Distinct proteolytic processes generate the C and N termini of MHC class I-binding peptides

Journal of Immunology

Volumn 163, Issue 11, 1999, Pages 5851-5859

  Mo, X Y ^a   Cascio, Paolo ^b   Lemerise, Kristen ^a   Goldberg, Alfred L ^b   Rock, Kenneth ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OLIGOPEPTIDE; PROTEASOME; VIRUS PROTEIN;

ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGENICITY; ARTICLE; HYBRIDOMA; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; VACCINIA;

NON-PROGRAMMATIC;

AMINOPEPTIDASES; ANTIGEN PRESENTATION; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; HISTOCOMPATIBILITY ANTIGENS CLASS I; MAJOR HISTOCOMPATIBILITY COMPLEX; MULTIENZYME COMPLEXES; NUCLEOCAPSID PROTEINS; NUCLEOPROTEINS; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; VIRAL CORE PROTEINS; VIRAL PROTEINS;

EID: 0033486008     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (53)

1. York, I. A., and K. L. Rock. 1996. Antigen processing and presentation by the class I major histocompatibility complex. Anna. Rev. Immunol. 14:369.
2. Coux, O., K. Tanaka, and A. L. Goldberg. 1996. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65:801.
3. Rock, K. L., and Goldberg, A.L. 1999. Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 17:739.
4. 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.
5. Pamer, E., and P. Cresswell. 1998. Mechanisms of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16:323.
6. 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 lactacystin. Science 268:726.
7. Dick, L. R., A. A. Cruikshank, L. Grenier, F. D. Melandri, S. L. Nunes, and R. L. Stein. 1996. Mechanistic studies on the inactivation of the proteasome by lactacystin: a central role for clasto-lactacystin β-lactone. J. Biol. Chem. 271: 7273.
8. 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 1 molecules. Cell 78:761.
9. Benham, A. M., and J. J. Neefjes. 1997. Proteasome activity limits the assembly of MHC class 1 molecules after IFN-γ stimulation. J. Immunol. 159:5896.
10. Craiu, A., M. Gaczynska, T. Akopian, C. F. Gramm, G. Fenteany, A. L. Goldberg, and K. L. Rock. 1997. Lactacystin and clasto-lactacystin β-lactone modify multiple proteasome β-subunits and inhibit intracellular protein degradation and major histocompatibility complex class I antigen presentation. J. Biol. Chem. 272:13437.
11. Harding, C. V., J France, R. Song, J. M. Farah, S. Chatterjee, M. Iqbal, and R. Siman. 1995. Novel dipeptide aldehydes are proteasome inhibitors and block the MHC-I antigen-processing pathway. J. Immunol. 155:1767.
12. Cerundolo, V., A. Benham, V. Braud, S. Mukherjee, K. Gould, B. Macino, J. Neefjes, and A. Townsend. 1997. The proteasome-specific inhibitor lactacystin blocks presentation of cytotoxic T lymphocyte epitopes in human and murine cells. Eur. J. Immunol. 27:336.
13. Brown, M. G., J. Driscoll, and J. J. Monaco. 1991. Structural and serological similarity of MHC-linked LMP and proteasome (multicatalytic proteinase) complexes. Nature 353:355.
14. Glynne, R., S. H. Powis, S. Beck, A. Kelly, L. A. Kerr, and J. Trowsdale. 1991. A proteasome-related gene between the two ABC transporter loci in the class II region of the human MHC. Nature 353:357.
15. Van Kaer, L., P. G. Ashton-Rickardt, M. Eichelberger, M. Gaczynska, K. Nagashima, K. L. Rock, A. L. Goldberg, P. C. Doherty, and S. Tonegawa. 1994. Altered peptidase and viral-specific T cell response in LMP2 mutant mice. Immunity 1:533.
16. Fehling, H. J., W. Swat, C. Laplace, R. Kuhn, K. Rajewsky, U. Muller, and H. von Boehmer. 1994. MHC class I expression in mice lacking the proteasome subunit LMP-7. Science 265:1234.
17. Cerundolo, V., A. Kelly, T. Elliott, J. Trowsdale, and A. Townsend. 1995. Genes encoded in the major histocompatibility complex affecting the generation of peptides for TAP transport. [Published erratum appears in 1995 Eur. J. Immunol. 25:1485.] Eur. J. Immunol. 25:554.
18. + proteasomes are required for the presentation of specific antigens to cytotoxic T lymphocytes. Curr. Biol. 5:923.
19. Driscoll, J., M. G. Brown, D. Finfey, and J. J. Monaco. 1993. MHC-linked LMP gene products specifically alter peptidase activities of the proteasome. Nature 365:262.
20. Gaczynska, M., K. L. Rock, and A. L. Goldberg. 1993. Gamma-interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. [Published erratum appears in 1995 Nature 374:290.] Nature 365:264.
21. Michalek, M. T., E. P. Grant, C. Gramm, A. L. Goldberg, and K. L. Rock. 1993. A role for the ubiquitin-dependent proteolytic pathway in MHC class I- restricted antigen presentation. Nature 363:552.
22. Michalek, M. T., E. P. Grant, and K. L. Rock. 1996. Chemical denaturation and modification of ovalbumin alters its dependence on ubiquitin conjugation for class I antigen presentation. J. Immunol. 157:617.
23. 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.
24. 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.
25. 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.
26. 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 329:506.
27. Madden, D. R., J. C. Gorga, J. L. Strominger, and D. C. Wiley. 1992. The three-dimensional structure of HLA-B27 at 2.1 A resolution suggests a general mechanism for tight peptide binding to MHC. Cell 70:1035.
28. Kisselev, A. F., T. N. Akopian, and A. L. Goldberg. 1998. Range of sizes of peptide products generated during degradation of different proteins by archaeal proteasomes. J. Biol. Chem. 273:1982.
29. Kisselev, A. F., T. N. Akopian, K. M. Woo, and A. L. Goldberg. 1999. The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes: implications for understanding the degradative mechanism and antigen presentation. J. Biol. Chem. 274:3363.
30. 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.
31. Harris, C. A., B. Hunte, M. R. Krauss, A. Taylor, and L. B. Epstein. 1992. Induction of leucine aminopeptidase by interferon-γ: identification by protein microsequencing after purification by preparative two-dimensional gel electrophoresis. J. Biol. Chem. 267:6865.
32. Beninga, J., K. L. Rock, and A. L. Goldberg. 1998. Interferon-γ can stimulate post-proteasomal trimming of the N terminus of an antigenic peptide by inducing leucine aminopeptidase. J. Biol. Chem. 273:18734.
33. + B cell hybridomas to H-2-restricled T cell hybridomas. Proc. Nail. Acad. Sci. USA 79:3604.
34. Deckhut, A. M., W. Allan, A. McMickle, M. Eichelberger, M. A. Blackman, P. C. Doherty, and D. L. Woodland. 1993. Prominent usage of Vβ 8.3 T cells in the H-2Db-reslricted response to an influenza A virus nucleoprotein epitope. J. Immunol. 151:2658.
35. Cole, G. A., T. L. Hogg, and D. L. Woodland. 1994. The MHC class I-restricted T cell response to Sendai virus infection in C57BL/6 mice: a single immunodominant epitope elicits an extremely diverse repertoire of T cells. Int. Immunol. 6:1767.
36. Rock, K. L., L. Rothstein, and S. Gamble. 1990. Generation of class I MHC-restricted T-T hybridomas. J. lmmunol. 145:804.
37. Gillis, S., M. M. Ferm, W. Ou, and K. A. Smith. 1978. T cell growth factor: parameters of production and a quantitative microassay for activity. J. Immunol. 120:2027.
38. 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.
39. Grant, E. P., M. T. Michalek, A. L. Goldberg, and K. L. Rock. 1995. Rate of antigen degradation by the ubiquitin-proteasome pathway influences MHC class I presentation. J. Immunol. 155:3750.
40. Stoltze, L., T. P. Dick, M. Deeg, B. Pommerl, H. G. Rammensee, and H. Schild. 1998. Generation of the vesicular stomatitis virus nucleoprotein cytotoxic T lymphocyte epitope requires proteasome-dependent and -independent proteolytic activities. Eur. J. Immunol. 28:4029.
41. Taylor, A. 1993. Aminopeptidases: structure and function. FASEB J. 7:290.
42. Taylor, A., M. Daims, J. Lee, and T. Surgenor. 1982. Identification and quantification of leucine aminopeptidase in aged normal and cataractous human lenses and ability of bovine lens LAP to cleave bovine crystallins. Curr. Eye Res. 2:47.
43. Anton, L. C., H. L. Snyder, J. R. Bennink, A. Vinitsky, M. Orlowski, A. Porgador, and J. W. Yewdell. 1998. Dissociation of proteasomal degradation of biosynthesized viral proteins from generation of MHC class I-associated antigenic peptides. J. Immunol. 160:4859.
44. Akopian, T. N., A. F. Kisselev, and A. L. Goldberg. 1997. Processive degradation of proteins and other catalytic properties of the proteasome from Thermoplasma acidophilum. J. Biol. Chem. 272:1791.
45. Cardozo, C., C. Michaud, and M. Orlowski. 1999. Components of the bovine pituitary multicatalytic proleinase complex (proteasome) cleaving bonds after hydrophobic residues. Biochemistry 38:9768.
46. Dick, L. R., C. Aldrich, S. C. Jameson, C. R. Moomaw, B. C. Pramanik, C. K. Doyle, G. N. DeMartino, M. J. Bevan, J. M. Forman, and C. A. Slaughter. 1994. Proteolytic processing of ovalbumin and β-galactosidase by the proteasome to a yield antigenic peptides. J. Immunol. 152:3884.
47. 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.
48. Snyder, H. L., J. W. Yewdell, and J. R. Bennink. 1994. Trimming of antigenic peptides in an early secretory compartment. J. Exp. Med. 180:2389.
49. Elliott, T., A Willis, V. Cerundolo, and A. Townsend. 1995. Processing of major histocompatibility class I-restricted antigens in the endoplasmic reticulum. J. Exp. Med. 181:1481.
50. 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.
51. 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.
52. Groettrup, M., A. Soza, M. Eggers, L. Kuehn, T. P. Dick, H. Schild, H. G. Rammensee, U. H Koszinowski, and P. M. Kloetzel. 1996. A role for the proteasome regulator PA28α in antigen presentation. Nature 381:166.
53. 2-microglobulin is necessary for Kb class I major histocompatibility complex binding of exogenous peptides. Proc. Natl. Acad. Sci. USA 87:7517.