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PMID: 18462680 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Multiple conformations of E. coli Hsp90 in solution: insights into the conformational dynamics of Hsp90.

Structure (London, England : 1993) ·Vol. 16 ·No. 5 ·2008-05-00 ·Pages 755-65

Krukenberg KA, Förster F, Rice LM, Sali A, Agard DA

Abstract

Hsp90, an essential eukaryotic chaperone, depends upon its intrinsic ATPase activity for function. Crystal structures of the bacterial Hsp90 homolog, HtpG, and the yeast Hsp90 reveal large domain rearrangements between the nucleotide-free and the nucleotide-bound forms. We used small-angle X-ray scattering and recently developed molecular modeling methods to characterize the solution structure of HtpG and demonstrate how it differs from known Hsp90 conformations. In addition to this HtpG conformation, we demonstrate that under physiologically relevant conditions, multiple conformations coexist in equilibrium. In solution, nucleotide-free HtpG adopts a more extended conformation than observed in the crystal, and upon the addition of AMPPNP, HtpG is in equilibrium between this open state and a closed state that is in good agreement with the yeast AMPPNP crystal structure. These studies provide a unique view of Hsp90 conformational dynamics and provide a model for the role of nucleotide in effecting conformational change.

MeSH Terms
Adenylyl Imidodiphosphate/metabolism Dimerization Escherichia coli/chemistry,genetics Escherichia coli Proteins/chemistry,genetics,isolation & purification,metabolism HSP90 Heat-Shock Proteins/chemistry,genetics,isolation & purification,metabolism Models, Molecular Protein Conformation Protein Structure, Tertiary Scattering, Small Angle Solutions X-Ray Diffraction
Chemicals
Escherichia coli Proteins HSP90 Heat-Shock Proteins Solutions Adenylyl Imidodiphosphate
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Krukenberg Kristin A
Graduate Program in Chemistry and Chemical Biology, Department of Biochemistry & Biophysics and the Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, CA 94158, USA.
Förster Friedrich
Rice Luke M
Sali Andrej
Agard David A
References (32)
32 references, click to expand
  1. Disassembly of transcriptional regulatory complexes by molecular chaperones.
    Science. 2002 Jun 21;296(5576):2232-5 PMID: 12077419
  2. Heat-shock protein 90, a chaperone for folding and regulation.
    Cell Mol Life Sci. 2002 Oct;59(10):1640-8 PMID: 12475174
  3. Comparative protein modelling by satisfaction of spatial restraints.
    J Mol Biol. 1993 Dec 5;234(3):779-815 PMID: 8254673
  4. Chaperoning steroid hormone action.
    Trends Endocrinol Metab. 2006 Aug;17(6):229-35 PMID: 16806964
  5. The ATPase cycle of the endoplasmic chaperone Grp94.
    J Biol Chem. 2007 Dec 7;282(49):35612-20 PMID: 17925398
  6. Hsp90: a specialized but essential protein-folding tool.
    J Cell Biol. 2001 Jul 23;154(2):267-73 PMID: 11470816
  7. Biochemical and structural studies of the interaction of Cdc37 with Hsp90.
    J Mol Biol. 2004 Jul 16;340(4):891-907 PMID: 15223329
  8. Determination of domain structure of proteins from X-ray solution scattering.
    Biophys J. 2001 Jun;80(6):2946-53 PMID: 11371467
  9. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone.
    Cell. 2005 Mar 11;120(5):715-27 PMID: 15766533
  10. Structural Analysis of E. coli hsp90 reveals dramatic nucleotide-dependent conformational rearrangements.
    Cell. 2006 Oct 20;127(2):329-40 PMID: 17055434
  11. HSP90 and the chaperoning of cancer.
    Nat Rev Cancer. 2005 Oct;5(10):761-72 PMID: 16175177
  12. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery.
    Exp Biol Med (Maywood). 2003 Feb;228(2):111-33 PMID: 12563018
  13. Molecular chaperones and protein kinase quality control.
    Trends Cell Biol. 2007 Feb;17(2):87-92 PMID: 17184992
  14. Structure and mechanism of the Hsp90 molecular chaperone machinery.
    Annu Rev Biochem. 2006;75:271-94 PMID: 16756493
  15. Structures of GRP94-nucleotide complexes reveal mechanistic differences between the hsp90 chaperones.
    Mol Cell. 2007 Oct 12;28(1):41-56 PMID: 17936703
  16. Statistical potential for assessment and prediction of protein structures.
    Protein Sci. 2006 Nov;15(11):2507-24 PMID: 17075131
  17. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing.
    Biophys J. 1999 Jun;76(6):2879-86 PMID: 10354416
  18. Hsp70 chaperones: cellular functions and molecular mechanism.
    Cell Mol Life Sci. 2005 Mar;62(6):670-84 PMID: 15770419
  19. Structures of the N-terminal and middle domains of E. coli Hsp90 and conformation changes upon ADP binding.
    Structure. 2005 Apr;13(4):579-90 PMID: 15837196
  20. Unliganded and hormone-bound glucocorticoid receptors interact with distinct hydrophobic sites in the Hsp90 C-terminal domain.
    Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18487-92 PMID: 17130446
  21. Progesterone receptor ligand binding pocket flexibility: crystal structures of the norethindrone and mometasone furoate complexes.
    J Med Chem. 2004 Jun 17;47(13):3381-7 PMID: 15189034
  22. Heat shock protein 90.
    Curr Opin Oncol. 2003 Nov;15(6):419-24 PMID: 14624223
  23. Altered states: selectively drugging the Hsp90 cancer chaperone.
    Trends Mol Med. 2004 Feb;10(2):47-51 PMID: 15106614
  24. All-atom empirical potential for molecular modeling and dynamics studies of proteins.
    J Phys Chem B. 1998 Apr 30;102(18):3586-616 PMID: 24889800
  25. Hsp90: chaperoning signal transduction.
    J Cell Physiol. 2001 Sep;188(3):281-90 PMID: 11473354
  26. Heat shock protein 90: the cancer chaperone.
    J Biosci. 2007 Apr;32(3):517-30 PMID: 17536171
  27. GroEL-substrate interactions: molding the fold, or folding the mold?
    Cell. 2000 Jan 21;100(2):193-6 PMID: 10660042
  28. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex.
    Nature. 2006 Apr 20;440(7087):1013-7 PMID: 16625188
  29. Energetics and mechanism of actomyosin adenosine triphosphatase.
    Biochemistry. 1976 Dec 28;15(26):5818-26 PMID: 12793
  30. Pathways of chaperone-mediated protein folding in the cytosol.
    Nat Rev Mol Cell Biol. 2004 Oct;5(10):781-91 PMID: 15459659
  31. Development of purine-scaffold small molecule inhibitors of Hsp90.
    Curr Cancer Drug Targets. 2003 Oct;3(5):371-6 PMID: 14529388
  32. Mechanisms of protein folding.
    Curr Opin Struct Biol. 2001 Feb;11(1):70-82 PMID: 11179895
Article Info
Journal
Structure (London, England : 1993)
Abbr.
Structure
ISSN
0969-2126
Published
2008-05-00
Pages
755-65
Language
English
Region
United States
NLM ID
101087697
PMCID
PMC2600884
Subset
IM
Grants
NCRR NIH HHS · P41 RR001209-286059 · United States
NCRR NIH HHS · P41 RR001209-277810 · United States
NCRR NIH HHS · P41 RR001209-286051 · United States
NCRR NIH HHS · P41 RR001209 · United States
NCRR NIH HHS · P41 RR001209-277826 · United States
Howard Hughes Medical Institute · United States
NEI NIH HHS · PN2 EY016525 · United States
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