Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA+ unfoldase

Nature Structural and Molecular Biology

Volumn 20, Issue 10, 2013, Pages 1164-1173

  Beckwith, Robyn ^a   Estrin, Eric ^a   Worden, Evan J ^a   Martin, Andreas ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PROTEASOME; PROTEASOME 26S; PROTEINASE; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME RECONSTITUTION; ESCHERICHIA COLI; EUKARYOTIC CELL; GEL FILTRATION CHROMATOGRAPHY; GEL PERMEATION CHROMATOGRAPHY; HETEROLOGOUS EXPRESSION; HYDROLYSIS; IN VITRO STUDY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; POTENTIAL DIFFERENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN QUALITY; SACCHAROMYCES CEREVISIAE; TITRIMETRY;

ENDOPEPTIDASE CLP; ESCHERICHIA COLI; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84885428073     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2659     Document Type: Article

References (64)

1. Finley, D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477-513 (2009).
2. Hochstrasser, M. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30, 405-439 (1996). (Pubitemid 27014474)
3. Groll, M. et al. A gated channel into the proteasome core particle. Nat. Struct. Biol. 7, 1062-1067 (2000).
4. Liu, C.W. et al. ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome. Mol. Cell 24, 39-50 (2006).
5. Thrower, J.S., Hoffman, L., Rechsteiner, M. & Pickart, C.M. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19, 94-102 (2000). (Pubitemid 30009229)
6. 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). (Pubitemid 28427580)
7. Smith, D.M. et al. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's α ring opens the gate for substrate entry. Mol. Cell 27, 731-744 (2007). (Pubitemid 47333222)
8. Tomko, R.J. Jr. & Hochstrasser, M. Order of the proteasomal ATPases and eukaryotic proteasome assembly. Cell Biochem. Biophys. 60, 13-20 (2011).
9. Lander, G.C. et al. Complete subunit architecture of the proteasome regulatory particle. Nature 482, 186-191 (2012).
10. Beck, F. et al. Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl. Acad. Sci. USA 109, 14870-14875 (2012).
11. Hamazaki, J. et al. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J. 25, 4524-4536 (2006). (Pubitemid 44498126)
12. Yao, T. & Cohen, R.E. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419, 403-407 (2002).
13. Verma, R. et al. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298, 611-615 (2002). (Pubitemid 35215317)
14. Sakata, E. et al. Localization of the proteasomal ubiquitin receptors Rpn10 and Rpn13 by electron cryomicroscopy. Proc. Natl. Acad. Sci. USA 109, 1479-1484 (2012).
15. Martin, A., Baker, T.A. & Sauer, R.T. Rebuilt AAA+ motors reveal operating principles for ATP-fuelled machines. Nature 437, 1115-1120 (2005). (Pubitemid 41509343)
16. Rabl, J. et al. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30, 360-368 (2008). (Pubitemid 351615314)
17. Kim, Y.C. & DeMartino, G.N. C termini of proteasomal ATPases play nonequivalent roles in cellular assembly of mammalian 26 S proteasome. J. Biol. Chem. 286, 26652-26666 (2011).
18. Gillette, T.G., Kumar, B., Thompson, D., Slaughter, C.A. & DeMartino, G.N. Differential roles of the COOH termini of AAA subunits of PA700 (19 S regulator) in asymmetric assembly and activation of the 26 S proteasome. J. Biol. Chem. 283, 31813-31822 (2008).
19. Sledź, P. et al. Structure of the 26S proteasome with ATP-γS bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc. Natl. Acad. Sci. USA 110, 7264-7269 (2013).
20. Matyskiela, M.E., Lander, G.C. & Martin, A. Conformational switching of the 26S proteasome enables substrate degradation. Nat. Struct. Mol. Biol. 20, 781-788 (2013).
21. Rubin, D.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). (Pubitemid 28408458)
22. Erales, J., Hoyt, M.A., Troll, F. & Coffno, P. Functional asymmetries of proteasome translocase pore. J. Biol. Chem. 287, 18535-18543 (2012).
23. Kim, Y.C., Li, X., Thompson, D. & Demartino, G.N. ATP binding by proteasomal ATPases regulates cellular assembly and substrate-induced functions of the 26S proteasome. J. Biol. Chem. 288, 3334-3345 (2013).
24. Lee, S.H., Moon, J.H., Yoon, S.K. & Yoon, J.B. Stable incorporation of ATPase subunits into 19 S regulatory particle of human proteasome requires nucleotide binding and C-terminal tails. J. Biol. Chem. 287, 9269-9279 (2012).
25. Köhler, 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). (Pubitemid 32607349)
26. Park, S. et al. Hexameric assembly of the proteasomal ATPases is templated through their C termini. Nature 459, 866-870 (2009).
27. Kumar, B., Kim, Y.C. & DeMartino, G.N. The C terminus of Rpt3, an ATPase subunit of PA700 (19 S) regulatory complex, is essential for 26 S proteasome assembly but not for activation. J. Biol. Chem. 285, 39523-39535 (2010).
28. Thompson, D., Hakala, K. & DeMartino, G.N. Subcomplexes of PA700, the 19 S regulator of the 26 S proteasome, reveal relative roles of AAA subunits in 26 S proteasome assembly and activation and ATPase activity. J. Biol. Chem. 284, 24891-24903 (2009).
29. Funakoshi, M., Tomko, R.J. Jr., Kobayashi, H. & Hochstrasser, M. Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 137, 887-899 (2009).
30. Roelofs, J. et al. Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459, 861-865 (2009).
31. Saeki, Y., Toh, E.A., Kudo, T., Kawamura, H. & Tanaka, K. Multiple proteasome-interacting proteins assist the assembly of the yeast 19S regulatory particle. Cell 137, 900-913 (2009).
32. Kaneko, T. et al. Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specifc chaperones. Cell 137, 914-925 (2009).
33. Park, S. et al. Reconfguration of the proteasome during chaperone-mediated assembly. Nature 497, 512-516 (2013).
34. Smith, D.M. et al. ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol. Cell 20, 687-698 (2005). (Pubitemid 41740691)
35. Verma, R., Oania, R., Graumann, J. & Deshaies, R.J. Multiubiquitin chain receptors defne a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118, 99-110 (2004). (Pubitemid 38902817)
36. Hersch, G.L., Burton, R.E., Bolon, D.N., Baker, T.A. & Sauer, R.T. Asymmetric interactions of ATP with the AAA+ ClpX6 unfoldase: allosteric control of a protein machine. Cell 121, 1017-1027 (2005). (Pubitemid 40884394)
37. Weibezahn, J., Bukau, B. & Mogk, A. Unscrambling an egg: protein disaggregation by AAA+ proteins. Microb. Cell Fact. 3, 1 (2004).
38. Gómez, E.B., Catlett, M.G. & Forsburg, S.L. Different phenotypes in vivo are associated with ATPase motif mutations in Schizosaccharomyces pombe minichromosome maintenance proteins. Genetics 160, 1305-1318 (2002). (Pubitemid 34454357)
39. Wang, J. et al. Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure 9, 177-184 (2001). (Pubitemid 32209191)
40. Martin, A., Baker, T.A. & Sauer, R.T. Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat. Struct. Mol. Biol. 15, 1147-1151 (2008).
41. Martin, A., Baker, T.A. & Sauer, R.T. Diverse pore loops of the AAA+ ClpX machine mediate unassisted and adaptor-dependent recognition of ssrA-tagged substrates. Mol. Cell 29, 441-450 (2008). (Pubitemid 351282539)
42. Yamada-Inagawa, T., Okuno, T., Karata, K., Yamanaka, K. & Ogura, T. Conserved pore residues in the AAA protease FtsH are important for proteolysis and its coupling to ATP hydrolysis. J. Biol. Chem. 278, 50182-50187 (2003). (Pubitemid 37548857)
43. Aubin-Tam, M.E., Olivares, A.O., Sauer, R.T., Baker, T.A. & Lang, M.J. Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145, 257-267 (2011).
44. Maillard, R.A. et al. ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 145, 459-469 (2011).
45. Park, E. et al. Role of the GYVG pore motif of HslU ATPase in protein unfolding and translocation for degradation by HslV peptidase. J. Biol. Chem. 280, 22892-22898 (2005). (Pubitemid 40853197)
46. Hinnerwisch, J., Fenton, W.A., Furtak, K.J., Farr, G.W. & Horwich, A.L. Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121, 1029-1041 (2005). (Pubitemid 40894633)
47. Glynn, S.E., Martin, A., Nager, A.R., Baker, T.A. & Sauer, R.T. Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine. Cell 139, 744-756 (2009).
48. Glynn, S.E., Nager, A.R., Baker, T.A. & Sauer, R.T. Dynamic and static components power unfolding in topologically closed rings of a AAA+ proteolytic machine. Nat. Struct. Mol. Biol. 19, 616-622 (2012).
49. Martin, A., Baker, T.A. & Sauer, R.T. Distinct static and dynamic interactions control ATPase-peptidase communication in a AAA+ protease. Mol. Cell 27, 41-52 (2007). (Pubitemid 46991379)
50. Barthelme, D. & Sauer, R.T. Bipartite determinants mediate an evolutionarily conserved interaction between Cdc48 and the 20S peptidase. Proc. Natl. Acad. Sci. USA 110, 3327-3332 (2013).
51. Tian, G. et al. An asymmetric interface between the regulatory and core particles of the proteasome. Nat. Struct. Mol. Biol. 18, 1259-1267 (2011).
52. Smith, D.M., Fraga, H., Reis, C., Kafri, G. & Goldberg, A.L. ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144, 526-538 (2011).
53. Li, X. & Demartino, G.N. Variably modulated gating of the 26S proteasome by ATP and polyubiquitin. Biochem. J. 421, 397-404 (2009).
54. Seong, I.S. et al. The C-terminal tails of HslU ATPase act as a molecular switch for activation of HslV peptidase. J. Biol. Chem. 277, 25976-25982 (2002). (Pubitemid 34967079)
55. Kim, D.Y. & Kim, K.K. Crystal structure of ClpX molecular chaperone from Helicobacter pylori. J. Biol. Chem. 278, 50664-50670 (2003). (Pubitemid 37548915)
56. 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). (Pubitemid 35417677)
57. Singleton, M.R., Sawaya, M.R., Ellenberger, T. & Wigley, D.B. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101, 589-600 (2000).
58. Thomsen, N.D. & Berger, J.M. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 139, 523-534 (2009).
59. Enemark, E.J. & Joshua-Tor, L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442, 270-275 (2006). (Pubitemid 44114897)
60. Costa, A. et al. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat. Struct. Mol. Biol. 18, 471-477 (2011).
61. Leggett, D.S., Glickman, M.H. & Finley, D. Purifcation of proteasomes, proteasome subcomplexes, and proteasome-associated proteins from budding yeast. Methods Mol. Biol. 301, 57-70 (2005).
62. Saeki, Y., Isono, E. & Toh-E, A. Preparation of ubiquitinated substrates by the PY motif-insertion method for monitoring 26S proteasome activity. Methods Enzymol. 399, 215-227 (2005). (Pubitemid 41772731)
63. Verma, R. et al. Proteasomal proteomics: identifcation of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affnity-purifed proteasomes. Mol. Biol. Cell 11, 3425-3439 (2000).
64. 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). (Pubitemid 28240488)