Intermediates in the formation of mouse 20S proteasomes: Implications for the assembly of precursor β subunits

EMBO Journal

Volumn 16, Issue 17, 1997, Pages 5363-5375

  Nandi, Dipankar ^a   Woodward, Elaine ^b   Ginsburg, David B ^a   Monaco, John J ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Macromolecular assembly; Precursor subunits; Proteasome biogenesis; Protein degradation

Indexed keywords

GAMMA INTERFERON; PROTEASOME; PROTEIN ANTIBODY; PROTEIN PRECURSOR; PROTEIN SUBUNIT;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; HALF LIFE TIME; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; ARCHAEAL PROTEINS; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; INTERFERON TYPE II; LIVER; MACROPHAGES; MICE; MODELS, BIOLOGICAL; MOLECULAR WEIGHT; MULTIENZYME COMPLEXES; PRECIPITIN TESTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; SPLEEN; TISSUE DISTRIBUTION; TUMOR CELLS, CULTURED;

ANIMALIA; MAMMALIA;

EID: 0030880547     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.17.5363     Document Type: Article

References (71)

1. Ahn, J.Y. et al. (1995) Primary structures of two homologous subunits of PA28, a γ-interferon-inducible protein activator of the 20S proteasome. FEBS Lett., 366, 37-42.
2. Aki, M. et al. (1994) Interferon-γ induces different subunit organizations and functional diversity of proteasomes. J. Biochem., 115, 257-269.
3. Boes, B., Hengel, H., Ruppert, T., Multhaup, G., Koszinowski, U.H. and Kloetzel, P.-M. (1994) IFN-γ stimulation modulates the proteolytic activity and cleavage site preference of 20S mouse proteasomes. J. Exp. Med., 179, 901-909.
4. 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.
5. Brown, M.G., Driscoll, J. and Monaco, J.J. (1993) MHC-linked low molecular mass polypeptide subunits define distinct subsets of proteasomes: implications for divergent function among distinct proteasome subsets. J. Immunol., 151, 1193-1204.
6. Cerundolo, V., Kelly, A., Elliott, T., Trowsdale, J. and Townsend, A. (1995) Genes encoded in the major histocompatibility complex affecting the generation of peptides for TAP transport. Eur. J. Immunol., 25, 554-562.
7. Cerundolo, V., Benham, A., Braud, V., Mukherjee, S., Gould, K., Macino, B., Neefjes, J. and Townsend, A. (1997) The proteasome-specific inhibitor lactacystin blocks presentation of cytotoxic T lymphocyte epitopes in human and murine cells. Eur. J. Immunol., 27, 336-341.
8. Chen, P. and Hochstrasser, M. (1995) Biogenesis, structure and function of the yeast 20S proteasome. EMBO J., 14, 2620-2630.
9. Chen, P and Hochstrasser, M. (1996) Autocatalytic subunit processing couples active site formation in the 20S proteasome to completion of assembly. Cell, 86, 961-972.
10. Coux, O., Tanaka, K. and Goldberg, A.L. (1996) Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem., 65, 80-47.
11. Cruz, M., Nandi, D., Hendil, K.B. and Monaco, J.J. (1997) Cloning and characterization of mouse Lmp3 cDNA, encoding a proteasome β subunit. Gene, 190, 251-256.
12. Cuervo, A.M., Palmer, A., Rivett, A.J. and Knecht, E. (1995) Degradation of proteasomes by lysosomes in rat liver. Eur. J. Biochem., 227, 792-800.
13. Dick, T.P., Ruppert, T., Groettrup, M., Kloetzel, P.M., Kuehn, L., Koszinowski, U.H., Stevanoviö, S., Schild, H. and Rammensee, H.-G. (1996) Coordinated dual cleavages induced by the proteasome regulator PA28 lead to dominant MHC ligands. Cell, 86, 253-262.
14. 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.
15. Dubiel, W., Pratt, G., Ferrell, K. and Rechsteiner, M. (1992) Purification of an 11S regulator of the multicatalytic protease. J. Biol. Chem., 267, 22369-22377.
16. Frangioni, J.V. and Neel, B.G. (1993) Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem., 210, 179-187.
17. 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.
18. Fenteany, G., Standaert, R.F., Lane, W.S., Choi, S., Corey, E.J. and Schreiber, S. (1995) Inhibition of proteasome activities and subunit-specific amino terminal threonine modification of lactacystin. Science, 268, 726-731.
19. Frentzel, S., Hurt-Pesold, B., Seelig, A. and Kloetzel, P.-M. (1994) 20S proteasomes are assembled via distinct precursor complexes. J. Mol. Biol. 236, 975-981.
20. Früh, K., Yang, Y., Arnold, D., Chambers, J., Wu, L., Waters, J.B., Spies, T. and Peterson, P. (1992) Alternative exon usage and processing of the major histocompatibility complex-encoded proteasome subunits. J. Biol. Chem., 267, 22131-22140.
21. Gaczynska, M., Rock, K.L. and Goldberg, A.L. (1993) γ-Interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature, 365, 264-267.
22. Gaczynska, M., Rock, K.L., Spies, T. and Goldberg, A.L. (1994) Peptidase activities of proteasomes are differentially regulated by the major histocompatibility complex-encoded genes for LMP2 and LMP7. Proc. Natl Acad. Sci. USA, 91, 9213-9217.
23. Gaczynska, M., Goldberg, A.L., Tanaka, K., Hendil, K.B. and Rock, K.L. (1996) Proteasome subunits X and Y alter peptidase activities in opposite ways to the interferon-γ-induced subunits LMP2 and LMP7. J. Biol. Chem., 271, 17275-17280.
24. Gray, C.W., Slaughter, C.A. and DeMartino, G.N. (1994) PA28 activator protein forms regulatory caps on proteasome stacked rings. J. Mol. Biol., 236, 7-15.
25. Groettrup, M., Ruppert, T., Kuehn, L., Seeger, M., Standera, S., Koszinowski, U. and Kloetzel, P.-M. (1995) The interferon-γ-inducible US regulator (PA28) and the LMP2/LMP7 subunits govern the peptide production by 20S proteasome in vitro. J. Biol. Chem., 270, 23808-23815.
26. Groettrup, M., Soza, A., Eggers, M., Kuehn, L., Dick, T.P., Schild, H., Rammensee, H.-G., Koszinowski, U.H. and Kloetzel, P.-M. (1996a) A role of the proteasome regulator PA28a in antigen presentation. Nature, 381, 166-168.
27. Groettrup, M., Kraft, R., Kostka, S., Standera, S., Stohwasser, R. and Kloetzel, P.-M. ( 1996b) A third interferon-γ-induced subunit exchange in the 20S proteasome. Eur. J. Immunol., 26, 863-869.
28. Groll, M., Ditzel, L., Löwe, J., Stock, D., Bochtler, M., Bartunik, H.D. and Huber, R. (1997) Structure of 20S proteasome from yeast at 2.4Å resolution. Nature, 386, 463-471.
29. Grossi de Sa, M.-F., Martins de Sa, C., Harper, F., Coux, O., Akhayat, O., Pal, J.K., Florentin, Y. and Scherrer, K. (1988) Cytolocalization of prosomes as a function of differentiation. J. Cell Sci., 89, 151-165.
30. Harrer, J.M., Kiss, E. and Kranias, E.G. (1995) Application of the immunoblot technique for quantification of protein levels in cardiac homogenates. Biotechniques, 18, 995-998.
31. Hendil, K.B. (1988) The 19S multicatalytic 'prosome' proteinase is a constitutive enzyme in HeLa cells. Biochem. Int., 17, 471-478.
32. Hisamatsu, H. et al. (1996) New pair of proteasomal subunits regulated reciprocally by interferon γ. J. Exp. Med., 183, 1807-1816.
33. Ichihara, A. and Tanaka, K. (1995) Role of proteasomes in cell growth. Mol. Biol. Rep., 21, 49-52.
34. Kopp, F., Dahlmann, B. and Hendil, K.B. (1993) Evidence indicating that the human proteasome is a complex dimer. J. Mol. Biol., 229, 14-19.
35. Kopp, F., Kristensen, P., Hendil, K.B., Johnsen, A., Sobek, A. and Dahlmann, B. (1995) The human proteasome subunit HsN3 is located in the inner rings of the complex dimer. J. Mol. Biol., 248, 264-272.
36. Kopp, F., Hendil, K.B., Dahlmann, B., Kristensen, P., Sobek, A. and Uerkvitz, W. (1997) Subunit arrangement in the human 20S proteasome. Proc. Natl Acad. Sci. USA, 94, 2939-2944.
37. Kuckelkorn, U., Frentzel, S., Kraft, R., Kostka, S., Groettrup, M. and Kloetzel, P.-M. (1995) Incorporation of major histocompatibility complex-encoded subunits LMP-2 and LMP-7 changes the quality of the 20S proteasome polypeptide processing products independent of interferon-γ. Eur. J. Immunol.,. 25, 2605-2611.
38. Kurnatori, A., Tanaka, K., Tamura, T., Fujiwara, T., Ichihara, A., Tokunaga, F., Onikura, A. and Iwanaga, S. (1990) cDNA cloning and sequencing of component C9 of proteasomes from rat hepatoma cells. FEBS Lett., 264, 279-282.
39. Lilley, K.S., Davison, M.D. and Rivett, A.J. (1990) N-terminal sequence similarities between components of the multicatalytic proteinase complex. FEBS Lett., 262, 327-329.
40. Löwe, J., Stock, D., Jap, B., Zwickl, P., Baumeister, W. and Huber, R. (1995) Crystal structure of the 20S proteasome from the archaeon T.acidophilus at 3.4 Å resolution. Science, 268, 533-539.
41. Ma, C.-P., Slaughter, C.A. and DeMartino, G.N. (1992) Identification, purification, and characterization of a protein activator (PA28) of the 20S proteasome (macropain). J. Biol. Chem., 267, 10515-10523.
42. 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.
43. Monaco, J.J. and Nandi, D. (1995) The genetics of proteasomes and antigen processing. Annu. Rev. Genet., 29, 729-754.
44. Nandi, D., Jiang, H. and Monaco, J.J. (1996a) Identification of MECL-1 (LMP-10) as the third IFNγ-inducible proteasome subunit. J. Immunol., 156, 2361-2364.
45. Nandi, D., Iyer, M.N. and Monaco, J.J. (1996b) Molecular and serological analysis of polymorphisms in the murine major histocompatibility-encoded proteasome subunits, LMP-2 and LMP-7. Exp. Clin. Immunogenet., 13, 20-29.
46. Olson, T.S. and Dice, J.F. (1989) Regulation of protein degradation rates in eukaryotes. Curr. Opin. Cell Biol., 1, 1194-1200.
47. Orino, E., Tanaka, K., Tamura, T., Sone, S., Ogura, T. and Ichihara, A. (1991) ATP-dependent reversible association of proteasomes with multiple protein components to form 26S complexes that degrade ubiquitinated proteins in human HL-60 cells. FEBS Lett., 284, 206-210.
48. 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.
49. Patel, S.D., Monaco, J.J. and McDevitt, H.O. (1994) Delineation of the subunit composition of human proteasomes using antisera against the major histocompatibility complex-encoded LMP2 and LMP7 subunits. Proc. Natl Acad. Sci. USA, 91, 296-300.
50. Peters, J.-M., Cejka, Z., Robin Harris, J., Kleinschmidt, J.A. and Baumeister, W. (1993) Structural features of the 26S proteasome complex. J. Mol. Biol., 234, 932-937.
51. Puhler, G., Pitzer, E. Zwickl, P. and Baumeister, W. (1994) Proteasomes: multisubunit proteinases common to Thermoplasma and eucaryotes. Syst. Appl. Microbiol., 16, 734-741.
52. Realini, C., Dubiel, W., Pratt, G., Ferrell, K. and Rechsteiner, M. (1994) Molecular cloning and expression of a γ-interferon-inducible activator of the multicatalytic protease. J. Biol. Chem., 269, 20727-20732.
53. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. and Goldberg, A.L. (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.
54. Schmidtke, G., Kraft, R., Kostka, S., Henklein, P., Frommel, C., Löwe, J., Huber, R., Kloetzel, P.M. and Schmidt, M. (1996) Analysis of mammalian 20S proteasome biogenesis: the maturation of β subunits is an ordered two-step mechanism involving autocatalysis. EMBO J., 15, 6887-6898.
55. 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.
56. Seemüller, E., Lupas, A. and Baumeister, W. (1996) Autocatalytic processing of the 20S proteasome. Nature, 382, 468-470.
57. Stein, R.L., Melandri, F. and Dick, L. (1996) Kinetic characterization of the chymotryptic activity of the 20S proteasome. Biochemistry, 35, 3899-3908.
58. Stohwasser, R., Kuckelkorn, U., Kraft, R., Kostka, S. and Kloetzel, P.-M. (1996) 20S proteasome from LMP7 knock out mice reveals altered proteolytic activities and cleavage site preferences. FEBS Lett., 383, 109-113.
59. Stohwasser, R., Standera, S., Peters, I., Kloetzel, P.-M. and Groettrup, M. (1997) Molecular cloning of the mouse proteasome subunits MC14 and MECL-1: reciprocally regulated tissue expression of interferon-γ-modulated proteasome subunits. Eur. J. Immunol., 27, 1182-1187.
60. Svensson, K., Lévy, E, Sundberg, U., Boman, H.-G., Hendil, K. and Kvist, S. (1996) Proteasomes generate in vitro a natural peptide ot influenza-A nucleoprotein functional in HLA-B27 antigen assembly. Int. Immunol., 8, 467-478.
61. Tamura, T., Nagy, I., Lupas, A., Lottspeich, F., Cejka, Z., Schoofs, G., Tanaka, K., De Mot, R. and Baumeister, W. (1995) The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr. Biol., 5, 766-774.
62. Tanaka, K. (1994) Role of proteasomes modified by interferon-γ in antigen processing. J. Leukemia Biol., 56, 571-575.
63. Tanaka, K. and Ichihara, A. (1989) Half-life of proteasomes (multiprotease complexes) in rat liver. Biochem. Biophys. Res. Commun., 159, 1309-1315.
64. Thompson, S. and Rivett, J.A. (1996) Processing of N3, a mammalian proteasome beta-type subunit. Biochem. J., 315, 733-738.
65. Ustrell, V., Realini, C., Pratt, G. and Rechsteiner, M. (1995a) Human lymphoblast and erythrocyte multicatalytic proteases: differential peptidase activities and responses to the 11S regulator. FEBS Lett., 376, 155-158.
66. Ustrell, V., Pratt, G. and Rechsteiner, M. (1995b) Effects of interferon γ and major histocompatibility complex-encoded subunits on peptidase activities of human multicatalytic proteases. Proc. Natl Acad. Sci. USA, 92, 584-588.
67. Van Kaer, L., Ashton-Rickardt, P.G., Eichelberger, M., Gaczynska, M., Nagashima, N., Rock, K.L., Goldberg, A.L., Doherty, P.C. and Tonegawa, S. (1994) Altered peptidase and viral-specific T cell response in Lmp2 mutant mice. Immunity, 1, 533-541.
68. Yang, Y., Früh, K., Ahn, K. and Peterson, P. (1995) In vivo assembly of the proteasomal complexes, implications for antigen processing. J. Biol. Chem., 270, 27687-27694.
69. Yoshimura, T. et al. (1993) Molecular characterization of the 26S proteasome complex from rat liver. J. Struct. Biol., 111, 200-211.
70. Zanelli, E., Zhou, P., Cao, H., Smart, M.K. and David, C.S. (1995) Genetic polymorphism of the mouse major histocompatibility complex-associated proteasome subunit Lmp7. Immunogenetics, 41, 251-254.
71. Zwickl, P., Kleinz, J. and Baumeister, W. (1994) Critical elements in proteasome assembly. Nature Struct. Biol., 1, 765-770.