Mechanistic Asymmetry in Hsp90 Dimers

Journal of Molecular Biology

Volumn 427, Issue 18, 2015, Pages 2904-2911

  Flynn, Julia M ^a   Mishra, Parul ^a   Bolon, Daniel N A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

ATPase; chaperone mechanism; co chaperone; kinase; steroid hormone receptor

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLIN DEPENDENT KINASE 4; DIMER; HEAT SHOCK PROTEIN 90; MONOMER; PROTEIN P23; PROTEIN P53; TAU PROTEIN; CHAPERONE; NUCLEOTIDE; PROTEIN BINDING;

BINDING SITE; CONFORMATIONAL TRANSITION; ENZYME STRUCTURE; EVOLUTIONARY ADAPTATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROLYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; RADIATION SCATTERING; REVIEW; STOICHIOMETRY; ULTRACENTRIFUGATION; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; MOLECULAR CHAPERONES; MUTATION; NUCLEOTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

EID: 84941185179     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.03.017     Document Type: Review

References (61)

1. Y. Miyata, H. Nakamoto, and L. Neckers The therapeutic target Hsp90 and cancer hallmarks Curr Pharm Des 19 2013 347 365
2. S. Lindquist Protein folding sculpting evolutionary change Cold Spring Harbor Symp Quant Biol 74 2009 103 108
3. S.L. McKenzie, S. Henikoff, and M. Meselson Localization of RNA from heat-induced polysomes at puff sites in Drosophila melanogaster Proc Natl Acad Sci U S A 72 1975 1117 1121
4. M. Taipale, I. Krykbaeva, M. Koeva, C. Kayatekin, K.D. Westover, G.I. Karras, and et al. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition Cell 150 2012 987 1001
5. N. Wayne, P. Mishra, and D.N. Bolon Hsp90 and client protein maturation Methods Mol Biol 787 2011 33 44
6. L. Whitesell, E.G. Mimnaugh, B. De Costa, C.E. Myers, and L.M. Neckers Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation Proc Natl Acad Sci U S A 91 1994 8324 8328
7. T. Taldone, S.O. Ochiana, P.D. Patel, and G. Chiosis Selective targeting of the stress chaperone as a therapeutic strategy Trends Pharmacol Sci 35 2014 592 603
8. A. Veri, and L.E. Cowen Progress and prospects for targeting Hsp90 to treat fungal infections Parasitology 141 2014 1127 1137
9. N. Rohner, D.F. Jarosz, J.E. Kowalko, M. Yoshizawa, W.R. Jeffery, R.L. Borowsky, and et al. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish Science 342 2013 1372 1375
10. S.L. Rutherford, and S. Lindquist Hsp90 as a capacitor for morphological evolution Nature 396 1998 336 342
11. R.T. Hietpas, C. Bank, J.D. Jensen, and D.N. Bolon Shifting fitness landscapes in response to altered environments Evolution 67 2013 3512 3522
12. W.B. Pratt, and D.O. Toft Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery Exp Biol Med (Maywood) 228 2003 111 133
13. Y.E. Kim, M.S. Hipp, A. Bracher, M. Hayer-Hartl, and F.U. Hartl Molecular chaperone functions in protein folding and proteostasis Annu Rev Biochem 82 2013 323 355
14. J.C. Young, V.R. Agashe, K. Siegers, and F.U. Hartl Pathways of chaperone-mediated protein folding in the cytosol Nat Rev Mol Cell Biol 5 2004 781 791
15. 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
16. Y. Kimura, S.L. Rutherford, Y. Miyata, I. Yahara, B.C. Freeman, L. Yue, and et al. Cdc37 is a molecular chaperone with specific functions in signal transduction Genes Dev 11 1997 1775 1785
17. N. Wayne, and D.N. Bolon Charge-rich regions modulate the anti-aggregation activity of Hsp90 J Mol Biol 401 2010 931 939
18. N.W. Pursell, P. Mishra, and D.N. Bolon Solubility-promoting function of Hsp90 contributes to client maturation and robust cell growth Eukaryot Cell 11 2012 1033 1041
19. B. Panaretou, C. Prodromou, S.M. Roe, R. O'Brien, J.E. Ladbury, P.W. Piper, 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
20. N. Wayne, and D.N. Bolon Dimerization of Hsp90 is required for in vivo function. Design and analysis of monomers and dimers J Biol Chem 282 2007 35386 35395
21. R. Zhao, M. Davey, Y.C. Hsu, P. Kaplanek, A. Tong, A.B. Parsons, and et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone Cell 120 2005 715 727
22. M.B. Cox, and J.L. Johnson The role of p23, Hop, immunophilins, and other co-chaperones in regulating Hsp90 function Methods Mol Biol 787 2011 45 66
23. S. Bose, T. Weikl, H. Bugl, and J. Buchner Chaperone function of Hsp90-associated proteins Science 274 1996 1715 1717
24. A.J. McClellan, M.D. Scott, and J. Frydman Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways Cell 121 2005 739 748
25. W. Xu, M. Marcu, X. Yuan, E. Mimnaugh, C. Patterson, and L. Neckers Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu Proc Natl Acad Sci U S A 99 2002 12847 12852
26. P. Mishra, and D.N. Bolon Designed Hsp90 heterodimers reveal an asymmetric ATPase-driven mechanism in vivo Mol Cell 53 2014 344 350
27. L.A. Lavery, J.R. Partridge, T.A. Ramelot, D. Elnatan, M.A. Kennedy, and D.A. Agard Structural asymmetry in the closed state of mitochondrial Hsp90 (TRAP1) supports a two-step ATP hydrolysis mechanism Mol Cell 53 2014 330 343
28. 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
29. G.E. Karagoz, A.M. Duarte, E. Akoury, H. Ippel, J. Biernat, T. Moran Luengo, and et al. Hsp90-Tau complex reveals molecular basis for specificity in chaperone action Cell 156 2014 963 974
30. S. Alvira, J. Cuellar, A. Rohl, S. Yamamoto, H. Itoh, C. Alfonso, and et al. Structural characterization of the substrate transfer mechanism in Hsp70/Hsp90 folding machinery mediated by Hop Nat Commun 5 2014 5484
31. O.R. Lorenz, L. Freiburger, D.A. Rutz, M. Krause, B.K. Zierer, S. Alvira, and et al. Modulation of the Hsp90 chaperone cycle by a stringent client protein Mol Cell 53 2014 941 953
32. C. Prodromou, S.M. Roe, R. O'Brien, J.E. Ladbury, P.W. Piper, and L.H. Pearl Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone Cell 90 1997 65 75
33. P. Meyer, C. Prodromou, B. Hu, C. Vaughan, S.M. Roe, B. Panaretou, and et al. Structural and functional analysis of the middle segment of hsp90: implications for ATP hydrolysis and client protein and cochaperone interactions Mol Cell 11 2003 647 658
34. 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
35. 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
36. M.M. Ali, S.M. Roe, C.K. Vaughan, P. Meyer, B. Panaretou, P.W. Piper, and et al. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex Nature 440 2006 1013 1017
37. 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
38. L. Pullen, and D.N. Bolon Enforced N-domain proximity stimulates Hsp90 ATPase activity and is compatible with function in vivo J Biol Chem 286 2011 11091 11098
39. C.K. Vaughan, U. Gohlke, F. Sobott, V.M. Good, M.M. Ali, C. Prodromou, and et al. Structure of an Hsp90-Cdc37-Cdk4 complex Mol Cell 23 2006 697 707
40. 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
41. O. Genest, M. Reidy, T.O. Street, J.R. Hoskins, J.L. Camberg, D.A. Agard, 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
42. F. Hagn, S. Lagleder, M. Retzlaff, J. Rohrberg, O. Demmer, K. Richter, and et al. Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53 Nat Struct Mol Biol 18 2011 1086 1093
43. L.C. Scherrer, D. Picard, E. Massa, J.M. Harmon, S.S. Simons, K.R. Yamamoto, and et al. Evidence that the hormone binding domain of steroid receptors confers hormonal control on chimeric proteins by determining their hormone-regulated binding to heat-shock protein 90 Biochemistry 32 1993 5381 5386
44. Y. Morishima, K.C. Kanelakis, A.M. Silverstein, K.D. Dittmar, L. Estrada, and W.B. Pratt The Hsp organizer protein hop enhances the rate of but is not essential for glucocorticoid receptor folding by the multiprotein Hsp90-based chaperone system J Biol Chem 275 2000 6894 6900
45. Y. Morishima, P.J. Murphy, D.P. Li, E.R. Sanchez, and W.B. Pratt Stepwise assembly of a glucocorticoid receptor·hsp90 heterocomplex resolves two sequential ATP-dependent events involving first hsp70 and then hsp90 in opening of the steroid binding pocket J Biol Chem 275 2000 18054 18060
46. D.R. Southworth, and D.A. Agard Client-loading conformation of the Hsp90 molecular chaperone revealed in the cryo-EM structure of the human Hsp90:Hop complex Mol Cell 42 2011 771 781
47. I.O. Ebong, N. Morgner, M. Zhou, M.A. Saraiva, S. Daturpalli, S.E. Jackson, and et al. Heterogeneity and dynamics in the assembly of the heat shock protein 90 chaperone complexes Proc Natl Acad Sci U S A 108 2011 17939 17944
48. J. Li, K. Richter, and J. Buchner Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle Nat Struct Mol Biol 18 2011 61 66
49. K. Richter, S. Walter, and J. Buchner The Co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle J Mol Biol 342 2004 1403 1413
50. G.E. Karagoz, A.M. Duarte, H. Ippel, C. Uetrecht, T. Sinnige, M. van Rosmalen, and et al. N-terminal domain of human Hsp90 triggers binding to the cochaperone p23 Proc Natl Acad Sci U S A 108 2011 580 585
51. C. Ratzke, B. Hellenkamp, and T. Hugel Four-colour FRET reveals directionality in the Hsp90 multicomponent machinery Nat Commun 5 2014 4192
52. S.M. Roe, M.M. Ali, P. Meyer, C.K. Vaughan, B. Panaretou, P. Piper, and et al. The Mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50(cdc37) Cell 116 2004 87 98
53. M. Retzlaff, F. Hagn, L. Mitschke, M. Hessling, F. Gugel, H. Kessler, and et al. Asymmetric activation of the hsp90 dimer by its cochaperone aha1 Mol Cell 37 2010 344 354
54. M. Hessling, K. Richter, and J. Buchner Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90 Nat Struct Mol Biol 16 2009 287 293
55. A.V. Koulov, P. LaPointe, B. Lu, A. Razvi, J. Coppinger, M.Q. Dong, and et al. Biological and structural basis for Aha1 regulation of Hsp90 ATPase activity in maintaining proteostasis in the human disease cystic fibrosis Mol Biol Cell 21 2010 871 884
56. G.P. Lotz, H. Lin, A. Harst, and W.M. Obermann Aha1 binds to the middle domain of Hsp90, contributes to client protein activation, and stimulates the ATPase activity of the molecular chaperone J Biol Chem 278 2003 17228 17235
57. M. Mollapour, D. Bourboulia, K. Beebe, M.R. Woodford, S. Polier, A. Hoang, and et al. Asymmetric Hsp90 N domain SUMOylation recruits Aha1 and ATP-competitive inhibitors Mol Cell 53 2014 317 329
58. N. Wayne, Y. Lai, L. Pullen, and D.N. Bolon Modular control of cross-oligomerization: analysis of superstabilized Hsp90 homodimers in vivo J Biol Chem 285 2010 234 241
59. D.E. Dollins, J.J. Warren, R.M. Immormino, and D.T. Gewirth Structures of GRP94-nucleotide complexes reveal mechanistic differences between the hsp90 chaperones Mol Cell 28 2007 41 56
60. P.D. Patel, P. Yan, P.M. Seidler, H.J. Patel, W. Sun, C. Yang, and et al. Paralog-selective Hsp90 inhibitors define tumor-specific regulation of HER2 Nat Chem Biol 9 2013 677 684
61. L. Neckers, and J.B. Trepel Stressing the development of small molecules targeting HSP90 Clin Cancer Res 20 2014 275 277