ATP binding to neighbouring subunits and intersubunit allosteric coupling underlie proteasomal ATPase function

Nature Communications

Volumn 6, Issue , 2015, Pages

  Kim, Young Chan ^a   Snoberger, Aaron ^a   Schupp, Jane ^a   Smith, David M ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPATRY; ENZYME ACTIVITY; EUKARYOTE; HYDROLYSIS; PROTEOMICS; TOPOLOGY;

EUKARYOTA;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ATP DEPENDENT 26S PROTEASE; PAN ENZYME; PROTEASOME;

ALLOSTERISM; HUMAN; HYDROLYSIS; METABOLISM;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ALLOSTERIC REGULATION; HUMANS; HYDROLYSIS; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 84944463457     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9520     Document Type: Article

References (53)

1. Tomko, R. J. & Hochstrasser, M. Molecular architecture and assembly of the eukaryotic proteasome. Annu. Rev. Biochem. 82, 415-445 (2013).
2. Finley, D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477-513 (2009).
3. Bhattacharyya, S., Yu, FL, Mini, C. & Matouschek, A. Regulated protein turnover: snapshots of the proteasome in action. Nat. Rev. Mol. Cell Biol. 15, 122-133 (2014).
4. Bar-Nun, S. & Glickman, M. H. Proteasomal AAA-ATPases: Structure and function. Biochim. Biophys. Acta 1823, 67-82 (2012).
5. Sledz, P. et al. Structure of the 26S proteasome with ATP-gammaS bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc. Natl Acad. Sei. USA 110, 7264-7269 (2013).
6. Unverdorben, P. et al. Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome. Proc. Natl Acad. Sei. USA 111, 5544-5549 (2014).
7. 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).
8. 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).
9. Peth, A., Uchiki, T. & Goldberg, A. L. ATP-dependent steps in the binding of ubiquitin conjugates to the 26S proteasome that commit to degradation. Mol. Cell 40, 671-681 (2010).
10. 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).
11. 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).
12. Prakash, S., Tian, L., Ratliff, K. S., Lehotzky, R. E. & Matouschek, A. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 11, 830-837 (2004).
13. Zhang, F. et al. Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol. Cell 34, 485-496 (2009).
14. Erales, J., Hoyt, M. A., Troll, F. & Coffino, P. Functional asymmetries of proteasome translocase pore. J. Biol. Chem. 287, 18535-18543 (2012).
15. 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).
16. 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).
17. Smith, D. M. et al. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol. Cell 27, 731-744 (2007).
18. Rabl, J. et al. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30, 360-368 (2008).
19. Gillette, T. G., Kumar, B., Thompson, D., Slaughter, C. A. & DeMartino, G. N. Differential roles of the COOH termini of AAA subunits of PA700 (19S regulator) in asymmetric assembly and activation of the 26S proteasome. J. Biol. Chem. 283, 31813-31822 (2008).
20. Kim, Y. C. & Demartino, G. N. C termini of proteasomal ATPases play nonequivalent roles in cellular assembly of Mammalian 26S proteasome. J. Biol. Chem. 286, 26652-26666 (2011).
21. Lander, G. C. et al. Complete subunit architecture of the proteasome regulatory particle. Nature 482, 186-191 (2012).
22. Lasker, K. et al. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl Acad. Sei. USA 109, 1380-1387 (2012).
23. Tian, G. et al. An asymmetric interface between the regulatory and core particles of the proteasome. Nat. Struct. Mol. Biol. 18, 1259-1267 (2011).
24. Rubin, D. M., Glickman, M. FL, 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).
25. 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).
26. Lyubimov, A. Y., Strycharska, M. & Berger, J. M. The nuts and bolts of ring-translocase structure and mechanism. Curr. Opin. Struct. Biol. 21, 240-248 (2011).
27. 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).
28. Stinson, B. M. et al. Nucleotide binding and conformational switching in the hexameric ring of a AAA+ machine. Cell 153, 628-639 (2013).
29. Martin, A., Baker, T. A. & Sauer, R. T. Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines. Nature 437, 1115-1120 (2005).
30. Wendler, P., Ciniawsky, S., Koek, M. & Kube, S. Structure and function of the AAA+ nucleotide binding pocket. Biochim. Biophys. Acta 1823, 2-14 (2012).
31. Hanson, P. I. & Whiteheart, S. W. AAA+ proteins: have engine, will work. Nat Rev. Mol Cell Biol 6, 519-529 (2005).
32. Erzberger, J. P. & Berger, J. M. Evolutionary relationships and structural mechanisms of AAA + proteins. Annu. Rev. Biophys. Biomol. Struct. 35, 93-114 (2006).
33. Ogura, T., Whiteheart, S. W. & Wilkinson, A. J. Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sens ing, and inter-subunit interactions in AAA and AAA + ATPases. J. Struct. Biol. 146, 106-112 (2004).
34. McCullough, J. & Sundquist, W. I. Putting a finger in the ring. Nat. Struct. Mol Biol. 21, 1025-1027 (2014).
35. 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).
36. Joshi, S. A., Hersch, G. L., Baker, T. A. & Sauer, R. T. Communication between ClpX and ClpP during substrate processing and degradation. Nat. Struct. Mol Biol. 11, 404-411 (2004).
37. Güldenhaupt, J. et al N-Ras forms dimers at POPC membranes. Biophys. J. 103, 1585-1593 (2012).
38. Zhang, F. et al Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol Cell 34, 473-484 (2009).
39. 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).
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. Beckwith, R., Estrin, E., Worden, E. J. & Martin, A. Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA + unfoldase. Nat. Struct. Mol Biol. 20, 1164-1172 (2013).
42. Peth, A., Nathan, J. A. & Goldberg, A. L. The ATP costs and time required to degrade ubiquitinated proteins by the 26S proteasome. J. Biol. Chem. 288, 29215-29222 (2013).
43. Stinson, B. M., Baytshtok, V., Schmitz, K. R., Baker, T. A. & Sauer, R. T. Subunit asymmetry and roles of conformational switching in the hexameric AAA + ring of ClpX. Nat. Struct. Mol Biol. 22, 411-416 (2015).
44. Sen, M. et al The ClpXP protease unfolds substrates using a constant rate of pulling but different gears. Cell 155, 636-646 (2013).
45. 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).
46. Zeymer, C., Fischer, S. & Reinstein, J. trans-Acting arginine residues in the AAA + chaperone ClpB aliosterically regulate the activity through inter-and intradomain communication, J. Biol. Chem. 289, 32965-32976 (2014).
47. Chen, B. et al Engagement of arginine finger to ATP triggers large conformational changes in NtrCl AAA+ ATPase for remodeling bacterial RNA polymerase. Structure 18, 1420-1430 (2010).
48. Beck, F. et al Near-atomic resolution structural model of the yeast 26S proteasome. Proc. Natl Acad. Sei. USA (2012).
49. Peskin, C. S., Odell, G. M. & Oster, G. F. Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys. J. 65, 316-324 (1993).
50. Augustin, S. et al. An intersubunit signaling network coordinates ATP hydrolysis by m-AAA proteases. Mol. Cell 35, 574-585 (2009).
51. Cordova, J. C. et al Stochastic but highly coordinated protein unfolding and translocation by the ClpXP proteolytic machine. Cell 158, 647-658 (2014).
52. Besehe, H. C., Haas, W., Gygi, S. P. & Goldberg, A. L. Isolation of mammalian 26S proteasomes and p97/VCP complexes using the ubiquitin-like domain from HHR23B reveals novel proteasome-associated proteins. Biochemistry 48, 2538-2549 (2009).
53. Lakowicz, J. Principles of Fluorescence Spectroscopy 3rd edn, Ch. 13 (Springer, 2006).