Uncovering a Region of Heat Shock Protein 90 Important for Client Binding in E. coli and Chaperone Function in Yeast

Molecular Cell

Volumn 49, Issue 3, 2013, Pages 464-473

  Genest, Olivier ^a   Reidy, Michael ^b   Street, Timothy O ^c   Hoskins, Joel R ^a   Camberg, Jodi L ^a   Agard, David A ^c,d   Masison, Daniel C ^b   Wickner, Sue ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 90; MUTANT PROTEIN;

ARTICLE; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; YEAST;

AMINO ACID SEQUENCE; AMINO ACIDS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HSP90 HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS);

EID: 84873420281     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.11.017     Document Type: Article

References (47)

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. Arifuzzaman M., Maeda M., Itoh A., Nishikata K., Takita C., Saito R., Ara T., Nakahigashi K., Huang H.C., Hirai A., et al. Large-scale identification of protein-protein interaction of Escherichia coli K-12. Genome Res. 2006, 16:686-691.
3. Bardwell J.C., Craig E.A. Ancient heat shock gene is dispensable. J. Bacteriol. 1988, 170:2977-2983.
4. Bohen S.P., Yamamoto K.R. Isolation of Hsp90 mutants by screening for decreased steroid receptor function. Proc. Natl. Acad. Sci. USA 1993, 90:11424-11428.
5. Butland G., Peregrín-Alvarez J.M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D., Beattie B., Krogan N., et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005, 433:531-537.
6. Didenko T., Duarte A.M., Karagöz G.E., Rüdiger S.G. Hsp90 structure and function studied by NMR spectroscopy. Biochim. Biophys. Acta 2012, 1823:636-647.
7. 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.
8. Genest O., Hoskins J.R., Camberg J.L., Doyle S.M., Wickner S. Heat shock protein 90 from Escherichia coli collaborates with the DnaK chaperone system in client protein remodeling. Proc. Natl. Acad. Sci. USA 2011, 108:8206-8211.
9. Graf C., Stankiewicz M., Kramer G., Mayer M.P. Spatially and kinetically resolved changes in the conformational dynamics of the Hsp90 chaperone machine. EMBO J. 2009, 28:602-613.
10. Hagn F., Lagleder S., Retzlaff M., Rohrberg J., Demmer O., Richter K., Buchner J., Kessler H. Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53. Nat. Struct. Mol. Biol. 2011, 18:1086-1093.
11. 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.
12. Hawle P., Siepmann M., Harst A., Siderius M., Reusch H.P., Obermann W.M. The middle domain of Hsp90 acts as a discriminator between different types of client proteins. Mol. Cell. Biol. 2006, 26:8385-8395.
13. Johnson J.L. Evolution and function of diverse Hsp90 homologs and cochaperone proteins. Biochim. Biophys. Acta 2012, 1823:607-613.
14. Jones G., Song Y., Chung S., Masison D.C. Propagation of Saccharomyces cerevisiae [PSI+] prion is impaired by factors that regulate Hsp70 substrate binding. Mol. Cell. Biol. 2004, 24:3928-3937.
15. Jung G., Masison D.C. Guanidine hydrochloride inhibits Hsp104 activity in vivo: a possible explanation for its effect in curing yeast prions. Curr. Microbiol. 2001, 43:7-10.
16. 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.
17. Krukenberg K.A., Southworth D.R., Street T.O., Agard D.A. pH-dependent conformational changes in bacterial Hsp90 reveal a Grp94-like conformation at pH 6 that is highly active in suppression of citrate synthase aggregation. J. Mol. Biol. 2009, 390:278-291.
18. Krukenberg K.A., Street T.O., Lavery L.A., Agard D.A. Conformational dynamics of the molecular chaperone Hsp90. Q. Rev. Biophys. 2011, 44:229-255.
19. Li J., Soroka J., Buchner J. The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim. Biophys. Acta 2012, 1823:624-635.
20. Louvion J.F., Warth R., Picard D. Two eukaryote-specific regions of Hsp82 are dispensable for its viability and signal transduction functions in yeast. Proc. Natl. Acad. Sci. USA 1996, 93:13937-13942.
21. Louvion J.F., Abbas-Terki T., Picard D. Hsp90 is required for pheromone signaling in yeast. Mol. Biol. Cell 1998, 9:3071-3083.
22. McLaughlin S.H., Smith H.W., Jackson S.E. Stimulation of the weak ATPase activity of human hsp90 by a client protein. J. Mol. Biol. 2002, 315:787-798.
23. 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.
24. Miot M., Reidy M., Doyle S.M., Hoskins J.R., Johnston D.M., Genest O., Vitery M.C., Masison D.C., Wickner S. Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation. Proc. Natl. Acad. Sci. USA 2011, 108:6915-6920.
25. Mollapour M., Tsutsumi S., Donnelly A.C., Beebe K., Tokita M.J., Lee M.J., Lee S., Morra G., Bourboulia D., Scroggins B.T., et al. Swe1Wee1-dependent tyrosine phosphorylation of Hsp90 regulates distinct facets of chaperone function. Mol. Cell 2010, 37:333-343.
26. Motojima-Miyazaki Y., Yoshida M., Motojima F. Ribosomal protein L2 associates with E. coli HtpG and activates its ATPase activity. Biochem. Biophys. Res. Commun. 2010, 400:241-245.
27. Nathan D.F., Lindquist S. Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Mol. Cell. Biol. 1995, 15:3917-3925.
28. Neidhardt F.C., VanBogelen R.A., Vaughn V. The genetics and regulation of heat-shock proteins. Annu. Rev. Genet. 1984, 18:295-329.
29. Panaretou B., Siligardi G., Meyer P., Maloney A., Sullivan J.K., Singh S., Millson S.H., Clarke P.A., Naaby-Hansen S., Stein R., et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 2002, 10:1307-1318.
30. Park S.J., Borin B.N., Martinez-Yamout M.A., Dyson H.J. The client protein p53 adopts a molten globule-like state in the presence of Hsp90. Nat. Struct. Mol. Biol. 2011, 18:537-541.
31. Picard D. Chaperoning steroid hormone action. Trends Endocrinol. Metab. 2006, 17:229-235.
32. 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.
33. Prodromou C., Panaretou B., Chohan S., Siligardi G., O'Brien R., Ladbury J.E., Roe S.M., Piper P.W., Pearl L.H. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J. 2000, 19:4383-4392.
34. Ratzke C., Mickler M., Hellenkamp B., Buchner J., Hugel T. Dynamics of heat shock protein 90 C-terminal dimerization is an important part of its conformational cycle. Proc. Natl. Acad. Sci. USA 2010, 107:16101-16106.
35. Retzlaff M., Stahl M., Eberl H.C., Lagleder S., Beck J., Kessler H., Buchner J. Hsp90 is regulated by a switch point in the C-terminal domain. EMBO Rep. 2009, 10:1147-1153.
36. 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.
37. Skowyra D., Wickner S. The interplay of the GrpE heat shock protein and Mg2+ in RepA monomerization by DnaJ and DnaK. J. Biol. Chem. 1993, 268:25296-25301.
38. 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.
39. 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.
40. Street T.O., Lavery L.A., Verba K.A., Lee C.T., Mayer M.P., Agard D.A. Cross-monomer substrate contacts reposition the Hsp90 N-terminal domain and prime the chaperone activity. J. Mol. Biol. 2012, 415:3-15.
41. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
42. Thomas J.G., Baneyx F. ClpB and HtpG facilitate de novo protein folding in stressed Escherichia coli cells. Mol. Microbiol. 2000, 36:1360-1370.
43. Ueguchi C., Kakeda M., Yamada H., Mizuno T. An analogue of the DnaJ molecular chaperone in Escherichia coli. Proc. Natl. Acad. Sci. USA 1994, 91:1054-1058.
44. 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.
45. Wandinger S.K., Richter K., Buchner J. The Hsp90 chaperone machinery. J. Biol. Chem. 2008, 283:18473-18477.
46. Wu S., Hong F., Gewirth D., Guo B., Liu B., Li Z. The molecular chaperone gp96/GRP94 interacts with Toll-like receptors and integrins via its C-terminal hydrophobic domain. J. Biol. Chem. 2012, 287:6735-6742.
47. Yosef I., Goren M.G., Kiro R., Edgar R., Qimron U. High-temperature protein G is essential for activity of the Escherichia coli clustered regularly interspaced short palindromic repeats (CRISPR)/Cas system. Proc. Natl. Acad. Sci. USA 2011, 108:20136-20141.