Structure of an endogenous yeast 26S proteasome reveals two major conformational states

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 10, 2016, Pages 2642-2647

  Luan, Bai ^a   Huang, Xiuliang ^a   Wu, Jianping ^a   Mei, Ziqing ^b   Wang, Yiwei ^a   Xue, Xiaobin ^a   Yan, Chuangye ^a   Wang, Jiawei ^a   J Finley, Daniel ^c   Shi, Yigong ^a   Wang, Feng ^a  

^a Tsinghua University   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cryo EM; Proteasome; Protein degradation; Structure

Indexed keywords

PROTEASOME; ATP DEPENDENT 26S PROTEASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOCHEMICAL ANALYSIS; CRYOELECTRON MICROSCOPY; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; PROTEIN DEGRADATION; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CONFORMATION; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84960934506     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1601561113     Document Type: Article

References (40)

1. Finley D, Chen X, Walters KJ (2016) Gates, channels, and switches: Elements of the proteasome machine. Trends Biochem Sci 41(1):77-93.
2. Yao T, Cohen RE (2002) A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419(6905):403-407.
3. Verma R, et al. (2002) Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298(5593):611-615.
4. Estrin E, Lopez-Blanco JR, Chacón P, Martin A (2013) Formation of an intricate helical bundle dictates the assembly of the 26S proteasome lid. Structure 21(9):1624-1635.
5. Tomko RJ, Jr, et al. (2015) A single α helix drives extensive remodeling of the proteasome lid and completion of regulatory particle assembly. Cell 163(2):432-444.
6. Zhang F, et al. (2009) Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol Cell 34(4):473-484.
7. Wang F, et al. (2011) Structure and mechanism of the hexameric MecA-ClpC molecular machine. Nature 471(7338):331-335.
8. Lander GC, et al. (2012) Complete subunit architecture of the proteasome regulatory particle. Nature 482(7384):186-191.
9. Löwe J, et al. (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268(5210):533-539.
10. Groll M, et al. (1997) Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386(6624):463-471.
11. Unno M, et al. (2002) The structure of the mammalian 20S proteasome at 2.75 Å resolution. Structure 10(5):609-618.
12. Lasker K, et al. (2012) Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci USA 109(5):1380-1387.
13. Beck F, et al. (2012) Near-atomic resolution structural model of the yeast 26S proteasome. Proc Natl Acad Sci USA 109(37):14870-14875.
14. da Fonseca PC, He J, Morris EP (2012) Molecular model of the human 26S proteasome. Mol Cell 46(1):54-66.
15. Matyskiela ME, Lander GC, Martin A (2013) Conformational switching of the 26S proteasome enables substrate degradation. Nat Struct Mol Biol 20(7):781-788.
16. Sledz P, et al. (2013) 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(18):7264-7269.
17. Unverdorben P, et al. (2014) Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome. Proc Natl Acad Sci USA 111(15): 5544-5549.
18. Aufderheide A, et al. (2015) Structural characterization of the interaction of Ubp6 with the 26S proteasome. Proc Natl Acad Sci USA 112(28):8626-8631.
19. Bohn S, et al. (2013) Localization of the regulatory particle subunit Sem1 in the 26S proteasome. Biochem Biophys Res Commun 435(2):250-254.
20. Leggett DS, Glickman MH, Finley D (2005) Purification of proteasomes, proteasome subcomplexes, and proteasome-associated proteins from budding yeast. Methods Mol Biol 301:57-70.
21. Tomko RJ, Jr, Hochstrasser M (2014) The intrinsically disordered Sem1 protein functions as a molecular tether during proteasome lid biogenesis. Mol Cell 53(3):433-443.
22. Pathare GR, et al. (2014) Crystal structure of the proteasomal deubiquitylation module Rpn8-Rpn11. Proc Natl Acad Sci USA 111(8):2984-2989.
23. Worden EJ, Padovani C, Martin A (2014) Structure of the Rpn11-Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation. Nat Struct Mol Biol 21(3):220-227.
24. Sharon M, Taverner T, Ambroggio XI, Deshaies RJ, Robinson CV (2006) Structural organization of the 19S proteasome lid: Insights from MS of intact complexes. PLoS Biol 4(8):e267.
25. Isono E, et al. (2007) The assembly pathway of the 19S regulatory particle of the yeast 26S proteasome. Mol Biol Cell 18(2):569-580.
26. Fukunaga K, Kudo T, Toh-e A, Tanaka K, Saeki Y (2010) Dissection of the assembly pathway of the proteasome lid in Saccharomyces cerevisiae. Biochem Biophys Res Commun 396(4):1048-1053.
27. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19(1):94-102.
28. Sakata E, et al. (2012) Localization of the proteasomal ubiquitin receptors Rpn10 and Rpn13 by electron cryomicroscopy. Proc Natl Acad Sci USA 109(5):1479-1484.
29. Dambacher CM, Worden EJ, Herzik MA, Jr, Martin A, Lander GC (2016) Atomic structure of the 26S proteasome lid reveals the mechanism of deubiquitinase inhibition. eLife 5:e13027.
30. Kleijnen MF, et al. (2007) Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites. Nat Struct Mol Biol 14(12): 1180-1188.
31. Scheres SH (2012) RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180(3):519-530.
32. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
33. Pettersen EF, et al. (2004) UCSF Chimera - A visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.
34. Adams PD, et al. (2002) PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58(Pt 11): 1948-1954.
35. DeLano WL (2002) The PyMOL Molecular Graphics System. Available at www. pymol.org.
36. Dong KC, et al. (2011) Preparation of distinct ubiquitin chain reagents of high purity and yield. Structure 19(8):1053-1063.
37. Li X, et al. (2013) Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 10(6):584-590.
38. Mindell JA, Grigorieff N (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142(3):334-347.
39. Chen S, et al. (2013) High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy 135:24-35.
40. Kucukelbir A, Sigworth FJ, Tagare HD (2014) Quantifying the local resolution of cryo-EM density maps. Nat Methods 11(1):63-65.