The Proteasome: Paradigm of a Self-Compartmentalizing Protease

The work of one of us (W. B.) was supported by a grant of the Human Frontiers Science Program. We wish to thank Drs. C. P. Hill (Salt Lake City) and J. M. Flanagan (Brookhaven) for making available to us structural data prior to publication. We are grateful to Drs. F. U. Hartl and M. Kania for critically reading the manuscript.

[1]  R. Huber,et al.  Crystal structure of heat shock locus V (HslV) from Escherichia coli. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[2]  W. Baumeister,et al.  Biochemical properties of the proteasome from Thermoplasma acidophilum. , 1992, European journal of biochemistry.

[3]  D. Wolf,et al.  Proteasomes: destruction as a programme. , 1996, Trends in biochemical sciences.

[4]  C. Hill,et al.  Structure of the proteasome activator REGα (PA28α) , 1997, Nature.

[5]  W. Baumeister,et al.  The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria , 1989, FEBS letters.

[6]  A. Goldberg,et al.  Identity of the 19S 'prosome' particle with the large multifunctional protease complex of mammalian cells (the proteasome) , 1988, Nature.

[7]  G. Paesen,et al.  A tick homologue of the human Ki nuclear autoantigen. , 1996, Biochimica et biophysica acta.

[8]  W. Baumeister,et al.  The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus , 1995, Current Biology.

[9]  Hans-Georg Rammensee,et al.  A role for the proteasome regulator PA28α in antigen presentation , 1996, Nature.

[10]  Hans-Georg Rammensee,et al.  Coordinated Dual Cleavages Induced by the Proteasome Regulator PA28 Lead to Dominant MHC Ligands , 1996, Cell.

[11]  C. Gordon,et al.  A Conditional Lethal Mutant in the Fission Yeast 26 S Protease Subunit mts3 Is Defective in Metaphase to Anaphase Transition (*) , 1996, The Journal of Biological Chemistry.

[12]  W Baumeister,et al.  Tricorn protease exists as an icosahedral supermolecule in vivo. , 1997, Molecular cell.

[13]  J. Kleinz,et al.  Critical elements in proteasome assembly , 1994, Nature Structural Biology.

[14]  W. Baumeister,et al.  Tricorn Protease—The Core of a Modular Proteolytic System , 1996, Science.

[15]  K. Ferrell,et al.  HIV-1 Tat Inhibits the 20 S Proteasome and Its 11 S Regulator-mediated Activation* , 1997, The Journal of Biological Chemistry.

[16]  W. Baumeister,et al.  Conformational constraints in protein degradation by the 20S proteasome , 1995, Nature Structural Biology.

[17]  R. Tampé,et al.  Effects of major-histocompatibility-complex-encoded subunits on the peptidase and proteolytic activities of human 20S proteasomes. Cleavage of proteins and antigenic peptides. , 1996, European journal of biochemistry.

[18]  L. Dick,et al.  Mechanistic Studies on the Inactivation of the Proteasome by Lactacystin , 1996, The Journal of Biological Chemistry.

[19]  C. Slaughter,et al.  PA28 activator protein forms regulatory caps on proteasome stacked rings. , 1994, Journal of molecular biology.

[20]  F. Confalonieri,et al.  A 200‐amino acid ATPase module in search of a basic function , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[21]  D. Meinke,et al.  A FUSCA gene of Arabidopsis encodes a novel protein essential for plant development. , 1994, The Plant cell.

[22]  W. Baumeister,et al.  Structural features of 26S and 20S proteasomes. , 1993, Enzyme & protein.

[23]  A. Gruhler,et al.  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. , 1993, The Journal of biological chemistry.

[24]  M. Glickman,et al.  The multiubiquitin-chain-binding protein Mcb1 is a component of the 26S proteasome in Saccharomyces cerevisiae and plays a nonessential, substrate-specific role in protein turnover , 1996, Molecular and cellular biology.

[25]  W. Baumeister,et al.  26S proteasome structure revealed by three-dimensional electron microscopy. , 1998, Journal of structural biology.

[26]  R F Standaert,et al.  Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin , 1995, Science.

[27]  W. Baumeister,et al.  Molecular characterization of the "26S" proteasome complex from rat liver. , 1993, Journal of structural biology.

[28]  E. Prochownik,et al.  Novel Regulation of the Helix-Loop-Helix Protein Id1 by S5a, a Subunit of the 26 S Proteasome* , 1997, The Journal of Biological Chemistry.

[29]  A. Murzin,et al.  A protein catalytic framework with an N-terminal nucleophile is capable of self-activation , 1995, Nature.

[30]  M. Hochstrasser,et al.  Identification of the yeast 20S proteasome catalytic centers and subunit interactions required for active-site formation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. Moore,et al.  Interaction of thyroid-hormone receptor with a conserved transcriptional mediator , 1995, Nature.

[32]  R. Huber,et al.  PROTEASOME FROM THERMOPLASMA ACIDOPHILUM , 1996 .

[33]  David M. Rubin,et al.  Identification of the gal4 suppressor Sug1 as a subunit of the yeast 26S proteasome , 1996, Nature.

[34]  W. Wang,et al.  Mammalian Sug1 and c-Fos in the nuclear 26S proteasome. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[35]  K. Ferrell,et al.  Tat-binding protein 7 is a subunit of the 26S protease. , 1994, Biological chemistry Hoppe-Seyler.

[36]  J. Peters,et al.  Proteasomes: protein degradation machines of the cell. , 1994, Trends in biochemical sciences.

[37]  D A Agard,et al.  The role of pro regions in protein folding. , 1993, Current opinion in cell biology.

[38]  J. Paramio,et al.  Changes in proteasome localization during the cell cycle. , 1994, European journal of cell biology.

[39]  C. Cardozo,et al.  Catalytic components of the bovine pituitary multicatalytic proteinase complex (proteasome). , 1993, Enzyme & protein.

[40]  W. Baumeister,et al.  Changes in intracellular localization of proteasomes in immortalized ovarian granulosa cells during mitosis associated with a role in cell cycle control. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[41]  C. Slaughter,et al.  Identification, purification, and characterization of a protein activator (PA28) of the 20 S proteasome (macropain). , 1992, The Journal of biological chemistry.

[42]  W. Baumeister,et al.  Structural features of the 26 S proteasome complex. , 1993, Journal of molecular biology.

[43]  A. Goldberg,et al.  Functions of the proteasome in antigen presentation. , 1995, Cold Spring Harbor symposia on quantitative biology.

[44]  F. R. Papa,et al.  The yeast SEN3 gene encodes a regulatory subunit of the 26S proteasome complex required for ubiquitin-dependent protein degradation in vivo , 1995, Molecular and cellular biology.

[45]  M. Hochstrasser.  Ubiquitin-dependent protein degradation. , 1996, Annual review of genetics.

[46]  P. Moore,et al.  The type 1 human immunodeficiency virus Tat binding protein is a transcriptional activator belonging to an additional family of evolutionarily conserved genes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[47]  W. Baumeister,et al.  Structure and function of the 20S proteasome and of its regulatory complexes. , 1995, Cold Spring Harbor symposia on quantitative biology.

[48]  K. Ferrell,et al.  Purification of an 11 S regulator of the multicatalytic protease. , 1992, The Journal of biological chemistry.

[49]  A. Goldberg,et al.  Functions of the proteasome in antigen presentation. , 1995, Cold Spring Harbor symposia on quantitative biology.

[50]  W. Baumeister,et al.  Import of human and Thermoplasma 20S proteasomes into nuclei of HeLa cells requires functional NLS sequences. , 1997, European journal of cell biology.

[51]  F. Blattner,et al.  Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. , 1993, Gene.

[52]  A. Rivett.  The multicatalytic proteinase. Multiple proteolytic activities. , 1989, The Journal of biological chemistry.

[53]  R. Huber,et al.  Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. , 1995, Science.

[54]  W. Baumeister,et al.  Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropolis. , 1998, Journal of molecular biology.

[55]  Q. Deveraux,et al.  A 26 S protease subunit that binds ubiquitin conjugates. , 1994, The Journal of biological chemistry.

[56]  I. Mett,et al.  A protein related to a proteasomal subunit binds to the intracellular domain of the p55 TNF receptor upstream to its ‘death domain’ , 1995, FEBS letters.

[57]  P. Kloetzel,et al.  Analysis of mammalian 20S proteasome biogenesis: the maturation of beta‐subunits is an ordered two‐step mechanism involving autocatalysis. , 1996, The EMBO journal.

[58]  Wolfgang Baumeister,et al.  The ATP-dependent HslVU protease from Escherichia coli is a four-ring structure resembling the proteasome , 1997, Nature Structural Biology.

[59]  T. Fujiwara,et al.  CDNA cloning of p112, the largest regulatory subunit of the human 26s proteasome, and functional analysis of its yeast homologue, sen3p. , 1996, Molecular biology of the cell.

[60]  S. Johnston,et al.  Isolation and Characterization of SUG2 , 1996, The Journal of Biological Chemistry.

[61]  C. Enenkel,et al.  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 , 1994, FEBS letters.

[62]  K Tanaka,et al.  Structure and functions of the 20S and 26S proteasomes. , 1996, Annual review of biochemistry.

[63]  J. Monaco,et al.  Intermediates in the formation of mouse 20S proteasomes: implications for the assembly of precursor β subunits , 1997 .

[64]  P. A. Peterson,et al.  In Vivo Characterization of the Proteasome Regulator PA28* , 1996, The Journal of Biological Chemistry.

[65]  C. Slaughter,et al.  A Model for the Quaternary Structure of the Proteasome Activator PA28* , 1996, The Journal of Biological Chemistry.

[66]  W. Baumeister,et al.  Functional significance of symmetrical versus asymmetrical GroEL-GroES chaperonin complexes , 1995, Science.

[67]  B L Trus,et al.  Homology in structural organization between E. coli ClpAP protease and the eukaryotic 26 S proteasome. , 1995, Journal of molecular biology.

[68]  H. McDonald,et al.  A Proteasome Cap Subunit Required for Spindle Pole Body Duplication in Yeast , 1997, The Journal of cell biology.

[69]  H. Ploegh,et al.  Generation, translocation, and presentation of MHC class I-restricted peptides. , 1995, Annual review of biochemistry.

[70]  J. Ferry,et al.  A Proteasome from the Methanogenic Archaeon Methanosarcina thermophila(*) , 1995, The Journal of Biological Chemistry.

[71]  W Baumeister,et al.  Subunit topology of the Rhodococcus proteasome , 1997, FEBS letters.

[72]  W. Baumeister,et al.  Dissecting the assembly pathway of the 20S proteasome , 1997, FEBS letters.

[73]  M. Hochstrasser,et al.  Autocatalytic Subunit Processing Couples Active Site Formation in the 20S Proteasome to Completion of Assembly , 1996, Cell.

[74]  Alexei F. Kisselev,et al.  Processive Degradation of Proteins and Other Catalytic Properties of the Proteasome from Thermoplasma acidophilum* , 1997, The Journal of Biological Chemistry.

[75]  R. Huber,et al.  Structure of 20S proteasome from yeast at 2.4Å resolution , 1997, Nature.

[76]  L. J. Veer,et al.  The XPB subunit of repair/transcription factor TFIIH directly interacts with SUG1, a subunit of the 26S proteasome and putative transcription factor. , 1997, Nucleic acids research.

[77]  A. Udvardy,et al.  S. cerevisiae 26S protease mutants arrest cell division in G2/metaphase , 1993, Nature.

[78]  B. Dahlmann,et al.  Subunit arrangement in the human 20S proteasome. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[79]  G. C. Johnston,et al.  Sug1 modulates yeast transcription activation by Cdc68 , 1995, Molecular and cellular biology.

[80]  K Tanaka,et al.  cDNA cloning and functional analysis of the p97 subunit of the 26S proteasome, a polypeptide identical to the type-1 tumor-necrosis-factor-receptor-associated protein-2/55.11. , 1996, European journal of biochemistry.

[81]  R. Jaenicke,et al.  Symmetric complexes of GroE chaperonins as part of the functional cycle. , 1994, Science.

[82]  W Baumeister,et al.  Proteasome from Thermoplasma acidophilum: a threonine protease. , 1995, Science.

[83]  W Baumeister,et al.  Self-compartmentalizing proteases. , 1997, Trends in biochemical sciences.

[84]  U. Aebi,et al.  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* , 1997, The Journal of Biological Chemistry.

[85]  Craig A. Richmond,et al.  Specific Interactions between ATPase Subunits of the 26 S Protease* , 1997, The Journal of Biological Chemistry.

[86]  T. E. Shrader,et al.  Inactivation of the 20S proteasome in Mycobacterium smegmatis , 1997, Molecular microbiology.

[87]  W. Baumeister,et al.  Autocatalytic processing of the 20S proteasome , 1996, Nature.

[88]  M. Rechsteiner,et al.  Human lymphoblast and erythrocyte multicatalytic proteases: differential peptidase activities and responses to the 11S regulator , 1995, FEBS letters.

[89]  W. Baumeister,et al.  The proteasome: a macromolecular assembly designed to confine proteolysis to a nanocompartment. , 1997, Biological chemistry.

[90]  Clive A. Slaughter,et al.  Proteolytic Processing of Ovalbumin and β-galactosidase by the Proteasome to Yield Antigenic Peptides , 1994 .

[91]  Bernd Bukau,et al.  The Hsp70 and Hsp60 Chaperone Machines , 1998, Cell.

[92]  W. Baumeister,et al.  Dissociation and reconstitution of the Thermoplasma proteasome. , 1994, European journal of biochemistry.

[93]  P. Kloetzel,et al.  The Interferon-γ-inducible 11 S Regulator (PA28) and the LMP2/LMP7 Subunits Govern the Peptide Production by the 20 S Proteasome in Vitro(*) , 1995, The Journal of Biological Chemistry.

[94]  W. Baumeister,et al.  Proteasomes from Dictyostelium discoideum: characterization of structure and function. , 1993, Journal of structural biology.

[95]  A. Horwich,et al.  The Hsp 70 and Hsp 60 Review Chaperone Machines , 1998 .

[96]  Wolfgang Baumeister,et al.  Potential Immunocompetence of Proteolytic Fragments Produced by Proteasomes before Evolution of the Vertebrate Immune System , 1997 .

[97]  W. Baumeister,et al.  Proteasome sequences in eubacteria. , 1994, Trends in biochemical sciences.

[98]  K. Ferrell,et al.  Molecular cloning and expression of a gamma-interferon-inducible activator of the multicatalytic protease. , 1994, The Journal of biological chemistry.

[99]  A. Varshavsky,et al.  The ubiquitin system. , 1997, Trends in biochemical sciences.

[100]  P. Chambon,et al.  SUG1, a Putative Transcriptional Mediator and Subunit of the PA700 Proteasome Regulatory Complex, Is a DNA Helicase* , 1997, The Journal of Biological Chemistry.

[101]  Jimin Wang,et al.  The Structure of ClpP at 2.3 Å Resolution Suggests a Model for ATP-Dependent Proteolysis , 1997, Cell.

[102]  Y. Shimizu,et al.  Yeast counterparts of subunits S5a and p58 (S3) of the human 26S proteasome are encoded by two multicopy suppressors of nin1-1. , 1997, Molecular biology of the cell.

[103]  P. Kloetzel,et al.  The multicatalytic proteinase: a high-Mr endopeptidase. , 1988, Biochemical Journal.

[104]  P. A. Peterson,et al.  In Vivo Assembly of the Proteasomal Complexes, Implications for Antigen Processing (*) , 1995, The Journal of Biological Chemistry.

[105]  P. Kloetzel,et al.  Maturation of mammalian 20 S proteasome: purification and characterization of 13 S and 16 S proteasome precursor complexes. , 1997, Journal of molecular biology.

[106]  M. Goebl,et al.  New human gene encoding a positive modulator of HIV Tat-mediated transactivation , 1992, Nature.

[107]  W. Baumeister,et al.  Nuclear localization signals of human and Thermoplasma proteasomal alpha subunits are functional in vitro. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[108]  W. Baumeister,et al.  Existence of a molecular ruler in proteasomes suggested by analysis of degradation products , 1994, FEBS letters.

[109]  W Baumeister,et al.  A repetitive sequence in subunits of the 26S proteasome and 20S cyclosome (anaphase-promoting complex). , 1997, Trends in biochemical sciences.

[110]  A. Horwich,et al.  CRYSTAL STRUCTURE OF THE ASYMMETRIC CHAPERONIN COMPLEX GROEL/GROES/(ADP)7 , 1997 .

[111]  M J Sternberg,et al.  Empirical scale of side-chain conformational entropy in protein folding. , 1993, Journal of molecular biology.

[112]  D C Rees,et al.  Crystal structure of a conserved protease that binds DNA: the bleomycin hydrolase, Gal6 , 1995, Science.