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PMID: 8144958 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Proteolytic processing of ovalbumin and beta-galactosidase by the proteasome to a yield antigenic peptides.

Journal of immunology (Baltimore, Md. : 1950) ·Vol. 152 ·No. 8 ·1994-04-15 ·Pages 3884-94

Dick LR, Aldrich C, Jameson SC, Moomaw CR, Pramanik BC, Doyle CK, DeMartino GN, Bevan MJ, Forman JM, Slaughter CA

Abstract

The identification of genes in the class II region of the MHC that are homologous to genes encoding subunits of the proteasome has led to intense interest in the possible role of this enzyme in the proteolytic processing of polypeptide Ags. We have tested the ability of the 20S proteasome to produce peptides that can be presented by class I molecules as targets for killing by OVA-specific and beta-galactosidase-specific CTL clones. Samples of intact OVA and beta-galactosidase were subjected to digestion in vitro by 20S proteasome purified from bovine red cells and the resulting peptide mixtures were fractionated by reverse-phase HPLC. The fractions were tested for their ability to sensitize appropriate mouse target cells for lysis by specific CTL clones. In both cases, components that under all chromatographic conditions eluted with retention times indistinguishable from synthetic peptides representing known epitopes of the naturally processed proteins were found to be able to sensitize the target cells. Moreover, in the case of OVA, the presence of the expected target peptides was demonstrated directly by amino acid sequence and mass spectrometric analysis. The results demonstrate that the pure 20S proteasome is capable of generating antigenic peptides from two proteins for presentation by class I molecules without the participation of additional components of the protein degradation system. This finding is consistent with the hypothesis of proteasome involvement in Ag processing in vivo.

MeSH Terms
Amino Acid Sequence Animals Cattle Cysteine Endopeptidases/metabolism In Vitro Techniques Mass Spectrometry Molecular Sequence Data Multienzyme Complexes/metabolism Ovalbumin/immunology,metabolism Peptide Fragments/immunology Proteasome Endopeptidase Complex beta-Galactosidase/immunology,metabolism
Chemicals
Multienzyme Complexes Peptide Fragments Ovalbumin beta-Galactosidase Cysteine Endopeptidases Proteasome Endopeptidase Complex
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Dick L R
Department of Biochemistry, University of Texas Southwestern Medical Center, Dallas 75235-9050.
Aldrich C
Jameson S C
Moomaw C R
Pramanik B C
Doyle C K
DeMartino G N
Bevan M J
Forman J M
Slaughter C A
References (54)
54 references, click to expand
  1. Subunit of the '20S' proteasome (multicatalytic proteinase) encoded by the major histocompatibility complex.
    Nature. 1991 Oct 17;353(6345):662-4 PMID: 1922384
  2. Homology of proteasome subunits to a major histocompatibility complex-linked LMP gene.
    Nature. 1991 Oct 17;353(6345):664-7 PMID: 1681432
  3. Second proteasome-related gene in the human MHC class II region.
    Nature. 1991 Oct 17;353(6345):667-8 PMID: 1922385
  4. Exact prediction of a natural T cell epitope.
    Eur J Immunol. 1991 Nov;21(11):2891-4 PMID: 1718764
  5. The minimum peptide epitope from the influenza virus matrix protein. Extra and intracellular loading of HLA-A2.
    J Immunol. 1991 Dec 15;147(12):4047-53 PMID: 1721637
  6. Flanking sequences influence the presentation of an endogenously synthesized peptide to cytotoxic T lymphocytes.
    J Exp Med. 1992 Feb 1;175(2):481-7 PMID: 1732413
  7. Ham-2 corrects the class I antigen-processing defect in RMA-S cells.
    Nature. 1992 Feb 13;355(6361):647-9 PMID: 1538753
  8. Extracellular processing of peptide antigens that bind class I major histocompatibility molecules.
    J Exp Med. 1992 May 1;175(5):1221-6 PMID: 1314884
  9. Proteasomes: protein and gene structures.
    New Biol. 1992 Mar;4(3):173-87 PMID: 1581288
  10. Serum angiotensin-1 converting enzyme activity processes a human immunodeficiency virus 1 gp160 peptide for presentation by major histocompatibility complex class I molecules.
    J Exp Med. 1992 Jun 1;175(6):1417-22 PMID: 1316930
  11. A molecular model of MHC class-I-restricted antigen processing.
    Immunol Today. 1992 May;13(5):173-9 PMID: 1386516
  12. The ubiquitin system for protein degradation.
    Annu Rev Biochem. 1992;61:761-807 PMID: 1323239
  13. Identification and localization of a cysteinyl residue critical for the trypsin-like catalytic activity of the proteasome.
    Biochemistry. 1992 Aug 18;31(32):7347-55 PMID: 1510924
  14. Dissection of major histocompatibility complex (MHC) and T cell receptor contact residues in a Kb-restricted ovalbumin peptide and an assessment of the predictive power of MHC-binding motifs.
    Eur J Immunol. 1992 Oct;22(10):2663-7 PMID: 1396971
  15. T cell receptor alpha-chain pairing determines the specificity of residue 262 within the Kb-restricted, ovalbumin257-264 determinant.
    Int Immunol. 1992 Aug;4(8):861-7 PMID: 1419956
  16. In vitro peptide binding to soluble empty class I major histocompatibility complex molecules isolated from transfected Drosophila melanogaster cells.
    J Biol Chem. 1992 Nov 25;267(33):23589-95 PMID: 1331092
  17. Proteasome subunits encoded in the MHC are not generally required for the processing of peptides bound by MHC class I molecules.
    Nature. 1992 Nov 12;360(6400):171-4 PMID: 1436094
  18. Proteasome subunits encoded by the major histocompatibility complex are not essential for antigen presentation.
    Nature. 1992 Nov 12;360(6400):174-7 PMID: 1299222
  19. Cell biology of antigen processing and presentation to major histocompatibility complex class I molecule-restricted T lymphocytes.
    Adv Immunol. 1992;52:1-123 PMID: 1442305
  20. Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination.
    Nature. 1992 Dec 10;360(6404):597-9 PMID: 1334232
  21. Evidence for the presence of five distinct proteolytic components in the pituitary multicatalytic proteinase complex. Properties of two components cleaving bonds on the carboxyl side of branched chain and small neutral amino acids.
    Biochemistry. 1993 Feb 16;32(6):1563-72 PMID: 8431436
  22. Primary in vivo responses to ovalbumin. Probing the predictive value of the Kb binding motif.
    J Immunol. 1993 Feb 15;150(4):1212-22 PMID: 7679422
  23. Presentation of endogenous peptides to MHC class I-restricted cytotoxic T lymphocytes in transport deletion mutant T2 cells.
    J Immunol. 1993 Mar 1;150(5):1763-71 PMID: 7679694
  24. The multicatalytic and 26 S proteases.
    J Biol Chem. 1993 Mar 25;268(9):6065-8 PMID: 8454582
  25. Proteasomes: multicatalytic proteinase complexes.
    Biochem J. 1993 Apr 1;291 ( Pt 1):1-10 PMID: 7682410
  26. Peptides naturally presented by MHC class I molecules.
    Annu Rev Immunol. 1993;11:213-44 PMID: 8476560
  27. The biochemistry and cell biology of antigen processing and presentation.
    Annu Rev Immunol. 1993;11:403-50 PMID: 8476568
  28. A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation.
    Nature. 1993 Jun 10;363(6429):552-4 PMID: 8389422
  29. The LMP antigens: a stable MHC-controlled multisubunit protein complex.
    Hum Immunol. 1986 Apr;15(4):416-26 PMID: 3700147
  30. Mapping the active site of papain with the aid of peptide substrates and inhibitors.
    Philos Trans R Soc Lond B Biol Sci. 1970 Feb 12;257(813):249-64 PMID: 4399049
  31. MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function, and responsiveness.
    Adv Immunol. 1979;27:51-177 PMID: 92183
  32. Identification of a fourth class of proteins linked to the murine major histocompatibility complex.
    Proc Natl Acad Sci U S A. 1982 May;79(9):3001-5 PMID: 6953443
  33. Evidence that pituitary cation-sensitive neutral endopeptidase is a multicatalytic protease complex.
    J Neurochem. 1983 Mar;40(3):842-9 PMID: 6338156
  34. H-2-linked low-molecular weight polypeptide antigens assemble into an unusual macromolecular complex.
    Nature. 1984 Jun 28-Jul 4;309(5971):797-9 PMID: 6738696
  35. A high molecular weight protease in the cytosol of rat liver. I. Purification, enzymological properties, and tissue distribution.
    J Biol Chem. 1986 Nov 15;261(32):15197-203 PMID: 3095325
  36. Introduction of soluble protein into the class I pathway of antigen processing and presentation.
    Cell. 1988 Sep 9;54(6):777-85 PMID: 3261634
  37. Defective presentation to class I-restricted cytotoxic T lymphocytes in vaccinia-infected cells is overcome by enhanced degradation of antigen.
    J Exp Med. 1988 Oct 1;168(4):1211-24 PMID: 2459295
  38. The high molecular weight multicatalytic proteinase, macropain, exists in a latent form in human erythrocytes.
    Biochim Biophys Acta. 1989 Apr 6;995(2):181-6 PMID: 2930796
  39. Antigen recognition by class I-restricted T lymphocytes.
    Annu Rev Immunol. 1989;7:601-24 PMID: 2469442
  40. Association of class I major histocompatibility heavy and light chains induced by viral peptides.
    Nature. 1989 Aug 10;340(6233):443-8 PMID: 2666863
  41. Role of substrate in reversible activation of proteasomes (multi-protease complexes) by sodium dodecyl sulfate.
    J Biochem. 1989 Sep;106(3):495-500 PMID: 2606900
  42. Characterization of naturally occurring minor histocompatibility peptides including H-4 and H-Y.
    Science. 1990 Jul 20;249(4966):283-7 PMID: 1695760
  43. The effect of mutations in the MHC class I peptide binding groove on the cytotoxic T lymphocyte recognition of the Kb-restricted ovalbumin determinant.
    Eur J Immunol. 1990 Nov;20(11):2431-7 PMID: 2253683
  44. Antigen processing. Transporters of delight.
    Nature. 1990 Dec 20-27;348(6303):674-5 PMID: 2259379
  45. MHC class II region encoding proteins related to the multidrug resistance family of transmembrane transporters.
    Nature. 1990 Dec 20-27;348(6303):738-41 PMID: 1979660
  46. Sequences encoded in the class II region of the MHC related to the 'ABC' superfamily of transporters.
    Nature. 1990 Dec 20-27;348(6303):741-4 PMID: 2259383
  47. A gene in the human major histocompatibility complex class II region controlling the class I antigen presentation pathway.
    Nature. 1990 Dec 20-27;348(6303):744-7 PMID: 2259384
  48. The multicatalytic proteinase complex, a major extralysosomal proteolytic system.
    Biochemistry. 1990 Nov 13;29(45):10289-97 PMID: 2175651
  49. Transport protein genes in the murine MHC: possible implications for antigen processing.
    Science. 1990 Dec 21;250(4988):1723-6 PMID: 2270487
  50. Degradation of oxidized insulin B chain by the multiproteinase complex macropain (proteasome).
    Biochemistry. 1991 Mar 12;30(10):2725-34 PMID: 2001360
  51. The Q7 alpha 3 domain alters T cell recognition of class I antigens.
    J Immunol. 1991 May 1;146(9):3082-90 PMID: 1849941
  52. Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter.
    Nature. 1991 May 23;351(6324):323-4 PMID: 2034277
  53. Structural and serological similarity of MHC-linked LMP and proteasome (multicatalytic proteinase) complexes.
    Nature. 1991 Sep 26;353(6342):355-7 PMID: 1922341
  54. A proteasome-related gene between the two ABC transporter loci in the class II region of the human MHC.
    Nature. 1991 Sep 26;353(6342):357-60 PMID: 1922342
Article Info
Journal
Journal of immunology (Baltimore, Md. : 1950)
Abbr.
J Immunol
ISSN
0022-1767
Published
1994-04-15
Pages
3884-94
Language
English
Region
United States
NLM ID
2985117R
PMCID
PMC2778727
Subset
IM
Grants
NIAID NIH HHS · R01 AI019335 · United States
NHLBI NIH HHS · P01 HL006296-370019 · United States
NIDDK NIH HHS · R01 DK046181 · United States
NIAID NIH HHS · AI-28382 · United States
NIAID NIH HHS · R01 AI019335-19 · United States
Howard Hughes Medical Institute · United States
NHLBI NIH HHS · P01 HL006296 · United States
NIAID NIH HHS · AI-19335 · United States
NIAID NIH HHS · AI-13111 · United States
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