Structural basis for specific recognition of Rpt1p, an ATPase subunit of 26 S proteasome, by proteasome-dedicated chaperone Hsm3p

Journal of Biological Chemistry

Volumn 287, Issue 15, 2012, Pages 12172-12182

  Takagi, Kenji ^a,b   Kim, Sangwoo ^b   Yukii, Haruka ^c   Ueno, Mika ^c   Morishita, Ryo ^d   Endo, Yaeta ^d   Kato, Koichi ^b,e   Tanaka, Keiji ^c   Saeki, Yasushi ^c   Mizushima, Tsunehiro ^a  

^a UNIVERSITY OF HYOGO   (Japan)

^b NAGOYA CITY UNIVERSITY   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^d EHIME UNIVERSITY   (Japan)

^e INSTITUTE FOR MOLECULAR SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

26 S PROTEASOME; C-SHAPED; C-TERMINAL DOMAINS; CHARGED SURFACES; CORE PARTICLES; EUKARYOTIC CELLS; HYDROPHOBIC CORE; IN-VITRO; MOLECULAR FUNCTION; MOLECULAR MACHINES; PROTEASOMES; REGULATORY PARTICLE; SPECIFIC RECOGNITION; STRUCTURAL BASIS; STRUCTURAL MODELS; TETRAMERIC COMPLEX; UBIQUITINATED PROTEINS;

MODEL STRUCTURES;

SURFACE DEFECTS;

26 S PROTEASOME; ADENOSINE TRIPHOSPHATASE; CHAPERONE; PROTEASOME; PROTEIN HSM3P; PROTEIN RPT1C; PROTEIN RPT1P; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; HYDROPHOBICITY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SUBSTITUTION; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SURFACE PROPERTIES;

EUKARYOTA;

EID: 84859487212     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.345876     Document Type: Article

References (43)

1. Baumeister, W., Walz, J., Zühl, F., and Seemüller, E. (1998) The proteasome. Paradigm of a self-compartmentalizing protease. Cell 92, 367-380
2. Coux, O., Tanaka, K., and Goldberg, A. L. (1996) Structure and functions of the 20 S and 26 S proteasomes. Annu. Rev. Biochem. 65, 801-847
3. Finley, D. (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477-513
4. 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)
5. Leggett, D. S., Glickman, M. H., and Finley, D. (2005) Purification of proteasomes, proteasome subcomplexes, and proteasome-associated proteins from budding yeast. Methods Mol. Biol. 301, 57-70
6. Bedford, L., Paine, S., Sheppard, P. W., Mayer, R. J., and Roelofs, J. (2010) Assembly, structure, and function of the 26 S proteasome. Trends Cell Biol. 20, 391-401
7. Murata, S., Yashiroda, H., and Tanaka, K. (2009) Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 10, 104-115
8. Tomko, R. J., Jr., and Hochstrasser, M. (2011) Order of the proteasomal ATPases and eukaryotic proteasome assembly. Cell. Biochem. Biophys. 60, 13-20
9. Hirano, Y., Kaneko, T., Okamoto, K., Bai, M., Yashiroda, H., Furuyama, K., Kato, K., Tanaka, K., and Murata, S. (2008) Dissecting β-ring assembly pathway of the mammalian 20 S proteasome. EMBO J. 27, 2204-2213
10. Ramos, P. C., Höckendorff, J., Johnson, E. S., Varshavsky, A., and Dohmen, R. J. (1998) Ump1p is required for proper maturation of the 20 S proteasome and becomes its substrate upon completion of the assembly. Cell 92, 489-499 (Pubitemid 28101112)
11. Hirano, Y., Hendil, K. B., Yashiroda, H., Iemura, S., Nagane, R., Hioki, Y., Natsume, T., Tanaka, K., and Murata, S. (2005) A heterodimeric complex that promotes the assembly of mammalian 20 S proteasomes. Nature 437, 1381-1385 (Pubitemid 41568686)
12. Le Tallec, B., Barrault, M. B., Courbeyrette, R., Guérois, R., Marsolier-Kergoat, M. C., and Peyroche, A. (2007) 20 S proteasome assembly is orchestrated by two distinct pairs of chaperones in yeast and in mammals. Mol. Cell 27, 660-674 (Pubitemid 47243701)
13. Hirano, Y., Hayashi, H., Iemura, S., Hendil, K. B., Niwa, S., Kishimoto, T., Kasahara, M., Natsume, T., Tanaka, K., and Murata, S. (2006) Cooperation of multiple chaperones required for the assembly of mammalian 20 S proteasomes. Mol. Cell 24, 977-984 (Pubitemid 44960093)
14. Kusmierczyk, A. R., Kunjappu, M. J., Funakoshi, M., and Hochstrasser, M. (2008) A multimeric assembly factor controls the formation of alternative 20 S proteasomes. Nat. Struct. Mol. Biol. 15, 237-244 (Pubitemid 351654044)
15. Yashiroda, H., Mizushima, T., Okamoto, K., Kameyama, T., Hayashi, H., Kishimoto, T., Niwa, S., Kasahara, M., Kurimoto, E., Sakata, E., Takagi, K., Suzuki, A., Hirano, Y., Murata, S., Kato, K., Yamane, T., and Tanaka, K. (2008) Crystal structure of a chaperone complex that contributes to the assembly of yeast 20 S proteasomes. Nat. Struct. Mol. Biol. 15, 228 -236
16. Funakoshi, M., Tomko, R. J., Jr., Kobayashi, H., and Hochstrasser, M. (2009) Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 137, 887-899
17. Le Tallec, B., Barrault, M. B., Guérois, R., Carré, T., and Peyroche, A. (2009) Hsm3/S5b participates in the assembly pathway of the 19 S regulatory particle of the proteasome. Mol. Cell 33, 389-399
18. Roelofs, J., Park, S., Haas, W., Tian, G., McAllister, F. E., Huo, Y., Lee, B. H., Zhang, F., Shi, Y., Gygi, S. P., and Finley, D. (2009) Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459, 861-865
19. Saeki, Y., Toh-e, A., Kudo, T., Kawamura, H., and Tanaka, K. (2009) Multiple proteasome-interacting proteins assist the assembly of the yeast 19 S regulatory particle. Cell 137, 900-913
20. Kim, S., Saeki, Y., Fukunaga, K., Suzuki, A., Takagi, K., Yamane, T., Tanaka, K., Mizushima, T., and Kato, K. (2010) Crystal structure of yeast rpn14, a chaperone of the 19 S regulatory particle of the proteasome. J. Biol. Chem. 285, 15159-15166
21. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
22. Schneider, T. R., and Sheldrick, G. M. (2002) Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (Pubitemid 35169744)
23. Otwinowski, Z. (1991) Proceedings of the CCP4 Study Weekend (Wolf, W. Evans, P. R., and Leslie, A. G. W., eds) pp. 80-86, Warrington, Daresbury Laboratory
24. Cowtan, K. (1999) Error estimation and bias correction in phase-improvement calculations. Acta Crystallogr. D Biol. Crystallogr. 55, 1555-1567
25. Morris, R. J., Perrakis, A., and Lamzin, V. S. (2003) ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol. 374, 229-244 (Pubitemid 37531812)
26. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
27. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
28. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (Pubitemid 127485985)
29. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733
30. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system. A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
31. DeLano, W. (2002) PyMOL, De Lano Scientific, San Carlos, CA
32. McNicholas, S., Potterton, E., Wilson, K. S., and Noble, M. E. (2011) Presenting your structures. The CCP4mg molecular graphics software. Acta Crystallogr. D Biol. Crystallogr. 67, 386-394
33. Goshima, N., Kawamura, Y., Fukumoto, A., Miura, A., Honma, R., Satoh, R., Wakamatsu, A., Yamamoto, J., Kimura, K., Nishikawa, T., Andoh, T., Iida, Y., Ishikawa, K., Ito, E., Kagawa, N., Kaminaga, C., Kanehori, K., Kawakami, B., Kenmochi, K., Kimura, R., Kobayashi, M., Kuroita, T., Kuwayama, H., Maruyama, Y., Matsuo, K., Minami, K., Mitsubori, M., Mori, M., Morishita, R., Murase, A., Nishikawa, A., Nishikawa, S., Okamoto, T., Sakagami, N., Sakamoto, Y., Sasaki, Y., Seki, T., Sono, S., Sugiyama, A., Sumiya, T., Takayama, T., Takayama, Y., Takeda, H., Togashi, T., Yahata, K., Yamada, H., Yanagisawa, Y., Endo, Y., Imamoto, F., Kisu, Y., Tanaka, S., Isogai, T., Imai, J., Watanabe, S., and Nomura, N. (2008) Human protein factory for converting the transcriptome into an in vitro-expressed proteome, Nat. Methods 5, 1011-1017
34. Takai, K., Sawasaki, T., and Endo, Y. (2010) Practical cell-free protein synthesis system using purified wheat embryos. Nat. Protoc. 5, 227-238
35. Sherman, F. (1991) Getting started with yeast. Methods Enzymol. 194, 3-21
36. Sikorski, R. S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27
37. Sasaki, T., Toh-e, A., and Kikuchi, Y. (2000) Yeast Krr1p physically and functionally interacts with a novel essential Kri1p, and both proteins are required for 40 S ribosome biogenesis in the nucleolus. Mol. Cell Biol. 20, 7971-7979
38. Tanaka, K., Yoshimura, T., Kumatori, A., Ichihara, A., Ikai, A., Nishigai, M., Kameyama, K., and Takagi, T. (1988) Proteasomes (multiprotease complexes) as 20 S ring-shaped particles in a variety of eukaryotic cells. J. Biol. Chem. 263, 16209-16217 (Pubitemid 18262038)
39. Holm, L., and Park, J. (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16, 566-567
40. Nakamura, Y., Umehara, T., Tanaka, A., Horikoshi, M., Padmanabhan, B., and Yokoyama, S. (2007) Structural basis for the recognition between the regulatory particles Nas6 and Rpt3 of the yeast 26 S proteasome. Biochem. Biophys. Res. Commun. 359, 503-509 (Pubitemid 46898980)
41. Gorbea, C., Taillandier, D., and Rechsteiner, M. (2000) Mapping subunit contacts in the regulatory complex of the 26 S proteasome. S2 and S5b form a tetramer with ATPase subunits S4 and S7. J. Biol. Chem. 275, 875- 882
42. Sakata, E., Stengel, F., Fukunaga, K., Zhou, M., Saeki, Y., Förster, F., Baumeister, W., Tanaka, K., and Robinson, C. V. (2011) The catalytic activity of Ubp6 enhances maturation of the proteasomal regulatory particle. Mol. Cell 42, 637-649
43. 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