Diversity of proteasomal missions: Fine tuning of the immune response

Biological Chemistry

Volumn 388, Issue 9, 2007, Pages 947-955

  Borissenko, Ljudmila ^a   Groll, Michael ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

interferon; Antigen; MHC class I; Ntn hydrolase; Splicing; Ubiquitin

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; CELL PROTEIN; GAMMA INTERFERON; HYDROLASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; PROTEASOME; PROTEIN NTN; PROTEINASE; UBIQUITIN; UNCLASSIFIED DRUG;

ANTIGENICITY; CELL SURFACE; CONFORMATIONAL TRANSITION; HUMAN; HYDROLYSIS; IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; REVIEW;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; EXTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; INTEINS; PEPTIDE HYDROLASES; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SPLICING; UBIQUITINS;

EID: 34547858920     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2007.109     Document Type: Review

References (53)

1. Beninga, J., Rock, K.L., and Goldberg, A.L. (1998). Interferon-γ can stimulate post-proteasomal trimming of the N-terminus of an antigenic peptide by inducing leucine aminopeptidase. J. Biol. Chem. 273, 18734-18742.
2. Boes, B., Hengel, H., Ruppert, T., Multhaup, G., Koszinowski, U.H., and Kloetzel, P.M. (1994). Interferon γ stimulation modulates the proteolytic activity and cleavage site preference of 20S mouse proteasomes. J. Exp. Med. 179, 901-909.
3. Borissenko, L. and Groll, M. (2007). 20S proteasome and its inhibitors: crystallographic knowledge for drug development. Chem. Rev. 107, 687-717.
4. Brannigan, J.A., Dodson, G., Duggleby, H.J., Moody, P.C., Smith, J.L., Tomchick, D.R., and Murzin, A.G. (1995). A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature 378, 416-419.
5. Brown, M.G., Driscoll, J., and Monaco, J.J. (1991). Structural and serological similarity of MHC-linked LMP and proteasome (multicatalytic proteinase) complexes. Nature 353, 355-357.
6. Buchholz, D., Scott, P., and Shastri, N. (1995). Presentation without proteolytic cleavage of endogenous precursors in the MHC class I antigen processing pathway. J. Biol. Chem. 270, 6515-6522.
7. Chu-Ping, M., Vu, J.H., Proske, R.J., Slaughter, C.A., and DeMartino, G.N. (1994). Identification, purification, and characterization of a high molecular weight, ATP-dependent activator (PA700) of the 20 S proteasome. J. Biol. Chem. 269, 3539-3547.
8. Ditzel, L., Huber, R., Mann, K., Heinemeyer, W., Wolf, D.H., and Groll, M. (1998). Conformational constraints for protein self-cleavage in the proteasome. J. Mol. Biol. 279, 1187-1191.
9. Driscoll, J., Brown, M.G., Finley, D., and Monaco, J.J. (1993). MHC-linked LMP gene products specifically alter peptidase activities of the proteasome. Nature 365, 262-264.
10. Engelhard, V.H. (1994). Structure of peptides associated with MHC class I molecules. Curr. Opin. Immunol. 6, 13-23.
11. Etlinger, J. and Goldberg, A. (1977). A soluble ATP-dependent proteolytic system responsible for the degradation of abnormal proteins in reticulocytes. Proc. Natl. Acad. Sci. USA 74, 54-58.
12. Fehling, H.J., Swat, W., Laplace, C., Kuhn, R., Rajewsky, K., Müller, U., and von Boehmer, H. (1994). MHC class I expression in mice lacking the proteasome subunit LMP-7. Science 265, 1234-1237.
13. Groettrup, M., Kraft, R., Kostka, S., Standera, S., Stohwasser, R., and Kloetzel, P.M. (1996). A third interferon-gamma-induced subunit exchange in the 20S proteasome. Eur. J. Immunol. 26, 863-869.
14. Groll, M. and Huber, R. (2003). Substrate access and processing by the 20S proteasome core particle. Int. J. Biochem. Cell Biol. 35, 606-616.
15. Groll, M., Ditzel, L., Löwe, J., Stock, D., Bochtler, M., Bartunik, H.D., and Huber, R. (1997). Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386, 463-471.
16. Groll, M., Heinemeyer, W., Jager, S., Ullrich, T., Bochtler, M., Wolf, D.H., and Huber, R. (1999). The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc. Natl. Acad. Sci. USA 96, 10976-10983.
17. Groll, M., Bajorek, M., Kohler, A., Moroder, L., Rubin, D.M., Huber, R., Glickman, M.H., and Finley, D. (2000). A gated channel into the proteasome core particle. Nat. Struct. Biol. 7, 1062-1067.
18. Groll, M., Koguchi, Y., Huber, R., and Kohno, J. (2001). Crystal structure of the 20 S proteasome:TMC-95A complex: a noncovalent proteasome inhibitor. J. Mol. Biol. 311, 543-548.
19. Groll, M., Brandstetter, H., Bartunik, H., Bourenkow, G., and Huber, R. (2003). Investigations on the maturation and regulation of archaebacterial proteasomes. J. Mol. Biol. 327, 75-83.
20. Groll, M., Bochtler, M., Brandstetter, H., Clausen, T., and Huber, R. (2005). Molecular machines for protein degradation. ChemBioChem 6, 222-256.
21. Groll, M., Götz, M., Kaiser, M., Weyher, E., and Moroder, L. (2006a). TMC-95-based inhibitor design provides evidence for the catalytic versatility of the proteasome. Chem. Biol. 13, 607-614.
22. Groll, M., Huber, R., and Potts, B.C. (2006b). Crystal structures of salinosporamide A (NPI-0052) and B (NPI-0047) in complex with the 20S proteasome reveal important consequences of beta-lactone ring opening and a mechanism for irreversible binding. J. Am. Chem. Soc. 128, 5136-5141.
23. Groll, M., Larionov, O.V., Huber, R., and de Meijere, A. (2006c). Inhibitor-binding mode of homobelactosin C to proteasomes: new insights into class I MHC ligand generation. Proc. Natl. Acad. Sci. USA 103, 4576-4579.
24. Hanada, K. and Yang, J.C. (2005). Novel biochemistry: post-translational protein splicing and other lessons from the school of antigen processing. J. Mol. Med. 83, 420-428.
25. Hanada, K., Yewdell, J.W., and Yang, J.C. (2004). Immune recognition of a human renal cancer antigen through post-translational protein splicing. Nature 427, 252-256.
26. Heinemeyer, W., Fischer, M., Krimmer, T., Stachon, U., and Wolf, D.H. (1997). The active sites of the eukaryotic 20 S proteasome and their involvement in subunit precursor processing. J. Biol. Chem. 272, 25200-25209.
27. Hoffman, L. and Rechsteiner, M. (1994). Activation of the multicatalytic protease. The 11S regulator and 20S ATPase complexes contain distinct 30-kilodalton subunits. J. Biol. Chem. 269, 16890-16895.
28. Hough, R., Pratt, G., and Rechsteiner, M. (1987). Purification of two high molecular weight proteases from rabbit reticulocyte lysate. J. Biol. Chem. 262, 8303-8313.
29. Jager, S., Groll, M., Huber, R., Wolf, D.H., and Heinemeyer, W. (1999). Proteasome beta-type subunits: unequal roles of propeptides in core particle maturation and a hierarchy of active site function. J. Mol. Biol. 291, 997-1013.
30. +-adenosine triphosphatase. Science 250, 651-657.
31. Kwon, Y., Nagy, I., Adams, P., Baumeister, W., and Jap, B. (2004). Crystal structures of the Rhodococcus proteasome with and without its pro-peptides: implications for the role of the pro-peptide in proteasome assembly. J. Mol. Biol. 335, 233-245.
32. Löwe, J., Stock, D., Jap, B., Zwickl, P., Baumeister, W., and Huber, R. (1995). Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268, 533-539.
33. Malarkannan, S., Goth, S., Buchholz, D.R., and Shastri, N. (1995). The role of MHC class I molecules in the generation of endogenous peptide/MHC complexes. J. Immunol. 154, 585-598.
34. Michalek, M.T., Grant, E.P., Gramm, C., Goldberg, A.L., and Rock, K.L. (1993). A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature 363, 552-554.
35. Nandi, D., Jiang, H., and Monaco, J.J. (1996). Identification of MECL-1 (LMP-10) as the third IFN-gamma-inducible proteasome subunit. J. Immunol. 156, 2361-2364.
36. Nussbaum, A.K., Dick, T.P., Keilholz, W., Schirle, M., Stevanovic, S., Dietz, K., Heinemeyer, W., Groll, M., Wolf, D.H., Huber, R., et al. (1998). Cleavage motifs of the yeast 20S proteasome beta subunits deduced from digests of enolase 1. Proc. Natl. Acad. Sci. USA 95, 12504-12509.
37. Orlowski, M., Cardozo, C., and Michaud, C. (1993). 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 32, 1563-1572.
38. Ortiz-Navarrete, V., Seelig, A., Gernold, M., Frentzel, S., Kloetzel, P.M., and Hammerling, G.J. (1991). Subunit of the '20S' proteasome (multicatalytic proteinase) encoded by the major histocompatibility complex. Nature 353, 662-664.
39. Princiotta, M.F., Finzi, D., Qian, S.B., Gibbs, J., Schuchmann, S., Buttgereit, F., Bennink, J.R., and Yewdell, J.W. (2003). Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18, 343-354.
40. Schechter, I. and Berger, A. (1968). On the active site of proteases. 3. Mapping the active site of papain; specific peptide inhibitors of papain. Biochem. Biophys. Res. Commun. 32, 898-902.
41. Seemüller, E., Lupas, A., Stock, D., Löwe, J., Huber, R., and Baumeister, W. (1995). Proteasome from Thermoplasma acidophilum: a threonine protease. Science 268, 579-582.
42. Sibille, C., Gould, K.G., Willard-Gallo, K., Thomson, S., Rivett, A.J., Powis, S., Butcher, G.W., and De Baetselier, P. (1995). LMP2+ proteasomes are required for the presentation of specific antigens to cytotoxic T lymphocytes. Curr. Biol. 5, 923-930.
43. Silver, M.L., Parker, K.C., and Wiley, D.C. (1991). Reconstitution by MHC-restricted peptides of HLA-A2 heavy chain with β2-microglobulin, in vitro. Nature 350, 619-622.
44. Sykulev, Y., Joo, M., Vturina, I., Tsomides, T.J., and Eisen, H.N. (1996). Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4, 565-571.
45. Unno, M., Mizushima, T., Morimoto, Y., Tomisugi, Y., Tanaka, K., Yasuoka, N., and Tsukihara, T. (2002). The structure of the mammalian 20S proteasome at 2.75 Å resolution. Structure 10, 609-618.
46. van der Bruggen, P. and van den Eynde, B.J. (2006). Processing and presentation of tumor antigens and vaccination strategies. Curr. Opin. Immunol. 18, 98-104.
47. Van Kaer, L., Ashton-Rickardt, P., Eichelberger, M., Gaczynska, M., Nagashima, K., Rock, K., Goldberg, A., Doherty, P., and Tonegawa, S. (1994). Altered peptidase and viral-specific T cell response in LMP2 mutant mice. Immunity 1, 533-541.
48. Vigneron, N., Stroobant, V., Chapiro, J., Ooms, A., Degiovanni, G., Morel, S., van der Bruggen, P., Boon, T., and van den Eynde, B.J. (2004). An antigenic peptide produced by peptide splicing in the proteasome. Science 304, 587-590.
49. Warren, E.H., Vigneron, N.J., Gavin, M.A., Coulie, P.G., Stroobant, V., Dalet, A., Tykodi, S.S., Xuereb, S.M., Mito, J.K., Riddell, S.R., and van den Eynde, B.J. (2006). An antigen produced by splicing of noncontiguous peptides in the reverse order. Science 313, 1444-1447.
50. Waxman, L., Fagan, J.M., and Goldberg, A.L. (1987). Demonstration of two distinct high molecular weight proteases in rabbit reticulocytes, one of which degrades ubiquitin conjugates. J. Biol. Chem. 262, 2451-2457.
51. Whitby, F.G., Masters, E.I., Kramer, L., Knowlton, J.R., Yao, Y., Wang, C.C., and Hill, C.P. (2000). Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408, 115-120.
52. York, I.A. and Rock, K.L. (1996). Antigen processing and presentation by the class I major histocompatibility complex. Annu. Rev. Immunol. 14, 369-396.
53. York, I.A., Goldberg, A.L., Mo, X.Y., and Rock, K.L. (1999). Proteolysis and class I major histocompatibility complex antigen presentation. Immunol. Rev. 172, 49-66.