Major histocompatibility complex class I viral antigen processing in the secretory pathway defined by the trans-Golgi network protease furin

Journal of Experimental Medicine

Volumn 188, Issue 6, 1998, Pages 1105-1116

  Gil Torregrosa, Beatriz C ^a   Castaño, A Raúl ^a   Del Val, Margarita ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Antigen processing; Furin; Major histocompatibility complex class I; Secretory pathway; Virus

Indexed keywords

FURIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEINASE; VIRUS ANTIGEN;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; GOLGI COMPLEX; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; VIRUS CELL INTERACTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CYSTEINE ENDOPEPTIDASES; CYTOMEGALOVIRUS; EPITOPES; FURIN; GOLGI APPARATUS; H-2 ANTIGENS; HEPATITIS B E ANTIGENS; IMMEDIATE-EARLY PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; OLIGOPEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; SUBTILISINS; TUMOR CELLS, CULTURED;

EID: 0032555922     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.6.1105     Document Type: Article

References (53)

1. Matsumura, M., D.H. Fremont, P.A. Peterson, and I.A. Wilson. 1992. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science. 257:927-934.
2. Bouvier, M., and D.C. Wiley. 1994. Importance of peptide amino and carboxyl termini to the stability of MHC class I molecules. Science. 265:398-402.
3. Del Val, M., H. Hengel, H. Hacker, U. Hatlaub, T. Ruppert, P. Lucin, and U.H. Koszinowski. 1992. Cytomegalovirus prevents antigen presentation by blocking the transport of peptide-loaded major histocompatibility complex class I molecules into the medial-Golgi compartment. J. Exp. Med. 176:729-738.
4. York, I.A., and K.L. Rock. 1996. Antigen processing and presentation by the class I major histocompatibility complex. Annu. Rev. Immunol. 14:369-396.
5. Coux, O., K. Tanaka, and A.L. Goldberg. 1996. Structure and functions of the 20S and 26S proteasome. Annu. Rev. Biochem. 65:801-847.
6. 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 beta-galactosidase by the proteasome to yield antigenic peptides. J. Immunol. 152:3884-3894.
7. Niedermann, G., S. Butz, H.G. Ihlengeldt, 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. 2:289-299.
8. Ossendorp, F., M. Eggers, A. Neisig, T. Ruppert, M. Groettrup, A. Sijts, E. Mengedé, P.M. Kloetzel, J. Neefjes, U.H. Koszinowski, and C. Melief. 1996. A single residue exchange within a viral CTL epitope alters proteasome-mediated degradation resulting in lack of antigen presentation. Immunity. 5:115-124.
9. 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. 265:1234-1237.
10. Rock, K.L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and generation of peptides presented on MHC class I molecules. Cell. 78:761-771.
11. 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. 86:253-262.
12. Fentenay, 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.
13. Spies, T., and R. DeMars. 1991. Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature. 351:323-324.
14. Momburg, F., J. Roelse, G.J. Hämmerling, and J.J. Neefjes. 1994. Peptide size selection by the major histocompatibility complex-encoded peptide transporter. J. Exp. Med. 179:1613-1623.
15. Yang, B., Y.S. Hahn, C.S. Hahn, and T.J. Braciale. 1996. The requirement for proteasome activity in class I major histocompatibility complex antigen presentation is dictated by the length of preprocessed antigen. J. Exp. Med. 183:1545-1552.
16. López, D., and M. Del Val. 1997. Selective involvement of proteasomes and cysteine proteases in MHC class I antigen presentation. J. Immunol. 159:5769-5772.
17. 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. 94:10850-10855.
18. Roelse, J., M. Grommé, F. Momburg, G. Hämmerling, 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.
19. 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. 71:963-972.
20. 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.
21. 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.
22. Elliot, T., A. Willis, V. Cerundolo, and A. Townsend. 1995. Processing of major histocompatibility class I-restricted antigens in the endoplasmic reticulum. J. Exp. Med. 181:1481-1491.
23. 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.
24. Snyder, H.L., I. Bacik, J.R. Bennink, G. Kearns, T.W. Behrens, T. Bachi, M. Orlowski, and J.W. Yewdell. 1997. Two alternative routes of transporter associated with antigen processing (TAP)-independent major histocompatibility complex class I antigen processing. J. Exp. Med. 186:1087-1098.
25. Hammond, S.A., R.C. Bollinger, T.W. Tobery, and R.F. Siliciano. 1993. Transporter-independent processing of HIV-1 envelope protein for CD8+ T cells. Nature. 364:158-161.
26. Barr, P.J. 1991. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell. 66:1-3.
27. Tobery, T.W., and R.F. Siliciano. 1997. Targeting of HIV-1 antigens for rapid intracellular degradation enhances cytotoxic T lymphocyte (CTL) recognition and the induction of de novo CTL responses in vivo after immunization. J. Exp. Med. 185:909-920.
28. Stoller, T.J., and D. Shields. 1989. The propeptide of preprosomatostatin mediates intracellular transport and secretion of alpha-globin from mammalian cells. J. Cell Biol. 108:1647-1655.
29. Garten, W., S. Hallenberger, D. Ortman, W. Schafer, M. Vey, H. Angliker, E. Shaw, and H.D. Klenk. 1994. Processing of viral glycoproteins by the subtilisin-like endoprotease furin and its inhibition by specific peptidylchloroalkylketones. Biochimie. 76:217-225.
30. Carbone, F.R., and M.J. Bevan. 1990. Class I-restricted processing and presentation of exogenous cell-associated antigen in vivo. J. Exp. Med. 171:377-387.
31. Crumpacker, D.B., J. Alexander, and P. Cresswell. 1992. Role of endogenous peptides in murine allogeneic cytotoxic T cell responses assessed using transfectants of the antigen-processing mutant 174xCEM.T2. J. Immunol. 148:3004-3011.
32. Del Val, M., H. Volkmer, J.B. Rothbard, S. Jonjic, M. Messerle, J. Schickedanz, M.J. Reddehase, and U.H. Koszinowski. 1988. Molecular basis of cytosolic T-lymphocyte recognition of the murine cytomegalovirus immediate-early protein pp89. J. Virol. 62:3965-3972.
33. Del Val, M., H.J. Schlicht, T. Ruppert, M.J. Reddehase, and U.H. Koszinowski. 1991. Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell. 66:1145-1153.
34. Schlicht, H.-J., and G. Wasenauer. 1991. The quaternary structure, antigenicity and aggregational behavior of the secretory core protein of human hepatitis B virus are determined by its signal sequence. J. Virol. 165:6817-6825.
35. Takahashi, K., A. Machida, G. Funatsu, M. Nomura, S. Usuda, S. Aoyagi, K. Tachibana, H. Miyamoto, M. Imai, T. Nakamura, et al. 1983. Immunochemical structure of hepatitis B e antigen in the serum. J. Immunol. 130:2903-2907.
36. Jean-Jean, O., M. Levrero, H. Will, M. Perricaudet, and J. Rossignol. 1989. Expression mechanism of the hepatitis B virus (HBV) C gene and biosynthesis of HBe antigen. Virology. 170:99-106.
37. Garcia, P.D., J.-H. Ou, W.J. Rutter, and P. Walter. 1988. Targeting of the hepatitis B virus precore protein to the endoplasmic reticulum membrane: after signal peptide cleavage translocation can be aborted and the product released into the cytoplasm. J. Cell Biol. 106:1093-1104.
38. Lippincott-Schwartz, J., J.G. Donaldson, A. Schweizer, E.G. Berger, H.P. Hauri, L.C. Yuan, and R.D. Klausner. 1990. Microtubule-dependent retrograde transport of proteins into the ER in the presence of Brefeldin A suggests an ER recycling pathway. Cell. 60:821-836.
39. Bond, J.S., and P.E. Butler. 1987. Intracellular proteases. Annu. Rev. Biochem. 57:333-364.
40. Wiertz, E.J.H.H., D. Tortorella, M. Bogyo, J. Wu, 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.
41. 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.
42. Nakayama, K. 1997. Furin: a mammalian subtilisin/kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem. J. 327:625-635.
43. Gabathuler, R., J. Alimonti, Q.-J. Zhang, G. Kolaitis, G. Reid, and W.A. Jefferies. 1998. Surrogate antigen processing mediated by TAP-dependent antigenic peptide secretion. J. Cell Biol. 140:17-27.
44. Hughes, E.A., B. Ortman, 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.
45. Biederer, T., C. Wolkwein, and T. Sommer. 1997. Role of Cuelp in ubiquitination and degradation at the ER surface. Science. 278:1806-1809.
46. d molecules capture peptides from endocytosed hepatitis B surface antigen particles for major histocompatibility complex class I-restricted presentation. Eur. J. Immunol. 26:2812-2822.
47. Miesenböck, G., and J.E. Rothman. 1995. The capacity to retrieve escaped ER proteins extends to the trans-most cisterna of the Golgi stack. J. Cell Biol. 129:309-319.
48. Cole, N.B., J. Ellenberg, J. Song, D. DiEuliis, and J. Lippincott-Schwartz. 1998. Retrograde transport of Golgi-localized proteins to the ER. J. Cell Biol. 140:1-15.
49. d molecules at the cell surface. J. Exp. Med. 178:2035-2046.
50. Flynn, G.C., J. Pohl, M.T. Flocco, and J.E. Rothman. 1991. Peptide-binding specificity of the molecular chaperone BiP. Nature. 353:726-730.
51. Suto, R., and P.K. Srivastava. 1995. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science. 269:1585-1588.
52. Lammert, E., S. Stevanovic, J. Brunner, H.G. Rammensee, and H. Schild. 1997. Protein disulfide isomerase is the dominant acceptor for peptides translocated into the endoplasmic reticulum. Eur. J. Immunol. 27:1685-1690.
53. Arnold, D., C. Wahl, S. Faath, H.G. Rammensee, and H. Schild. 1997. Influences of transporter associated with antigen presentation (TAP) on the repertoire of peptides associated with the endoplasmic reticulum-resident stress protein gp96. J. Exp. Med. 186:461-466.