Functional asymmetries of proteasome translocase pore

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18535-18543

  Erales, Jenny ^a   Hoyt, Martin A ^a,b   Troll, Fabian ^a   Coffino, Philip ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Department of Biocatalyst Characterization and Design   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP HYDROLYSIS; ATP-ASE ACTIVITY; ATPASES; BIDIRECTIONAL COUPLING; CELL CYCLE; CYCLINS; DEGRADATION ACTIVITY; HEXAMERS; MUTANT CELLS; PROTEASOMES; PROTEIN SUBSTRATE; REGULATORY PROTEIN; S.CEREVISIAE; TRANSLOCASES; UBIQUITIN-PROTEASOME SYSTEM; WILD TYPES; YEAST STRAIN;

AMINO ACIDS; DEFECTS; DEGRADATION; HYDROLYSIS; PROTEINS;

SUBSTRATES;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE RPT; ADENOSINE TRIPHOSPHATASE RPT 1; ADENOSINE TRIPHOSPHATASE RPT 2; ADENOSINE TRIPHOSPHATASE RPT 3; ADENOSINE TRIPHOSPHATASE RPT 4; ADENOSINE TRIPHOSPHATASE RPT 5; ADENOSINE TRIPHOSPHATASE RPT 6; ADENOSINE TRIPHOSPHATE; ALANINE; ARGININE; CARRIER PROTEIN; CYCLIN G1; PROTEASOME; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL CYCLE REGULATION; CELL GROWTH; CELL STRESS; CELL VIABILITY; CLUSTER ANALYSIS; CONTROLLED STUDY; CROSS COUPLING REACTION; ENZYME ACTIVATION; ENZYME SUBSTRATE; ENZYME SUBUNIT; FUNGAL STRAIN; GENE; HYDROLYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; RESIDUE ANALYSIS; RPT3 GENE; RPT4 GENE; RPT5 GENE; SACCHAROMYCES CEREVISIAE; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; KINETICS; PROTEASOME ENDOPEPTIDASE COMPLEX; UNFOLDED PROTEIN RESPONSE;

EID: 84861553163     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.357327     Document Type: Article

References (37)

1. Glickman, M. H., Rubin, D. M., Fried, V. A., and Finley, D. (1998) The regulatory particle of the Saccharomyces cerevisiae proteasome. Mol. Cell Biol. 18, 3149-3162 (Pubitemid 28240488)
2. Groll, M., Ditzel, L., Löwe, J., Stock, D., Bochtler, M., Bartunik, H. D., and Huber, R. (1997) Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386, 463-471 (Pubitemid 27164066)
3. Glickman, M. H., Rubin, D. M., Coux, O., Wefes, I., Pfeifer, G., Cjeka, Z., Baumeister, W., Fried, V. A., and Finley, D. (1998) A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94, 615-623 (Pubitemid 28427580)
4. Tomko, R. J., Jr., Funakoshi, M., Schneider, K., Wang, J., and Hochstrasser, M. (2010) Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases. Implications for proteasome structure and assembly. Mol. Cell 38, 393-403
5. Lasker, K., Förster, F., Bohn, S., Walzthoeni, T., Villa, E., Unverdorben, P., Beck, F., Aebersold, R., Sali, A., and Baumeister, W. (2012) Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc. Natl. Acad. Sci. U.S.A. 109, 1380-1387
6. Lander, G. C., Estrin, E., Matyskiela, M. E., Bashore, C., Nogales, E., and Martin, A. (2012) Complete subunit architecture of the proteasome regulatory particle. Nature 482, 186-191
7. Sauer, R. T., and Baker, T. A. (2011) AAA+ proteases. ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 80, 587-612
8. Prakash, S., Tian, L., Ratliff, K. S., Lehotzky, R. E., and Matouschek, A. (2004) An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 11, 830-837 (Pubitemid 39128798)
9. Henderson, A., Erales, J., Hoyt, M. A., and Coffino, P. (2011) Dependence of proteasome processing rate on substrate unfolding. J. Biol. Chem. 286, 17495-17502
10. Takeuchi, J., Chen, H., and Coffino, P. (2007) Proteasome substrate degradation requires association plus extended peptide.EMBOJ. 26, 123-131 (Pubitemid 46094705)
11. Zhang, F., Hu, M., Tian, G., Zhang, P., Finley, D., Jeffrey, P. D., and Shi, Y. (2009) Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol. Cell 34, 473-484
12. Zhang, F., Wu, Z., Zhang, P., Tian, G., Finley, D., and Shi, Y. (2009) Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol. Cell 34, 485-496
13. Hinnerwisch, J., Fenton, W. A., Furtak, K. J., Farr, G. W., and Horwich, A. L. (2005) Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121, 1029-1041 (Pubitemid 40894633)
14. Martin, A., Baker, T. A., and Sauer, R. T. (2008) Pore loops of the AAA+ClpX machine grip substrates to drive translocation and unfolding. Nat. Struct. Mol. Biol. 15, 1147-1151
15. Sambrook, J., and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
16. Guthrie, C., and Fink, G. R., eds. (2002) Guide to Yeast Genetics and Molecular Biology, Academic Press, Inc., San Diego
17. Pringle, J. R., and Mor, J. R. (1975) Methods for monitoring the growth of yeast cultures and for dealing with the clumping problem. Methods Cell Biol. 11, 131-168
18. Elsasser, S., Schmidt, M., and Finley, D. (2005) Characterization of the proteasome using native gel electrophoresis. Methods Enzymol. 398, 353-363 (Pubitemid 41578897)
19. Gerlinger, U. M., Gückel, R., Hoffmann, M., Wolf, D. H., and Hilt, W. (1997) Yeast cycloheximide-resistant crl mutants are proteasome mutants defective in protein degradation. Mol. Biol. Cell 8, 2487-2499 (Pubitemid 27528216)
20. Hilt, W., Enenkel, C., Gruhler, A., Singer, T., and Wolf, D. H. (1993) The PRE4 gene codes for a subunit of the yeast proteasome necessary for peptidylglutamyl- peptide-hydrolyzing activity. J. Biol. Chem. 268, 3479-3486
21. Murakami, Y., Matsufuji, S., Kameji, T., Hayashi, S., Igarashi, K., Tamura, T., Tanaka, K., and Ichihara, A. (1992) Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination. Nature 360, 597-599 (Pubitemid 23000711)
22. Crosas, B., Hanna, J., Kirkpatrick, D. S., Zhang, D. P., Tone, Y., Hathaway, N. A., Buecker, C., Leggett, D. S., Schmidt, M., King, R. W., Gygi, S. P., and Finley, D. (2006) Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell 127, 1401-1413 (Pubitemid 44960408)
23. Kern, A. D., Oliveira, M. A., Coffino, P., and Hackert, M. L. (1999) Structure of mammalian ornithine decarboxylase at 1.6 Å resolution. Stereo-chemical implications of PLP-dependent amino acid decarboxylases. Structure 7, 567-581 (Pubitemid 29230491)
24. Hoyt, M. A., Zich, J., Takeuchi, J., Zhang, M., Govaerts, C., and Coffino, P. (2006) Glycine-alanine repeats impair proper substrate unfolding by the proteasome. EMBO J. 25, 1720-1729
25. Hoyt, M. A., Zhang, M., and Coffino, P. (2003) Ubiquitin-independent mechanisms of mouse ornithine decarboxylase degradation are conserved between mammalian and fungal cells. J. Biol. Chem. 278, 12135-12143 26.
26. van Daalen Wetters, T., Macrae, M., Brabant, M., Sittler, A., and Coffino, P. (1989) Polyamine-mediated regulation of mouse ornithine decarboxylase is posttranslational. Mol. Cell. Biol. 9, 5484-5490
27. Li, H., Carrion-Vazquez, M., Oberhauser, A. F., Marszalek, P. E., and Fernandez, J. M. (2000) Point mutations alter the mechanical stability of immunoglobulin modules. Nat. Struct. Biol. 7, 1117-1120
28. Joly, N., and Buck, M. (2010) Engineered interfaces of an AAA+ ATPase reveal a new nucleotide-dependent coordination mechanism. J. Biol. Chem. 285, 15178-15186
29. Lee, S.H., Moon, J. H., Yoon, S. K., and Yoon, J. B. (2012) Stable incorporation of ATPase subunits into 19S regulatory particle of human proteasome requires nucleotide binding and C-terminal tails. J. Biol. Chem. 287, 9269-9279
30. Rubin, D. M., Glickman, M. H., Larsen, C. N., Dhruvakumar, S., and Finley, D. (1998) Active site mutants in the six regulatory particle ATPases reveal multiple roles for ATP in the proteasome. EMBO J. 17, 4909-4919 (Pubitemid 28408458)
31. Smith, D. M., Fraga, H., Reis, C., Kafri, G., and Goldberg, A. L. (2011) ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144, 526-538
32. Tian, G., Park, S., Lee, M. J., Huck, B., McAllister, F., Hill, C. P., Gygi, S. P., and Finley, D. (2011) An asymmetric interface between the regulatory and core particles of the proteasome. Nat. Struct. Mol. Biol. 18, 1259-1267
33. Singleton, M. R., Sawaya, M. R., Ellenberger, T., and Wigley, D. B. (2000) Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101, 589-600
34. Yu, J., Moffitt, J., Hetherington, C. L., Bustamante, C., and Oster, G. (2010) Mechanochemistry of a viral DNA packaging motor. J. Mol. Biol. 400, 186-203
35. Djuranovic, S., Hartmann, M. D., Habeck, M., Ursinus, A., Zwickl, P., Martin, J., Lupas, A. N., and Zeth, K. (2009) Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol. Cell 34, 580-590
36. Jorgensen, P., Nishikawa, J. L., Breitkreutz, B. J., and Tyers, M. (2002) Systematic identification of pathways that couple cell growth and division in yeast. Science 297, 395-400 (Pubitemid 34790768)
37. Sudbery, P. E., Goodey, A. R., and Carter, B. L. (1980) Genes which control cell proliferation in the yeast Saccharomyces cerevisiae. Nature 288, 401-404