Proteasomes and their kin: proteases in the machine age (original) (raw)

References

1. Groll, M. et al. Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386, 463–471 (1997). Despite being assembled from 14 unique polypeptides, the eukaryotic 20S proteasome is remarkably similar to its archaebacterial cousin. Furthermore, the closed state of the axial pore indicated that the 19S complex would regulate pore gating.
   CAS PubMed Google Scholar
2. Unno, M. et al. The stucture of the mammalian 20S proteasome at 2.75 Å resolution. Structure 10, 609–618 (2002).
   CAS PubMed Google Scholar
3. Lowe, J. et al. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268, 533–539 (1995).
   CAS PubMed Google Scholar
4. Whitby, F. G. et al. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408, 115–120 (2000). The structure of a non-ATPase regulatory complex bound to the yeast 20S complex led to a persuasive molecular model for protease pore opening by a regulatory complex.
   CAS PubMed Google Scholar
5. Wang, J., Hartling, J. A. & Flanagan, J. M. The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell 91, 447–456 (1997).
   CAS PubMed Google Scholar
6. Bochtler, M., Ditzel, L., Groll, M. & Huber, R. Crystal structure of heat shock locus V (HslV) from Escherichia coli. Proc. Natl Acad. Sci. USA 94, 6070–6074 (1997).
   CAS PubMed PubMed Central Google Scholar
7. Baumeister, W., Walz, J., Zuhl, F. & Seemuller, E. The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367–380 (1998).
   CAS PubMed Google Scholar
8. Ogura, T. & Wilkinson, A. J. AAA+ superfamily ATPases: common structure — diverse function. Genes Cells 6, 575–597 (2001).
   CAS PubMed Google Scholar
9. Wolf, S. et al. Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropolis. J. Mol. Biol. 277, 13–25 (1998).
   CAS PubMed Google Scholar
10. Zwickl, P., Ng, D., Woo, K. M., Klenk, H. P. & Goldberg, A. L. An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26 S proteasome, activates protein breakdown by 20 S proteasomes. J. Biol. Chem. 274, 26008–26014 (1999).
    CAS PubMed Google Scholar
11. Glickman, M. H. et al. A subcomplex of the proteasome regulatory particle required for ubiquitin–conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94, 615–623 (1998). The 19S complex consists of two discrete subcomplexes — the first (lid) has homology to two other complexes and the second (base) is similar to the simpler regulatory complexes of bacteria.
    CAS PubMed Google Scholar
12. Rubin, C. M., Glickman, M. H., Larsen, C. N., Dhruvakumar, S. & Finley, D. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 17, 4909–4919 (1998). The six ATPases in the base of the 19S complex are functionally distinct.
    CAS PubMed PubMed Central Google Scholar
13. Fu, H., Reis, N., Lee, Y., Glickman, M. H. & Vierstra, R. D. Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome. EMBO J. 20, 7096–7107 (2001).
    CAS PubMed PubMed Central Google Scholar
14. Verma, R. et al. Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes. Mol. Biol. Cell 11, 3425–3439 (2000).
    CAS PubMed PubMed Central Google Scholar
15. Leggett, D. S. et al. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10, 495–507 (2002).
    CAS PubMed Google Scholar
16. Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 67, 425–479 (1998).
    Article CAS PubMed Google Scholar
17. Pickart, C. M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503–533 (2001).
    CAS PubMed Google Scholar
18. Deshaies, R. J. SCF and cullin/RING H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15, 435–467 (1999).
    CAS PubMed Google Scholar
19. Conaway, R. C. & Conaway, J. W. The von Hippel–Lindau tumor suppressor complex and regulation of hypoxia-inducible transcription. Adv. Cancer Res. 85, 1–12 (2002).
    CAS PubMed Google Scholar
20. Peters, J. M. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9, 931–943 (2002).
    CAS PubMed Google Scholar
21. Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J. & Howley, P. M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129–1136 (1990).
    CAS PubMed Google Scholar
22. Thrower, J. S., Hoffman, L., Rechsteiner, M. & Pickart, C. M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19, 94–102 (2000). A polyubiquitin chain that is four ubiquitins long is the minimum signal required for efficient targeting to 26S proteasomes.
    CAS PubMed PubMed Central Google Scholar
23. Deveraux, Q., Ustrell, V., Pickart, C. & Rechsteiner, M. A 26S protease subunit that binds ubiquitin conjugates. J. Biol. Chem. 269, 7059–7061 (1994).
    CAS PubMed Google Scholar
24. Elsasser, S. et al. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nature Cell Biol. 4, 725–730 (2002).
    CAS PubMed Google Scholar
25. Hartmann-Petersen, R., Seeger, M. & Gordon, C. Transferring substrates to the 26S proteasome. Trends Biochem. Sci. 28, 26–31 (2003).
    CAS PubMed Google Scholar
26. Lam, Y. A., Lawson, T. G., Velayutham, M., Zweier, J. L. & Pickart, C. M. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 416, 763–767 (2002).
    CAS PubMed Google Scholar
27. van Nocker, S. 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. Mol. Cell. Biol. 16, 6020–6028 (1996).
    CAS PubMed PubMed Central Google Scholar
28. Xie, Y. & Varshavsky, A. UFD4 lacking the proteasome-binding region catalyses ubiquitination but is impaired in proteolysis. Nature Cell Biol. 4, 1003–1007 (2002).
    CAS PubMed Google Scholar
29. You, J. & Pickart, C. M. A hect domain E3 enzyme assembles novel polyubiquitin chains. J. Biol. Chem. 276, 19871–19878 (2001).
    CAS PubMed Google Scholar
30. Wilkinson, C. R. et al. Proteins containing the UBA domain are able to bind multi-ubiquitin chains. Nature Cell Biol. 3, 939–943 (2001).
    CAS PubMed Google Scholar
31. Schauber, C. et al. Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 391, 715–718 (1997).
    Google Scholar
32. Raasi, S. & Pickart, C. M. Rad23 ubiquitin-associated domains (UBA) inhibit 26S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J. Biol. Chem. 278, 8951–8959 (2003).
    CAS PubMed Google Scholar
33. Glockzin, S., Ogi, F. -X., Hengstermann, A., Scheffner, M. & Blattner, C. Involvement of the DNA repair protein hHR23 in p53 degradation. Mol. Cell. Biol. 23, 8960–8969 (2003).
    CAS PubMed PubMed Central Google Scholar
34. Bloom, J., Amador, V., Bartolini, F., DeMartino, G. & Pagano, M. Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell 115, 71–82 (2003).
    CAS PubMed Google Scholar
35. Flynn, J. M. et al. Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. Proc. Natl Acad. Sci. USA 98, 10584–10589 (2001).
    CAS PubMed PubMed Central Google Scholar
36. Hoskins, J. R., Yanagihara, K., Mizuuchi, K. & Wickner, S. ClpAP and ClpXP degrade proteins with tags located in the interior of the primary sequence. Proc. Natl Acad. Sci. USA 17, 11037–11042 (2002).
    Google Scholar
37. Levchenko, I., Yamauchi, M. & Baker, T. A. ClpX and MuB interact with overlapping regions of Mu transposase: implications for control of the transposition pathway. Genes Dev. 11, 1561–1572 (1997).
    CAS PubMed Google Scholar
38. Gonzalez, M., Rasulova, F., Maurizi, M. R. & Woodgate, R. Subunit-specific degradation of the UmuD/D′ heterodimer by the ClpXP protease: the role of trans recognition in UmuD′ stability. EMBO J. 19, 5251–5258 (2000).
    CAS PubMed PubMed Central Google Scholar
39. Gonciarz-Swiatek, M. et al. Recognition, targeting, and hydrolysis of the λ O replication protein by the ClpP/ClpX protease. J. Biol. Chem. 274, 13999–14005 (1999).
    CAS PubMed Google Scholar
40. Karzai, A. W., Roche, E. D. & Sauer, R. T. The SsrA–SmpB system for protein tagging, directed degradation and ribosome rescue. Nature Struct. Biol. 7, 449–445 (2000).
    CAS PubMed Google Scholar
41. Zhang, M., Pickart, C. M. & Coffino, P. Determinants of proteasome recognition of ornithine decarboxylase, a ubiquitin-independent substrate. EMBO J. 22, 1488–1496 (2003).
    CAS PubMed PubMed Central Google Scholar
42. Coffino, P. Regulation of cellular polyamines by antizyme. Nature Rev. Mol. Cell Biol. 2, 188–194 (2001).
    CAS Google Scholar
43. Lee, C., Schwartz, M. P., Prakash, S., Iwakura, M. & Matouschek, A. ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell 7, 627–637 (2001). Prokaryotic chambered proteases unfold their substrates starting at the degradation signal, and without reference to the thermodynamic stability of the substrate.
    CAS PubMed Google Scholar
44. Burton, R. E., Siddiqui, S. M., Kim, Y. -I., Baker, T. A. & Sauer, R. T. Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine. EMBO J. 20, 3092–3100 (2001).
    CAS PubMed PubMed Central Google Scholar
45. Kenniston, J. A., Baker, T. A., Fernandez, J. M. & Sauer, R. T. Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of a AAA+ degradation machine. Cell 114, 511–520 (2003). Studies with a prokaryotic protease show that the cost of translocation consumes much of the energy that is used in degradation.
    CAS PubMed Google Scholar
46. Grantcharova, V., Alm, E. J., Baker, D. & Horwich, A. L. Mechanisms of protein folding. Curr. Opin. Struct. Biol. 11, 70–82 (2001).
    CAS PubMed Google Scholar
47. Weber-Ban, E. U., Reid, G. B., Miranker, A. D. & Horwich, A. L. Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 410, 90–93 (1999).
    Google Scholar
48. Matouschek, A. Protein unfolding — an important process in vivo? Curr. Opin. Struct. Biol. 13, 98–109 (2003).
    CAS PubMed Google Scholar
49. Verma, R., McDonald, H., Yates, J. R. & Deshaies, R. J. Selective degradation of ubiquitinated Sic1 by purified 26S proteasome yields active S phase cyclin–Cdk. Mol. Cell 8, 439–448 (2001).
    CAS PubMed Google Scholar
50. Levchenko, I., Luo, L. & Baker, T. A. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 9, 2399–2408 (1995).
    CAS PubMed Google Scholar
51. Wickner, S. et al. A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc. Natl Acad. Sci. USA 91, 12218–12222 (1994).
    CAS PubMed PubMed Central Google Scholar
52. Russell, S. J., Reed, S. H., Huang, W., Friedberg, E. C. & Johnston, S. A. The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol. Cell 3, 687–695 (1999).
    CAS PubMed Google Scholar
53. Ferdous, A., Gonzalez, F., Sun, L., Kodadek, T. & Johnston, S. A. The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol. Cell 7, 981–991 (2001).
    CAS PubMed Google Scholar
54. Braun, B. C. et al. The base of the proteasome regulatory particle exhibits chaperone-like activity. Nature Cell Biol. 1, 221–226 (1999).
    CAS PubMed Google Scholar
55. Strickland, E., Hakala, K., Thomas, P. J. & DeMartino, G. N. Recognition of misfolded proteins by PA700, the regulatory subcomplex of the 26S proteasome. J. Biol. Chem. 275, 5565–5572 (2000).
    CAS PubMed Google Scholar
56. Liu, C. et al. Conformational remodeling of proteasomal substrates by PA700, the 19S regulatory complex of the 26S proteasome. J. Biol. Chem. 277, 26815–26820 (2002).
    CAS PubMed Google Scholar
57. Johnson, E. S., Gonda, D. K. & Varshavsky, A. cis_–_trans recognition and subunit-specific degradation of short-lived proteins. Nature 346, 287–291 (1990).
    CAS PubMed Google Scholar
58. Chen, Z. et al. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin–proteasome pathway. Genes Dev. 9, 1586–1597 (1995).
    CAS PubMed Google Scholar
59. Hoskins, J. R., Singh, S. K., Maruizi, M. R. & Wickner, S. Protein binding and unfolding by the chaperone ClpA and degradation by the protease ClpAP. Proc. Natl Acad. Sci. USA 97, 8892–8897 (2000).
    CAS PubMed PubMed Central Google Scholar
60. Singh, S. K., Grimaud, R., Hoskins, J. R., Wickner, S. & Maurizi, M. R. Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP. Proc. Natl Acad. Sci. USA 97, 8898–8903 (2000).
    CAS PubMed PubMed Central Google Scholar
61. Kim, Y. -I., Burton, R. E., Burton, B. M., Sauer, R. T. & Baker, T. A. Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol. Cell 5, 639–648 (2000).
    CAS PubMed Google Scholar
62. Flynn, J. M., Neher, S. B., Kim, Y. -I., Sauer, R. T. & Baker, T. A. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell 11, 1671–1683 (2003).
    Google Scholar
63. Ortega, J., Singh, S. K., Ishikawa, T., Maurizi, M. R. & Steven, A. C. Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. Mol. Cell 6, 1515–1521 (2000). Presents especially dramatic electron-microscopy images of substrate internalization by ClpXP.
    CAS PubMed Google Scholar
64. Sousa, M. C. et al. Crystal and solution structures of an HslUV protease–chaperone complex. Cell 103, 633–643 (2000).
    CAS PubMed Google Scholar
65. Wang, J. et al. Crystal structures of the HslVU peptidase–ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure 9, 177–184 (2001).
    CAS PubMed Google Scholar
66. Guo, F., Maurizi, M. R., Esser, L. & Xia, D. Crystal structure of ClpA, an Hsp100 chaperone and regulator of ClpAP protease. J. Biol. Chem. 277, 46743–46752 (2002).
    CAS PubMed Google Scholar
67. Benaroudj, N., Zwickl, P., Seemuller, E., Baumeister, W. & Goldberg, A. L. ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. Mol. Cell 11, 69–78 (2003).
    CAS PubMed Google Scholar
68. Carrion-Vasquez, M. et al. The mechanical stability of ubiquitin is linkage-dependent. Nature Struct. Biol. 10, 738–743 (2003).
    Google Scholar
69. Yao, T. & Cohen, R. E. A cryptic protease couples deubiquitination and degradation by the 26S proteasome. Nature 419, 403–407 (2002).
    CAS PubMed Google Scholar
70. Petroski, M. D. & Deshaies, R. J. Context of multiubiquitin chain attachment influences the rate of Sic1 degradation. Mol. Cell 11, 1435–1444 (2003).
    CAS PubMed Google Scholar
71. Rape, M. & Jentsch, S. Taking a bite: proteasomal processing. Nature Cell Biol. 4, E113–E116 (2002).
    CAS PubMed Google Scholar
72. Verma, R. & Deshaies, R. A proteasome howdunit: the case of the missing signal. Cell 101, 341–344 (2000).
    CAS PubMed Google Scholar
73. Lin, L. & Kobayashi, M. Stability of the Rel homology domain is critical for generation of NF-κB p50 subunits. J. Biol. Chem. 278, 31479–31485 (2003).
    CAS PubMed Google Scholar
74. Wang, J. et al. Nucleotide-dependent conformational changes in a protease-associated ATPase HslU. Structure 9, 1107–1116 (2001).
    CAS PubMed Google Scholar
75. Kohler, A. et al. The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. Mol. Cell 7, 1143–1152 (2001). One of the six ATPase subunits of the 19S complex has a specific role in opening the axial pore of the 20S complex.
    CAS PubMed Google Scholar
76. Groll, M. et al. A gated channel into the proteasome core particle. Nature Struct. Biol. 7, 1062–1067 (2000).
    CAS PubMed Google Scholar
77. Kloetzel, P. -M. Antigen processing by the proteasome. Nature Rev. Mol. Cell Biol. 2, 179–187 (2001).
    CAS Google Scholar
78. Forster, A. & Hill, C. P. Proteasome degradation: enter the substrate. Trends Cell Biol. 13, 550–553 (2003).
    CAS PubMed Google Scholar
79. Reid, B. G., Fenton, W. A., Horwich, A. L. & Weber-Ban, E. U. ClpA mediates directional translocation of substrate proteins into the ClpP protease. Proc. Natl Acad. Sci. USA 98, 3768–3772 (2001).
    CAS PubMed PubMed Central Google Scholar
80. Lee, C., Prakash, S. & Matouschek, A. Concurrent translocation of multiple polypeptide chains through the proteasomal degradation channel. J. Biol. Chem. 277, 34750–34765 (2002).
    Google Scholar
81. Orian, A. et al. Structural motifs involved in ubiquitin-mediated processing of the NFκB precursor p105: roles of the glycine-rich region and a downstream ubiquitination domain. Mol. Cell. Biol. 19, 3664–3673 (1999).
    CAS PubMed PubMed Central Google Scholar
82. Liu, C. -W., Corboy, M. J., DeMartino, G. N. & Thomas, P. J. Endoproteolytic activity of the proteasome. Science 299, 408–411 (2003). Provides some of the clearest evidence that proteasome proteolysis can begin at an internal loop of the polypeptide chain of the substrate.
    CAS PubMed Google Scholar
83. Kisselev, A. F., Kaganovich, D. & Goldberg, A. L. Binding of hydrophobic peptides to several non-catalytic sites promotes peptide hydrolysis by all active sites of 20S proteasomes. Evidence for peptide-induced channel opening in the α-rings. J. Biol. Chem. 277, 22260–22770 (2002).
    CAS PubMed Google Scholar
84. Cascio, P., Call, M., Petre, B. M., Walz, T. & Goldberg, A. L. Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes. EMBO J. 21, 2636–2645 (2002).
    CAS PubMed PubMed Central Google Scholar
85. Tanahashi, N. et al. Hybrid proteasomes. Induction by interferon-γ and contribution to ATP-dependent proteolysis. J. Biol. Chem. 275, 4336–4345 (2000).
    Google Scholar
86. Wintrode, P. L., Makhatadze, G. I. & Privalov, P. L. Thermodynamics of ubiquitin unfolding. Proteins 18, 246–253 (1994).
    CAS PubMed Google Scholar
87. Tran, H. J., Allen, M. D., Lowe, J. & Bycroft, M. Structure of the Jab1/MPN domain and its implications for proteasome function. Biochemistry 42, 11460–11465 (2003).
    CAS PubMed Google Scholar
88. Ambroggio, X. I., Rees, D. C. & Deshaies, R. J. JAMM: a metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol. Jan 2004 (doi:10.1371/journal.pbio.0020002).
89. Maytal-Kivity, V., Reis, N., Hofmann, K. & Glickman, M. MPN+, a putative catalytic motif found in a subset of MPN domain proteins from eukaryotes and prokayotes, is critical for Rpn11 function. BMC Biochem. 3, 28–38 (2002).
    PubMed PubMed Central Google Scholar
90. Verma, R. et al. Role of Rpn11 metalloprotease motif in deubiquitination and degradation by the 26S proteasome. Science 298, 611–615 (2002).
    CAS PubMed Google Scholar
91. Borodovsky, A. et al. A novel active site directed probe specific for deubiquitinating enzyme reveals proteasome association of Usp14. EMBO J. 20, 5187–5196 (2001).
    CAS PubMed PubMed Central Google Scholar
92. Lam, Y. A., Xu, W., DeMartino, G. N. & Cohen, R. E. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385, 737–740 (1997).
    CAS PubMed Google Scholar
93. Li, T., Naqvi, N. I., Hang, H. & Teo, T. S. Identification of a 26S proteasome-associated UCH in fission yeast. Biochem. Biophys. Res. Commun. 272, 170–175 (2000).
    Google Scholar
94. Holzl, H. et al. The regulatory complex of Drosophila melanogaster 26S proteasomes. Subunit composition and localization of a deubiquitylating enzyme. J. Cell Biol. 150, 119–130 (2000).
    CAS PubMed PubMed Central Google Scholar
95. Glickman, M. H., Rubin, D. M., Fried, V. A. & Finley, D. The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol. Cell. Biol. 18, 3149–3162 (1998).
    CAS PubMed PubMed Central Google Scholar
96. Amerik, A. Y., Nowak, J., Swaminathan, S. & Hochstrasser, M. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11, 3365–3380 (2000).
    CAS PubMed PubMed Central Google Scholar
97. Adams, J. Proteasome inhibitors as new anticancer drugs. Curr. Opin. Oncol. 14, 628–634 (2002).
    CAS PubMed Google Scholar
98. Peng, J. et al. A proteomics approach to understanding protein ubiquitination. Nature Biotechnol. 21, 921–926 (2003).
    CAS Google Scholar
99. Finley, D. Ubiquitin chained and crosslinked. Nature Cell Biol. 4, E121–E123 (2002).
    CAS PubMed Google Scholar
100. Ortega, J., Lee, H. S., Maurizi, M. R. & Steven, A. C. Alternating translocation of protein substrates from both ends of ClpXP protease. EMBO J. 21, 4938–4949 (2002).
     CAS PubMed PubMed Central Google Scholar

Download references