Hsp90 interaction with clients

Trends in Biochemical Sciences

Volumn 40, Issue 2, 2015, Pages 117-125

  Karagöz, G Elif ^a   Rüdiger, Stefan G D ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Alzheimer disease; Heat shock proteins; Intrinsically disordered proteins; Molecular chaperones; Protein folding; Protein protein interactions

Indexed keywords

CHAPERONE; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; TAU PROTEIN; HEAT SHOCK PROTEIN 72; INTRINSICALLY DISORDERED PROTEIN; LIGAND; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; ENZYME SPECIFICITY; HUMAN; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SEQUENCE HOMOLOGY; SUMOYLATION; UPREGULATION; ALZHEIMER DISEASE; CHEMISTRY; GENETICS; METABOLISM; PATHOLOGY;

ALZHEIMER DISEASE; HSP72 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; LIGANDS; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION MAPS; SUBSTRATE SPECIFICITY;

EID: 84921610700     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2014.12.002     Document Type: Review

References (87)

1. Daggett V., Fersht A. The present view of the mechanism of protein folding. Nat. Rev. Mol. Cell Biol. 2003, 4:497-502.
2. Winkler J., et al. Chaperone networks in protein disaggregation and prion propagation. J. Struct. Biol. 2012, 179:152-160.
3. Saibil H. Chaperone machines for protein folding, unfolding and disaggregation. Nat. Rev. Mol. Cell Biol. 2013, 14:630-642.
4. Kim Y.E., et al. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 2013, 82:323-355.
5. Mayer M.P. Gymnastics of molecular chaperones. Mol. Cell 2010, 39:321-331.
6. Bukau B., et al. Molecular chaperones and protein quality control. Cell 2006, 125:443-451.
7. Clare D.K., Saibil H.R. ATP-driven molecular chaperone machines. Biopolymers 2013, 99:846-859.
8. Taipale M., et al. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
9. Ritossa F. A new puffing pattern induced by temperature shock and DNP in drosophila. Experientia 1962, 18:571-573.
10. Mayer M.P. Hsp70 chaperone dynamics and molecular mechanism. Trends Biochem. Sci. 2013, 38:507-514.
11. Rüdiger S., et al. Interaction of Hsp70 chaperones with substrates. Nat. Struct. Biol. 1997, 4:342-349.
12. Pearl L.H., Prodromou C. Structure and mechanism of the hsp90 molecular chaperone machinery. Annu. Rev. Biochem. 2006, 75:271-294.
13. Vaughan C.K., et al. Understanding of the Hsp90 molecular chaperone reaches new heights. Nat. Struct. Mol. Biol. 2010, 17:1400-1404.
14. Harris S.F., et al. The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure (Camb.) 2004, 12:1087-1097.
15. Karagöz G.E., et al. Hsp90-Tau complex reveals molecular basis for specificity in chaperone action. Cell 2014, 156:963-974.
16. Shiau A.K., et al. Structural analysis of E. coli hsp90 reveals dramatic nucleotide-dependent conformational rearrangements. Cell 2006, 127:329-340.
17. Meyer P., et al. 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. Prodromou C., et al. A molecular clamp in the crystal structure of the N-terminal domain of the yeast Hsp90 chaperone. Nat. Struct. Biol. 1997, 4:477-482.
19. Lavery L.A., et al. Structural asymmetry in the closed state of mitochondrial Hsp90 (TRAP1) supports a two-step ATP hydrolysis mechanism. Mol. Cell 2014, 53:330-343.
20. Dollins D.E., et al. Structures of GRP94-nucleotide complexes reveal mechanistic differences between the hsp90 chaperones. Mol. Cell 2007, 28:41-56.
21. Ali M.M.U., et al. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 2006, 440:1013-1017.
22. Orlova E.V., Saibil H.R. Structural analysis of macromolecular assemblies by electron microscopy. Chem. Rev. 2011, 111:7710-7748.
23. Wüthrich K. NMR studies of structure and function of biological macromolecules (Nobel lecture). Angew. Chem. Int. Ed. 2003, 42:3340-3363.
24. Didenko T., et al. Hsp90 structure and function studied by NMR spectroscopy. Biochim. Biophys. Acta 2012, 1823:636-647.
25. Richter K., Buchner J. Hsp90: chaperoning signal transduction. J. Cell Physiol. 2001, 188:281-290.
26. Pratt W.B., Toft D.O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 1997, 18:306-360.
27. Dou F., et al. Chaperones increase association of tau protein with microtubules. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:721-726.
28. Blagosklonny M.V., et al. Geldanamycin selectively destabilizes and conformationally alters mutated p53. Oncogene 1995, 11:933-939.
29. Loo M.A., et al. Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J. 1998, 17:6879-6887.
30. Vaughan C.K., et al. Structure of an Hsp90-Cdc37-Cdk4 complex. Mol. Cell 2006, 23:697-707.
31. Taipale M., et al. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 2012, 150:987-1001.
32. Lorenz O.R., et al. Modulation of the Hsp90 chaperone cycle by a stringent client protein. Mol. Cell 2014, 53:941-953.
33. Blair L.J., et al. Targeting Hsp90 and its co-chaperones to treat Alzheimer's disease. Expert Opin. Ther. Targets 2014, 18:1219-1232.
34. Mandelkow E.M., Mandelkow E. Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb. Perspect. Med. 2012, 2:a006247.
35. Mandelkow E., et al. Tau - a natively unfolded protein that aggregates in Alzheimer disease. FEBS J. 2008, 275:27.
36. Ludolph A.C., et al. Tauopathies with parkinsonism: clinical spectrum, neuropathologic basis, biological markers, and treatment options. Eur. J. Neurol. 2009, 16:297-309.
37. Dickey C.A., et al. The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J. Clin. Invest. 2007, 117:648-658.
38. Tugarinov V., Kay L.E. Methyl groups as probes of structure and dynamics in NMR studies of high-molecular-weight proteins. Chembiochem 2005, 6:1567-1577.
39. Tugarinov V., Kay L.E. An isotope labeling strategy for methyl TROSY spectroscopy. J. Biomol. NMR 2004, 28:165-172.
40. Karagöz G.E., et al. N-terminal domain of human Hsp90 triggers binding to the cochaperone p23. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:580-585.
41. Saibil H.R., et al. Structure and allostery of the chaperonin GroEL. J. Mol. Biol. 2013, 425:1476-1487.
42. Zuiderweg E.R., et al. Allostery in the Hsp70 chaperone proteins. Top. Curr. Chem. 2013, 328:99-153.
43. Tompa P. Intrinsically unstructured proteins. Trends Biochem. Sci. 2002, 27:527-533.
44. Mukrasch M.D., et al. Structural polymorphism of 441-residue Tau at single residue resolution. PLoS Biol. 2009, 7:399-414.
45. van der Lee R., et al. Classification of intrinsically disordered regions and proteins. Chem. Rev. 2014, 114:6589-6631.
46. Uversky V.N. The triple power of D(3): protein intrinsic disorder in degenerative diseases. Front. Biosci. 2014, 19:181-258.
47. Oldfield C.J., Dunker A.K. Intrinsically disordered proteins and intrinsically disordered protein regions. Annu. Rev. Biochem. 2014, 83:553-584.
48. McLaughlin S.H., Jackson S.E. Folding and stability of the ligand-binding domain of the glucocorticoid receptor. Protein Sci. 2002, 11:1926-1936.
49. Sanchez E.R., et al. Relationship of the 90-kDa murine heat shock protein to the untransformed and transformed states of the L cell glucocorticoid receptor. J. Biol. Chem. 1987, 262:6986-6991.
50. Kirschke E., et al. Glucocorticoid receptor function regulated by coordinated action of the Hsp90 and Hsp70 chaperone cycles. Cell 2014, 157:1685-1697.
51. Hagn F., et al. Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53. Nat. Struct. Mol. Biol. 2011, 18:1086-1093.
52. Park S.J., et al. Dynamic interaction of Hsp90 with its client protein p53. J. Mol. Biol. 2011, 411:158-173.
53. Street T.O., et al. Substrate binding drives large-scale conformational changes in the Hsp90 molecular chaperone. Mol. Cell 2011, 42:96-105.
54. Genest O., et al. Uncovering a region of heat shock protein 90 important for client binding in E. coli and chaperone function in yeast. Mol. Cell 2013, 49:464-473.
55. Panaretou B., et al. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J. 1998, 17:4829-4836.
56. Prodromou C., et al. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997, 90:65-75.
57. Prodromou C., et al. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J. 2000, 19:4383-4392.
58. 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.
59. Trepel J., et al. Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 2010, 10:537-549.
60. Neckers L., Trepel J.B. Stressing the development of small molecules targeting HSP90. Clin. Cancer Res. 2014, 20:275-277.
61. Li J., et al. The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochim. Biophys. Acta 2012, 1823:624-635.
62. Panaretou B., et al. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 2002, 10:1307-1318.
63. Meyer P., et al. Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J. 2004, 23:511-519.
64. Mishra P., Bolon D.N. Designed Hsp90 heterodimers reveal an asymmetric ATPase-driven mechanism in vivo. Mol. Cell 2014, 53:344-350.
65. Retzlaff M., et al. Asymmetric activation of the hsp90 dimer by its cochaperone aha1. Mol. Cell 2010, 37:344-354.
66. Roe S.M., et al. The mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50(cdc37). Cell 2004, 116:87-98.
67. Schmid A.B., et al. The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop. EMBO J. 2012, 31:1506-1517.
68. Southworth D.R., Agard D.A. Client-loading conformation of the Hsp90 molecular chaperone revealed in the cryo-EM structure of the human Hsp90:Hop complex. Mol. Cell 2011, 42:771-781.
69. Johnson B.D., et al. Hop modulates Hsp70/Hsp90 interactions in protein folding. J. Biol. Chem. 1998, 273:3679-3686.
70. Zhang M., et al. Chaperoned ubiquitylation - crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol. Cell 2005, 20:525-538.
71. Ballinger C.A., et al. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 1999, 19:4535-4545.
72. Mollapour M., Neckers L. Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim. Biophys. Acta 2012, 1823:648-655.
73. Soroka J., et al. Conformational switching of the molecular chaperone Hsp90 via regulated phosphorylation. Mol. Cell 2012, 45:517-528.
74. Walton-Diaz A., et al. Contributions of co-chaperones and post-translational modifications towards Hsp90 drug sensitivity. Future Med. Chem. 2013, 5:1059-1071.
75. Muller P., et al. C-terminal phosphorylation of Hsp70 and Hsp90 regulates alternate binding to co-chaperones CHIP and HOP to determine cellular protein folding/degradation balances. Oncogene 2013, 32:3101-3110.
76. Duval M., et al. Src-mediated phosphorylation of Hsp90 in response to vascular endothelial growth factor (VEGF) is required for VEGF receptor-2 signaling to endothelial NO synthase. Mol. Biol. Cell 2007, 18:4659-4668.
77. Lei H., et al. Protein kinase A-dependent translocation of Hsp90 alpha impairs endothelial nitric-oxide synthase activity in high glucose and diabetes. J. Biol. Chem. 2007, 282:9364-9371.
78. Zhu X., et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 1996, 272:1606-1614.
79. Rüdiger S., et al. CRINEPT-TROSY NMR reveals p53 core domain bound in an unfolded form to the chaperone Hsp90. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11085-11090.
80. Seidler P.M., et al. Characterization of the Grp94/OS-9 chaperone-lectin complex. J. Mol. Biol. 2014, 426:3590-3605. 10.1016/j.jmb.2014.08.024.
81. Daturpalli S., et al. Hsp90 inhibits α-synuclein aggregation by interacting with soluble oligomers. J. Mol. Biol. 2013, 425:4614-4628. 10.1016/j.jmb.2013.08.006.
82. Bonvin A.M., et al. NMR analysis of protein interactions. Curr. Opin. Chem. Biol. 2005, 9:501-508.
83. Putnam C.D., et al. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q. Rev. Biophys. 2007, 40:191-285.
84. Petoukhov M.V., Svergun D.I. Applications of small-angle X-ray scattering to biomacromolecular solutions. Int. J. Biochem. Cell Biol. 2013, 45:429-437.
85. Mertens H.D., Svergun D.I. Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J. Struct. Biol. 2010, 172:128-141.
86. Cheng Y., Walz T. The advent of near-atomic resolution in single-particle electron microscopy. Annu. Rev. Biochem. 2009, 78:723-742.
87. Kityk R., et al. Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol. Cell 2012, 48:863-874.