Modulation of the Hsp90 Chaperone Cycle by a Stringent Client Protein

Molecular Cell - Tập 53 - Trang 941-953 - 2014
Oliver Robin Lorenz1, Lee Freiburger1,2, Daniel Andreas Rutz1, Maike Krause1, Bettina Karolina Zierer1, Sara Alvira3, Jorge Cuéllar3, José María Valpuesta3, Tobias Madl1,2, Michael Sattler1,2, Johannes Buchner1
1Center for Integrated Protein Science Munich, Department Chemie, Technische Universität München, 85478 Garching, Germany
2Institute of Structural Biology, Helmholtz Zentrum München, 85764 Neuherberg, Germany
3Centro Nacional de Biotecnología (CNB-CSIC), Darwin 3, 28049 Madrid, Spain

Tài liệu tham khảo

Ali, 2006, Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex, Nature, 440, 1013, 10.1038/nature04716 Bledsoe, 2002, Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition, Cell, 110, 93, 10.1016/S0092-8674(02)00817-6 Bohen, 1993, Isolation of Hsp90 mutants by screening for decreased steroid receptor function, Proc. Natl. Acad. Sci. USA, 90, 11424, 10.1073/pnas.90.23.11424 Buchner, 1998, Purification of Hsp90 partner proteins Hop/p60, p23, and FKBP52, Methods Enzymol., 290, 418, 10.1016/S0076-6879(98)90035-0 Cadepond, 1993, Interaction of glucocorticosteroid receptor and wild-type or mutated 90-kDa heat shock protein coexpressed in baculovirus-infected Sf9 cells, Proc. Natl. Acad. Sci. USA, 90, 10434, 10.1073/pnas.90.22.10434 Chang, 1997, In vivo analysis of the Hsp90 cochaperone Sti1 (p60), Mol. Cell. Biol., 17, 318, 10.1128/MCB.17.1.318 Chen, 1998, Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery, J. Biol. Chem., 273, 35194, 10.1074/jbc.273.52.35194 Chen, 2011, A general strategy for the evolution of bond-forming enzymes using yeast display, Proc. Natl. Acad. Sci. USA, 108, 11399, 10.1073/pnas.1101046108 Dehner, 2003, NMR chemical shift perturbation study of the N-terminal domain of Hsp90 upon binding of ADP, AMP-PNP, geldanamycin, and radicicol, ChemBioChem, 4, 870, 10.1002/cbic.200300658 Delaglio, 1995, NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR, 6, 277, 10.1007/BF00197809 Dittmar, 1997, Folding of the glucocorticoid receptor by the heat shock protein (hsp) 90-based chaperone machinery. The role of p23 is to stabilize receptor.hsp90 heterocomplexes formed by hsp90.p60.hsp70, J. Biol. Chem., 272, 21213, 10.1074/jbc.272.34.21213 Fang, 2006, Unliganded and hormone-bound glucocorticoid receptors interact with distinct hydrophobic sites in the Hsp90 C-terminal domain, Proc. Natl. Acad. Sci. USA, 103, 18487, 10.1073/pnas.0609163103 Freeman, 2002, Disassembly of transcriptional regulatory complexes by molecular chaperones, Science, 296, 2232, 10.1126/science.1073051 Freeman, 2000, The p23 molecular chaperones act at a late step in intracellular receptor action to differentially affect ligand efficacies, Genes Dev., 14, 422, 10.1101/gad.14.4.422 Galigniana, 2001, Evidence that the peptidylprolyl isomerase domain of the hsp90-binding immunophilin FKBP52 is involved in both dynein interaction and glucocorticoid receptor movement to the nucleus, J. Biol. Chem., 276, 14884, 10.1074/jbc.M010809200 Genest, 2013, Uncovering a region of heat shock protein 90 important for client binding in E. coli and chaperone function in yeast, Mol. Cell, 49, 464, 10.1016/j.molcel.2012.11.017 Graf, 2009, Spatially and kinetically resolved changes in the conformational dynamics of the Hsp90 chaperone machine, EMBO J., 28, 602, 10.1038/emboj.2008.306 Hagn, 2011, Structural analysis of the interaction between Hsp90 and the tumor suppressor protein p53, Nat. Struct. Mol. Biol., 18, 1086, 10.1038/nsmb.2114 Harris, 2004, The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site, Structure, 12, 1087, 10.1016/j.str.2004.03.020 Hawle, 2006, The middle domain of Hsp90 acts as a discriminator between different types of client proteins, Mol. Cell. Biol., 26, 8385, 10.1128/MCB.02188-05 Heitzer, 2007, Glucocorticoid receptor physiology, Rev. Endocr. Metab. Disord., 8, 321, 10.1007/s11154-007-9059-8 Hernández, 2002, HSP40 binding is the first step in the HSP90 chaperoning pathway for the progesterone receptor, J. Biol. Chem., 277, 11873, 10.1074/jbc.M111445200 Hessling, 2009, Dissection of the ATP-induced conformational cycle of the molecular chaperone Hsp90, Nat. Struct. Mol. Biol., 16, 287, 10.1038/nsmb.1565 Howard, 1990, Mapping the HSP90 binding region of the glucocorticoid receptor, J. Biol. Chem., 265, 11928, 10.1016/S0021-9258(19)38489-3 Jackson, 2013, Hsp90: Structure and Function, 155 Jakob, 1995, Transient interaction of Hsp90 with early unfolding intermediates of citrate synthase. Implications for heat shock in vivo, J. Biol. Chem., 270, 7288, 10.1074/jbc.270.13.7288 Kastner, 2008, GraFix: sample preparation for single-particle electron cryomicroscopy, Nat. Methods, 5, 53, 10.1038/nmeth1139 Krukenberg, 2011, Conformational dynamics of the molecular chaperone Hsp90, Q. Rev. Biophys., 44, 229, 10.1017/S0033583510000314 Kumar, 1999, The structure of the nuclear hormone receptors, Steroids, 64, 310, 10.1016/S0039-128X(99)00014-8 Laue, T.M., Shah, B.D., Ridgeway, T.M., and Pelletier, S.L. (1992). Computer-aided interpretation of analytical sedimentation data for proteins. In Analytical Ultracentrifugation in Biochemistry and Polymer Science), pp. 90–125. Lee, 2012, Dynamics of the regulation of Hsp90 by the co-chaperone Sti1, EMBO J., 31, 1518, 10.1038/emboj.2012.37 Li, 2011, Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle, Nat. Struct. Mol. Biol., 18, 61, 10.1038/nsmb.1965 Li, 2012, The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones, Biochim. Biophys. Acta, 1823, 624, 10.1016/j.bbamcr.2011.09.003 Li, 2013, Integration of the accelerator Aha1 in the Hsp90 co-chaperone cycle, Nat. Struct. Mol. Biol., 20, 326, 10.1038/nsmb.2502 Marley, 2001, A method for efficient isotopic labeling of recombinant proteins, J. Biomol. NMR, 20, 71, 10.1023/A:1011254402785 McClellan, 2005, Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways, Cell, 121, 739, 10.1016/j.cell.2005.03.024 McClellan, 2007, Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches, Cell, 131, 121, 10.1016/j.cell.2007.07.036 McLaughlin, 2002, Stimulation of the weak ATPase activity of human hsp90 by a client protein, J. Mol. Biol., 315, 787, 10.1006/jmbi.2001.5245 Mickler, 2009, The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis, Nat. Struct. Mol. Biol., 16, 281, 10.1038/nsmb.1557 Nathan, 1995, Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase, Mol. Cell. Biol., 15, 3917, 10.1128/MCB.15.7.3917 Nathan, 1997, In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone, Proc. Natl. Acad. Sci. USA, 94, 12949, 10.1073/pnas.94.24.12949 Panaretou, 2002, Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1, Mol. Cell, 10, 1307, 10.1016/S1097-2765(02)00785-2 Park, 2011, The client protein p53 adopts a molten globule-like state in the presence of Hsp90, Nat. Struct. Mol. Biol., 18, 537, 10.1038/nsmb.2045 Philo, 2006, Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques, Anal. Biochem., 354, 238, 10.1016/j.ab.2006.04.053 Picard, 2002, Heat-shock protein 90, a chaperone for folding and regulation, Cell. Mol. Life Sci., 59, 1640, 10.1007/PL00012491 Picard, 1990, Reduced levels of hsp90 compromise steroid receptor action in vivo, Nature, 348, 166, 10.1038/348166a0 Pratt, 1998, Studies with Purified Chaperones Advance the Understanding of the Mechanism of Glucocorticoid Receptor-hsp90 Heterocomplex Assembly, Trends Endocrinol. Metab., 9, 244, 10.1016/S1043-2760(98)00059-9 Pratt, 1997, Steroid receptor interactions with heat shock protein and immunophilin chaperones, Endocr. Rev., 18, 306 Pullen, 2011, Enforced N-domain proximity stimulates Hsp90 ATPase activity and is compatible with function in vivo, J. Biol. Chem., 286, 11091, 10.1074/jbc.M111.223131 Retzlaff, 2010, Asymmetric activation of the hsp90 dimer by its cochaperone aha1, Mol. Cell, 37, 344, 10.1016/j.molcel.2010.01.006 Richter, 2003, Sti1 is a non-competitive inhibitor of the Hsp90 ATPase. Binding prevents the N-terminal dimerization reaction during the atpase cycle, J. Biol. Chem., 278, 10328, 10.1074/jbc.M213094200 Richter, 2004, The Co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle, J. Mol. Biol., 342, 1403, 10.1016/j.jmb.2004.07.064 Röhl, 2013, The chaperone Hsp90: changing partners for demanding clients, Trends Biochem. Sci., 38, 253, 10.1016/j.tibs.2013.02.003 Rosen, 1996, Selective methyl group protonation of perdeuterated proteins, J. Mol. Biol., 263, 627, 10.1006/jmbi.1996.0603 Rüdiger, 2002, CRINEPT-TROSY NMR reveals p53 core domain bound in an unfolded form to the chaperone Hsp90, Proc. Natl. Acad. Sci. USA, 99, 11085, 10.1073/pnas.132393699 Schmid, 2012, The architecture of functional modules in the Hsp90 co-chaperone Sti1/Hop, EMBO J., 31, 1506, 10.1038/emboj.2011.472 Schuck, 2000, Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling, Biophys. J., 78, 1606, 10.1016/S0006-3495(00)76713-0 Seitz, 2010, Enhancing the stability and solubility of the glucocorticoid receptor ligand-binding domain by high-throughput library screening, J. Mol. Biol., 403, 562, 10.1016/j.jmb.2010.08.048 Siligardi, 2004, Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle, J. Biol. Chem., 279, 51989, 10.1074/jbc.M410562200 Smith, 1993, Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes, Mol. Endocrinol., 7, 1418 Southworth, 2008, Species-dependent ensembles of conserved conformational states define the Hsp90 chaperone ATPase cycle, Mol. Cell, 32, 631, 10.1016/j.molcel.2008.10.024 Street, 2011, Substrate binding drives large-scale conformational changes in the Hsp90 molecular chaperone, Mol. Cell, 42, 96, 10.1016/j.molcel.2011.01.029 Taipale, 2012, Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition, Cell, 150, 987, 10.1016/j.cell.2012.06.047 Vaughan, 2006, Structure of an Hsp90-Cdc37-Cdk4 complex, Mol. Cell, 23, 697, 10.1016/j.molcel.2006.07.016 Vranken, 2005, The CCPN data model for NMR spectroscopy: development of a software pipeline, Proteins, 59, 687, 10.1002/prot.20449 Wegele, 2003, Dissection of the contribution of individual domains to the ATPase mechanism of Hsp90, J. Biol. Chem., 278, 39303, 10.1074/jbc.M305751200 Weikl, 2000, C-terminal regions of Hsp90 are important for trapping the nucleotide during the ATPase cycle, J. Mol. Biol., 303, 583, 10.1006/jmbi.2000.4157