A unified mechanism for proteolysis and autocatalytic activation in the 20S proteasome

Nature Communications

Volumn 7, Issue , 2016, Pages

  Huber, Eva M ^a   Heinemeyer, Wolfgang ^a   Li, Xia ^b,d   Arendt, Cassandra S ^c,e   Hochstrasser, Mark ^b   Groll, Michael ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

20S PROTEASOME; ASPARTIC ACID; CYSTEINE; HYDROXYL GROUP; LYSINE; PROTEASOME; SERINE; THREONINE; UNCLASSIFIED DRUG; PROTEIN PRECURSOR; SACCHAROMYCES CEREVISIAE PROTEIN;

BIOASSAY; CATALYSIS; CELLS AND CELL COMPONENTS; CRYSTALLOGRAPHY; ENZYME ACTIVITY; HYDROXYL RADICAL; PROTEOMICS;

AMINO ACID SUBSTITUTION; ARTICLE; BETA SHEET; BIOCHEMICAL ANALYSIS; CATALYSIS; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME INACTIVATION; ENZYME MECHANISM; ENZYME STRUCTURE; IN VITRO STUDY; MUTAGENESIS; MUTATION; NUCLEOPHILICITY; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTON TRANSPORT; TEMPERATURE SENSITIVITY; WILD TYPE; X RAY CRYSTALLOGRAPHY; AUTOLYSIS; GENETICS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS;

ASPARTIC ACID; AUTOLYSIS; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; LYSINE; MUTAGENESIS, SITE-DIRECTED; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PRECURSORS; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SERINE; THREONINE;

EID: 84960840621     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10900     Document Type: Article

References (41)

1. Chen, P. & Hochstrasser, M. Autocatalytic subunit processing couples active site formation in the 20S proteasome to completion of assembly. Cell 86, 961-972 (1996).
2. Groll, M. et al. Structure of 20S proteasome from yeast at 2.4 Å resolution. Nature 386, 463-471 (1997).
3. Krüger, E., Kloetzel, P. M. & Enenkel, C. 20S proteasome biogenesis. Biochimie 83, 289-293 (2001).
4. Groll, M. et al. The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc. Natl Acad. Sci. USA 96, 10976-10983 (1999).
5. Ditzel, L. et al. Conformational constraints for protein self-cleavage in the proteasome. J. Mol. Biol. 279, 1187-1191 (1998).
6. Huber, E. M. et al. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell 148, 727-738 (2012).
7. Huber, E. M. et al. Systematic analyses of substrate preferences of 20S proteasomes using peptidic epoxyketone inhibitors. J. Am. Chem. Soc. 137, 7835-7842 (2015).
8. Marques, A. J., Palanimurugan, R., Matias, A. C., Ramos, P. C. & Dohmen, R. J. Catalytic mechanism and assembly of the proteasome. Chem. Rev. 109, 1509-1536 (2009).
9. Löwe, J. et al. Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268, 533-539 (1995).
10. Brannigan, J. A. et al. A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature 378, 416-419 (1995).
11. Seemüller, E. et al. Proteasome from Thermoplasma acidophilum: a threonine protease. Science 268, 579-582 (1995).
12. Dick, T. P. et al. Contribution of proteasomal beta-subunits to the cleavage of peptide substrates analyzed with yeast mutants. J. Biol. Chem. 273, 25637-25646 (1998).
13. Heinemeyer, W., Fischer, M., Krimmer, T., Stachon, U. & Wolf, D. H. The active sites of the eukaryotic 20S proteasome and their involvement in subunit precursor processing. J. Biol. Chem. 272, 25200-25209 (1997).
14. Arendt, C. S. & Hochstrasser, M. Identification of the yeast 20S proteasome catalytic centers and subunit interactions required for active-site formation. Proc. Natl Acad. Sci. USA 94, 7156-7161 (1997).
15. Jäger, S., Groll, M., Huber, R., Wolf, D. H. & Heinemeyer, W. Proteasome betatype subunits: unequal roles of propeptides in core particle maturation and a hierarchy of active site function. J. Mol. Biol. 291, 997-1013 (1999).
16. Arendt, C. S. & Hochstrasser, M. Eukaryotic 20S proteasome catalytic subunit propeptides prevent active site inactivation by N-terminal acetylation and promote particle assembly. EMBO J. 18, 3575-3585 (1999).
17. Polgar, L. The catalytic triad of serine peptidases. Cell. Mol. Life Sci. 62, 2161-2172 (2005).
18. Li, X., Li, Y., Arendt, C. S. & Hochstrasser, M. Distinct elements in the proteasomal beta5 subunit propeptide required for autocatalytic processing and proteasome assembly. J. Biol. Chem. 291, 1991-2003 (2015).
19. Schmidtke, G. et al. Analysis of mammalian 20S proteasome biogenesis: the maturation of beta-subunits is an ordered two-step mechanism involving autocatalysis. EMBO J. 15, 6887-6898 (1996).
20. Wlodawer, A. Proteasome: a complex protease with a new fold and a distinct mechanism. Structure 3, 417-420 (1995).
21. Seemüller, E., Lupas, A. & Baumeister, W. Autocatalytic processing of the 20S proteasome. Nature 382, 468-471 (1996).
22. Groll, M., Berkers, C. R., Ploegh, H. L. & Ovaa, H. Crystal structure of the boronic acid-based proteasome inhibitor bortezomib in complex with the yeast 20S proteasome. Structure 14, 451-456 (2006).
23. Huber, E. M., Heinemeyer, W. & Groll, M. Bortezomib-resistant mutant proteasomes: structural and biochemical evaluation with carfilzomib and ONX 0914. Structure 23, 407-417 (2015).
24. Bochtler, M., Ditzel, L., Groll, M. & Huber, R. Crystal structure of heat shock locus V (HslV) from Escherichia coli. Proc. Natl Acad. Sci. USA 94, 6070-6074 (1997).
25. Zwickl, P., Kleinz, J. & Baumeister, W. Critical elements in proteasome assembly. Nat. Struct. Biol. 1, 765-770 (1994).
26. Groll, M., Brandstetter, H., Bartunik, H., Bourenkow, G. & Huber, R. Investigations on the maturation and regulation of archaebacterial proteasomes. J. Mol. Biol. 327, 75-83 (2003).
27. Lubkowski, J., Dauter, M., Aghaiypour, K., Wlodawer, A. & Dauter, Z. Atomic resolution structure of Erwinia chrysanthemi L-asparaginase. Acta Crystallogr. D Biol. Crystallogr. 59, 84-92 (2003).
28. Gutteridge, A. & Thornton, J. M. Understanding nature's catalytic toolkit. Trends Biochem. Sci. 30, 622-629 (2005).
29. Hines, J., Groll, M., Fahnestock, M. & Crews, C. M. Proteasome inhibition by fellutamide B induces nerve growth factor synthesis. Chem. Biol. 15, 501-512 (2008).
30. Stein, M. L. et al. Systematic comparison of peptidic proteasome inhibitors highlights the alpha-ketoamide electrophile as an auspicious reversible lead motif. Angew. Chem. Int. Ed. 53, 1679-1683 (2014).
31. Groll, M., Larionov, O. V., Huber, R. & de Meijere, A. Inhibitor-binding mode of homobelactosin C to proteasomes: new insights into class I MHC ligand generation. Proc. Natl Acad. Sci. USA 103, 4576-4579 (2006).
32. Groll, M., Huber, R. & Potts, B. C. Crystal structures of Salinosporamide A (NPI-0052) and B (NPI-0047) in complex with the 20S proteasome reveal important consequences of beta-lactone ring opening and a mechanism for irreversible binding. J. Am. Chem. Soc. 128, 5136-5141 (2006).
33. Choi, K. S., Kim, J. A. & Kang, H. S. Effects of site-directed mutations on processing and activities of penicillin G acylase from Escherichia coli ATCC 11105. J. Bacteriol. 174, 6270-6276 (1992).
34. Khan, J. A., Dunn, B. M. & Tong, L. Crystal structure of human Taspase1, a crucial protease regulating the function of MLL. Structure 13, 1443-1452 (2005).
35. Kisselev, A. F., Songyang, Z. & Goldberg, A. L. Why does threonine, and not serine, function as the active site nucleophile in proteasomes? J. Biol. Chem. 275, 14831-14837 (2000).
36. Gallastegui, N. & Groll, M. Analysing properties of proteasome inhibitors using kinetic and X-ray crystallographic studies. Methods Mol. Biol. 832, 373-390 (2012).
37. Groll, M. & Huber, R. Purification, crystallization, and X-ray analysis of the yeast 20S proteasome. Methods Enzymol. 398, 329-336 (2005).
38. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
39. Vagin, A. A. et al. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr. 60, 2184-2195 (2004).
40. Turk, D. MAIN software for density averaging, model building, structure refinement and validation. Acta Crystallogr. D Biol. Crystallogr. 69, 1342-1357 (2013).
41. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).