Specific proteolytic cleavages limit the diversity of the pool of peptides available to MHC class I molecules in living cells

Journal of Immunology

Volumn 162, Issue 8, 1999, Pages 4712-4719

  Serwold, Thomas ^a   Shastri, Nilabh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE C; CELL EXTRACT; LACTACYSTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OVALBUMIN; OVALBUMIN [139-265]; OVALBUMIN [257-264]; PEPTIDE; PROTEASOME; PROTEASOME INHIBITOR; PROTEINASE; PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LINE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; T LYMPHOCYTE;

EID: 0033561553     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. York, I. A., and K. L. Rock. 1996. Antigen processing and presentation by the class I major histocompatibility complex. Annu. Rev. Immunol. 14:369.
2. Rammensee, H. G., K. Falk, and O. Rotzschke. 1993. Peptides naturally presented by MHC class I molecules. Annu. Rev. Immunol. 11:213.
3. Hunt, D. F., R. A. Henderson, J. Shabanowitz, K. Sakaguchi, H. Michel, N. Sevilir, A. L. Cox, E. Appella, and V. H. Engelhard. 1992. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science 255:1261.
4. Falk, K., O. Rotzschke, K. Deres, J. Metzger, G. Jung, and H. G. Rammensee. 1991. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. J. Exp. Med. 174:425.
5. Henderson, R. A., A. L. Cox, K. Sakaguchi, E. Appella, J. Shabanowitz, D. F. Hunt, and V. H. Engelhard. 1993. Direct identification of an endogenous peptide recognized by multiple HLA-A2.1-specific cytotoxic T cells. Proc. Natl. Acad. Sci. USA 90:10275.
6. Rotzschke, O., K. Falk, K. Deres, H. Schild, M. Norda, J. Metzger, G. Jung, and H. G. Rammensee. 1990. Isolation and analysis of naturally processed viral peptides as recognized by cytotoxic T cells. Nature 348:252.
7. Van Bleek, G. M., and S. G. Nathenson. 1990. Isolation of an endogenously processed immunodominant viral peptide from the class I H-2Kb molecule. Nature 348:213.
8. Rotzschke, O., K. Falk, S. Stevanovic, G. Jung, P. Walden, and H. G. Rammensee. 1991. Exact prediction of a natural T cell epitope. Eur. J. Immunol. 21:2891.
9. Malarkannan, S., S. Goth, D. R. Buchholz, and N. Shastri. 1995. The role of MHC class I molecules in the generation of endogenous peptide/MHC complexes. J. Immunol. 154:585.
10. Falk, K., O. Rotzschke, S. Stevanovic, G. Jung, and H. G. Rammensee. 1991. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351:290.
11. Shastri, N., T. Serwold, and P. Paz. 1998. Reading within the lines: naturally processed peptides displayed by MHC class I molecules. Curr. Opin. Immunol. 10:137.
12. Pamer, E., and P. Cresswell. 1998. Mechanisms of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16:323.
13. 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.
14. Heemels, M. T., and H. Ploegh. 1995. Generation, translocation, and presentation of MHC class I-restricted peptides. Annu. Rev. Biochem. 64:463.
15. Rock, K. L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A. L. Goldberg. 1994. 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.
16. Neefjes, J. J., F. Momburg, and G. J. Hammerling. 1993. Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. [Published erratum appears in 1994; Science;264:16]. Science 261:769.
17. Shepherd, J. C., T. N. Schumacher, P. G. Ashton-Rickardt, S. Imaeda, H. L. Ploegh, C. A. Janeway, Jr., and S. Tonegawa. 1993. TAP1-dependent peptide translocation in vitro is ATP dependent and peptide selective. [Published erratum appears in 1993; Cell 75:613]. Cell 74:577.
18. Jackson, M. R., M. R. Cohen-Doyle, P. A. Peterson, and D. B. Williams. 1994. Regulation of MHC class I transport by the molecular chaperone, calnexin (p88, IP90). Science 263:384.
19. Ortmann, B., M. J. Androlewicz, and P. Cresswell. 1994. MHC class I/β 2-microglobulin complexes associate with TAP transporters before peptide binding. Nature 368:864.
20. Ortmann, B., J. Copeman, P. J. Lehner, B. Sadasivan, J. A. Herberg, A. G. Grandea, S. R. Riddell, R. Tampe, T. Spies, J. Trowsdale, et al. 1997. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 277:1306.
21. Peace-Brewer, A. L., L. G. Tussey, M. Matsui, G. Li, d. G. Quinn, and J. A. Frelinger. 1996. A point mutation in HLA-A*0201 results in failure to bind the TAP complex and to present virus-derived peptides to CTL. Immunity 4:505.
22. Suh, W. K., M. F. Cohen-Doyle, K. Fruh, K. Wang, P. A. Peterson, and D. B. Williams. 1994. Interaction of MHC class I molecules with the transporter associated with antigen processing. Science 264:1322.
23. Hughes, E. A., and P. Cresswell. 1998. The thiol oxidoreductase ERp57 is a component of the MHC class I peptide-loading complex. Curr. Biol 8:709.
24. Lindquist, J. A., O. N. Jensen, M. Mann, and G. J. Haemmerling. 1998. ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J. 17:2186.
25. Morrice, N. A., and S. J. Powis. 1998. A role for thiol-dependent reductase ERp57 in the assembly of MHC class I molecules. Curr. Biol. 8:713.
26. Yewdell, J. W., and J. R. Bennink. 1989. Brefeldin A specifically inhibits presentation of protein antigens to cytotoxic T lymphoctyes. Science 244:1072.
27. Neisig, A., J. Roelse, A. J. Sijts, F. Ossendorp, M. C. Feltkamp, W. M. Kast, C. J. Melief, and J. J. Neefjes. 1995. Major differences in transporter associated with antigen presentation (TAP)-dependent translocation of MHC class I-presentable peptides and the effect of flanking sequences. J. Immunol. 154:1273.
28. Ossendorp, F., M. Eggers, A. Neisig, T. Ruppert, M. Groettrup, A. Sijts, E. Mengede, P. M. Kloetzel, J. Neefjes, U. Koszinowski, et al. 1996. A single residue exchange within a viral CTL epitope alters proteasome-mediated degradation resulting in lack of antigen presentation. Immunity 5:115.
29. Gaczynska, M., K. L. Rock, and A. L. Goldberg. 1993. γ-Interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. [Published erratum appears in 1995; Nature 374:290]. Nature 365:264.
30. Driscoll, J., M. G. Brown, D. Finley, and J. J. Monaco. 1993. MHC-linked LMP gene products specifically alter peptidase activities of the proteasome. Nature 365:262.
31. Heemels, M. T., and H. L. Ploegh. 1994. Substrate specificity of allelic variants of the TAP peptide transporter. Immunity 1:775.
32. Momburg, F., J. Roelse, J. C. Howard, G. W. Butcher, G. J. Hammerling, and J. J. Neefjes. 1994. Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature 367:648.
33. Powis, S. J., L. L. Young, E. Joly, P. J. Barker, L. Richardson, R. P. Brandt, C. J. Melief, J. C. Howard, and G. W. Butcher. 1996. The rat cim effect: TAP allele-dependent changes in a class I MHC anchor motif and evidence against C-terminal trimming of peptides in the ER. Immunity 4:159.
34. Niedermann, G., S. Butz, H. G. Ihlenfeldt, R. Grimm, M. Lucchiari, H. Hoschutzky, G. Jung, B. Maier, and K. Eichmann. 1995. Contribution of proteasome-mediated proteolysis to the hierarchy of epitopes presented by major histocompatibility complex class I molecules. Immunity 2:289.
35. Deng, Y., J. W. Yewdell, L. C. Eisenlohr, and J. R. Bennink. 1997. MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J. Immunol. 158:1507.
36. Dick, T. P., T. Ruppert, M. Groettrup, P. M. Kloetzel, L. Kuehn, U. H. Koszinowski, S. Stevanovic, H. Schild, and H. G. Rammensee. 1996. Coordinated dual cleavages induced by the proteasome regulator PA28 lead to dominant MHC ligands. Cell 86:253.
37. Androlewicz, M. J., and P. Cresswell. 1996. How selective is the transporter associated with antigen processing? Immunity 5:1.
38. Karttunen, J., S. Sanderson, and N. Shastri. 1992. Detection of rare antigen-presenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens. Proc. Natl. Acad. Sci. USA 89:6020.
39. Shastri, N., and F. Gonzlalez. 1993. Endogenous generation and presentation of the ovalbumin peptide/Kb complex to T cells. J. Immunol. 150:2724.
40. Shastri, N., T. Serwold, and F. Gonzalez. 1995. Presentation of endogenous peptide/MHC class I complexes is profoundly influenced by specific C-terminal flanking residues. J. Immunol. 155:4339.
41. Sanderson, S., and N. Shastri. 1994. LacZ inducible, antigen/MHC-specific T cell hybrids. Int. Immunol. 6:369.
42. Kuhn, R. W., K. A. Walsh, and H. Neurath. 1974. Isolation and partial characterization of an acid carboxypeptidase from yeast. Biochemistry 13:3871.
43. Hayashi, R., S. Aibara, and T. Hata. 1970. A unique carboxypeptidase activity of yeast proteinase C. Biochim. Biophys. Acta 212:359.
44. Falk, K., O. Rotzschke, and H. G. Rammensee. 1990. Cellular peptide composition governed by major histocompatibility complex class I molecules. Nature 348:248.
45. Storkus, W. J., H. J. d. Zeh, R. D. Salter, and M. T. Lotze. 1993. Identification of T-cell epitopes: rapid isolation of class I-presented peptides from viable cells by mild acid elution. J. Immunother. 14:94.
46. Yellen-Shaw, A. J., C. E. Laughlin, R. M. Metrione, and L. C. Eisenlohr. 1997. Murine transporter associated with antigen presentation (TAP) preferences influence class I-restricted T cell responses. J. Exp. Med. 186:1655.
47. Joyce, S., K. Kuzushima, G. Kepecs, R. H. Angeletti, and S. G. Nathenson. 1994. Characterization of an incompletely assembled major histocompatibility class I molecule (H-2Kb) associated with unusually long peptides: implications for antigen processing and presentation. Proc. Natl. Acad. Sci. USA 91:4145.
48. Braell, W. A., and H. F. Lodish. 1982. Ovalbumine utilizes an NH2-terminal signal sequence. J. Biol. Chem. 257:4578.
49. Fenteany, G., R. F. Standaert, W. S. Lane, S. Choi, E. J. Corey, and S. L. Schreiber. 1995. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystine. Science 268:726.
50. Fremont, D. H., M. Matsumura, E. A. Stura, P. A. Peterson, and I. A. Wilson. 1992. Crystal structures of two viral peptides in complex with murine MHC class I H-2Kb. Science 257:919.
51. Collins, E. J., D. N. Garboczi, and D. C. Wiley. 1994. Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature 371:626.
52. Guo, H. C., T. S. Jardetzky, T. P. Garrett, W. S. Lane, J. L. Strominger, and D. C. Wiley. 1992. Different length peptides bind to HLA-Aw68 similarly at their ends but bulge out in the middle. Nature 360:364.
53. 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.
54. Villanueva, M. S., P. Fischer, K. Feen, and E. G. Pamer. 1994. Efficiency of MHC class I antigen processing: a quantitative analysis. Immunity 1:479.
55. Craiu, A., T. Akopian, A. Goldberg, and K. L. Rock. 1997. Two distinct proteolytic processes in the generation of a major histocompatibility complex class I-presented peptide. Proc. Natl. Acad. Sci. USA 94:10850.
56. Benham, A. M., M. Gromme, and J. Neefjes. 1998. Allelic differences in the relationship between proteasome activity and MHC class I peptide loading. J. Immunol. 161:83.
57. Glas, R., M. Bogyo, J. S. McMaster, M. Gaczynska, and H. L. Ploegh. 1998. A proteolytic system that compensates for loss of proteasome function. Nature 392: 618.
58. Luckey, C. J., G. M. King, J. A. Marto, S. Venketeswaran, B. F. Maier, V. L. Crotzer, T. A. Colella, J. Shabanowitz, D. F. Hunt, and V. H. Engelhard. 1998. Proteasomes can either generate or destroy MHC class I epitopes: evidence for nonproteasomal epitope generation in the cytosol. J. Immunol. 161:112.
59. Lopez, D., and M. Del Val. 1997. Selective involvement of proteasomes and cysteine proteases in MHC class I antigen presentation. J. Immunol. 159:5769.
60. Schmidtke, G., M. Eggers, T. Ruppert, M. Groettrup, U. H. Koszinowski, and P. M. Kloetzel. 1998. Inactivation of a defined active site in the mouse 20S proteasome complex enhances major histocompatibility complex class I antigen presentation of a murine cytomegalovirus protein. J. Exp. Med. 187:1641.
61. Vinitsky, A., L. C. Anton, H. L. Snyder, M. Orlowski, J. R. Bennink, and J. W. Yewdell. 1997. The generation of MHC class I-associated peptides is only partially inhibited by proteasome inhibitors: involvement of nonproteasomal cytosolic proteases in antigen processing? J. Immunol. 159:554.