni, and J. Godet. 1985. α-Thalassaemia associated with the deletion of two nucleotides at position -2 and -3 preceding the AUG codon. EMBO (Eur. Mol. Biol. Organ.) J. 4:1245-1250.
23. Kozak, M. 1987. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J. Mol. Biol. 196:947-950.
24. Bullock, T.N.J., and L.C. Eisenlohr. 1996. Ribosomal scanning past the primary initiation codon as a mechanism for expression of CTL epitopes encoded in alternative reading frames. J. Exp. Med. 184:1319-1330.
25. Bonetti, B., L. Fu, J. Moon, and D.M. Bedwell. 1995. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J. Mol. Biol. 251:334-345.
26. Eisenlohr, L.C., I. Bacik, J.R. Bennink, K. Bernstein, and J.W. Yewdell. 1992. Expression of a membrane protease enhances presentation of endogenous antigens to MHC class I-restricted T lymphocytes. Cell. 71:963-972.
27. Yewdell, J.W., J.R. Bennink, G.L. Smith, and B. Moss. 1985. Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA. 82:1785-1789.
28. Luukkonen, B.G.M., W. Tan, and S. Schwartz. 1995. Efficiency of reinitiation of translation on human immunodeficiency virus type 1 mRNAs is determined by the length of the upstream open reading frame and by intercistronic distance. J. Virol. 69:4086-4094.
29. Abastado, J.-P., P.F. Miller, B.M. Jackson, and A.G. Hinnebusch. 1991. Suppression of ribosomal reinitiation at upstream open reading frames in amino acid-starved cells forms the basis for GCN4 translational control. Mol. Cell. Biol. 11:486-496.
30. Kozak, M. 1987. Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol. Cell. Biol. 7:3438-3445.
31. Kozak, M. 1995. Adherence to the first-AUG rule when a second AUG codon follows closely upon the first. Proc. Natl. Acad. Sci. USA. 92:2662-2666.
32. Kozak, M. 1988. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 44:283-292.
33. b major histocompatibility complex class I molecule to alloreactive T cells. J. Exp. Med. 182:1739-1750.
34. Christinck, E.R., M.A. Luscher, B.H. Barber, and D.B. Williams. 1991. Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature (Lond.). 352:67-70.
35. Eisen, H.N., Y. Sykulev, and T.J. Tsomides. 1996. Antigen-specific T-cell receptors and their reactions with complexes formed by peptides with major histocompatibility complex proteins. Adv. Prot. Chem. 49:1-56.
36. Yellen-Shaw, A.J., E.J. Wherry, G.C. Dubois, and L.C. Eisenlohr. 1997. Point mutation flanking a CTL epitope ablates in vitro and in vivo recognition of a full-length viral protein. J. Immunol. 158:3227-3234.
37. Antón, L.C., J.W. Yewdell, and J.R. Bennink. 1997. MHC class I-associated peptides produced from endogenous gene products with vastly different efficiencies. J. Immunol. 158:2535-2542.
38. Daly, D., P. Nguyen, D.L. Woodland, and M.A. Blackman. 1995. Immunodominance of major histocompatibility complex class I-restricted influenza virus epitopes can be influenced by the T-cell receptor repertoire. J. Virol. 69:7416-7422.
39. Fearon, K., V. McClendon, B. Bonetti, and D.M. Bedwell. 1994. Premature translation termination mutations are efficiently suppressed in a highly conserved region of yeast Ste6p, a member of the ATP-binding cassette (ABC) transporter family. J. Biol. Chem. 269:17802-17808.
40. Kozak, M. 1986. Regulation of protein synthesis in virus-infected animal cells. Adv. Virus Res. 31:229-292.
41. Donzé, O., P. Damay, and P.-F. Spahr. 1995. The first and third uORFs in RSV leader RNA are efficiently translated: implications for translational regulation and viral RNA packaging. Nucl. Acids Res. 23:861-868.