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Endocrine Reviews 18 (3): 306-360
Copyright © 1997 by The Endocrine Society

Steroid Receptor Interactions with Heat Shock Protein and Immunophilin Chaperones1

William B. Pratt and David O. Toft

Department of Pharmacology (W.B.P.), The University of Michigan Medical School, Ann Arbor, Michigan 48109; and Department of Biochemistry and Molecular Biology (D.O.T.), Mayo Graduate School, Rochester, Minnesota 55905

I. Introduction
II. 9S Receptors
A. Estrogen receptors (ERs)
B. Progesterone receptors (PRs)
C. Androgen receptors (ARs)
D. Glucocorticoid receptors (GRs)
E. Mineralocorticoid receptors (MRs)
F. Dioxin receptors (DRs)
G. Antheridiol receptors
III. Receptor Transformation
A. Transformed receptors bind polyanions
B. Artifactual transforming conditions
C. Models of cytosolic receptor transformation
D. Physiological relevance of receptor transformation before the discovery of hsp90 binding
IV. Molybdate Stabilization of Receptors
A. Stabilization of steroid binding activity
B. Inhibition of transformation
C. Mechanism of molybdate stabilization
V. Purification of Untransformed Receptors Leads to hsp90
A. The untransformed receptor is a heterocomplex
B. Antibodies against the 90-kDa protein
C. The 90-kDa receptor-associated protein is hsp90
VI. Role of hsp90 in Receptor Function
A. General properties of hsp90
B. Stoichiometry of receptor·hsp90 complex
C. hsp90 Binds to the receptor HBD
D. Region of hsp90 that binds receptor
E. Requirement of hsp90 for steroid binding
F. Receptor transformation and hsp90 dissociation
G. Receptor inactivation by hsp90
H. Evidence that hsp90 is a physiologically significant regulator of receptor function
I. Potential roles of hsp90 in receptor turnover and trafficking
VII. Other Proteins Recovered in Native Receptor Heterocomplexes
A. hsp70
B. p23
C. Immunophilins
VIII. The Receptor Heterocomplex Assembly Mechanism
A. The receptor·hsp90 heterocomplex assembly activity in reticulocyte lysate
B. Components of the heterocomplex assembly system
C. Effect of geldanamycin on heterocomplex assembly
D. The concept of a dynamic heterocomplex assembly machine
E. Heterocomplex assembly with hsp90 is a very basic and conserved process
IX. Other Proteins That Are Bound to hsp90
X. Summary




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L. A. Moraes, M. J. Paul-Clark, A. Rickman, R. J. Flower, N. J. Goulding, and M. Perretti
Ligand-specific glucocorticoid receptor activation in human platelets
Blood, December 15, 2005; 106(13): 4167 - 4175.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
M. Fan, A. Park, and K. P. Nephew
CHIP (Carboxyl Terminus of Hsc70-Interacting Protein) Promotes Basal and Geldanamycin-Induced Degradation of Estrogen Receptor-{alpha}
Mol. Endocrinol., December 1, 2005; 19(12): 2901 - 2914.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. Tranguch, J. Cheung-Flynn, T. Daikoku, V. Prapapanich, M. B. Cox, H. Xie, H. Wang, S. K. Das, D. F. Smith, and S. K. Dey
From The Cover: Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation
PNAS, October 4, 2005; 102(40): 14326 - 14331.
[Abstract] [Full Text] [PDF]

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 J Mol EndocrinolHome page
M Maggiolini, A G Recchia, D Bonofiglio, S Catalano, A Vivacqua, A Carpino, V Rago, R Rossi, and S Ando
The red wine phenolics piceatannol and myricetin act as agonists for estrogen receptor {alpha} in human breast cancer cells
J. Mol. Endocrinol., October 1, 2005; 35(2): 269 - 281.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
A. Papapetropoulos, Z. Zhou, C. Gerassimou, G. Yetik, R. C. Venema, C. Roussos, W. C. Sessa, and J. D. Catravas
Interaction between the 90-kDa Heat Shock Protein and Soluble Guanylyl Cyclase: Physiological Significance and Mapping of the Domains Mediating Binding
Mol. Pharmacol., October 1, 2005; 68(4): 1133 - 1141.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
G. Buchanan, S. N. Birrell, A. A. Peters, T. Bianco-Miotto, K. Ramsay, E. J. Cops, M. Yang, J. M. Harris, H. A. Simila, N. L. Moore, et al.
Decreased Androgen Receptor Levels and Receptor Function in Breast Cancer Contribute to the Failure of Response to Medroxyprogesterone Acetate
Cancer Res., September 15, 2005; 65(18): 8487 - 8496.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
P. Farla, R. Hersmus, J. Trapman, and A. B. Houtsmuller
Antiandrogens prevent stable DNA-binding of the androgen receptor
J. Cell Sci., September 15, 2005; 118(18): 4187 - 4198.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
L. Pascual-Le Tallec and M. Lombes
The Mineralocorticoid Receptor: A Journey Exploring Its Diversity and Specificity of Action
Mol. Endocrinol., September 1, 2005; 19(9): 2211 - 2221.
[Abstract] [Full Text] [PDF]

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 JCOHome page
A. A. Adjei and M. Hidalgo
Intracellular Signal Transduction Pathway Proteins As Targets for Cancer Therapy
J. Clin. Oncol., August 10, 2005; 23(23): 5386 - 5403.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
Y. S. Kim, S.-W. Jang, H. J. Sung, H. J. Lee, I. S. Kim, D. S. Na, and J. Ko
Role of 14-3-3{eta} as a Positive Regulator of the Glucocorticoid Receptor Transcriptional Activation
Endocrinology, July 1, 2005; 146(7): 3133 - 3140.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
D. Wang and S. S. Simons Jr.
Corepressor Binding to Progesterone and Glucocorticoid Receptors Involves the Activation Function-1 Domain and Is Inhibited by Molybdate
Mol. Endocrinol., June 1, 2005; 19(6): 1483 - 1500.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
M. J. M. Schaaf, L. J. Lewis-Tuffin, and J. A. Cidlowski
Ligand-Selective Targeting of the Glucocorticoid Receptor to Nuclear Subdomains Is Associated with Decreased Receptor Mobility
Mol. Endocrinol., June 1, 2005; 19(6): 1501 - 1515.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
K. Chwalisz, M. C. Perez, D. DeManno, C. Winkel, G. Schubert, and W. Elger
Selective Progesterone Receptor Modulator Development and Use in the Treatment of Leiomyomata and Endometriosis
Endocr. Rev., May 1, 2005; 26(3): 423 - 438.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
N. Yoshikawa, K. Yamamoto, N. Shimizu, S. Yamada, C. Morimoto, and H. Tanaka
The Distinct Agonistic Properties of the Phenylpyrazolosteroid Cortivazol Reveal Interdomain Communication within the Glucocorticoid Receptor
Mol. Endocrinol., May 1, 2005; 19(5): 1110 - 1124.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
J. Fagart, C. Seguin, G. M. Pinon, and M.-E. Rafestin-Oblin
The Met852 Residue Is a Key Organizer of the Ligand-Binding Cavity of the Human Mineralocorticoid Receptor
Mol. Pharmacol., May 1, 2005; 67(5): 1714 - 1722.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. F. Walther, E. Atlas, A. Carrigan, Y. Rouleau, A. Edgecombe, L. Visentin, C. Lamprecht, G. C. Addicks, R. J. G. Hache, and Y. A. Lefebvre
A Serine/Threonine-rich Motif Is One of Three Nuclear Localization Signals That Determine Unidirectional Transport of the Mineralocorticoid Receptor to the Nucleus
J. Biol. Chem., April 29, 2005; 280(17): 17549 - 17561.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. De Nardo, P. Masendycz, S. Ho, M. Cross, A. J. Fleetwood, E. C. Reynolds, J. A. Hamilton, and G. M. Scholz
A Central Role for the Hsp90{middle dot}Cdc37 Molecular Chaperone Module in Interleukin-1 Receptor-associated-kinase-dependent Signaling by Toll-like Receptors
J. Biol. Chem., March 18, 2005; 280(11): 9813 - 9822.
[Abstract] [Full Text] [PDF]

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 BloodHome page
P. S. Bachmann, R. Gorman, K. L. MacKenzie, L. Lutze-Mann, and R. B. Lock
Dexamethasone resistance in B-cell precursor childhood acute lymphoblastic leukemia occurs downstream of ligand-induced nuclear translocation of the glucocorticoid receptor
Blood, March 15, 2005; 105(6): 2519 - 2526.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. E. Carrigan, D. L. Riggs, M. Chinkers, and D. F. Smith
Functional Comparison of Human and Drosophila Hop Reveals Novel Role in Steroid Receptor Maturation
J. Biol. Chem., March 11, 2005; 280(10): 8906 - 8911.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. J. Burd, C. E. Petre, H. Moghadam, E. M. Wilson, and K. E. Knudsen
Cyclin D1 Binding to the Androgen Receptor (AR) NH2-Terminal Domain Inhibits Activation Function 2 Association and Reveals Dual Roles for AR Corepression
Mol. Endocrinol., March 1, 2005; 19(3): 607 - 620.
[Abstract] [Full Text] [PDF]

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 JCOHome page
M. P. Goetz, D. Toft, J. Reid, M. Ames, B. Stensgard, S. Safgren, A. A. Adjei, J. Sloan, P. Atherton, V. Vasile, et al.
Phase I Trial of 17-Allylamino-17-Demethoxygeldanamycin in Patients With Advanced Cancer
J. Clin. Oncol., February 20, 2005; 23(6): 1078 - 1087.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
G. M. Wochnik, J. Ruegg, G. A. Abel, U. Schmidt, F. Holsboer, and T. Rein
FK506-binding Proteins 51 and 52 Differentially Regulate Dynein Interaction and Nuclear Translocation of the Glucocorticoid Receptor in Mammalian Cells
J. Biol. Chem., February 11, 2005; 280(6): 4609 - 4616.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
N. Balashova, F.-J. Chang, M. Lamothe, Q. Sun, and A. Beuve
Characterization of a Novel Type of Endogenous Activator of Soluble Guanylyl Cyclase
J. Biol. Chem., January 21, 2005; 280(3): 2186 - 2196.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. J. Squires, T. Sueyoshi, and M. Negishi
Cytoplasmic Localization of Pregnane X Receptor and Ligand-dependent Nuclear Translocation in Mouse Liver
J. Biol. Chem., November 19, 2004; 279(47): 49307 - 49314.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
B. M. Necela and J. A. Cidlowski
Mechanisms of Glucocorticoid Receptor Action in Noninflammatory and Inflammatory Cells
Proceedings of the ATS, November 1, 2004; 1(3): 239 - 246.
[Full Text] [PDF]

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 Clin Med ResHome page
T. Iwasaki
Recent Advances in the Treatment of Graft-Versus-Host Disease
Clin. Med. Res., November 1, 2004; 2(4): 243 - 252.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Szatmary, M. J. Garabedian, and J. Vilcek
Inhibition of Glucocorticoid Receptor-mediated Transcriptional Activation by p38 Mitogen-activated Protein (MAP) Kinase
J. Biol. Chem., October 15, 2004; 279(42): 43708 - 43715.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
B. M. Necela and J. A. Cidlowski
A Single Amino Acid Change in the First Zinc Finger of the DNA Binding Domain of the Glucocorticoid Receptor Regulates Differential Promoter Selectivity
J. Biol. Chem., September 17, 2004; 279(38): 39279 - 39288.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Prince and R. L. Matts
Definition of Protein Kinase Sequence Motifs That Trigger High Affinity Binding of Hsp90 and Cdc37
J. Biol. Chem., September 17, 2004; 279(38): 39975 - 39981.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y.-C. Hu, S. Yeh, S.-D. Yeh, E. R. Sampson, J. Huang, P. Li, C.-L. Hsu, H.-J. Ting, H.-K. Lin, L. Wang, et al.
Functional Domain and Motif Analyses of Androgen Receptor Coregulator ARA70 and Its Differential Expression in Prostate Cancer
J. Biol. Chem., August 6, 2004; 279(32): 33438 - 33446.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
A. R. Buskirk, Y.-C. Ong, Z. J. Gartner, and D. R. Liu
Directed evolution of ligand dependence: Small-molecule-activated protein splicing
PNAS, July 20, 2004; 101(29): 10505 - 10510.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. J. M. Murphy, M. D. Galigniana, Y. Morishima, J. M. Harrell, R. P. S. Kwok, M. Ljungman, and W. B. Pratt
Pifithrin-{alpha} Inhibits p53 Signaling after Interaction of the Tumor Suppressor Protein with hsp90 and Its Nuclear Translocation
J. Biol. Chem., July 16, 2004; 279(29): 30195 - 30201.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Jiang, Y. E. Liu, I. D. Goldberg, and Y. E. Shi
{gamma} Synuclein, a Novel Heat-Shock Protein-Associated Chaperone, Stimulates Ligand-Dependent Estrogen Receptor {alpha} Signaling and Mammary Tumorigenesis
Cancer Res., July 1, 2004; 64(13): 4539 - 4546.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
Q. Wang, J. A. Blackford Jr., L.-N. Song, Y. Huang, S. Cho, and S. S. Simons Jr.
Equilibrium Interactions of Corepressors and Coactivators with Agonist and Antagonist Complexes of Glucocorticoid Receptors
Mol. Endocrinol., June 1, 2004; 18(6): 1376 - 1395.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
B. Wu, P. Li, Y. Liu, Z. Lou, Y. Ding, C. Shu, S. Ye, M. Bartlam, B. Shen, and Z. Rao
3D structure of human FK506-binding protein 52: Implications for the assembly of the glucocorticoid receptor/Hsp90/immunophilin heterocomplex
PNAS, June 1, 2004; 101(22): 8348 - 8353.
[Abstract] [Full Text] [PDF]


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