N-terminal coiled-coil structure of ATPase subunits of 26S proteasome is crucial for proteasome function

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Inobe, Tomonao ^a   Genmei, Reiko ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

26S PROTEASOME; ADENOSINE TRIPHOSPHATASE; PROTEASOME; PROTEIN RPT1; PROTEIN RPT2; PROTEIN RPT3; PROTEIN RPT4; PROTEIN RPT5; PROTEIN RPT6; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME CONFORMATION; HETEROLOGOUS EXPRESSION; MUTATIONAL ANALYSIS; NONHUMAN; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; CYTOPLASM; DNA MUTATIONAL ANALYSIS; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATASES; CYTOPLASM; DNA MUTATIONAL ANALYSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE;

EID: 84941730004     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134056     Document Type: Article

References (41)

1. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annual review of biochemistry. 2009; 78(1):477-513. doi: 10.1146/annurev.biochem.78.081507.101607 PMID: 19489727; PubMed Central PMCID: PMCPMC3431160.
2. Inobe T, Matouschek A. Paradigms of protein degradation by the proteasome. Curr Opin Struct Biol. 2014; 24C:156-64. doi: 10.1016/j.sbi.2014.02.002 PMID: 24632559.
3. Tomko RJ Jr, Hochstrasser M. Molecular Architecture and Assembly of the Eukaryotic Proteasome. Annual review of biochemistry. 2013; 82(1):415-45. doi: 10.1146/annurev-biochem-060410-150257
4. Sauer RT, Baker TA. AAA+ proteases: ATP-fueled machines of protein destruction. Annual review of biochemistry. 2011; 80:587-612. doi: 10.1146/annurev-biochem-060408-172623 PMID: 21469952.
5. Hinnerwisch J, Fenton W, Furtak K, Farr G, Horwich A. Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell. 2005; 121(7):1029-1041. PMID: 15989953.
6. Farrell C, Baker T, Sauer R. Altered specificity of a AAA+ protease. Molecular cell. 2007; 25(1):161-166. PMID: 17218279.
7. Kim Y-C, Li X, Thompson D, DeMartino GN. ATP binding by proteasomal ATPases regulates cellular assembly and substrate-induced functions of the 26 S proteasome. The Journal of biological chemistry. 2013; 288(5):3334-345. doi: 10.1074/jbc.M112.424788 PMID: 23212908; PubMed Central PMCID: PMCPMC3561553.
8. Rubin DM, Glickman MH, Larsen CN, Dhruvakumar S, Finley D. Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. The EMBO journal. 1998; 17 (17):4909-4919. doi: 10.1093/emboj/17.17.4909 PMID: 9724628; PubMed Central PMCID: PMC1170820.
9. Erales J, Hoyt MA, Troll F, Coffino P. Functional asymmetries of the proteasome translocase pore. The Journal of biological chemistry. 2012. doi: 10.1074/jbc.M112.357327 PMID: 22493437.
10. Kohler A, Cascio P, Leggett D, Woo K, Goldberg A, Finley D. The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. Molecular cell. 2001; 7(6):1143-1152. PMID: 11430818.
11. Thompson D, Hakala K, DeMartino GN. 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. The Journal of biological chemistry. 2009; 284(37):24891-24903. doi: 10.1074/jbc.M109. 023218 PMID: 19589775.
12. Beckwith R, Estrin E, Worden EJ, Martin A. Reconstitution of the 26S proteasome reveals functional asymmetries in its AAA+ unfoldase. Nature structural & molecular biology. 2013; 20(10):1164-1172. doi: 10.1038/nsmb.2659 PMID: 24013205.
13. Lander GC, Estrin E, Matyskiela ME, Bashore C, Nogales E, Martin A. Complete subunit architecture of the proteasome regulatory particle. Nature. 2012; 482(7384):186-191. doi: 10.1038/nature10774 PMID: 22237024; PubMed Central PMCID: PMCPMC3285539.
14. Lasker K, Förster F, Bohn S, Walzthoeni T, Villa E, Unverdorben P, et al. Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(5):1380-1387. doi: 10.1073/pnas. 1120559109 PMID: 22307589; PubMed Central PMCID: PMCPMC3277140.
15. Beck F, Unverdorben P, Bohn S, Schweitzer A, Pfeifer G, Sakata E, et al. Near-atomic resolution structural model of the yeast 26S proteasome. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(37):14870-14875. doi: 10.1073/pnas.1213333109 PMID: 22927375; PubMed Central PMCID: PMCPMC3443124.
16. Matyskiela ME, Lander GC, Martin A. Conformational switching of the 26S proteasome enables substrate degradation. Nature structural & molecular biology. 2013;: 20(7):781-788. doi: 10.1038/nsmb. 2616 PMID: 23770819; PubMed Central PMCID: PMCPMC3712289.
17. ͆ledź P, Unverdorben P, Beck F, Pfeifer G, Schweitzer A, Förster F, et al. Structure of the 26S proteasome with ATP-γS bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(18):7264-7269. doi: 10.1073/pnas.1305782110 PMID: 23589842; PubMed Central PMCID: PMCPMC3645540.
18. Hughes TR, Marton MJ, Jones AR, Roberts CJ, Stoughton R, Armour CD, et al. Functional discovery via a compendium of expression profiles. Cell. 2000; 102(1):109-126. PMID: 10929718.
19. Mnaimneh S, Davierwala AP, Haynes J, Moffat J, Peng WT, Zhang W, et al. Exploration of essential gene functions via titratable promoter alleles. Cell. 2004; 118(1):31-44. doi: 10.1016/j.cell.2004.06.013 PMID: 15242642.
20. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, et al. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes & development. 2005; 19(23):2816-2826. doi: 10.1101/gad.1362105 PMID: 16322557; PubMed Central PMCID: PMC1315389.
21. Sopko R, Huang D, Preston N, Chua G, Papp B, Kafadar K, et al. Mapping pathways and phenotypes by systematic gene overexpression. Molecular cell. 2006; 21(3):319-330. doi: 10.1016/j.molcel.2005. 12.011 PMID: 16455487.
22. Moriya H, Shimizu-Yoshida Y, Kitano H. In vivo robustness analysis of cell division cycle genes in Saccharomyces cerevisiae. PLoS genetics. 2006; 2(7):e111. doi: 10.1371/journal.pgen.0020111 PMID: 16839182; PubMed Central PMCID: PMCPMC1500812.
23. Smith D, Chang S, Park S, Finley D, Cheng Y, Goldberg A. Docking of the Proteasomal ATPases Carboxyl Termini in the 20S Proteasomes alpha Ring Opens the Gate for Substrate Entry. Molecular cell. 2007; 27(5):731-744. PMID: 17803938.
24. Rabl J, Smith DM, Yu Y, Chang S-C, Goldberg AL, Cheng Y. Molecular Cell-Mechanism of Gate Opening in the 20S Proteasome by the Proteasomal ATPases. Molecular cell. 2008; 30(3):360-368. doi: 10.1016/j.molcel.2008.03.004
25. Kim YC, DeMartino GN. C termini of proteasomal ATPases play nonequivalent roles in cellular assembly of mammalian 26 S proteasome. The Journal of biological chemistry. 2011; 286(30):26652-26666. doi: 10.1074/jbc.M111.246793 PMID: 21628461; PubMed Central PMCID: PMC3143629.
26. Gillette TG, Kumar B, Thompson D, Slaughter CA, DeMartino GN. Differential roles of the COOH termini of AAA subunits of PA700 (19 S regulator) in asymmetric assembly and activation of the 26 S proteasome. The Journal of biological chemistry. 2008; 283(46):31813-31822. doi: 10.1074/jbc. M805935200 PMID: 18796432; PubMed Central PMCID: PMC2581596.
27. Lupas AN, Gruber M. The structure of alpha-helical coiled coils. Adv Protein Chem. 2005; 70:37-78. doi: 10.1016/S0065-3233(05)70003-6 PMID: 15837513.
28. Tomko RJ Jr, Hochstrasser M. Molecular architecture and assembly of the eukaryotic proteasome. Annual review of biochemistry. 2013; 82:415-445. doi: 10.1146/annurev-biochem-060410-150257 PMID: 23495936; PubMed Central PMCID: PMC3827779.
29. Tomko RJ Jr, Hochstrasser M. Order of the proteasomal ATPases and eukaryotic proteasome assembly. Cell Biochem Biophys. 2011; 60(1-2):13-20. doi: 10.1007/s12013-011-9178-4 PMID: 21461838; PubMed Central PMCID: PMC3256250.
30. Kimura Y, Kurata Y, Ishikawa A, Okayama A, Kamita M, Hirano H. N-Terminal methylation of proteasome subunit Rpt1 in yeast. Proteomics. 2013; 13(21):3167-3174. doi: 10.1002/pmic.201300207 PMID: 24038880.
31. Benaroudj N, Zwickl P, Seemuller E, Baumeister W, Goldberg AL. ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. Molecular cell. 2003; 11 (1):69-78. PMID: 12535522.
32. Singh Gautam AK, Balakrishnan S, Venkatraman P. Direct ubiquitin independent recognition and degradation of a folded protein by the eukaryotic proteasomes-origin of intrinsic degradation signals. PloS one. 2012; 7(4):e34864. doi: 10.1371/journal.pone.0034864 PMID: 22506054; PubMed Central PMCID: PMC3323579.
33. Kim YC, Li X, Thompson D, DeMartino GN. ATP binding by proteasomal ATPases regulates cellular assembly and substrate-induced functions of the 26 S proteasome. The Journal of biological chemistry. 2013; 288(5):3334-3345. doi: 10.1074/jbc.M112.424788 PMID: 23212908; PubMed Central PMCID: PMC3561553.
34. Fu H, Doelling JH, Rubin DM, Vierstra RD. Structural and functional analysis of the six regulatory particle triple-A ATPase subunits from the Arabidopsis 26S proteasome. The Plant journal: for cell and molecular biology. 1999; 18(5):529-539. PMID: 10417703.
35. Li Z, Zou CB, Yao Y, Hoyt MA, McDonough S, Mackey ZB, et al. An easily dissociated 26 S proteasome catalyzes an essential ubiquitin-mediated protein degradation pathway in Trypanosoma brucei. The Journal of biological chemistry. 2002; 277(18):15486-15498. doi: 10.1074/jbc.M109029200 PMID: 11854272.
36. Park S, Kim W, Tian G, Gygi SP, Finley D. Structural defects in the regulatory particle-core particle interface of the proteasome induce a novel proteasome stress response. The Journal of biological chemistry. 2011; 286(42):36652-36666. doi: 10.1074/jbc.M111.285924 PMID: 21878652; PubMed Central PMCID: PMC3196138.
37. Zhang Y, Werling U, Edelmann W. SLiCE: a novel bacterial cell extract-based DNA cloning method. Nucleic acids research. 2012; 40(8):e55-e. doi: 10.1093/nar/gkr1288 PMID: 22241772
38. Benatuil L, Perez JM, Belk J, Hsieh CM. An improved yeast transformation method for the generation of very large human antibody libraries. Protein engineering, design & selection: PEDS. 2010; 23(4):155-159. doi: 10.1093/protein/gzq002 PMID: 20130105.
39. Cox JS, Chapman RE, Walter P. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol Biol Cell. 1997; 8(9):1805-1814. PMID: 9307975; PubMed Central PMCID: PMC305738.
40. Lupas A, Van Dyke M, Stock J. Predicting coiled coils from protein sequences. Science. 1991; 252 (5009):1162-1164. doi: 10.1126/science.252.5009.1162 PMID: 2031185.
41. McDonnell AV, Jiang T, Keating AE, Berger B. Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics. 2006; 22(3):356-358. doi: 10.1093/bioinformatics/bti797 PMID: 16317077.