Hsp70 and Hsp90 of E. coli Directly Interact for Collaboration in Protein Remodeling

Journal of Molecular Biology

Volumn 427, Issue 24, 2015, Pages 3877-3889

  Genest, Olivier ^a,b   Hoskins, Joel R ^a   Kravats, Andrea N ^a   Doyle, Shannon M ^a   Wickner, Sue ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

CbpA; DnaJ; Hsp40; molecular chaperone; protein remodeling

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MUTANT PROTEIN; PROTEIN CBPA; PROTEIN DNAK; UNCLASSIFIED DRUG; DNAK PROTEIN, E COLI; PROTEIN BINDING;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; AMINO ACID SUBSTITUTION; CHEMISTRY; GENETICS; PROTEIN REFOLDING;

AMINO ACID SUBSTITUTION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; PROTEIN BINDING; PROTEIN REFOLDING;

EID: 84948397326     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.10.010     Document Type: Article

References (55)

1. J.L. Johnson Evolution and function of diverse Hsp90 homologs and cochaperone proteins Biochim. Biophys. Acta 1823 2012 607 613
2. M.P. Mayer Gymnastics of molecular chaperones Mol. Cell 39 2010 321 331
3. L.H. Pearl, and C. Prodromou Structure and mechanism of the Hsp90 molecular chaperone machinery Annu. Rev. Biochem. 75 2006 271 294
4. A. Rohl, J. Rohrberg, and J. Buchner The chaperone Hsp90: Changing partners for demanding clients Trends Biochem. Sci. 38 2013 253 262
5. O. Genest, and et al. Uncovering a region of heat shock protein 90 important for client binding in E. coli and chaperone function in yeast Mol. Cell 49 2013 464 473
6. C. Prodromou The "active life" of Hsp90 complexes Biochim. Biophys. Acta 1823 2012 614 623
7. D.R. Southworth, and D.A. Agard Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle Mol. Cell 32 2008 631 640
8. C. Graf, M. Stankiewicz, G. Kramer, and M.P. Mayer Spatially and kinetically resolved changes in the conformational dynamics of the Hsp90 chaperone machine EMBO J. 28 2009 602 613
9. K.A. Krukenberg, F. Forster, L.M. Rice, A. Sali, and D.A. Agard Multiple conformations of E. coli Hsp90 in solution: Insights into the conformational dynamics of Hsp90 Structure 16 2008 755 765
10. K.A. Krukenberg, D.R. Southworth, T.O. Street, and D.A. Agard 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. 390 2009 278 291
11. K.A. Krukenberg, T.O. Street, L.A. Lavery, and D.A. Agard Conformational dynamics of the molecular chaperone Hsp90 Q. Rev. Biophys. 44 2011 229 255
12. C. Ratzke, M. Mickler, B. Hellenkamp, J. Buchner, and T. Hugel Dynamics of heat shock protein 90 C-terminal dimerization is an important part of its conformational cycle Proc. Natl. Acad. Sci. U. S. A. 107 2010 16101 16106
13. A.K. Shiau, S.F. Harris, D.R. Southworth, and D.A. Agard Structural analysis of E. coli hsp90 reveals dramatic nucleotide-dependent conformational rearrangements Cell 127 2006 329 340
14. M. Taipale, D.F. Jarosz, and S. Lindquist HSP90 at the hub of protein homeostasis: Emerging mechanistic insights Nat. Rev. Mol. Cell Biol. 11 2010 515 528
15. M.M. Ali, and et al. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex Nature 440 2006 1013 1017
16. Y. Motojima-Miyazaki, M. Yoshida, and F. Motojima Ribosomal protein L2 associates with E. coli HtpG and activates its ATPase activity Biochem. Biophys. Res. Commun. 400 2010 241 245
17. T.O. Street, L.A. Lavery, and D.A. Agard Substrate binding drives large-scale conformational changes in the Hsp90 molecular chaperone Mol. Cell 42 2011 96 105
18. H. Wegele, L. Muller, and J. Buchner Hsp70 and Hsp90 - A relay team for protein folding Rev. Physiol. Biochem. Pharmacol. 151 2004 1 44
19. H. Wegele, S.K. Wandinger, A.B. Schmid, J. Reinstein, and J. Buchner Substrate transfer from the chaperone Hsp70 to Hsp90 J. Mol. Biol. 356 2006 802 811
20. J.C. Bardwell, and E.A. Craig Eukaryotic Mr 83,000 heat shock protein has a homologue in Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 84 1987 5177 5181
21. J.G. Thomas, and F. Baneyx ClpB and HtpG facilitate de novo protein folding in stressed Escherichia coli cells Mol. Microbiol. 36 2000 1360 1370
22. I. Yosef, M.G. Goren, R. Kiro, R. Edgar, and U. Qimron 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. U. S. A. 108 2011 20136 20141
23. M.O. Press, and et al. Genome-scale co-evolutionary inference identifies functions and clients of bacterial Hsp90 PLoS Genet. 9 2013 e1003631
24. J.P. Grenert, B.D. Johnson, and D.O. Toft The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes J. Biol. Chem. 274 1999 17525 17533
25. B.D. Johnson, R.J. Schumacher, E.D. Ross, and D.O. Toft Hop modulates Hsp70/Hsp90 interactions in protein folding J. Biol. Chem. 273 1998 3679 3686
26. O. Genest, J.R. Hoskins, J.L. Camberg, S.M. Doyle, and S. Wickner Heat shock protein 90 from Escherichia coli collaborates with the DnaK chaperone system in client protein remodeling Proc. Natl. Acad. Sci. U. S. A. 108 2011 8206 8211
27. P.C. Echeverria, A. Bernthaler, P. Dupuis, B. Mayer, and D. Picard An interaction network predicted from public data as a discovery tool: Application to the Hsp90 molecular chaperone machine PLoS One 6 2011 e26044
28. S. Alvira, and et al. Structural characterization of the substrate transfer mechanism in Hsp70/Hsp90 folding machinery mediated by Hop Nat. Commun. 5 2014 5484
29. E. Kirschke, D. Goswami, D. Southworth, P.R. Griffin, and D.A. Agard Glucocorticoid receptor function regulated by coordinated action of the Hsp90 and Hsp70 chaperone cycles Cell 157 2014 1685 1697
30. N. Morgner, and et al. Hsp70 forms antiparallel dimers stabilized by post-translational modifications to position clients for transfer to Hsp90 Cell Rep. 11 2015 759 769
31. G. Banumathy, V. Singh, S.R. Pavithra, and U. Tatu Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes J. Biol. Chem. 278 2003 18336 18345
32. D.G. Freitag, P.M. Ouimet, T.L. Girvitz, and M. Kapoor Heat shock protein 80 of Neurospora crassa, a cytosolic molecular chaperone of the eukaryotic stress 90 family, interacts directly with heat shock protein 70 Biochemistry 36 1997 10221 10229
33. P.J. Murphy, K.C. Kanelakis, M.D. Galigniana, Y. Morishima, and W.B. Pratt Stoichiometry, abundance, and functional significance of the hsp90/hsp70-based multiprotein chaperone machinery in reticulocyte lysate J. Biol. Chem. 276 2001 30092 30098
34. H. Nakamoto, and et al. Physical interaction between bacterial heat shock protein (Hsp) 90 and Hsp70 chaperones mediates their cooperative action to refold denatured proteins J. Biol. Chem. 289 2014 6110 6119
35. T. Laufen, and et al. Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones Proc. Natl. Acad. Sci. U. S. A. 96 1999 5452 5457
36. S. Rudiger, M.P. Mayer, J. Schneider-Mergener, and B. Bukau Modulation of substrate specificity of the DnaK chaperone by alteration of a hydrophobic arch J. Mol. Biol. 304 2000 245 251
37. T.K. Barthel, J. Zhang, and G.C. Walker ATPase-defective derivatives of Escherichia coli DnaK that behave differently with respect to ATP-induced conformational change and peptide release J. Bacteriol. 183 2001 5482 5490
38. B. Panaretou, and et al. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo EMBO J. 17 1998 4829 4836
39. S.F. Harris, A.K. Shiau, and D.A. Agard The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site Structure 12 2004 1087 1097
40. A. Rohl, and et al. Hsp90 regulates the dynamics of its cochaperone Sti1 and the transfer of Hsp70 between modules Nat. Commun. 6 2015 6655
41. A.B. Schmid, and et al. The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop EMBO J. 31 2012 1506 1517
42. B. Bukau, and A.L. Horwich The Hsp70 and Hsp60 chaperone machines Cell 92 1998 351 366
43. S.M. Doyle, O. Genest, and S. Wickner Protein rescue from aggregates by powerful molecular chaperone machines Nat. Rev. Mol. Cell Biol. 14 2013 617 629
44. S.M. Doyle, J.R. Hoskins, and S. Wickner Collaboration between the ClpB AAA + remodeling protein and the DnaK chaperone system Proc. Natl. Acad. Sci. U. S. A. 104 2007 11138 11144
45. J.R. Glover, and S. Lindquist Hsp104, Hsp70, and Hsp40: A novel chaperone system that rescues previously aggregated proteins Cell 94 1998 73 82
46. M. Carroni, and et al. Head-to-tail interactions of the coiled-coil domains regulate ClpB activity and cooperation with Hsp70 in protein disaggregation Elife 3 2014 e02481
47. S.M. Doyle, and et al. Interplay between E. coli DnaK, ClpB and GrpE during protein disaggregation J. Mol. Biol. 427 2015 312 327
48. J. Lee, and et al. Heat shock protein (Hsp) 70 is an activator of the Hsp104 motor Proc. Natl. Acad. Sci. U. S. A. 110 2013 8513 8518
49. R. Rosenzweig, S. Moradi, A. Zarrine-Afsar, J.R. Glover, and L.E. Kay Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction Science 339 2013 1080 1083
50. B. Sielaff, and F.T. Tsai The M-domain controls Hsp104 protein remodeling activity in an Hsp70/Hsp40-dependent manner J. Mol. Biol. 402 2010 30 37
51. 2 + in RepA monomerization by DnaJ and DnaK J. Biol. Chem. 268 1993 25296 25301
52. M. Miot, and et al. Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation Proc. Natl. Acad. Sci. U. S. A. 108 2011 6915 6920
53. C. Ueguchi, M. Kakeda, H. Yamada, and T. Mizuno An analogue of the DnaJ molecular chaperone in Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 91 1994 1054 1058
54. J.R. Hoskins, M. Pak, M.R. Maurizi, and S. Wickner The role of the ClpA chaperone in proteolysis by ClpAP Proc. Natl. Acad. Sci. U. S. A. 95 1998 12135 12140
55. G. Karimova, J. Pidoux, A. Ullmann, and D. Ladant A bacterial two-hybrid system based on a reconstituted signal transduction pathway Proc. Natl. Acad. Sci. U. S. A. 95 1998 5752 5756