Dynamic and static components power unfolding in topologically closed rings of a AAA+ proteolytic machine

Nature Structural and Molecular Biology

Volumn 19, Issue 6, 2012, Pages 616-622

  Glynn, Steven E ^a   Nager, Andrew R ^a   Baker, Tania A ^a   Sauer, Robert T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; CLPXP PROTEASE; UNCLASSIFIED DRUG;

ARTICLE; ATPASE ASSOCIATED WITH VARIOUS CELLULAR ACTIVITY; CELL ACTIVITY; CONTROLLED STUDY; DISULFIDE BOND; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN HYDROLYSIS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ENDOPEPTIDASE CLP; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEIN UNFOLDING; PROTEOLYSIS;

ESCHERICHIA COLI;

EID: 84861876642     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2288     Document Type: Article

References (42)

1. Hanson, P.I. & Whiteheart, S.W. AAA+ proteins: have engines, will work. Nat. Rev. Mol. Cell Biol. 6, 519-529 (2005).
2. White, S.R. & Lauring, B. AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 8, 1657-1667 (2007).
3. Baker, T.A. & Sauer, R.T. ClpXP, an ATP-powered unfolding and protein-degradation machine. Biochim. Biophys. Acta 1823, 15-28 (2012).
4. Kim, D.Y. & Kim, K.K. Crystal structure of ClpX molecular chaperone from Helicobacter pylori. J. Biol. Chem. 278, 50664-50670 (2003).
5. Glynn, S.E., Martin, A., Nager, A.R., Baker, T.A. & Sauer, R.T. Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine. Cell 139, 744-756 (2009).
6. Jeruzalmi, D., O'Donnell, M. & Kuriyan, J. Crystal structure of the processivity clamp loader gamma (γ) complex of E. coli DNA polymerase III. Cell 106, 429-441 (2001).
7. Skordalakes, E. & Berger, J.M. Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 114, 135-146 (2003).
8. Erzberger, J.P., Mott, M.L. & Berger, J.M. Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling. Nat. Struct. Mol. Biol. 13, 676-683 (2006).
9. Mott, M.L., Erzberger, J.P., Coons, M.M. & Berger, J.M. Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell 135, 623-634 (2008).
10. Simonetta, K.R. et al. The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Cell 137, 659-671 (2009).
11. Singh, S.K. et al. Functional domains of the ClpA and ClpX molecular chaperones identified by limited proteolysis and deletion analysis. J. Biol. Chem. 276, 29420-29429 (2001).
12. Wojtyra, U.A., Thibault, G., Tuite, A. & Houry, W.A. The N-terminal zinc binding domain of ClpX is a dimerization domain that modulates the chaperone function. J. Biol. Chem. 278, 48981-48990 (2003).
13. Ortega, J. et al. ATPases bind simultaneously to opposite ends of ClpP peptidase to form active hybrid complexes. J. Struct. Biol. 146, 217-226 (2004).
14. Siddiqui, S.M., Sauer, R.T. & Baker, T.A. Role of the processing pore of the ClpX AAA+ ATPase in the recognition and engagement of specific protein substrates. Genes Dev. 18, 369-374 (2004).
15. Martin, A., Baker, T.A. & Sauer, R.T. Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines. Nature 437, 1115-1120 (2005).
16. 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. 15, 1147-1151 (2008).
17. Martin, A., Baker, T.A. & Sauer, R.T. Diverse pore loops of the AAA+ ClpX machine mediate unassisted and adaptor-dependent recognition of ssrA-tagged substrates. Mol. Cell 29, 441-450 (2008).
18. Hersch, G.L., Burton, R.E., Bolon, D.N., Baker, T.A. & Sauer, R.T. Asymmetric interactions of ATP with the AAA+ ClpX6 unfoldase: allosteric control of a protein machine. Cell 121, 1017-1027 (2005).
19. Martin, A., Baker, T.A. & Sauer, R.T. Distinct static and dynamic interactions control ATPase-peptidase communication in a AAA+ protease. Mol. Cell 27, 41-52 (2007).
20. 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 114, 511-520 (2003).
21. Kim, Y.I., Burton, R.E., Burton, B.M., Sauer, R.T. & Baker, T.A. Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol. Cell 5, 639-648 (2000).
22. Martin, A., Baker, T.A. & Sauer, R.T. Protein unfolding by a AAA+ protease: critical dependence on ATP-hydrolysis rates and energy landscapes. Nat. Struct. Mol. Biol. 15, 139-145 (2008).
23. Nager, A.R., Baker, T.A. & Sauer, R.T. Stepwise unfolding of a β-barrel protein by the AAA+ ClpXP protease. J. Mol. Biol. 413, 4-16 (2011).
24. Ando, R., Hama, H., Yamamoto-Hino, M., Mizuno, H. & Miyawaki, A. An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 12651-12656 (2002).
25. 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, 3092-3100 (2001).
26. Hoskins, J.R., Yanagihara, K., Mizuuchi, K. & Wickner, S. ClpAP and ClpXP degrade proteins with tags located in the interior of the primary sequence. Proc. Natl. Acad. Sci. USA 99, 11037-11042 (2002).
27. Bolon, D.N., Grant, R.A., Baker, T.A. & Sauer, R.T. Nucleotide-dependent substrate handoff from the SspB adaptor to the AAA+ ClpXP protease. Mol. Cell 16, 343-350 (2004).
28. Kenniston, J.A., Baker, T.A. & Sauer, R.T. Partitioning between unfolding and release of native domains during ClpXP degradation determines substrate selectivity and partial processing. Proc. Natl. Acad. Sci. USA 102, 1390-1395 (2005).
29. Aubin-Tam, M.E., Olivares, A.O., Sauer, R.T., Baker, T.A. & Lang, M.J. Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 145, 257-267 (2011).
30. Bochtler, M. et al. The structures of HslU and the ATP-dependent protease HslU-HsIV. Nature 403, 800-805 (2000).
31. Sousa, M.C. et al. Crystal and solution structures of an HslUV protease-chaperone complex. Cell 103, 633-643 (2000).
32. 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, 46743-46752 (2002).
33. Krzywda, S. et al. The crystal structure of the AAA domain of the ATP-dependent protease FtsH of Escherichia coli at 1.5 Å resolution. Structure 10, 1073-1083 (2002).
34. Cha, S.S. et al. Crystal structure of Lon protease: molecular architecture of gated entry to a sequestered degradation chamber. EMBO J. 29, 3520-3530 (2010).
35. Duman, R.E. & Löwe, J. Crystal structures of Bacillus subtilis Lon protease. J. Mol. Biol. 401, 653-670 (2010).
36. Wang, F. et al. Structure and mechanism of the hexameric MecA-ClpC molecular machine. Nature 471, 331-335 (2011).
37. Joshi, S.A., Baker, T.A. & Sauer, R.T. C-terminal domain mutations in ClpX uncouple substrate binding from an engagement step required for unfolding. Mol. Microbiol. 48, 67-76 (2003).
38. Joshi, S.A., Hersch, G.L., Baker, T.A. & Sauer, R.T. Communication between ClpX and ClpP during substrate processing and degradation. Nat. Struct. Mol. Biol. 11, 404-411 (2004).
39. Crooks, G.E., Hon, G., Chandonia, J.M. & Brenner, S.E. WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190 (2004).
40. Dombkowski, A.A. Disulfide by Design™: a computational method for the rational design of disulfide bonds in proteins. Bioinformatics 19, 1852-1853 (2003).
41. +-ATPase activity. Methods Enzymol. 156, 116-119 (1988).
42. Levchenko, I., Seidel, M., Sauer, R.T. & Baker, T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science 289, 2354-2356 (2000).