The class I antigen-processing pathway for the membrane protein tyrosinase involves translation in the endoplasmic reticulum and processing in the cytosol

Journal of Experimental Medicine

Volumn 187, Issue 1, 1998, Pages 37-48

  Mosse, Claudio A ^a   Meadows, Leslie ^b   Luckey, Chance J ^a   Kittlesen, David J ^a   Huczko, Eric L ^a   Slingluff Jr , Craig L ^a   Shabanowitz, Jeffrey ^b   Hunt, Donald F ^a,b   Engelhard, Victor H ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MONOPHENOL MONOOXYGENASE; PROTEASOME;

ANTIGEN PRESENTATION; ARTICLE; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOBLOTTING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE; CYTOSOL; ENDOPLASMIC RETICULUM; EPITOPES; GENE EXPRESSION; GENES, MHC CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA-A ANTIGENS; HUMANS; MEMBRANE PROTEINS; MONOPHENOL MONOOXYGENASE; OLIGODEOXYRIBONUCLEOTIDES; PROTEIN BIOSYNTHESIS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0031973735     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.1.37     Document Type: Article

References (74)

1. Engelhard, V.H. 1994. Structure of peptides associated with MHC class I molecules. Curr. Opin. Immunol. 6:13-23.
2. Goldberg, A.L., and K.L. Rock. 1992. Proteolysis, proteasomes and antigen presentation. Nature. 357:375-379.
3. Bevan, M.J. 1995. Antigen presentation to cytotoxic T lymphocytes in vivo. J. Exp. Med. 182:639-641.
4. Hill, A., and H. Ploegh. 1995. Getting the inside out: the transporter associated with antigen processing (TAP) and the presentation of viral antigen. Proc. Natl. Acad. Sci. USA. 92: 341-343.
5. Germain, R.N. 1994. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell. 76:287-299.
6. Monaco, J.J. 1995. Pathways for the processing and presentation of antigens to T cells. J. Leukocyte Biol. 57:543-547.
7. 2-microglobulin complexes associate with TAP transporters before peptide binding. Nature. 368:864-867.
8. 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. 264:1322-1326.
9. Sadasivan, B., P.J. Lehner, B. Ortmann, T. Spies, and P. Cresswell. 1996. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity. 5:103-114.
10. Degen, E., and D.B. Williams. 1991. Participation of a novel 88-kD protein in the biogenesis of murine class I histocompatibility molecules J. Cell Biol. 112:1099-1115.
11. Henderson, R.A., H. Michel, K. Sakaguchi, J. Shabanowitz, E. Appella, D.F. Hunt, and V.H. Engelhard. 1992. HLA-A2.1 associated peptides from a mutant cell line: a second pathway of antigen presentation. Science. 255:1264-1266.
12. Wei, M.L., and P. Cresswell. 1992. HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides. Nature. 356:443-146.
13. + T cells. Nature. 364:158-161.
14. Lee, S.P., W.A. Thomas, N.W. Blake, and A.B. Rickinson. 1996. Transporter (TAP)-independent processing of a multiple membrane-spanning protein, the Epstein-Barr virus latent membrane protein 2. Eur.J. Immunol. 26:1875-1883.
15. Henderson, R.A., A.L. Cox, K. Sakaguchi, E. Appella, J. Shabanowitz, D.E. 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. 90:10275-10279.
16. Hughes, E.A., B. Ortmann, M. Surman, and P. Cresswell. 1996. The protease inhibitor, N-acetyl-L-leucyl-L-leucyl-leucyl-L-norleucinal, decreases the pool of major histocompatibility complex class I-binding peptides and inhibits peptide trimming in the endoplasmic reticulum. J. Exp. Med. 183:1569-1578.
17. Elliott, T., A. Willis, V. Cerundolo, and A. Townsend. 1995. Processing of major histocompatibiliry class I-restricted antigens in the endoplasmic reticulum. J. Exp. Med. 181:1481-1491.
18. Bacik, I., J.H. Cox, R. Anderson, J.W. Yewdell, and J.R. Bennink. 1994. TAP (transporter associated with antigen processing)-independent presentation of endogenously synthesized peptides is enhanced by endoplasmic reticulum insertion sequences located at the amino-but not carboxyl-terminus of the peptide. J. Immunol. 152:381-387.
19. Anderson, K., P. Cresswell, M. Gammon, J. Hermes, A. Williamson, and H. Zweerink. 1991. Endogenously synthesized peptide with an endoplasmic reticulum signal sequence sensitizes antigen processing mutant cells to class I-restricted cell-mediated lysis. J. Exp. Med. 174:489-492.
20. Snyder, H.L., J.W. Yewdell, and J.R. Bennink. 1994. Trimming of antigenic peptides in an early secretory compartment. J. Exp. Med. 180:2389-2394.
21. van Binnendijk, R.S., C.A. van Baalen, M.C. Poelen, P. de Vries, J. Does, V. Cerundolo, A.D. Osterhaus, and F.G. Uyt de Haag. 1992. Measles virus transmembrane fusion protein synthesized de novo or presented in immunostimulating complexes is endogenously processed for HLA class I- and class II-restricted cytotoxic T cell recognition. J. Exp. Med. 176:119-128.
22. + CTL. J Immunol. 154:6140-6156.
23. b antigens on cells lacking a functional TAP-2 transporter. J. Immunol. 149:3773-3777.
24. Aldrich, C.J., A. DeCloux, A.S. Woods, R.J. Cotter, M.J. Soloski, and J. Forman. 1994. Identification ot a TAP-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen. Cell. 79:649-658.
25. Hombach, J., H. Pircher, S. Tonegawa, and R.M. Zinkernagel. 1995. Strictly transporter of antigen presentation (TAP)-dependent presentation of an immunodominant cytotoxic T lymphocyte epitope in the signal sequence of a virus protein. J. Exp. Med. 182:1615-1619.
26. Roelse, J., M. Gromme, F. Momburg. G. Hammerling, and J. Neefjes. 1994. Trimming of TAP-translocated peptides in the endoplasmic reticulum and in the cytosol during recycling. J. Exp. Med. 180:1591-1597.
27. 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.
28. Lurquin, C., A. Van Pel, B. Mariame, E. De Plaen, J.P. Szikora, C. Janssens, M.J. Reddehase, J. Lejeune, and T. Boon. 1989. Structure of the gene of tum-transplantation antigen P91A: the mutated exon encodes a peptide recognized with Ld by cytolytic T cells. Cell. 58:293-303.
29. Boon, T., and A. Van Pel. 1989. T cell-recognized antigenic peptides derived from the cellular genome are not protein degradation products but can be generated directly by transcription and translation of short subgenic regions. A hypothesis [see comments]. Immunogenetics. 29:75-79.
30. Sibille, C., P. Chomez, C. Wildmann, A. Van Pel, E. De Plaen, J.L. Maryanski, V. de Bergeyck, and T. Boon. 1990. Structure of the gene of tum-transplantation antigen P198: a point mutation generates a new antigenic peptide. J. Exp. Med. 172:35-45.
31. Chomez, P., E. De Plaen, A. Van Pel, C. de Smet, J.P. Szikora, C. Lurquin, A.M. Lebacq-Verheyden, and T. Boon. 1992. Efficient expression of tum-antigen P91A by transfected subgenic fragments. Immunogenetics. 35:241-252.
32. Scott, D.M., I.E. Ehrmann, P.S. Ellis, E. Simpson, A.I. Agulnik, C.E. Bishop, and M.J. Mitchell. 1995. Identification of a mouse male-specific transplantation antigen, H-Y. Neture. 376:695-698.
33. 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.
34. 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. 184:1319-1329.
35. Leonard, C.K., M.W. Spellman, L. Riddle, R.J. Harris, J.N. Thomas, and T.J. Gregory. 1990. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 265:10373-10382.
36. Ferris, R.L., C. Buck, S.A. Hammond, A.S. Woods, R.J. Cotter, M. Takiguchi, Y. Igarashi, Y. Ichikawa, and R.F. Siliciano. 1996. Class I-restricted presentation of an HIV-1 gp41 epitope containing an N-linked glycosylation site. Implications for the mechanism of processing of viral envelope proteins. J. Immunol. 156:834-840.
37. McCracken, A.A., and J.L. Brodsky. 1996. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J. Cell Biol. 132:291-298.
38. Werner, E.D., J.L. Brodsky, and A.A. McCracken. 1996. Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc. Natl. Acad. Sci. USA. 93:13797-13801.
39. Hiller, M.M., A. Finger, M. Schweiger, and D.H. Wolf. 1996. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science. 273:1725-1728.
40. Jensen, T.J., M.A. Loo, S. Pind, D.B. Williams, A.L. Goldberg, and J.R. Riordan. 1995. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell. 83:129-135.
41. Ward, C.L., S. Omura, and R.R. Kopito. 1995. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell. 83: 121-127.
42. Hughes, E.A., C. Hammond, and P. Cresswell. 1997. Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. USA 94:1896-1901.
43. Huppa, J.B., and H.L. Ploegh. 1997. The alpha chain of the T cell antigen receptor is degraded in the cytosol. Immunity. 7:113-122.
44. Kopito, R.R. 1997. ER quality control: the cytoplasmic connection. Cell. 88:427-430.
45. Yu, H., G. Kaung, S. Kobayashi, and R.R. Kopito. 1997. Cytosolic degradation of T-cell receptor alpha chains by the proteasome. J. Biol. Chem. 272:20800-20804.
46. Brodsky, J.L., and A.A. McCracken. 1997. ER-associated and proteasome-mediated protein degradation: how two topologically restricted events came together. Trends Cell Biol. 7:151-156.
47. Wiertz, E.J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T.R. Jones, T.A. Rapoport, and H.L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature. 384: 432-438.
48. Wiertz, E.J., T.R. Jones, L. Sun, M. Bogyo, H.J. Geuze, and H.L. Ploegh. 1996. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell. 84:769-779.
49. Skipper, J.C.A., R.C. Hendrickson, P.H. Gulden, V. Brichard, A. Van Pel, Y. Chen, J. Shabanowitz, T. Wolfel, C.L. Slingluff, T. Boon, D.F. Hunt, and V.H. Engelhard. 1996. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel processing pathway for membrane proteins. J. Exp. Med. 183:527-534.
50. Suzuki, T., A. Seko, K. Kitajima, Y. Inoue, and S. Inoue. 1993. Identification of peptide: N-glycanase activity in mammalian-derived cultured cells. Biochem. Biophys. Res. Commun. 194:1124-1130.
51. Wolfel, T., A. Van Pel, V. Brichard, J. Schneider, B. Seliger, K.H. Meyer zum Buschenfelde, and T. Boon. 1994. Two tyrosinase nonapeptides recognized on HLA-A2 melanomas by autologous cytolytic T lymphocytes. Eur. J. Immunol. 24: 759-764.
52. Salter, R.D., D.N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics. 21:235-246.
53. Henderson, R.A., H. Michel, K. Sakaguchi, J. Shabanowitz, E. Appella, D.F. Hunt, and V.H. Engelhard. 1992. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science. 255:1264-1266.
54. Hahn, Y.S., V.L. Braciale, and T.J. Braciale. 1991. Presentation of viral antigen to class I major histocompatibility complex-restricted cytotoxic T lymphocyte. Recognition of an immunodominant influenza hemagglutinin site by cytotoxic T lymphocyte is independent of the position of the site in the hemagglutinin translation product. J. Exp. Med. 174:733-736.
55. Mackett, M., G.L. Smith, and B. Moss. 1984. General method for product on and selection of infectious vaccinia virus recombinants expressing foreign genes. J. Virol. 49:857-864.
56. Newberg, M.H., J.P. Ridge, D.R. Vining, R.D. Salter, and V.H. Engelhard. 1992. Species specificity in the interaction of CD8 with the α3 domain of MHC class I molecules. J. Immunol. 149:136-142.
57. Hunt, D.F., R.A. Henderson, J. Shabanowitz, K. Sakaguchi, H. Michel, N. Sevilir, A. 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. 255:1261-1263.
58. 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. 268:726-731.
59. 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. 78:761-771.
60. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
61. Chen, Y.T., E. Stockert, S. Tsang, K.A. Coplan, and L.J. Old. 1995. Immunophenotyping of melanomas for tyrosinase: implications for vaccine development. Proc. Natl. Acad. Sci. USA. 92:8125-8129.
62. Androlewicz, M.J. 1996. An N-glycosylated tyrosinase epitope associates with newly synthesized MHC class I molecules in melanoma cells. Hum. Immunol. 51:81-88.
63. Deverson, E.V., I.R. Gow, W.J. Coadwell, J.J. Monaco. G.W. Butcher, and J.C. Howard. 1990. MHC class II region encoding proteins related to the multidrug resistance family of transmembrane transportors. Nature. 348:738-741.
64. Sadasivan, U., P.J. Lehner, B. Ortmann, T. Spies, and P. Cresswell. 1996. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity. 5:103-114.
65. Lee, S.H., W.A. Thomas, N.W. Blake, and A.M. Rickinson. 1996. Transporter (TAP)-independent processing of a multiple membrane-spanning protein, the Epstein-Barr virus latent membrane protein 2. Eur. J. Immunol. 26:1875-1883.
66. Yewdell, J.W., and J.R. Bennink. 1989. Brefeldin A specifically inhibits presentation of protein antigens to cytotoxic T lymphocytes. Science. 244:1072-1075.
67. Nuchtern, J.G., J.S. Bonifacino, W.E. Biddison, and R.D. Klausner. 1989. Brefeldin A implicates egress from endoplasmic reticulum in class I-restricted antigen presentation. Nature. 339:223-226.
68. Lippincott-Schwartz, J., L.C. Yuan, J.S. Bonifacino, and R.D. Klausner. 1989. Rapid redistribution of Golgi proteins in the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell. 56:801-813.
69. Jimenez, M., W.L. Maloy, and V.J. Hearing. 1989. Specific identification of an authentic clone for mammalian tyrosinase. J. Biol. Chem. 264:3397-3403.
70. Kwon, B.S., A.K. Haq, S.H. Pomerantz, and R. Halaban. 1987. Isolation and sequence of a cDNA for human tyrosinase that maps at the mouse c-albino locus. Proc. Natl. Acad. Sci. USA. 84:7473-7477.
71. Bouchard, B., B.B Fuller, S. Vijayasaradhi, and A.N. Houghton. 1989. Induction of pigmentation in mouse fibroblasts by expression of human tyrosinase cDNA. J. Exp. Med. 169: 2029-2042.
72. Arfin, S.M., R.L. Kendall, L. Hall, L.H. Weaver, A.E. Stewart, B.W. Matthews, and R.A. Bradshaw. 1995. Eukaryotic methionyl aminopeptidases: two classes of cobalt-dependent enzymes. Proc. Natl. Acad. Sci. USA. 92:7714-7718.
73. Schumacher, T.N., D.V. Kantesaria, M.T. Heemels, P.G. Ashton-Rickardt, J.C. Shepherd, K. Fruh, Y. Yang, P.A. Peterson, S. Tonegawa, and H.L. Ploegh. 1994. Peptide length and sequence specificity of the mouse TAP1/TAP2 translocator. J. Exp. Med. 179:533-540.
74. Halaban, R., E. Cheng, Y. Zhang, G. Moellmann, D. Hanlon, M. Michalak, V. Setaluri, and D.N. Hebert. 1997. Aberrant retention of tyrosinase in the endoplasmic reticulum mediates accelerated degradation of the enzyme and contributes to the dedifferentiated phenotype of amelanotic melanoma cells. Proc. Natl. Acad. Sci. USA. 94:6210-6215.