Quantitative aspects of T cell activation - Peptide generation and editing by MHC class I molecule

Seminars in Immunology

Volumn 11, Issue 6, 1999, Pages 375-384

  Stevanovic, Stefan ^a   Schild, Hansjorg ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Antigen processing; MHC ligands; Peptide motifs; Proteasome

Indexed keywords

CELL PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; PROTEASOME; PROTEIN SUBUNIT;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CYTOSOL; HUMAN; NONHUMAN; PROTEIN DEGRADATION; PROTEIN TRANSPORT; REVIEW; SPECIES DIFFERENCE; T LYMPHOCYTE ACTIVATION;

EID: 0033399166     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1006/smim.1999.0195     Document Type: Article

References (85)

1. Valitutti S, Muller S, Cella M, Padovan E, Lanzavecchia A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature. 375:1995;148-151.
2. Valitutti S, Lanzavecchia A. Serial triggering of TCRs: a basis for the sensitivity and specificity of antigen recognition. Immunol Today. 18:1997;299-304.
3. Davis MM, Boniface JJ, Reich Z, Lyons D, Hampl J, Arden B, Chien Y. Ligand recognition by alpha beta T cell receptors. Annu Rev Immunol. 16:1998;523-544.
4. Rogers S, Wells R, Rechsteiner M. The PEST hypothesis. Science. 234:1988;364-368.
5. Varshavsky A. The N-end rule. Cell. 69:1992;725-735.
6. Glotzer M, Murray AW, Kirschner MW. Cyclin is degraded by the ubiquitin pathway. Nature. 349:1991;132-138.
7. Yewdell JW, Anton LC, Bennink JR. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J Immunol. 157:1996;1823-1826.
8. Groll M, Ditzel L, Löwe J, Stock D, Bochtler M, Bartunik HD, Huber R. Structure of 20S proteasome from yeast at 2.4 Angstrom resolution. Nature. 386:1997;463-471.
9. Hilt W, Wolf DH. Proteasomes: destruction as a programme. Trends Biochem Sci. 21:1996;96-102.
10. Dick TP, Ruppert T, Groettrup M, Kloetzel PM, Kuehn L, Koszinowski UH, Stevanović S, Schild H, Rammensee HG. Coordinated dual cleavages induced by the proteasome regulator PA28 lead to dominant MHC ligands. Cell. 86:1996;253-262.
11. Niedermann G, Grimm R, Geier E, Maurer M, Realini C, Gartmann C, Soll J, Omura S, Rechsteiner MC, Baumeister W, Eichmann K. Potential immunocompetence of proteolytic fragments produced by proteasomes before evolution of the vertebrate immune system. J Exp Med. 186:1997;209-220.
12. Cox JH, Galardy P, Bennink JR, Yewdell JW. Presentation of endogenous and exogenous antigens is not affected by inactivation of E1 ubiquitin-activating enzyme in temperature-sensitive cell lines. J Immunol. 154:1995;511-519.
13. Michalek MT, Grant EP, Gramm C, Goldberg AL, Rock KL. A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature. 363:1993;552-554.
14. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D, Goldberg AL. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell. 78:1994;761-771.
15. Cerundolo V, Benham A, Braud V, Mukherjee S, Gould K, Macino B, Neefjes J, Townsend A. The proteasome-specific inhibitor lactacystin blocks presentation of cytotoxic T lymphocyte epitopes in human and murine cells. Eur J Immunol. 27:1997;336-341.
16. Niedermann G, Butz S, Ihlenfeldt HG, Grimm R, Lucchiari M, Hoschutzky H, Jung G, Maier B, Eichmann K. Contribution of proteasome-mediated proteolysis to the hierarchy of epitopes presented by major histocompatibility complex class I molecules. Immunity. 2:1995;289-299.
17. Eggers M, Boes Fabian B, Ruppert T, Kloetzel PM, Koszinowski UH. The cleavage preference of the proteasome governs the yield of antigenic peptides. J Exp Med. 182:1995;1865-1870.
18. Groettrup M, Soza A, Eggers M, Kuehn L, Dick TP, Schild H, Rammensee HG, Koszinowski UH, Kloetzel PM. A role for the proteasome regulator PA28alpha in antigen presentation. Nature. 381:1996;166-168.
19. Ossendorp F, Eggers M, Neisig A, Ruppert T, Groettrup M, Sijts A, Mengede E, Kloetzel PM, Neefjes J, Koszinowski U, Melief C. A single residue exchange within a viral CTL epitope alters proteasome-mediated degradation resulting in lack of antigen presentation. Immunity. 5:1996;115-124.
20. Rammensee HG, Falk K, Rötzschke O. MHC molecules as peptide receptors. Curr Opin Immunol. 5:1993;35-44.
21. Dick TP, Stevanović S, Keilholz W, Ruppert T, Koszinowski U, Schild H, Rammensee HG. The making of the dominant MHC class I ligand SYFPEITHI. Eur J Immunol. 28:1998;2478-2486.
22. Falk K, Rötzschke O, Rammensee HG. Cellular peptide composition governed by major histocompatibility complex class I molecules. Nature. 348:1990;248-251.
23. Beninga J, Rock KL, Goldberg AL. Interferon-gamma can stimulate post-proteasomal trimming of the N terminus of an antigenic peptide by inducing leucine aminopeptidase. J Biol Chem. 273:1998;18734-18742.
24. Wilk S, Wilk E, Magnusson RP. Purification, characterization, and cloning of a cytosolic aspartyl aminopeptidase. J Biol Chem. 273:1998;15961-15970.
25. Glas R, Bogyo M, McMaster JS, Gaczynska M, Ploegh HL. A proteolytic system that compensates for loss of proteasome function. Nature. 392:1998;618-622.
26. Coux O, Tanaka K, Goldberg AL. Structure and functions of the 20S and 26S proteasomes. Annu Rev Immunol. 65:1996;801-847.
27. Cardozo C, Vinitsky A, Michaud C, Orlowski M. Evidence that the nature of amino acid residues in the P3 position directs substrates to distinct catalytic sites of the pituitary multicatalytic proteinase complex (proteasome). Biochemistry. 33:1994;6483-6489.
28. Vinitsky A, Cardozo C, Sepp Lorenzino L, Michaud C, Orlowski M. Inhibition of the proteolytic activity of the multicatalytic proteinase complex (proteasome) by substrate-related peptidyl aldehydes. J Biol Chem. 269:1994;29860-29866.
29. del Val M, Schlicht HJ, Ruppert T, Reddehase MJ, Koszinowski UH. Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell. 66:1991;1145-1153.
30. Craiu A, Gaczynska M, Akopian T, Gramm CF, Fenteany G, Goldberg AL, Rock KL. Lactacystin and clasto-lactacystin beta-lactone modify multiple proteasome beta-subunits and inhibit intracellular protein degradation and major histocompatibility complex class I antigen presentation. J Biol Chem. 272:1997;13437-13445.
31. Stoltze L, Dick TP, Deeg M, Pömmerl B, Rammensee H-G, Schild H. Generation of the vesicular stomatitis virus nucleoprotein cytotoxic T lymphocyte epitope requires proteasome-dependent and -independent proteolytic activities. Eur J Immunol. 28:1998;4029-4036.
32. Heinemeyer W, Fischer M, Krimmer T, Stachon U, Wolf DH. The activ e sites of the eukaryotic 20S proteasome and their involvement in subunit precursor processing. J Biol Chem. 272:1997;25200-25209.
33. Nussbaum AK, Dick TP, Keilholz W, Schirle M, Stevanovićs, Dietz K, Heinemeyer W, Groll M, Wolf DH, Huber R, Rammensee H-G, Schild H. Cleavage motifs of the yeast 20S proteasome beta-subunits deduced from digests of enolase 1. Proc Natl Acad Sci USA. 95:1998;12504-12509.
34. Shimbara N, Ogawa K, Hidaka Y, Nakajima H, Yamasaki N, Niwa S, Tanahashi N, Tanaka K. Contribution of proline residue for efficient production of MHC class I ligands by proteasomes. J Biol Chem. 273:1998;23062-23071.
35. Wenzel T, Eckerskorn C, Lottspeich F, Baumeister W. Existence of a molecular ruler in proteasomes suggested by analysis of degradation products. FEBS Lett. 349:1998;205-209.
36. Androlewicz MJ, Anderson KS, Cresswell P. Evidence that transporters associated with antigen processing translocate a major histocompatibility complex class I-binding peptide into the endoplasmic reticulum in an ATP-dependent manner. Proc Natl Acad Sci USA. 90:1993;9130-9134.
37. Shepherd JC, Schumacher TN, Ashton Rickardt PG, Imaeda S, Ploegh HL, Janeway CA Jr., Tonegawa S. TAP1-dependent peptide translocation in vitro is ATP dependent and peptide selective. Cell. 74:1993;577-584.
38. Neefjes JJ, Momburg F, Hämmerling GJ. Selective and ATP-depen dent translocation of peptides by the MHC- encoded transporter. Science. 261:1993;769-771.
39. Koopmann JO, Hämmerling GJ, Momburg F. Generation, intracellu lar transport and loading of peptides associated with MHC class I molecules. Curr Opin Immunol. 9:1997;80-88.
40. Pamer E, Cresswell P. Mechanisms of MHC class I-restricted antigen processing. Annu Rev Immunol. 16:1998;323-358.
41. Srivastava PK, Udono H, Blachere NE, Li Z. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics. 39:1994;93-98.
42. Arnold D, Faath S, Rammensee H, Schild H. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. J Exp Med. 182:1995;885-889.
43. Srivastava PK, Menoret A, Basu S, Binder RJ, McQuade KL. Heat shock proteins come of age: primitive functions acquire new roles in an adaptive world. Immunity. 8:1998;657-665.
44. Lammert E, Stevanović S, Brunner J, Rammensee HG, Schild H. Prot ein disulfide isomerase is the dominant acceptor for peptides translocated into the endoplasmic reticulum. Eur J Immunol. 27:1997;1685-1690.
45. Spee P, Neefjes J. TAP-translocated peptides specifically bind pr oteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Eur J Immunol. 27:1997;2441-2449.
46. Koopmann JO, Post M, Neefjes JJ, Hämmerling GJ, Momburg F. Translocation of long peptides by transporters associated with antigen processing (TAP). Eur J Immunol. 26:1996;1720-1728.
47. Anderson K, Cresswell P, Gammon M, Hermes J, Williamson A, Zweerink H. Endogenously synthesized peptide with an endoplasmic reticulum signal sequence sensitizes antigen processing mutant cells to class I-restricted cell-mediated lysis. J Exp Med. 174:1991;489-492.
48. Elliott T, Willis A, Cerundolo V, Townsend A. Processing of major histocompatibility class I-restricted antigens in the endoplasmic reticulum. J Exp Med. 181:1995;1481-1491.
49. Rammensee HG, Falk K, Rötzschke O. Peptides naturally presented by MHC class I molecules. Annu Rev Immunol. 11:1993;213-244.
50. Hunt DF, Henderson RA, Shabanowitz J, Sakaguchi K, Michel H, Sevilir N, Cox AL, Appella E, Engelhard VH. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science. 255:1992;1261-1263.
51. +T cells binds very tightly to the restricting class I major histocompatibility complex protein on intact cells but not to the purified class I protein. Proc Natl Acad Sci USA. 88:1991;11276-11280.
52. Christinck ER, Luscher MA, Barber BH, Williams DB. Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature. 352:1991;67-70.
53. Falk K, Rötzschke O, Deres K, Metzger J, Jung G, Rammensee HG. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. J Exp Med. 174:1991;425-434.
54. McMichael A. Natural selection at work on the surface of virus-infected cells. Science. 260:1993;1771-1772.
55. Falk K, Rötzschke O, Grahovac B, Schendel D, Stevanović S, Gnau V, Jung G, Strominger JL, Rammensee HG. Allele-specific ligand motifs of HLA-C molecules. Proc Natl Acad Sci USA. 90:1993;12005-12009.
56. Rötzschke O, Falk K, Stevanović S, Grahovac B, Soloski MJ, Jung G, Rammensee HG. Qa-2 molecules are peptide receptors of higher stringency than ordinary class I molecules. Nature. 361:1993;642-644.
57. Korber B, Hood L, Stroynowski I. Regulation of murine class I genes by interferons is controlled by regions located both 5′ and 3′ to the transcription initiation site. Proc Natl Acad Sci USA. 84:1987;3380-3384.
58. Fruh K, Ahn K, Peterson PA. Inhibition of MHC class I antigen processing by viral proteins. J Mol Med. 75:1997;18-27.
59. bmolecule. Nature. 348:1990;213-216.
60. Falk K, Rötzschke O, Stevanović S, Jung G, Rammensee HG. Alle le-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature. 351:1991;290-296.
61. Schmidt W, Buschle M, Zauner W, Kirlappos H, Mechtler K, Trska B, Birnstiel ML. Cell-free tumor antigen peptide-based cancer vaccines. Proc Natl Acad Sci USA. 94:1997;3262-3267.
62. Pamer EG. Direct sequence identification and kinetic analysis of an MHC class I-restricted Listeria monocytogenes CTL epitope. J Immunol. 152:1994;686-694.
63. Henderson RA, Cox AL, Sakaguchi S, Appella E, Shabanowitz J, Hunt DF, Engelhard VH. Direct identification of an endogenous peptide recognized by multiple HLA-A2.1-specific cytotoxic T cells. Proc Natl Acad Sci USA. 90:1993;10275-10279.
64. Demotz S, Grey HM, Appella E, Sette A. Characterization of a naturally processed MHC class II-restricted T-cell determinant of hen egg lysozyme. Nature. 342:1989;682-684.
65. Wallny HJ, Deres K, Faath S, Jung G, Van Pel A, Boon T, Rammensee HG. Identification and quantification of a naturally presented peptide as recognized by cytotoxic T lymphocytes specific for an immunogenic tumor variant. Int Immunol. 4:1992;1085-1090.
66. Rotzschke O, Falk K, Stevanovic S, Jung G, Walden P, Rammensee, H G. Exact prediction of a natural T cell epitope. Eur J Immunol. 21:1991;2891-2894.
67. +CTL. Mol Immunol. 31:1994;1285-1293.
68. Sykulev Y, Joo M, Vturina I, Tsomides TJ, Eisen HN. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity. 4:1996;565-571.
69. Rötzschke O, Falk K, Strominger JL. Superactivation of an immune response triggered by oligomerized T cell epitopes. Proc Natl Acad Sci USA. 94:1997;14642-14647.
70. Jardetzky TS, Lane WS, Robinson RA, Madden DR, Wiley DC. Identification of self peptides bound to purified HLA-B27. Nature. 353:1991;326-329.
71. Duncan R, McConkey EH. How many proteins are there in a typical mammalian cell? Clin Chem. 28:1982;749-755.
72. Celis JE, Rasmussen HH, Gromov P, Olsen E, Madsen P, Leffers H, Honore B, Dejgaard K, Vorum H, Kristensen DB. The human keratinocyte two-dimensional gel protein database (update 1995): mapping components of signal transduction pathways. Electrophoresis. 16:1995;2177-2240.
73. Falk K, Rötzschke O, Stevanović S, Gnau V, Sparbier K, Jung G, Rammensee HG, Walden P. Analysis of a naturally occurring HLA class I-restricted viral epitope. Immunology. 82:1994;337-342.
74. Reddehase MJ, Rothbard JB, Koszinowski UH. A pentapeptide as minimal antigenic determinant for MHC class I-restricted T lymphocytes. Nature. 337:1989;651-653.
75. Schulz M, Aichele P, Schneider R, Hansen TH, Zinkernagel RM, Hengartner H. Major histocompatibility complex binding and T cell recognition of a viral nonapeptide containing a minimal tetrapeptide. Eur J Immunol. 21:1991;1181-1185.
76. Rammensee HG, Bachmann J, Stevanović S. MHC ligands and peptide motifs. 1997;Landes Bioscience, Austin
77. Ruppert J, Sidney J, Celis E, Kubo RT, Grey HM, Sette A. Prominent role of secondary anchor residues in peptide binding to HLA-A2.1 molecules. Cell. 74:1993;929-937.
78. Zinkernagel RM, Doherty PC. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature. 1974:1974;701-702.
79. Klavinskis LS, Whitton JL, Joly E, Oldstone MBA. Vaccination and protection from a lethal viral infection: identification, incorporation, and use of a cytotoxic T lymphocyte glycoprotein epitope. Virology. 178:1990;393-400.
80. Gallimore A, Hombach J, Dumrese T, Rammensee HG, Zinkernagel RM, Hengartner H. A protective cytotoxic T cell response to a subdominant epitope is influenced by the stability of the MHC class I peptide complex and the overall spectrum of viral peptides generated within infected cells. Eur J Immunol. 28:1998;3301-3311.
81. Gavioli R, Kurilla MG, de Campos-Lima PO, Wallace LE, Dolcetti R, Murray RJ, Rickinson AB, Masucci MG. Multiple A11-restricted cytotoxic T lymphocyte epitopes of different immunogenicities in the Epstein-Barr virus-encoded nuclear antigen 4. J Virol. 67:1993;1572-1578.
82. Sijts AJAM, Neisig A, Neefjes J, Pamer EG. Two Listeria monocytogenes CTL epitopes are processed from the same antigen with different efficiencies. J Immunol. 156:1996;685-692.
83. Pamer EG, Harty JT, Bevan MJ. Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes. Nature. 353:1991;852-855.
84. Bruder D, Darji A, Gakamsky DM, Chakraborty T, Pecht I, Wehland J, Weiss S. Efficient induction of cytotoxic CD8(+) T cells against exogenous proteins: establishment and characterization of a T cell line specific for the membrane protein ActA of Listeria monocytogenes. Eur J Immunol. 28:1998;2630-2639.
85. Hill AVS, Elvin J, Willis AC, Aidoo M, Allsopp CEM, Gotch FM, Gao XM, Takiguchi M, Greenwood BM, Townsend ARM, McMichael AJ, Whittle HC. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature. 360:1992;434-439.