Client-Loading Conformation of the Hsp90 Molecular Chaperone Revealed in the Cryo-EM Structure of the Human Hsp90:Hop Complex

Molecular Cell

Volumn 42, Issue 6, 2011, Pages 771-781

  Southworth, Daniel R ^a,b   Agard, David A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; HUMAN; HYDROPHOBICITY; NONHUMAN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATE; CRYOELECTRON MICROSCOPY; DISULFIDES; HOMEODOMAIN PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SURFACE PROPERTIES; TUMOR SUPPRESSOR PROTEINS;

EID: 79959344309     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.04.023     Document Type: Article

References (39)

1. Ali M.M., Roe S.M., Vaughan C.K., Meyer P., Panaretou B., Piper P.W., Prodromou C., Pearl L.H. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 2006, 440:1013-1017.
2. Bose S., Weikl T., Bügl H., Buchner J. Chaperone function of Hsp90-associated proteins. Science 1996, 274:1715-1717.
3. Brinker A., Scheufler C., Von Der Mulbe F., Fleckenstein B., Herrmann C., Jung G., Moarefi I., Hartl F.U. Ligand discrimination by TPR domains. Relevance and selectivity of EEVD-recognition in Hsp70 x Hop x Hsp90 complexes. J. Biol. Chem. 2002, 277:19265-19275.
4. Chen S., Smith D.F. Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. J. Biol. Chem. 1998, 273:35194-35200.
5. Dutta R., Inouye M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 2000, 25:24-28.
6. Fang L., Ricketson D., Getubig L., Darimont B. Unliganded and hormone-bound glucocorticoid receptors interact with distinct hydrophobic sites in the Hsp90 C-terminal domain. Proc. Natl. Acad. Sci. USA 2006, 103:18487-18492.
7. Flom G., Behal R.H., Rosen L., Cole D.G., Johnson J.L. Definition of the minimal fragments of Sti1 required for dimerization, interaction with Hsp70 and Hsp90 and in vivo functions. Biochem. J. 2007, 404:159-167.
8. 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.
9. Harris S.F., Shiau A.K., Agard D.A. The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure 2004, 12:1087-1097.
10. Hernández M.P., Sullivan W.P., Toft D.O. The assembly and intermolecular properties of the hsp70-Hop-hsp90 molecular chaperone complex. J. Biol. Chem. 2002, 277:38294-38304.
11. Holt S.E., Aisner D.L., Baur J., Tesmer V.M., Dy M., Ouellette M., Trager J.B., Morin G.B., Toft D.O., Shay J.W., et al. Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev. 1999, 13:817-826.
12. Johnson B.D., Schumacher R.J., Ross E.D., Toft D.O. Hop modulates Hsp70/Hsp90 interactions in protein folding. J. Biol. Chem. 1998, 273:3679-3686.
13. 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 2008, 16:755-765.
14. Krukenberg K.A., Böttcher U.M., Southworth D.R., Agard D.A. Grp94, the endoplasmic reticulum Hsp90, has a similar solution conformation to cytosolic Hsp90 in the absence of nucleotide. Protein Sci. 2009, 18:1815-1827.
15. Li J., Richter K., Buchner J. Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle. Nat. Struct. Mol. Biol. 2011, 18:61-66.
16. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 1999, 128:82-97.
17. Meyer P., Prodromou C., Hu B., Vaughan C., Roe S.M., Panaretou B., Piper P.W., Pearl L.H. Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions. Mol. Cell 2003, 11:647-658.
18. Mindell J.A., Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 2003, 142:334-347.
19. Nathan D.F., Vos M.H., Lindquist S. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc. Natl. Acad. Sci. USA 1997, 94:12949-12956.
20. Neckers L. Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol. Med. 2002, 8(4, Suppl):S55-S61.
21. Ohi M., Li Y., Cheng Y., Walz T. Negative Staining and Image Classification - Powerful Tools in Modern Electron Microscopy. Biol. Proced. Online 2004, 6:23-34.
22. Onuoha S.C., Coulstock E.T., Grossmann J.G., Jackson S.E. Structural studies on the co-chaperone Hop and its complexes with Hsp90. J. Mol. Biol. 2008, 379:732-744.
23. 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.
24. Picard D. Heat-shock protein 90, a chaperone for folding and regulation. Cell. Mol. Life Sci. 2002, 59:1640-1648.
25. Picard D., Khursheed B., Garabedian M.J., Fortin M.G., Lindquist S., Yamamoto K.R. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 1990, 348:166-168.
26. Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., Pearl L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997, 90:65-75.
27. Prodromou C., Siligardi G., O'Brien R., Woolfson D.N., Regan L., Panaretou B., Ladbury J.E., Piper P.W., Pearl L.H. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J. 1999, 18:754-762.
28. Retzlaff M., Hagn F., Mitschke L., Hessling M., Gugel F., Kessler H., Richter K., Buchner J. Asymmetric activation of the hsp90 dimer by its cochaperone aha1. Mol. Cell 2010, 37:344-354.
29. Richter K., Muschler P., Hainzl O., Reinstein J., Buchner J. Sti1 is a non-competitive inhibitor of the Hsp90 ATPase. Binding prevents the N-terminal dimerization reaction during the atpase cycle. J. Biol. Chem. 2003, 278:10328-10333.
30. Sanchez E.R., Toft D.O., Schlesinger M.J., Pratt W.B. Evidence that the 90-kDa phosphoprotein associated with the untransformed L-cell glucocorticoid receptor is a murine heat shock protein. J. Biol. Chem. 1985, 260:12398-12401.
31. Sato S., Fujita N., Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc. Natl. Acad. Sci. USA 2000, 97:10832-10837.
32. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H., Hartl F.U., Moarefi I. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000, 101:199-210.
33. Schumacher T.N., Mayr L.M., Minor D.L., Milhollen M.A., Burgess M.W., Kim P.S. Identification of D-peptide ligands through mirror-image phage display. Science 1996, 271:1854-1857.
34. 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 2006, 127:329-340.
35. Southworth D.R., Agard D.A. Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle. Mol. Cell 2008, 32:631-640.
36. Street T.O., Lavery L.A., Agard D.A. Substrate binding drives large-scale conformational changes in the Hsp90 molecular chaperone. Mol. Cell 2011, 42:96-105.
37. Van Heel M. Angular reconstitution: a posteriori assignment of projection directions for 3D reconstruction. Ultramicroscopy 1987, 21:111-123.
38. Vaughan C.K., Gohlke U., Sobott F., Good V.M., Ali M.M., Prodromou C., Robinson C.V., Saibil H.R., Pearl L.H. Structure of an Hsp90-Cdc37-Cdk4 complex. Mol. Cell 2006, 23:697-707.
39. Young J.C., Obermann W.M., Hartl F.U. Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90. J. Biol. Chem. 1998, 273:18007-18010.