Proteasomes and their kin: proteases in the machine age

'Chambered proteases', including the eukaryotic 26S proteasome, use the energy of ATP to drive the unfolding and translocation of a polypeptide substrate into a chamber of sequestered proteolytic active sites. These proteases have diverse functions and are found in all three kingdoms of life. Understanding chambered proteases requires answers to two questions — how do these remarkable machines select the correct target proteins and how do they bring about the processive degradation of these molecules?

[1]  Jan-Michael Peters,et al.  The anaphase-promoting complex: proteolysis in mitosis and beyond. , 2002, Molecular cell.

[2]  C. Hill,et al.  Proteasome degradation: enter the substrate. , 2003, Trends in cell biology.

[3]  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.

[4]  Alexander Varshavsky,et al.  The ubiquitin system. , 1998, Annual review of biochemistry.

[5]  Li Chen,et al.  Rad23 links DNA repair to the ubiquitin/proteasome pathway , 1998, Nature.

[6]  H. Ploegh,et al.  Multiple associated proteins regulate proteasome structure and function. , 2002, Molecular cell.

[7]  W. Baumeister,et al.  The Regulatory Complex of Drosophila melanogaster 26s Proteasomes , 2000, The Journal of cell biology.

[8]  Erica S. Johnson,et al.  Cis-trans recognition and subunit-specific degradation of short-lived proteins , 1990, Nature.

[9]  R. Woodgate,et al.  Subunit‐specific degradation of the UmuD/D′ heterodimer by the ClpXP protease: the role of trans recognition in UmuD′ stability , 2000, The EMBO journal.

[10]  H. Yang,et al.  Identification of a 26S proteasome-associated UCH in fission yeast. , 2000, Biochemical and biophysical research communications.

[11]  M. Pagano,et al.  Proteasome-Mediated Degradation of p21 via N-Terminal Ubiquitinylation , 2003, Cell.

[12]  J. Yates,et al.  Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes. , 2000, Molecular biology of the cell.

[13]  P. Kloetzel,et al.  The base of the proteasome regulatory particle exhibits chaperone-like activity , 1999, Nature Cell Biology.

[14]  P. Coffino.  Ubiquitin and proteasomes: Regulation of cellular polyamines by antizyme , 2001, Nature Reviews Molecular Cell Biology.

[15]  J. Wang,et al.  Nucleotide-dependent conformational changes in a protease-associated ATPase HsIU. , 2001, Structure.

[16]  P. Thomas,et al.  Endoproteolytic Activity of the Proteasome , 2002, Science.

[17]  Li Lin,et al.  Stability of the Rel Homology Domain Is Critical for Generation of NF-κB p50 Subunit* , 2003, Journal of Biological Chemistry.

[18]  T. Mizushima,et al.  The structure of the mammalian 20S proteasome at 2.75 A resolution. , 2002, Structure.

[19]  Y. Murakami,et al.  Hybrid Proteasomes , 2000, The Journal of Biological Chemistry.

[20]  A. Matouschek,et al.  Concurrent Translocation of Multiple Polypeptide Chains through the Proteasomal Degradation Channel* , 2002, The Journal of Biological Chemistry.

[21]  R. Deshaies,et al.  A Proteasome Howdunit The Case of the Missing Signal , 2000, Cell.

[22]  Tania A. Baker,et al.  Linkage between ATP Consumption and Mechanical Unfolding during the Protein Processing Reactions of an AAA+ Degradation Machine , 2003, Cell.

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

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

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

[26]  A. Goldberg,et al.  Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes , 2002, The EMBO journal.

[27]  R. Sauer,et al.  The SsrA–SmpB system for protein tagging, directed degradation and ribosome rescue , 2000, Nature Structural Biology.

[28]  J. Hoskins,et al.  Protein binding and unfolding by the chaperone ClpA and degradation by the protease ClpAP. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Goldberg,et al.  ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. , 2003, Molecular cell.

[30]  Noa Reis,et al.  Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome , 2001, The EMBO journal.

[31]  J R Yates,et al.  Selective degradation of ubiquitinated Sic1 by purified 26S proteasome yields active S phase cyclin-Cdk. , 2001, Molecular cell.

[32]  A. Ciechanover,et al.  Structural Motifs Involved in Ubiquitin-Mediated Processing of the NF-κB Precursor p105: Roles of the Glycine-Rich Region and a Downstream Ubiquitination Domain , 1999, Molecular and Cellular Biology.

[33]  T. Baker,et al.  Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  R. Deshaies.  SCF and Cullin/Ring H2-based ubiquitin ligases. , 1999, Annual review of cell and developmental biology.

[35]  A. Varshavsky,et al.  UFD4 lacking the proteasome-binding region catalyses ubiquitination but is impaired in proteolysis , 2002, Nature Cell Biology.

[36]  Christine B. Trame,et al.  Crystal and Solution Structures of an HslUV Protease–Chaperone Complex , 2000, Cell.

[37]  C. Pickart,et al.  A HECT Domain E3 Enzyme Assembles Novel Polyubiquitin Chains* , 2001, The Journal of Biological Chemistry.

[38]  A. Amerik,et al.  The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. , 2000, Molecular biology of the cell.

[39]  T. Yao,et al.  A cryptic protease couples deubiquitination and degradation by the proteasome , 2002, Nature.

[40]  A. Goldberg,et al.  An Archaebacterial ATPase, Homologous to ATPases in the Eukaryotic 26 S Proteasome, Activates Protein Breakdown by 20 S Proteasomes* , 1999, The Journal of Biological Chemistry.

[41]  A. Goldberg,et al.  The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. , 2001, Molecular cell.

[42]  R. Hartmann-Petersen,et al.  Transferring substrates to the 26S proteasome. , 2003, Trends in biochemical sciences.

[43]  J. Hoskins,et al.  Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  A. Wilkinson,et al.  AAA+ superfamily ATPases: common structure–diverse function , 2001, Genes to cells : devoted to molecular & cellular mechanisms.

[45]  J. Adams,et al.  Proteasome inhibitors as new anticancer drugs , 2002, Current opinion in oncology.

[46]  L. Millen,et al.  Conformational Remodeling of Proteasomal Substrates by PA700, the 19 S Regulatory Complex of the 26 S Proteasome* , 2002, The Journal of Biological Chemistry.

[47]  C. Pickart,et al.  Mechanisms underlying ubiquitination. , 2001, Annual review of biochemistry.

[48]  A. Matouschek,et al.  ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. , 2001, Molecular cell.

[49]  A. Matouschek.  Protein unfolding--an important process in vivo? , 2003, Current opinion in structural biology.

[50]  M. Glickman,et al.  MPN+, a putative catalytic motif found in a subset of MPN domain proteins from eukaryotes and prokaryotes, is critical for Rpn11 function , 2002, BMC Biochemistry.

[51]  Steven P Gygi,et al.  A proteomics approach to understanding protein ubiquitination , 2003, Nature Biotechnology.

[52]  T. Kodadek,et al.  The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. , 2001, Molecular cell.

[53]  T. Baker,et al.  Disassembly of the Mu transposase tetramer by the ClpX chaperone. , 1995, Genes & development.

[54]  T. Krieg,et al.  Activation of p70 Ribosomal Protein S6 Kinase Is an Essential Step in the DNA Damage-dependent Signaling Pathway Responsible for the Ultraviolet B-mediated Increase in Interstitial Collagenase (MMP-1) and Stromelysin-1 (MMP-3) Protein Levels in Human Dermal Fibroblasts* , 2000, The Journal of Biological Chemistry.

[55]  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.

[56]  E. Friedberg,et al.  The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. , 1999, Molecular cell.

[57]  T. Baker,et al.  ClpX and MuB interact with overlapping regions of Mu transposase: implications for control of the transposition pathway. , 1997, Genes & development.

[58]  J. Zweier,et al.  A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal , 2002, Nature.

[59]  M. Bycroft,et al.  Structure of the Jab1/MPN domain and its implications for proteasome function. , 2003, Biochemistry.

[60]  H. Ploegh,et al.  A novel active site‐directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14 , 2001, The EMBO journal.

[61]  Arnold J. Levine,et al.  The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53 , 1990, Cell.

[62]  Mingsheng Zhang,et al.  Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin‐independent substrate , 2003, The EMBO journal.

[63]  M. Glickman,et al.  Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome , 1998, The EMBO journal.

[64]  D. Rees,et al.  JAMM: A Metalloprotease-Like Zinc Site in the Proteasome and Signalosome , 2003, PLoS biology.

[65]  G. Dittmar,et al.  Proteasome subunit Rpn1 binds ubiquitin-like protein domains , 2002, Nature Cell Biology.

[66]  R. Deshaies,et al.  Context of multiubiquitin chain attachment influences the rate of Sic1 degradation. , 2003, Molecular cell.

[67]  D Baker,et al.  Mechanisms of protein folding. , 2001, Current opinion in structural biology.

[68]  T. Baker,et al.  Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine , 2001, The EMBO journal.

[69]  M. Glickman,et al.  Proteasome cerevisiae Saccharomyces The Regulatory Particle of the , 1997 .

[70]  Y. Murakami,et al.  Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. , 2000, The Journal of biological chemistry.

[71]  L. Aravind,et al.  Role of Rpn11 Metalloprotease in Deubiquitination and Degradation by the 26S Proteasome , 2002, Science.

[72]  T. Maniatis,et al.  Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. , 1995, Genes & development.

[73]  T. Baker,et al.  Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. , 2003, Molecular cell.

[74]  Wolfgang Baumeister,et al.  The Proteasome: Paradigm of a Self-Compartmentalizing Protease , 1998, Cell.

[75]  Martin Rechsteiner,et al.  Recognition of the polyubiquitin proteolytic signal , 2000, The EMBO journal.

[76]  P. Privalov,et al.  Thermodynamics of ubiquitin unfolding , 1994, Proteins.

[77]  Kiyoshi Mizuuchi,et al.  ClpAP and ClpXP degrade proteins with tags located in the interior of the primary sequence , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[78]  A. Horwich,et al.  ClpA mediates directional translocation of substrate proteins into the ClpP protease , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[79]  S. Jentsch,et al.  Taking a bite: proteasomal protein processing , 2002, Nature Cell Biology.

[80]  A. Steven,et al.  Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. , 2000, Molecular cell.

[81]  C. Georgopoulos,et al.  Recognition, Targeting, and Hydrolysis of the λ O Replication Protein by the ClpP/ClpX Protease* , 1999, Journal of Biological Chemistry.

[82]  A. Hengstermann,et al.  Involvement of the DNA Repair Protein hHR23 inp53Degradation , 2003, Molecular and Cellular Biology.

[83]  E. Strickland,et al.  Recognition of Misfolding Proteins by PA700, the Regulatory Subcomplex of the 26 S Proteasome* , 2000, The Journal of Biological Chemistry.

[84]  J. Wang,et al.  Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. , 2001, Structure.

[85]  C. Pickart,et al.  Rad23 Ubiquitin-associated Domains (UBA) Inhibit 26 S Proteasome-catalyzed Proteolysis by Sequestering Lysine 48-linked Polyubiquitin Chains* , 2003, The Journal of Biological Chemistry.

[86]  R. Huber,et al.  A gated channel into the proteasome core particle , 2000, Nature Structural Biology.

[87]  A. Horwich,et al.  Global unfolding of a substrate protein by the Hsp100 chaperone ClpA , 1999, Nature.

[88]  W. Baumeister,et al.  A Subcomplex of the Proteasome Regulatory Particle Required for Ubiquitin-Conjugate Degradation and Related to the COP9-Signalosome and eIF3 , 1998, Cell.

[89]  L. Esser,et al.  Crystal Structure of ClpA, an Hsp100 Chaperone and Regulator of ClpAP Protease* , 2002, The Journal of Biological Chemistry.

[90]  A. Steven,et al.  Alternating translocation of protein substrates from both ends of ClpXP protease , 2002, The EMBO journal.

[91]  Hui Lu,et al.  The mechanical stability of ubiquitin is linkage dependent , 2003, Nature Structural Biology.

[92]  A. Goldberg,et al.  Binding of Hydrophobic Peptides to Several Non-catalytic Sites Promotes Peptide Hydrolysis by All Active Sites of 20 S Proteasomes , 2002, The Journal of Biological Chemistry.

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

[94]  S. Gottesman,et al.  A molecular chaperone, ClpA, functions like DnaK and DnaJ. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[96]  Colin Gordon,et al.  Proteins containing the UBA domain are able to bind to multi-ubiquitin chains , 2001, Nature Cell Biology.

[97]  T. Baker,et al.  Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. , 2000, Molecular cell.

[98]  D. Finley.  Ubiquitin chained and crosslinked , 2002, Nature Cell Biology.

[99]  Wei Xu,et al.  Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome , 1997, Nature.

[100]  R. Conaway,et al.  The von Hippel-Lindau tumor suppressor complex and regulation of hypoxia-inducible transcription. , 2002, Advances in cancer research.