Local and global mobility in the ClpA AAA+ chaperone detected by cryo-electron microscopy: Functional connotations

Structure

Volumn 18, Issue 5, 2010, Pages 553-562

  Effantin, Grégory ^a   Ishikawa, Takashi ^a,b   De Donatis, Gian Marco ^c   Maurizi, Michael R ^c   Steven, Alasdair C ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b ETH ZURICH   (Switzerland)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CELLBIO; CELLCYCLE; PROTEINS

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; CLPA CHAPERONE; CLPP CHAPERONE; MONOMER; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL TRANSLOCATION; CELL DENSITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DELETION MUTANT; ENZYME ACTIVITY; ENZYME BINDING; ENZYME SUBSTRATE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

ADENOSINE TRIPHOSPHATE; ANTIGENS, NEOPLASM; CRYOELECTRON MICROSCOPY; DNA TOPOISOMERASES, TYPE II; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA-BINDING PROTEINS; ENDOPEPTIDASE CLP; ENDOPEPTIDASES; HYDROLYSIS; MACROMOLECULAR SUBSTANCES; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS);

EID: 77952592280     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.02.016     Document Type: Article

References (59)

1. Ammelburg M., Frickey T., Lupas A.N. Classification of AAA+ proteins. J. Struct. Biol. 2006, 156:2-11.
2. Baker T.A., Sauer R.T. ATP-dependent proteases of bacteria: recognition logic and operating principles. Trends Biochem. Sci. 2006, 31:647-653.
3. Beuron F., Maurizi M.R., Belnap D.M., Kocsis E., Booy F.P., Kessel M., Steven A.C. At sixes and sevens: characterization of the symmetry mismatch of the ClpAP chaperone-assisted protease. J. Struct. Biol. 1998, 123:248-259.
4. Bewley M.C., Graziano V., Griffin K., Flanagan J.M. The asymmetry in the mature amino-terminus of ClpP facilitates a local symmetry match in ClpAP and ClpXP complexes. J. Struct. Biol. 2006, 153:113-128.
5. 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 2000, 403:800-805.
6. Bohon J., Jennings L.D., Phillips C.M., Licht S., Chance M.R. Synchrotron protein footprinting supports substrate translocation by ClpA via ATP-induced movements of the D2 loop. Structure 2008, 16:1157-1165.
7. Choi K.H., Licht S. Control of peptide product sizes by the energy-dependent protease ClpAP. Biochemistry 2005, 44:13921-13931.
8. Cranz-Mileva S., Imkamp F., Kolygo K., Maglica Z., Kress W., Weber-Ban E. The flexible attachment of the N-domains to the ClpA ring body allows their use on demand. J. Mol. Biol. 2008, 378:412-424.
9. DasGupta S., Mukhopadhyay G., Papp P.P., Lewis M.S., Chattoraj D.K. Activation of DNA binding by the monomeric form of the P1 replication initiator RepA by heat shock proteins DnaJ and DnaK. J. Mol. Biol. 1993, 232:23-34.
10. Davies J.M., Brunger A.T., Weis W.I. Improved structures of full-length p97, an AAA ATPase: implications for mechanisms of nucleotide-dependent conformational change. Structure 2008, 16:715-726.
11. De Donatis G.M., Singh S.K., Viswanathan S., Maurizi M.R. A single ClpS monomer is sufficient to direct the activity of the ClpA hexamer. J. Biol. Chem. 2010, 285:8771-8781.
12. DeLaBarre B., Brunger A.T. Nucleotide dependent motion and mechanism of action of p97/VCP. J. Mol. Biol. 2005, 347:437-452.
13. Diemand A.V., Lupas A.N. Modeling AAA+ ring complexes from monomeric structures. J. Struct. Biol. 2006, 156:230-243.
14. Djuranovic S., Hartmann M.D., Habeck M., Ursinus A., Zwickl P., Martin J., Lupas A.N., Zeth K. Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol. Cell 2009, 34:580-590.
15. Effantin G., Maurizi M.R., Steven A.C. Binding of the CLP-A unfoldase opens the axial gate of CLP-P peptidase. J. Biol. Chem. 2010, in press. Published online March 16, 2010. 10.1016/j.tcb.2010.02.001.
16. Erzberger J.P., Berger J.M. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:93-114.
17. Farbman M.E., Gershenson A., Licht S. Role of a conserved pore residue in the formation of a prehydrolytic high substrate affinity state in the AAA+ chaperone ClpA. Biochemistry 2008, 47:13497-13505.
18. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 1996, 116:190-199.
19. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature 2003, 426:895-899.
20. Gottesman S. Proteolysis in bacterial regulatory circuits. Annu. Rev. Cell Dev. Biol. 2003, 19:565-587.
21. Gribun A., Kimber M.S., Ching R., Sprangers R., Fiebig K.M., Houry W.A. The ClpP double ring tetradecameric protease exhibits plastic ring-ring interactions, and the N termini of its subunits form flexible loops that are essential for ClpXP and ClpAP complex formation. J. Biol. Chem. 2005, 280:16185-16196.
22. Guo F., Maurizi M.R., Esser L., Xia D. Crystal structure of ClpA, an Hsp100 chaperone and regulator of ClpAP protease. J. Biol. Chem. 2002, 277:46743-46752.
23. Hanson P.I., Whiteheart S.W. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 2005, 6:519-529.
24. Heckman K.L., Pease L.R. Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protoc. 2007, 2:924-932.
25. Heymann J.B., Belnap D.M. Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 2007, 157:3-18.
26. Hinnerwisch J., Fenton W.A., Furtak K.J., Farr G.W., Horwich A.L. Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 2005, 121:1029-1041.
27. Ishikawa T., Maurizi M.R., Belnap D., Steven A.C. Docking of components in a bacterial complex. Nature 2000, 408:667-668.
28. Ishikawa T., Beuron F., Kessel M., Wickner S., Maurizi M.R., Steven A.C. Translocation pathway of protein substrates in ClpAP protease. Proc. Natl. Acad. Sci. USA 2001, 98:4328-4333.
29. Ishikawa T., Maurizi M.R., Steven A.C. The N-terminal substrate-binding domain of ClpA unfoldase is highly mobile and extends axially from the distal surface of ClpAP protease. J. Struct. Biol. 2004, 146:180-188.
30. Katayama Y., Gottesman S., Pumphrey J., Rudikoff S., Clark W.P., Maurizi M.R. The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J. Biol. Chem. 1988, 263:15226-15236.
31. Kenniston J.A., Baker T.A., Fernandez J.M., Sauer R.T. Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 2003, 114:511-520.
32. 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. 1995, 250:587-594.
33. Kim D.Y., Kim K.K. Crystal structure of ClpX molecular chaperone from Helicobacter pylori. J. Biol. Chem. 2003, 278:50664-50670.
34. Kim Y.I., Levchenko I., Fraczkowska K., Woodruff R.V., Sauer R.T., Baker T.A. Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat. Struct. Biol. 2001, 8:230-233.
35. Lee S., Sowa M.E., Watanabe Y.H., Sigler P.B., Chiu W., Yoshida M., Tsai F.T. The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 2003, 115:229-240.
36. Lee S., Choi J.M., Tsai F.T. Visualizing the ATPase cycle in a protein disaggregating machine: structural basis for substrate binding by ClpB. Mol. Cell 2007, 25:261-271.
37. Lenzen C.U., Steinmann D., Whiteheart S.W., Weis W.I. Crystal structure of the hexamerization domain of N-ethylmaleimide-sensitive fusion protein. Cell 1998, 94:525-536.
38. Martin A., Baker T.A., Sauer R.T. Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat. Struct. Mol. Biol. 2008, 15:1147-1151.
39. Maurizi M.R., Thompson M.W., Singh S.K., Kim S.H. Endopeptidase Clp: ATP-dependent Clp protease from Escherichia coli. Methods Enzymol. 1994, 244:314-331.
40. Ortega J., Heymann J.B., Kajava A.V., Ustrell V., Rechsteiner M., Steven A.C. The axial channel of the 20S proteasome opens upon binding of the PA200 activator. J. Mol. Biol. 2005, 346:1221-1227.
41. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
42. Reid B.G., Fenton W.A., Horwich A.L., Weber-Ban E.U. ClpA mediates directional translocation of substrate proteins into the ClpP protease. Proc. Natl. Acad. Sci. USA 2001, 98:3768-3772.
43. Roseman A.M., Chen S., White H., Braig K., Saibil H.R. The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 1996, 87:241-251.
44. Rotanova T.V., Botos I., Melnikov E.E., Rasulova F., Gustchina A., Maurizi M.R., Wlodawer A. Slicing a protease: structural features of the ATP-dependent Lon proteases gleaned from investigations of isolated domains. Protein Sci. 2006, 15:1815-1828.
45. Singh S.K., Maurizi M.R. Mutational analysis demonstrates different functional roles for the two ATP-binding sites in ClpAP protease from Escherichia coli. J. Biol. Chem. 1994, 269:29537-29545.
46. Singh S.K., Grimaud R., Hoskins J.R., Wickner S., Maurizi M.R. Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP. Proc. Natl. Acad. Sci. USA 2000, 97:8898-8903.
47. Singh S.K., Rozycki J., Ortega J., Ishikawa T., Lo J., Steven A.C., Maurizi M.R. Functional domains of the ClpA and ClpX molecular chaperones identified by limited proteolysis and deletion analysis. J. Biol. Chem. 2001, 276:29420-29429.
48. Snider J., Houry W.A. AAA+ proteins: diversity in function, similarity in structure. Biochem. Soc. Trans. 2008, 36:72-77.
49. 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 2000, 103:633-643.
50. Striebel F., Kress W., Weber-Ban E. Controlled destruction: AAA+ ATPases in protein degradation from bacteria to eukaryotes. Curr. Opin. Struct. Biol. 2009, 19:209-217.
51. Szyk A., Maurizi M.R. Crystal structure at 1.9Å of E. coli ClpP with a peptide covalently bound at the active site. J. Struct. Biol. 2006, 156:165-174.
52. Trame C.B., McKay D.B. Structure of Haemophilus influenzae HslU protein in crystals with one-dimensional disorder twinning. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:1079-1090.
53. Wang J. Nucleotide-dependent domain motions within rings of the RecA/AAA(+) superfamily. J. Struct. Biol. 2004, 148:259-267.
54. 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 2001, 9:177-184.
55. 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 HsIU. Structure 2001, 9:1107-1116.
56. Weber-Ban E.U., Reid B.G., Miranker A.D., Horwich A.L. Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 1999, 401:90-93.
57. Wickner S., Maurizi M.R., Gottesman S. Posttranslational quality control: folding, refolding, and degrading proteins. Science 1999, 286:1888-1893.
58. Xia D., Esser L., Singh S.K., Guo F., Maurizi M.R. Crystallographic investigation of peptide binding sites in the N-domain of the ClpA chaperone. J. Struct. Biol. 2004, 146:166-179.
59. Yu A.Y., Houry W.A. ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett. 2007, 581:3749-3757.