Structure and assembly of the 20S proteasome

Cellular and Molecular Life Sciences

Volumn 54, Issue 3, 1998, Pages 253-262

  Gerards, W L H ^a   De Jong, W W ^a   Boelens, W ^a   Bloemendal, H ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

20s proteasome; Assembly; Circular structure; Proteasomal subunits; Proteolytic activity

Indexed keywords

PROTEASOME;

ARCHAEBACTERIUM; DIMERIZATION; ENZYME STRUCTURE; ENZYME SUBUNIT; EUBACTERIUM; EUKARYOTE; HUMAN; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; REVIEW;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CYSTEINE ENDOPEPTIDASES; HUMANS; HYDROLYSIS; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; PROTEASOME ENDOPEPTIDASE COMPLEX; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0031982133     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050147     Document Type: Review

References (78)

1. Rock K. L., Gramm C., Rothstein L., Clark K., Stein R., Dick L. et al. (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
2. Hershko A. and Ciechanover A. (1992) The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61: 761-807
3. Hilt W. and Wolf D. H. (1996) Proteasomes: destruction as a programme. Trends Biochem. Sci. 21: 96-102
4. Smith S. E., Koegl M. and Jentsch S. (1996) Role of the ubiquitin proteasome system in regulated protein degradation in Saccharomyces cerevisiae. Biol. Chem. 377: 437-446
5. Hochstrasser M. (1995) Ubiquitin, proteasomes and the regulation of intracellular protein degradation. Curr. Opin. Cell Biol. 7: 215-223
6. Ciechanover A. (1994) The ubiquitin proteasome proteolytic pathway. Cell 79: 13-21
7. Jentsch S. and Schlenker S. (1995) Selective protein degradation: a journey's end within the proteasome. Cell 82: 881-884
8. Coux O., Tanaka K. and Goldberg A. L. (1996) Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65: 801-847
9. Dahlmann B., Kopp F., Kuehn L., Niedel B., Pfeifer G., Hegerl R. et al. (1989) The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria. FEBS Lett. 251: 125-131
10. Tamura T., Nagy I., Lupas A., Lottspeich F., Cejka Z., Schoofs G. et al. (1995) The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr. Biol. 5: 766-774
11. Tanaka K., Ii K., Ichihara A., Waxman L. and Goldberg A. L. (1986) A high molecular weight protease in the cytosol of rat liver. I. Purification, enzymological properties and tissue distribution. J. Biol. Chem. 261: 15197-15203
12. Machiels B. M., Henfling M. E. R., Broers J. L. V., Hendil K. B. and Ramaekers F. C. S. (1995) Changes in immunocytochemical detectability of proteasome epitopes depending on cell growth and fixation conditions of lung cancer cell lines. Eur. J. Cell Biol. 66: 282-292
13. Scherrer K. and Bey F. (1994) The prosomes (multicatalytic proteinases: proteasomes) and their relationship to the untranslated messenger ribonucleoproteins, the cytoskeleton and cell differentiation. Prog. Nucleic Acid Res. Mol. Biol. 49: 1-64
14. Spohr G., Granboulan N., Morel C. and Scherrer K. (1970) Messenger RNA in HeLa cells: an investigation of free and polyribosome-bound cytoplasmic messenger ribonucleoprotein particles by kinetic labelling and electron microscopy. Eur. J. Biochem. 17: 296-318
15. Schmid H. P., Akhayat O., Martins de Sa C., Puvion F., Koehler K. and Scherrer K. (1984) The prosome: an ubiquitous morphologically distinct RNP particle associated with repressed mRNPs and containing specific ScRNA and a characteristic set of proteins. EMBO J. 3: 29-34
16. DeMartino G. N. and Goldberg A. L. (1979) Identification and partial purification of an ATP-stimulated alkaline protease in rat liver. J. Biol. Chem. 254: 3712-3715
17. Wilk S. and Orlowski M. (1980) Cation-sensitive neutral endopeptidase: isolation and specificity of the bovine pituitary enzyme. J. Neurochem. 35: 1172-1182
18. Wilk S. and Orlowski M. (1983) Evidence that pituitary cation-sensitive neutral endopeptidase is a multicatalytic protease complex. J. Neurochem. 40: 842-849
19. Monaco J. J. and McDevitt H. O. (1984) H-2-linked low-molecular weight polypeptide antigens assemble into an unusual macromolecular complex. Nature 309: 797-799
20. Arrigo A. P., Tanaka K., Goldberg A. L. and Welch W. J. (1988) Identity of the 19S 'prosome' particle with the large multifunctional protease complex of mammalian cells (the proteasome). Nature 331: 192-194
21. Falkenburg P. E., Haass C., Kloetzel P. M., Niedel B., Kopp F., Kuehn L. et al. (1988) Drosophila small cytoplasmic 19S ribonucleoprotein is homologous to the rat multicatalytic proteinase. Nature 331: 190-192
22. 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
23. Tanaka K., Yoshimura T., Kumatori A., Ichihara A., Ikai A., Nishigai M. et al. (1988) Proteasomes (multi-protease complexes) as 20 S ring-shaped particles in a variety of eukaryotic cells. J. Biol. Chem. 263: 16209-16217
24. Baumeister W., Cejka Z., Kania M. and Seemuller E. (1997) The proteasome: a macromolecular assembly designed to confine proteolysis to a nanocompartment. Biol. Chem. 378: 121-130
25. Grziwa A., Baumeister W., Dahlmann B. and Kopp F. (1991) Localization of subunits in proteasomes from Thermoplasma acidophilum by immunoelectron microscopy. FEBS Lett. 290: 186-190
26. 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 A resolution. Science 268: 533-539
27. Zwickl P., Grziwa A., Pühler G., Dahlmann B., Lottspeich F. and Baumeister W. (1992) Primary structure of the Thermoplasma proteasome and its implications for the structure, function and evolution of the multicatalytic proteinase. Biochemistry 31: 964-972
28. Heinemeyer W., Tröndle N., Albrecht G. and Wolf D. H. (1994) PRE5 and PRE6, the last missing genes encoding 20S proteasome subunits from yeast? Indication for a set of 14 different subunits in the eukaryotic proteasome core. Biochemistry 33: 12229-12237
29. Coux O., Nothwang H. G., Silva-Pereira I., Recillas Targa F., Bey F. and Scherrer K. (1994) Phylogenic relationships of the amino acid sequences of prosome (proteasome, MCP) subunits. Mol. Gen. Genet. 245: 769-780
30. Groll M., Ditzel L., Löwe J., Stock D., Bochtler M., Bartunik H. D. et al. (1997) Structure of 20S proteasome from yeast at 2.4Å resolution. Nature 386: 463-471
31. 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
32. 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
33. Schauer T. M., Nesper M., Kehl M., Lottspeich F., Müller-Taubenberger A., Gerisch G. et al. (1993) Proteasomes from Dictyostelium discoideum: characterization of structure and function. J. Struct. Biol. 111: 135-147
34. 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
35. Groettrup M., Soza A., Kuckelkorn U. and Kloetzel P. M. (1996) Peptide antigen production by the proteasome: complexity provides efficiency. Immunol. Today 17: 429-435
36. Tanaka K. and Tsurumi C. (1997) The 26S proteasome: subunits and functions. Mol. Biol. Rep. 24: 3-11
37. Brannigan J. A., Dodson G., Duggleby H. J., Moody P. C., Smith J. L., Tomchick D. R. et al. (1995) A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature 378: 416-419
38. Tikkanen R., Riikonen A., Oinonen C., Rouvinen R. and Peltonen L. (1996) Functional analyses of active site residues of human lysosomal aspartylglucosaminidase: implications for catalytic mechanism and autocatalytic activation. EMBO J. 15: 2954-2960
39. Hoffman L. and Rechsteiner M. (1994) Activation of the multicatalytic protease. The 11 S regulator and 20 S ATPase complexes contain distinct 30-kilodalton subunits. J. Biol. Chem. 269: 16890-16895
40. 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
41. Orlowski M. (1990) The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry 29: 10289-10297
42. Rivett A. J. (1993) Proteasomes: multicatalytic proteinase complexes. Biochem. J. 291: 1-10
43. Akopian T. N., Kisselev A. F. and Goldberg A. L. (1997) Processive degradation of proteins and other catalytic properties of the proteasome from Thermoplasma acidophilum. J. Biol. Chem. 272: 1791-1798
44. Rawlings N. D. and Barrett A. J. (1993) Evolutionary families of peptidases. Biochem. J. 290: 205-218
45. Seemüller E., Lupas A., Zühl F., Zwickl P. and Baumeister W. (1995) The proteasome from Thermoplasma acidophilum is neither a cysteine nor a serine protease. FEBS Lett. 359: 173-178
46. 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
47. 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
48. Fenteany G., Standaert R. F., Lane W. S., Choi S., Corey E. J. and Schreiber S. L. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268: 726-731
49. Heinemeyer W., Kleinschmidt J. A., Saidowsky J., Escher C. and Wolf D. H. (1991) Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J. 10: 555-562
50. Heinemeyer W., Gruhler A., Mohrle V., Mahe Y. and Wolf D. H. (1993) PRE2, highly homologous to the human major histocompatibility complex-linked RING10 gene, codes for a yeast proteasome subunit necessary for chrymotryptic activity and degradation of ubiquitinated proteins. J. Biol. Chem. 268: 5115-5120
51. Enenkel C., Lehmann H., Kipper J., Guckel R., Hilt W. and Wolf D. H. (1994) PRE3, highly homologous to the human major histocompatibility complex-linked LMP2 (RING12) gene, codes for a yeast proteasome subunit necessary for the peptidylglutamyl-peptide hydrolyzing activity. FEBS Lett. 341: 193-196
52. Wenzel T., Eckerskorn C., Lottspeich F. and Baumeister W. (1994) Existence of a molecular ruler in proteasomes suggested by analysis of degradation products. FEBS Lett. 349: 205-209
53. Tokunaga F., Goto T., Koide T., Murakami Y., Hayashi S., Tamura T. et al. (1994) ATP- and antizyme-dependent endoproteolysis of ornithine decarboxylase to oligopeptides by the 26 S proteasome. J. Biol. Chem. 269: 17382-17385
54. Boes B., Hengel H., Ruppert T., Multhaup G., Koszinowski U. H. and Kloetzel P. M. (1994) Interferon gamma stimulation modulates the proteolytic activity and cleavage site preference of 20S mouse proteasomes. J. Exp. Med. 179: 901-909
55. Dick L. R., Aldrich C., Jameson S. C., Moomaw C. R., Pramanik B. C., Doyle C. K. et al. (1994) Proteolytic processing of ovalbumin and beta-galactosidase by the proteasome to a yield antigenic peptides. J. Immunol. 152: 3884-3894
56. Ehring B., Meyer T. H., Eckerskorn C., Lottspeich F. and Tampe R. (1996) Effects of major-histocompatibility-complex-encoded subunits on the peptidase and proteolytic activities of human 20S proteasomes cleavage of proteins and antigenic peptides. Eur. J. Biochem. 235: 404-415
57. Cardozo C., Vinitsky A., Michaud C. and Orlowski M. (1994) Evidence that the nature of amino acid residues in the P3 position directs substrates to distinct catalytic sites of the pituitary multicatalytic proteinase complex (proteasome). Biochemistry 33: 6483-6489
58. Pacifici R. E., Kono Y. and Davies K. J. A. (1993) Hydrophobicity as the signal for selective degradation of hydroxyl radical-modified hemoglobin by the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 268: 15405-15411
59. Wenzel T. and Baumeister W. (1995) Conformational constraints in protein degradation by the 20S proteasome. Nature Struct. Biol. 2: 199-204
60. Koster A. J., Walz J., Lupas A. and Baumeister W. (1995) Structural features of archaebacterial and eukaryotic proteasomes. Mol. Biol. Rep. 21: 11-20
61. Maupin-Furlow J. A. and Ferry J. G. (1995) A proteasome from the methanogenic archaeon Methanosarcina thermophila. J. Biol. Chem. 270: 28617-28622
62. Zwickl P., Lottspeich F. and Baumeister W. (1992) Expression of functional Thermoplasma acidophilum proteasomes in Escherichia coli. FEBS Lett. 312: 157-160
63. Zwickl P., Kleinz J. and Baumeister W. (1994) Critical elements in proteasome assembly. Nature Struct. Biol. 1: 765-770
64. Seemüller E., Lupas A. and Baumeister W. (1996) Autocatalytic processing of the 20S proteasome. Nature 382: 468-470
65. Zühl F., Tamura T., Dolenc I., Cejka Z., Nagy I., Demot R. et al. (1997) Subunit topology of the Rhodococcus proteasome. FEBS Lett. 400: 83-90
66. Lupas A., Zühl F., Tamura T., Wolf S., Nagy I., De Mot R. et al. (1997) Eubacterial proteasomes. Mol. Biol. Rep. 24: 125-131
67. Zühl F., Seemüller E., Golbik R. and Baumeister W. (1997) Dissecting the assembly pathway of the 20 S proteasome. FEBS Lett., in press
68. Frentzel S., Pesold-Hurt B., Seelig A. and Kloetzel P. M. (1994) 20 S proteasomes are assembled via distinct precursor complexes. Processing of LMP2 and LMP7 proproteins takes place in 13-16 S preproteasome complexes. J. Mol. Biol. 236: 975-981
69. 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
70. Yang Y., Früh K., Ahn K. and Peterson P. A. (1995) In vivo assembly of the proteasomal complexes, implications for antigen processing. J. Biol. Chem. 270: 27687-27694
71. Schmidtke G., Schmidt M. and Kloetzel P. M. (1997) Maturation of mammalian 20 S proteasome: purification and characterization of 13 S and 16 S proteasome precursor complexes. J. Mol. Biol. 268: 95-106
72. Schmidt M., Schmidtke G. and Kloetzel P. M. (1997) Structure and structure formation of the 20S proteasome. Mol. Biol. Rep. 24: 103-112
73. Gerards W. L. H., Enzlin J., Häner M., Hendrix I. L. A. M., Aebi U., Bloemendal H. and Boelens W. (1997) The human α-type proteasomal subunit HsC8 forms a double ringlike structure, but does not assemble into proteasome-like particles with the β-type subunits HsDelta or HsBPROS26. J. Biol. Chem. 272: 10080-10086
74. Gerards W. L. H., de Jong W. W., Bloemendal H. and Boelens W. (1998) The human proteasomal subunit HsC8 induces ring formation of other α-type subunits. J. Mol. Biol. 275: 113-121
75. Schmidtke G., Kraft R., Kostka S., Henklein P., Frömmel C., Löwe J. et al. (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
76. Baker D., Shiau A. K. and Agard D. A. (1997) The role of pro regions in protein folding. Curr. Opin. Cell Biol. 5: 966-970
77. Chen P. and Hochstrasser M. (1995) Biogenesis, structure and function of the yeast 20S proteasome. EMBO J. 14: 2620-2630
78. Ciechanover A., Hargrove J. L. and Gross-Mesilaty S. (1997) Ubiquitin-mediated degradation of tyrosine aminotransferase (TAT) in vitro and in vivo. Mol. Biol. Rep. 24: 27-33