Structural basis of degradation signal recognition by SspB, a specificity-enhancing factor for the ClpXP proteolytic machine

Molecular Cell

Volumn 12, Issue 1, 2003, Pages 75-86

  Song, Hyun Kyu ^a,b   Eck, Michael J ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; PROTEIN; PROTEIN CLPXP; PROTEIN SSPB; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; ENZYME SUBSTRATE; HYDROPHOBICITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN FOLDING; SIGNAL TRANSDUCTION;

PROKARYOTA;

EID: 0043128700     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00271-5     Document Type: Article

References (60)

1. Banecki B., Wawrzynow A., Puzewicz J., Georgopoulos C., Zylicz M. Structure-function analysis of the zinc-binding region of the ClpX molecular chaperone. J. Biol. Chem. 276:2001;18843-18848.
2. Barton G.J. Alscript. A tool to format multiple sequence alignments Protein Eng. 6:1993;37-40.
3. Blattner F.R., Plunkett G. 3rd, Bloch C.A., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D., Rode C.K., Mayhew G.F.et al. The complete genome sequence of Escherichia coli K-12. Science. 277:1997;1453-1474.
4. 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.
5. Brunger 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.et al. Crystallography & NMR system. A new software suite for macromolecular structure determination Acta Crystallogr. D. 54:1998;905-921.
6. Bukau B., Horwich A.L. The Hsp70 and Hsp60 chaperone machines. Cell. 92:1998;351-366.
7. Bukau B., Deuerling E., Pfund C., Craig E.A. Getting newly synthesized proteins into shape. Cell. 101:2000;119-122.
8. CCP4 The CCP4 (Collaborative Computational Project 4) suite. programs for protein crystallography Acta Crystallogr. D. 50:1994;760-763.
9. Conaway R.C., Brower C.S., Conaway J.W. Emerging roles of ubiquitin in transcription regulation. Science. 296:2002;1254-1258.
10. Doublies S. Preparation of selenomethionyl proteins for phase determination. Carter C.W. Jr., Sweet R.M. Methods in Enzymology. 1997;Academic Press, New York. 523-530.pp.
11. Dougan D.A., Mogk A., Zeth K., Turgay K., Bukau B. AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett. 529:2002;6-10. a.
12. Dougan D.A., Reid B.G., Horwich A.L., Bukau B. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell. 9:2002;673-683. b.
13. Flynn J.M., Levchenko I., Seidel M., Wickner S.H., Sauer R.T., Baker T.A. Overlapping recognition determinants within the SsrA degradation tag allow modulation of proteolysis. Proc. Natl. Acad. Sci. USA. 98:2001;10584-10589.
14. Gillet R., Felden B. Emerging views on tmRNA-mediated protein tagging and ribosome rescue. Mol. Microbiol. 42:2001;879-885.
15. Gottesman S., Maurizi M.R., Wickner S. Regulatory subunits of energy-dependent proteases. Cell. 91:1997;435-438.
16. Gottesman S., Roche E., Zhou Y., Sauer R.T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev. 12:1998;1338-1347.
17. Grimaud R., Kessel M., Beuron F., Steven A.C., Maurizi M.R. Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J. Biol. Chem. 273:1998;12476-12481.
18. Guo F., Esser L., Singh S.K., Maurizi M.R., Xia D. Crystal structure of the heterodimeric complex of the adaptor, ClpS, with the N-domain of the AAA+ chaperone, ClpA. J. Biol. Chem. 277:2002;46753-46762. a.
19. Guo F., Maurizi M.R., Esser L., Xia D. Crystal structure of ClpA, an Hsp100 chaperone and regulator of ClpAP protease. J. Biol. Chem. 277:2002;46743-46752. b.
20. Hartl F.U. Molecular chaperones in cellular protein folding. Nature. 381:1996;571-579.
21. Hayes C.S., Bose B., Sauer R.T. Proline residues at the C terminus of nascent chains induce SsrA tagging during translation termination. J. Biol. Chem. 277:2002;33825-33832. a.
22. Hayes C.S., Bose B., Sauer R.T. Stop codons preceded by rare arginine codons are efficient determinants of SsrA tagging in Escherichia coli. Proc. Natl. Acad. Sci. USA. 99:2002;3440-3445. b.
23. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67:1998;425-479.
24. Honig B., Nicholls A. Classical electrostatics in biology and chemistry. Science. 268:1995;1144-1149.
25. Hoskins J.R., Singh S.K., Maurizi M.R., Wickner S. Protein binding and unfolding by the chaperone ClpA and degradation by the protease ClpAP. Proc. Natl. Acad. Sci. USA. 97:2000;8892-8897.
26. Jones S., Thornton J.M. Principles of protein-protein interactions. Proc. Natl. Acad. Sci. USA. 93:1996;13-20.
27. Jones T.A., Zou J.-Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47:1991;110-119.
28. Kambach C., Walke S., Young R., Avis J.M., de la Fortelle E., Raker V.A., Luhrmann R., Li J., Nagai K. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell. 96:1999;375-387.
29. Keiler K.C., Waller P.R., Sauer R.T. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science. 271:1996;990-993.
30. Kessel M., Maurizi M.R., Kim B., Kocsis E., Trus B.L., Singh S.K., Steven A.C. Homology in structural organization between E. coli ClpAP protease and the eukaryotic 26 S proteasome. J. Mol. Biol. 250:1995;587-594.
31. Kraulis P.J. Molscript. a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24:1991;946-950.
32. Laney J.D., Hochstrasser M. Substrate targeting in the ubiquitin system. Cell. 97:1999;427-430.
33. Lanzetta P.A., Alvarez L.J., Reinach P.S., Candia O.A. An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100:1979;95-97.
34. Laskowski R., MacArthur M., Hutchinson E., Thorton J. Procheck. a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26:1993;283-291.
35. Levchenko I., Luo L., Baker T.A. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 9:1995;2399-2408.
36. Levchenko I., Seidel M., Sauer R.T., Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science. 289:2000;2354-2356.
37. Merritt E.A., Bacon D.J. Raster3D. photorealistic molecular graphics Carter C.W. Jr., Sweet R.M. Methods in Enzymolpgy. 1997;Academic Press, New York. 505-524.pp.
38. Nevskaya N., Tischenko S., Fedorov R., Al-Karadaghi S., Liljas A., Kraft A., Piendl W., Garber M., Nikonov S. Archaeal ribosomal protein L1. the structure provides new insights into RNA binding of the L1 protein family Structure. 8:2000;363-371.
39. Ortega J., Singh S.K., Ishikawa T., Maurizi M.R., Steven A.C. Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. Mol. Cell. 6:2000;1515-1521.
40. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W. Jr., Sweet R.M. Methods in Enzymology. 1997;Academic Press, New York. 307-326.pp.
41. Retallack D.M., Friedman D.I. A role for a small stable RNA in modulating the activity of DNA-binding proteins. Cell. 83:1995;227-235.
42. Roche E.D., Sauer R.T. SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity. EMBO J. 18:1999;4579-4589.
43. Roche E.D., Sauer R.T. Identification of endogenous SsrA-tagged proteins reveals tagging at positions corresponding to stop codons. J. Biol. Chem. 276:2001;28509-28515.
44. Sack J.S. Chain. a crystallographic modeling program J. Mol. Graph. 6:1988;244-245.
45. Schweder T., Lee K.H., Lomovskaya O., Matin A. Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J. Bacteriol. 178:1996;470-476.
46. 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.
47. 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.
48. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D. 55:1999;849-861.
49. Vagin A., Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D. 56:2000;1622-1624.
50. Verma R., Deshaies R.J. A proteasome howdunit. the case of the missing signal Cell. 101:2000;341-344.
51. Voges D., Zwickl P., Baumeister W. The 26S proteasome. a molecular machine designed for controlled proteolysis Annu. Rev. Biochem. 68:1999;1015-1068.
52. Wah D.A., Levchenko I., Baker T.A., Sauer R.T. Characterization of a specificity factor for an AAA+ ATPase. assembly of SspB dimers with ssrA-tagged proteins and the ClpX hexamer Chem. Biol. 9:2002;1237-1245.
53. Wallace A.C., Laskowski R.A., Thornton J.M. Ligplot. a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 8:1995;127-134.
54. Wang J., Hartling J.A., Flanagan J.M. The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell. 91:1997;447-456.
55. Wang L., Elliott M., Elliott T. Conditional stability of the HemA protein (glutamyl-tRNA reductase) regulates heme biosynthesis in Salmonella typhimurium. J. Bacteriol. 181:1999;1211-1219.
56. Wang J., Song J.J., Franklin M.C., Kamtekar S., Im Y.J., Rho S.H., Seong I.S., Lee C.S., Chung C.H., Eom S.H. Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure. 9:2001;177-184.
57. Williams M.D., Ouyang T.X., Flickinger M.C. Starvation-induced expression of SspA and SspB. the effects of a null mutation in sspA on Escherichia coli protein synthesis and survival during growth and prolonged starvation Mol. Microbiol. 11:1994;1029-1043.
58. Withey J.H., Friedman D.I. The biological roles of trans-translation. Curr. Opin. Microbiol. 5:2002;154-159.
59. Wojtkowiak D., Georgopoulos C., Zylicz M. Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J. Biol. Chem. 268:1993;22609-22617.
60. Zeth K., Ravelli R.B., Paal K., Cusack S., Bukau B., Dougan D.A. Structural analysis of the adaptor protein ClpS in complex with the N-terminal domain of ClpA. Nat. Struct. Biol. 9:2002;906-911.