Molecular architecture of the ATP-dependent CodWX protease having an N-terminal serine active site

EMBO Journal

Volumn 22, Issue 12, 2003, Pages 2893-2902

  Kang, Min Suk ^a   Kim, Soon Rae ^b   Kwack, Pyeongsu ^b   Lim, Byung Kook ^a   Ahn, Sung Won ^a   Rho, Young Min ^a   Seong, Ihn Sik ^a   Park, Seong Chul ^b   Eom, Soo Hyun ^c   Cheong, Gang Won ^b   Chung, Chin Ha ^a  

^a Seoul National University   (South Korea)

^b Gyeongsang National University   (South Korea)

^c Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

ATP dependent protease; CodWX; EzrA; HsIVU; N terminal serine protease

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ALKALINE PROTEINASE; CODW PEPTIDASE; CODWX PROTEASE; CODX ADENOSINE TRIPHOSPHATASE; PEPTIDASE; SERINE PROTEINASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CELL DIVISION; CRYSTAL STRUCTURE; ENZYME STRUCTURE; HYDROLYSIS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATE; ATP-DEPENDENT PROTEASES; BACTERIAL PROTEINS; BINDING SITES; HEAT-SHOCK PROTEINS; MACROMOLECULAR SUBSTANCES; PROTEIN STRUCTURE, QUATERNARY; SERINE; SERINE ENDOPEPTIDASES;

BACILLUS SUBTILIS;

EID: 0038714407     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg289     Document Type: Article

References (54)

1. Baumeister, W., Dahlmann, B., Hegerl, R., Kopp, F., Luehn, L. and Pfeifer, G. (1988) Electron microscopy and image analysis of the multicatalytic proteinase. FEBS Lett., 241, 239-245.
2. Baumeister, W., Walz, J., Zuhl, F. and Seemüller, E. (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell, 92, 367-380.
3. Benaroudj, N. and Goldberg, A.L. (2000) PAN, the proteasome-activating nucleotidase from archaebacteria, is a protein-unfolding molecular chaperone. Nat. Cell Biol., 2, 833-839.
4. Benaroudj, N., Zwickl, P., Seemüller E., Baumeister, W. and Goldberg, A.L. (2003) ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. Mol. Cell, 11, 69-78.
5. Beuron, F., Maurizi, M.R., Belnap, D.M., Kocsis, E., Booy, F.P., Kessel, M. and Steven, A.C. (1998) At sixes and sevens: characterization of the symmetry mismatch of the ClpAP chaperone-assisted protease. J. Struct. Biol., 123, 248-259.
6. Bochtler, M., Ditzel, L., Groll, M. and Huber, R. (1997) Crystal structure of heat shock locus V (HsIV) from Escherichia coli. Proc. Natl Acad. Sci. USA, 94, 6070-6074.
7. Bochtler, M., Hartmann, C., Song, H.K., Bourenkov, G.P., Bartunik, H.D. and Huber, R. (2000) The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature, 403, 800-805.
8. Chung, C.H. (1993) Proteases in Escherichia coli. Science, 262, 372-374.
9. Chung, C.H., Yoo, S.J., Seol, J.H. and Kang, M.S. (1997) Characterization of energy-dependent proteases in bacteria. Biochem. Biophys. Res. Commun., 241, 613-616.
10. Coux, O., Tanaka, K. and Goldberg, A.L. (1996) Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem., 65, 801-847.
11. Dürr, R. (1991) Displacement field analysis: calculation of distortion measures from displacement maps. Ultramicroscopy, 38, 135-141.
12. Fenteany, G., Standaert, R.F., Lane, W.S., Choi, S., Corey, E.J. and Schreiber, S.L. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science, 268, 726-731.
13. Goldberg, A.L. (1992) The mechanism and function of ATP-dependent protease in bacterial and animal cells. Eur. J. Biochem., 203, 9-23.
14. Gottesman, S. (1996) Proteases and their targets in Escherichia coli. Annu. Rev. Genet., 30, 465-506.
15. Gottesman, S., Maurizi, M.R. and Wickner, S. (1997) Regulatory subunits of energy-dependent proteases. Cell, 91, 435-438.
16. Gottesman, S., Roche, E., Zhou, Y. and Sauer, R.T. (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev., 12, 1338-1347.
17. Grimaud, R., Kessel, M., Beuron, F., Steven, A.C. and Maurizi, M.R. (1998) Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J. Biol. Chem., 273, 12476-12481.
18. Groll, M., Ditzel, L., Lowe, J., Stock, D., Bochtler, M., Bartunik, H.D. and Huber, R. (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature, 386, 463-471.
19. Hegerl, R. (1996) The EM program package: a platform for image processing in biological electron microscopy. J. Struct. Biol., 116, 30-34.
20. Hochstrasser, M. (1996) Ubiquitin-dependent protein degradation. Annu. Rev. Genet., 30, 405-439.
21. Huang, H.C. and Goldberg, A.L. (1997) Proteolytic activity of the ATP-dependent protease HsIVU can be uncoupled from ATP hydrolysis. J. Biol. Chem., 272, 21364-21372.
22. Ishikawa, T., Maurizi, M.R., Belnap, D. and Steven, A.C. (2000) Docking of components in a bacterial complex. Nature, 408, 667-668.
23. Ishikawa, T., Beuron, F., Kessel, M., Wickner, S., Maurizi, M.R. and Steven, A.C. (2001) Translocation pathway of protein substrates in ClpAP protease. Proc. Natl Acad. Sci. USA, 98, 4328-4333.
24. Kang, M.S., Lim, B.K., Seong, I.S., Seol, J.H., Tanahashi, N., Tanaka, K. and Chung, C.H. (2001) The ATP-dependent CodWX (HsIVU) protease in Bacillus subtilis is an N-terminal serine protease. EMBO J., 20, 734-742.
25. Kessel, M., Wu, W., Gottesman, S., Kocsis, E., Steven, A.C., and Maurizi, M.R. (1996) Six-fold rotational symmetry of ClpQ, the E. coli homolog of the 20S proteasome and its ATP-dependent activator, Clp Y. FEBS Lett., 398, 274-278.
26. Khattar, M.M. (1997) Overexpression of the hsIVU operon suppresses SOS-mediated inhibition of cell division in Escherichia coli. FEBS Lett., 414, 402-404.
27. Kim, K.I., Cheong, G.W., Park, S.C., Ha, J.S., Woo, K.M., Choi, S.J. and Chung, C.H (2000) Heptameric ring structure of the heat-shock protein ClpB, a protein-activated ATPase in Escherichia coli. J. Mol. Biol., 303, 655-666.
28. Krojer, T., Garrido-Franco, M., Huber, R., Ehrmann, M. and Clausen, T. (2002) Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature, 416, 455-459.
29. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
30. Larsen, N.C. and Finley, D. (1997) Protein translocation channels in the proteasome and other proteases. Cell, 91, 431-434.
31. Levin, P.A., Kurtser, I.G. and Grossman, A.D. (1999) Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc. Natl Acad. Sci. USA, 96, 9642-9647.
32. Marco, S., Urena, D., Carrascosa, J.L., Waldmann, T., Peter, J., Hegerl, R., Pfeifer, G., Sack-Kongehl, H. and Baumeister, W. (1994) The molecular chaperone TF55: assessment of symmetry. FEBS Lett., 341, 152-155.
33. Missiakas, D., Schwager, F., Betton, J.M., Georgopoulos, C. and Raina, S. (1996) Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli. EMBO J., 15, 6899-6909.
34. +: a class of chaperone-like ATPases associated with the assembly, operation and disassembly of protein complexes. Genome Res., 9, 27-43.
35. Ortega, J., Singh, S.K., Ishikawa, T., Maurizi, M.R. and Steven, A.C. (2000) Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. Mol. Cell, 6, 1515-1521.
36. Rohrwild, M., Coux, O., Huang, H.C., Moerschell, R.P., Yoo, S.J., Seol, J.H., Chung, C.H. and Goldberg, A.L. (1996) HsIV-HsIU: a novel ATP-dependent protease complex in Escherichia coli related to the eukaryotic proteasome. Proc. Natl Acad. Sci. USA, 93, 5808-5813.
37. Rohrwild, M., Pfeifer, G., Santarius, U., Müller, S.A., Huang, H.C., Engel, A., Baumeister, W. and Goldberg, A.L. (1997) The ATP-dependent HsIVU protease from Escherichia coli is a four-ring structure resembling the proteasome. Nat. Struct. Biol., 4, 133-139.
38. Saxton, W.O., Pitt, T.J. and Horner, M. (1979) Digital image processing: the Semper system. Ultramicroscopy, 4, 343-354.
39. Seemüller, E., Lupas, A., Stock, D., Löwe, J., Huber, R. and Baumeister, W. (1995) Proteasome from Thermoplasma acidophilum: a threonine protease. Science, 268, 579-582.
40. Seol, J.H., Yoo, S.J., Shin, D.H., Shim, Y.K., Kang, M.S., Goldberg, A.L. and Chung, C.H. (1997) The heat-shock protein HsIVU from Escherichia coli is a protein-activated ATPase as well as an ATP-dependent proteinase. Eur. J. Biochem. 247, 1143-1150.
41. Seong, I.S., Oh, J.Y., Yoo, S.J., Seol, J.H. and Chung, C.H. (1999) ATP-dependent degradation of SulA, a cell division inhibitor, by the HsIVU protease in Escherichia coli, FEBS Lett., 456, 211-214.
42. Seong, I.S., Oh, J.Y., Lee, J.W., Tanaka, K. and Chung, C.H. (2000) The HsIU ATPase acts as a molecular chaperone in prevention of aggregation of SulA, an inhibitor of cell division in Escherichia coli. FEBS Lett., 477, 224-228.
43. Seong, I.S., Kang, M.S., Choi, M.K., Lee, J.W., Koh, O.J., Wang, J., Eom, S.H. and Chung, C.H. (2002) The C-terminal tails of HsIU ATPase act as a molecular switch for activation of HsIV peptidase. J. Biol. Chem., 277, 25976-25982.
44. Seufert, W. and Jentsch, S. (1992) In vivo function of the proteasome in the ubiquitin pathway. EMBO J., 11, 3077-3080.
45. Slack, F.J., Serror, P., Joyce, E. and Sonenshein, A.L. (1995) A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol. Microbiol., 15, 689-702.
46. Sousa, M.C., Trame, C.B., Tsuruta, S., Wilbanks, S.M., Reddy, R.S. and Mckay, D. (2000) Crystal and solution structures of an HsIUV protease-chaperone complex. Cell, 103, 633-643.
47. van Heel, M. and Frank, J. (1981) Use of multivariate statistics in analyzing the images of biological macromolecules. Ultramicroscopy, 6, 187-194.
48. Wang, J., Hartling, J.A. and Flanagan, J.M. (1997) The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell, 91, 447-456.
49. Wang, J. et al. (2001a) Crystal structures of the HsIVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure, 9, 177-184.
50. Wang, J., Song, J.J., Seong, I.S., Franklin, M.C., Kamtekar, S., Eom, S.H. and Chung, C.H. (2001b) Nucleotide-dependent conformational changes in a protease-associated ATPase HsIU. Structure, 9, 1107-1116.
51. Yoo, S.J., Seol, J.H., Shin, D.H., Rohrwild, M., Kang, M.S., Tanaka, K., Goldberg, A.L. and Chung, C.H. (1996) Purification and characterization of the heat shock proteins HSIV and HsIU that form a new ATP-dependent protease in Escherichia coli. J. Biol. Chem., 271, 14035-14040.
52. Yoo, S.J., Seol, J.H., Seong, I.S., Kang, M.S. and Chung, C.H. (1997a) ATP binding, but not its hydrolysis, is required for assembly and proteolytic activity of the HsIVU protease in Escherichia coli. Biochem. Biophys. Res. Commun., 238, 581-585.
53. Yoo, S.J., Shim, Y.K., Seong, I.S., Seol, J.H., Kang, M.S. and Chung, C.H., (1997b) Mutagenesis of two N-terminal Thr and five Ser residues in HsIV, the proteolytic component of the ATP-dependent HsIVU protease. FEBS Lett., 412, 57-60.
54. Yoo, S.J., Kim, H.H., Shin, D.H., Lee, C.S., Seong, I.S., Seol, J.H., Shimbara, N., Tanaka, K. and Chung, C.H. (1998) Effects of the Cys mutations on structure and function of the ATP-dependent HsIVU protease in Escherichia coli. J. Biol. Chem., 273, 22929-22935.