Structure and reactivity of an asymmetric complex between HslV and I-domain deleted HslU, a prokaryotic homolog of the eukaryotic proteasome

Journal of Molecular Biology

Volumn 330, Issue 2, 2003, Pages 185-195

  Kwon, Ae Ran ^a   Kessler, Benedikt M ^b   Overkleeft, Herman S ^b   McKay, David B ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

AAA proteins; Clp Hsp100 proteins; HslUV (H. influenzae); Proteasome; Vinyl sulfone

Indexed keywords

BACTERIAL PROTEIN; HAEMOPHILUS INFLUENZAE IU PROTEIN; HAEMOPHILUS INFLUENZAE IV PROTEIN; PROTEASOME; SULFONE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY;

EUKARYOTA; PROKARYOTA;

EID: 0038122858     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00580-1     Document Type: Article

References (43)

1. Rohrwild M., Coux O., Huang H.C., Moerschell R.P., Yoo S.J., Seol J.H., et al. HslV-HslU: a novel ATP-dependent protease complex in Escherichia coli related to the eukaryotic proteasome. Proc. Natl Acad. Sci. USA. 93:1996;5808-5813.
2. Missiakas D., Schwager F., Betton J.M., Georgopoulos C., Raina S. Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli. EMBO J. 15:1996;6899-6909.
3. Kessel M., Wu W., Gottesman S., Kocsis E., Steven A.C., Maurizi M.R. Six-fold rotational symmetry of ClpQ, the E. coli homolog of the 20 S proteasome, and its ATP-dependent activator, ClpY. FEBS Letters. 398:1996;274-278.
4. Yoo S.J., Seol J.H., Shin D.H., Rohrwild M., Kang M.S., Tanaka K., et al. Purification and characterization of the heat shock proteins HslV and HslU that form a new ATP-dependent protease in Escherichia coli. J. Biol. Chem. 271:1996;14035-14040.
5. Huang H., Goldberg A.L. Proteolytic activity of the ATP-dependent protease HslVU can be uncoupled from ATP hydrolysis. J. Biol. Chem. 272:1997;21364-21372.
6. Seol J.H., Yoo S.J., Shin D.H., Shim Y.K., Kang M.S., Goldberg A.L., Chung C.H. The heat-shock protein HslVU from Escherichia coli is a protein-activated ATPase as well as an ATP-dependent proteinase. Eur. J. Biochem. 247:1997;1143-1150.
7. Yoo S.J., Seol J.H., Seong I.S., Kang M.S., Chung C.H. ATP binding, but not its hydrolysis, is required for assembly and proteolytic activity of the HslVU protease in Escherichia coli. Biochem. Biophys. Res. Commun. 238:1997;581-585.
8. Kanemori M., Yanagi H., Yura T. The ATP-dependent HslVU/ClpQY protease participates in turnover of cell division inhibitor SulA in Escherichia coli. J. Bacteriol. 181:1999;3674-3680.
9. Bochtler M., Ditzel L., Groll M., Huber R. Crystal structure of heat shock locus V (HslV) from Escherichia coli. Proc. Natl Acad. Sci. USA. 94:1997;6070-6074.
10. Sousa M.C., McKay D.B. Structure of Haemophilus influenzae HslV protein at 1.9 Ångstrom resolution, revealing a cation binding site near the catalytic site. Acta Crystallog. sect. D. 57:2001;1950-1954.
11. Löwe J., Stock D., Jap B., Zwickl P., Baumeister W., Huber R. Crystal structure of the 20 S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science. 268:1995;533-539.
12. Groll M., Ditzel L., Löwe J., Stock D., Bochtler M., Bartunik H.D., Huber R. Structure of 20 S proteasome from yeast at 2.4 Å resolution. Nature. 386:1997;463-471.
13. Seemüller E., Lupas A., Stock D., Löwe J., Huber R., Baumeister W. Proteasome from Thermoplasma acidophilum: a threonine protease. Science. 268:1995;579-582.
14. Bochtler M., Hartmann C., Song H.K., Bourenkov G.P., Bartunik H.D., Huber R. The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature. 403:2000;800-805.
15. Sousa M.C., Trame C.B., Tsuruta H., Wilbanks S.M., Reddy V.S., McKay D.B. Crystal and solution structures of an HslUV protease-chaperone Complex. Cell. 103:2000;633-643.
16. Trame C.B., McKay D.B. Structure of Haemophilus influenzae HslU protein in crystals with one-dimensional disorder twinning. Acta Crystallog. sect. D. 57:2001;1079-1090.
17. Schirmer E.C., Glover J.R., Singer M.A., Lindquist S. HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem. Sci. 21:1996;289-295.
18. Song H.K., Hartmann C., Ramachandran R., Bochtler M., Behrendt R., Moroder L., Huber R. Mutational studies on HslU and its docking mode with HslV. Proc. Natl Acad. Sci. USA. 97:2000;14103-14108.
19. Wang J., Song J.J., Franklin M.C., Kamtekar S., Im Y.J., Rho S.H., et al. Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure. 9:2001;177-184.
20. Ramachandran R., Hartmann C., Song H.K., Huber R., Bochtler M. Functional interactions of HslV (ClpQ) with the ATPase HslU (ClpY). Proc. Natl Acad. Sci. USA. 99:2002;7396-7401.
21. Seong I.S., Kang M.S., Choi M.K., Lee J.W., Koh O.J., Wang J., et al. The C-terminal tails of HslU ATPase act as a molecular switch for activation of HslV peptidase. J. Biol. Chem. 277:2002;25976-25982.
22. Wang J., Song J.J., Seong I.S., Franklin M.C., Kamtekar S., Eom S.H., Chung C.H. Nucleotide-dependent conformational changes in a protease-associated ATPase HslU. A corrected quaternary arrangement of the peptidase hslv and atpase hslu in a cocrystal structure. Structure. 9:2001;1107-1116.
23. Sousa M.C., Kessler B.M., Overkleeft H.S., McKay D.B. Crystal structure of HslUV complexed with a vinyl sulfone inhibitor: corroboration of a proposed mechanism of allosteric activation of HslV by HslU. J. Mol. Biol. 318:2002;779-785.
24. Bogyo M., McMaster J.S., Gaczynska M., Tortorella D., Goldberg A.L., Ploegh H. Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HslV by a new class of inhibitors. Proc. Natl Acad. Sci. USA. 94:1997;6629-6634.
25. Luzzati V. Traitment statistique des erreurs dans la determination des structures cristallines. Acta Crystallog. 5:1952;802-810.
26. Glusker J.P., et al. Structural aspects of metal liganding to functional groups in proteins. Anfinsen C.B., Edsall J.T., Richards F.M., Eisenberg D.S. Advances in Protein Chemistry. vol. 42:1991;1-76 Academic Press, Orlando.
27. Walker J.E., Saraste M., Runswick M.J., Gay N.J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:1982;945-951.
28. Smith C.A., Rayment I. Active site comparisons highlight structural similarities between myosin and other P-loop proteins. Biophys. J. 70:1996;1590-1602.
29. Groll M., Nazif T., Huber R., Bogyo M. Probing structural determinants distal to the site of hydrolysis that control substrate specificity of the 20 S proteasome. Chem. Biol. 9:2002;655-662.
30. Vershon A.K., Youderian P., Susskind M.M., Sauer R.T. The bacteriophage P22 arc and mnt repressors. Overproduction, purification, and properties. J. Biol. Chem. 260:1985;12124-12129.
31. Burton R.E., Siddiqui S.M., Kim Y.I., Baker T.A., Sauer R.T. Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine. EMBO J. 20:2001;3092-3100.
32. Ishii Y., Sonezaki S., Iwasaki Y., Miyata Y., Akita K., Kato Y., Amano F. Regulatory role of C-terminal residues of SulA in its degradation by Lon protease in Escherichia coli. J. Biochem. (Tokyo). 127:2000;837-844.
33. Groll M., Bajorek M., Köhler A., Moroder L., Rubin D.M., Huber R., et al. A gated channel into the proteasome core particle. Nature Struct. Biol. 7:2000;1062-1067.
34. Whitby F.G., Masters E.I., Kramer L., Knowlton J.R., Yao Y., Wang C.C., Hill C.P. Structural basis for the activation of 20 S proteasomes by 11 S regulators. Nature. 408:2000;115-120.
35. Seong I.S., Oh J.Y., Yoo S.J., Seol J.H., Chung C.H. ATP-dependent degradation of SulA, a cell division inhibitor, by the HslVU protease in Escherichia coli. FEBS Letters. 456:1999;211-214.
36. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
37. Bailey S. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
38. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
39. Jones A. A graphics model building and refinement system for macromolecules. J. Appl. Crystallog. 11:1978;268-272.
40. Jones T.A., Zhou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for the building of protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
41. Kraulis P. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
42. Esnouf R.M. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallog. sect. D. 55:1999;938-940.
43. Merritt E.A., Bacon D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.