The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis

Nature Structural and Molecular Biology

Volumn 16, Issue 3, 2009, Pages 281-286

  Mickler, Moritz ^a   Hessling, Martin ^b   Ratzke, Christoph ^a   Buchner, Johannes ^b   Hugel, Thorsten ^a,b  

^a IMETUM   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DIMER; HEAT SHOCK PROTEIN 90; NUCLEOTIDE;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ASSAY; FUNGAL EXAMINATION; KINETICS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; REACTION TIME; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HSP90 HEAT-SHOCK PROTEINS; KINETICS; PROTEIN STRUCTURE, QUATERNARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 61949212626     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1557     Document Type: Article

References (32)

1. Pearl, L.H. & Prodromou, C. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 75, 271-294 (2006).
2. Richter, K. & Buchner, J. hsp90: twist and fold. Cell 127, 251-253 (2006).
3. Richter, K., Reinstein, J. & Buchner, J. A Grp on the Hsp90 mechanism. Mol. Cell 28, 177-179 (2007).
4. Whitesell, L. & Lindquist, S.L. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer 5, 761-772 (2005).
5. Ali, M.M.U. et al. Crystal structure of an Hsp90-nucleotide-p23/ Sba1 closed chaperone complex. Nature 440, 1013-1017 (2006).
6. Shiau, A.K., Harris, S.F., Southworth, D.R. & Agard, D.A. Structural analysis of E. coli Hsp90 reveals dramatic nucleotide-dependent conformational rearrangements. Cell 127, 329-340 (2006).
7. Brown, M.A., Zhu, L., Schmidt, C. & Tucker, P.W. Hsp90-from signal transduction to cell transformation. Biochem. Biophys. Res. Commun. 363, 241-246 (2007).
8. Siligardi, G. et al. Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J. Biol. Chem. 279, 51989-51998 (2004).
9. Richter, K., Muschler, P., Hainzl, O. & Buchner, J. Coordinated ATP hydrolysis by the Hsp90 dimer. J. Biol. Chem. 276, 33689-33696 (2001).
10. Weikl, T. et al. C-terminal regions of Hsp90 are important for trapping the nucleotide during the ATPase cycle. J. Mol. Biol. 303, 583-592 (2000).
11. Richter, K., Reinstein, J. & Buchner, J. N-terminal residues regulate the catalytic efficiency of the Hsp90 ATPase cycle. J. Biol. Chem. 277, 44905-44910 (2002).
12. Dietz, H., Bornschlogl, T., Heym, R., Konig, F. & Rief, M. Programming protein self assembly with coiled coils. New J. Phys. 9, 424, 1-8 (2007).
13. Bornschlogl, T. & Rief, M. Single-molecule dynamics of mechanical coiled-coil unzipping. Langmuir 24, 1338-1342 (2008).
14. Ali, J.A., Jackson, P.A., Howells, A.J. & Maxwell, A. The 43-kilodalton N-terminal fragment of the DNA gyrase B protein hydrolyzes ATP and binds coumarin drugs. Biochemistry 32, 2717-2724 (1993).
15. Panaretou, B. et al. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 17, 4829-4836 (1998).
16. Ha, T. et al. Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. USA 93, 6264-6268 (1996).
17. Hugel, T. et al. Experimental test of connector rotation during DNA packaging into bacteriophage phi 29 capsids. PLoS Biol. 5, e59 (2007).
18. Cisse, I., Okumus, B., Joo, C. & Ha, T. Fueling protein-DNA interactions inside porous nanocontainers. Proc. Natl. Acad. Sci. USA 104, 12646-12650 (2007).
19. Gebhardt, J.C.M., Clemen, A.E.M., Jaud, J. & Rief, M. Myosin-V is a mechanical ratchet. Proc. Natl. Acad. Sci. USA 103, 8680-8685 (2006).
20. Bron, P. et al. Apo-Hsp90 coexists in two open conformational states in solution. Biol. Cell 100, 413-425 (2008).
21. Krukenberg, K.A., Förster, F., Rice, L.M., Sali, A. & Agard, D.A. Multiple Conformations of E. coli Hsp90 in solution: insights into the conformational dynamics of Hsp90. Structure 16, 755-765 (2008).
22. Bracher, A. & Hartl, F.U. Hsp90 structure: when two ends meet. Nat. Struct. Mol. Biol. 13, 478-480 (2006).
23. Pearl, L.H., Prodromou, C. & Workman, P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J. 410, 439-453 (2008).
24. Richter, K., Reinstein, J. & Buchner, J. N-terminal residues regulate the catalytic efficiency of the Hsp90 ATPase cycle. J. Biol. Chem. 277, 44905-44910 (2002).
25. Sacho, E.J., Kadyrov, F.A., Modrich, P., Kunkel, T.A. & Erie, D.A. Direct visualization of asymmetric adenine nucleotide-induced conformational changes in MutL. Mol. Cell [alpha] 29, 112-121 (2008).
26. Howard, J. Mechanics of Motor Proteins and the Cytoskeleton (Sinauer, Sunderland, MA, 2001).
27. Roy, R., Hohng, S. & Ha, T. A practical guide to single-molecule FRET. Nat. Methods 5, 507-516 (2008).
28. Jackson, S.E. The solution to multiple structures. Structure 16, 659-661 (2008).
29. Wayne, N. & Bolon, D.N. Dimerization of Hsp90 is required for in vivo function: design and analysis of monomers and dimers. J. Biol. Chem. 282, 35386-35395 (2007).
30. Vogelsang, J.R.K. et al. A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes. Angew. Chem. Int. Ed. Engl. 47, 5465-5469 (2008).
31. Lapidus, L.J., Eaton, W.A. & Hofrichter, J. Measuring the rate of intramolecular contact formation in polypeptides. Proc. Natl. Acad. Sci. USA 97, 7220-7225 (2000).
32. Yang, W.Y. & Gruebele, M. Folding at the speed limit. Nature 423, 193-197 (2003).