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Experimental Biology and Medicine 228:111-133 (2003)
© 2003 Society for Experimental Biology and Medicine

MINIREVIEW

Regulation of Signaling Protein Function and Trafficking by the hsp90/hsp70-Based Chaperone Machinery1

William B. Pratt* and David O. Toft{dagger}

* Department of Pharmacology, University of Michigan Medical School, Ann Arbor, Michigan 48109; and
{dagger} Department of Biochemistry and Molecular Biology, Mayo Graduate School, Rochester, Minnesota 55905

To whom requests for reprints should be addressed at Reprint requests should be addressed to either author. William B. Pratt at Department of Pharmacology, University of Michigan Medical School, 1301 MSRB III, Ann Arbor, MI 48109–0632. David O. Toft at Department of Biochemistry and Molecular Biology, Mayo Clinic, 200 1st Street SW, Rochester, MN 55905–0001. E-mail: toft{at}mayo.edu

Nearly 100 proteins are known to be regulated by hsp90. Most of these substrates or ‘‘client proteins’’ are involved in signal transduction, and they are brought into complex with hsp90 by a multiprotein hsp90/hsp70-based chaperone machinery. In addition to binding substrate proteins at the chaperone site(s), hsp90 binds cofactors at other sites that are part of the heterocomplex assembly machinery as well as immunophilins that connect assembled substrate•hsp90 complexes to protein-trafficking systems. In the 5 years since we last reviewed this subject, much has been learned about hsp90 structure, nucleotide-binding, and cochaperone interactions; the most important concept is that ATP hydrolysis by an intrinsic ATPase activity results in a conformational change in hsp90 that is required to induce conformational change in a substrate protein. The conformational change induced in steroid receptors is an opening of the steroid-binding cleft so that it can be accessed by steroid. We have now developed a minimal system of five purified proteins—hsp90, hsp70, Hop, hsp40, and p23— that assembles stable receptor•hsp90 heterocomplexes. An hsp90•Hop•hsp70•hsp40 complex opens the cleft in an ATP-dependent process to produce a receptor•hsp90 heterocomplex with hsp90 in its ATP-bound conformation, and p23 then interacts with the hsp90 to stabilize the complex. Stepwise assembly experiments have shown that hsp70 and hsp40 first interact with the receptor in an ATP-dependent reaction to produce a receptor•hsp70•hsp40 complex that is ‘‘primed’’ to be activated to the steroid-binding state in a second ATP-dependent step with hsp90, Hop, and p23. Successful use of the five-protein system with other substrates indicates that it can assemble signal protein•hsp90 heterocomplexes whether the substrate is a receptor, a protein kinase, or a transcription factor. This purified system should facilitate understanding of how eukaryotic hsp70 and hsp90 work together as essential components of a process that alters the conformations of substrate proteins to states that respond in signal transduction.

Key Words: hsp90 • chaperone proteins • signal transduction • steroid receptors • protein trafficking • protein kinases




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 GeneticsHome page
C. M. Wright, S. W. Fewell, M. L. Sullivan, J. M. Pipas, S. C. Watkins, and J. L. Brodsky
The Hsp40 Molecular Chaperone Ydj1p, Along With the Protein Kinase C Pathway, Affects Cell-Wall Integrity in the Yeast Saccharomyces cerevisiae
Genetics, April 1, 2007; 175(4): 1649 - 1664.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
S. Salim and D. C. Eikenburg
Role of 90-kDa Heat Shock Protein (Hsp 90) and Protein Degradation in Regulating Neuronal Levels of G Protein-Coupled Receptor Kinase 3
J. Pharmacol. Exp. Ther., March 1, 2007; 320(3): 1106 - 1112.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
Y. Chen, M. P. Schnetz, C. E. Irarrazabal, R.-F. Shen, C. K. Williams, M. B. Burg, and J. D. Ferraris
Proteomic identification of proteins associated with the osmoregulatory transcription factor TonEBP/OREBP: functional effects of Hsp90 and PARP-1
Am J Physiol Renal Physiol, March 1, 2007; 292(3): F981 - F992.
[Abstract] [Full Text] [PDF]

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 ReproductionHome page
J. Hong, S. T. Kim, S. Tranguch, D. F Smith, and S. K Dey
Deficiency of co-chaperone immunophilin FKBP52 compromises sperm fertilizing capacity
Reproduction, February 1, 2007; 133(2): 395 - 403.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
T. Naito, F. Momose, A. Kawaguchi, and K. Nagata
Involvement of Hsp90 in Assembly and Nuclear Import of Influenza Virus RNA Polymerase Subunits
J. Virol., February 1, 2007; 81(3): 1339 - 1349.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
R. Jasavala, H. Martinez, J. Thumar, A. Andaya, A.-C. Gingras, J. K. Eng, R. Aebersold, D. K. Han, and M. E. Wright
Identification of Putative Androgen Receptor Interaction Protein Modules: Cytoskeleton and Endosomes Modulate Androgen Receptor Signaling in Prostate Cancer Cells
Mol. Cell. Proteomics, February 1, 2007; 6(2): 252 - 271.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
J. L. Johnson, A. Halas, and G. Flom
Nucleotide-Dependent Interaction of Saccharomyces cerevisiae Hsp90 with the Cochaperone Proteins Sti1, Cpr6, and Sba1
Mol. Cell. Biol., January 15, 2007; 27(2): 768 - 776.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
R. Geller, M. Vignuzzi, R. Andino, and J. Frydman
Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance
Genes & Dev., January 15, 2007; 21(2): 195 - 205.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
R. L. Arnett-Mansfield, J. D. Graham, A. R. Hanson, P. A. Mote, A. Gompel, L. L. Scurr, N. Gava, A. de Fazio, and C. L. Clarke
Focal Subnuclear Distribution of Progesterone Receptor Is Ligand Dependent and Associated with Transcriptional Activity
Mol. Endocrinol., January 1, 2007; 21(1): 14 - 29.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
L. Fang, D. Ricketson, L. Getubig, and B. Darimont
Unliganded and hormone-bound glucocorticoid receptors interact with distinct hydrophobic sites in the Hsp90 C-terminal domain
PNAS, December 5, 2006; 103(49): 18487 - 18492.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
I. Grad, T. A. McKee, S. M. Ludwig, G. W. Hoyle, P. Ruiz, W. Wurst, T. Floss, C. A. Miller III, and D. Picard
The Hsp90 Cochaperone p23 Is Essential for Perinatal Survival
Mol. Cell. Biol., December 1, 2006; 26(23): 8976 - 8983.
[Abstract] [Full Text] [PDF]

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 Integr. Comp. Biol.Home page
M. E. Baker
Evolution of metamorphosis: role of environment on expression of mutant nuclear receptors and other signal-transduction proteins
Integr. Comp. Biol., December 1, 2006; 46(6): 808 - 814.
[Abstract] [Full Text] [PDF]

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 Eukaryot CellHome page
L. E. Cowen, A. E. Carpenter, O. Matangkasombut, G. R. Fink, and S. Lindquist
Genetic Architecture of Hsp90-Dependent Drug Resistance
Eukaryot. Cell, December 1, 2006; 5(12): 2184 - 2188.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
P. Hawle, M. Siepmann, A. Harst, M. Siderius, H. P. Reusch, and W. M. J. Obermann
The Middle Domain of Hsp90 Acts as a Discriminator between Different Types of Client Proteins
Mol. Cell. Biol., November 15, 2006; 26(22): 8385 - 8395.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. C. Y. Fan, M. K. Bhangoo, and J. C. Young
Hsp90 Functions in the Targeting and Outer Membrane Translocation Steps of Tom70-mediated Mitochondrial Import
J. Biol. Chem., November 3, 2006; 281(44): 33313 - 33324.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. G. Evans, S. Wisen, and J. E. Gestwicki
Heat Shock Proteins 70 and 90 Inhibit Early Stages of Amyloid beta-(1-42) Aggregation in Vitro
J. Biol. Chem., November 3, 2006; 281(44): 33182 - 33191.
[Abstract] [Full Text] [PDF]

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 CarcinogenesisHome page
L.G. Wang, X.M. Liu, and J.W. Chiao
Repression of androgen receptor in prostate cancer cells by phenethyl isothiocyanate
Carcinogenesis, October 1, 2006; 27(10): 2124 - 2132.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
N. S. Cintron and D. Toft
Defining the Requirements for Hsp40 and Hsp70 in the Hsp90 Chaperone Pathway
J. Biol. Chem., September 8, 2006; 281(36): 26235 - 26244.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. Murtagh, H. Lu, and E. L. Schwartz
Taxotere-Induced Inhibition of Human Endothelial Cell Migration Is a Result of Heat Shock Protein 90 Degradation
Cancer Res., August 15, 2006; 66(16): 8192 - 8199.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
C. Y. Chen and W. E. Balch
The Hsp90 Chaperone Complex Regulates GDI-dependent Rab Recycling
Mol. Biol. Cell, August 1, 2006; 17(8): 3494 - 3507.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
B. R. Keppler, A. T. Grady, and M. B. Jarstfer
The Biochemical Role of the Heat Shock Protein 90 Chaperone Complex in Establishing Human Telomerase Activity
J. Biol. Chem., July 21, 2006; 281(29): 19840 - 19848.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
F. Shinozaki, M. Minami, T. Chiba, M. Suzuki, K. Yoshimatsu, Y. Ichikawa, K. Terasawa, Y. Emori, K. Matsumoto, T. Kurosaki, et al.
Depletion of Hsp90beta Induces Multiple Defects in B Cell Receptor Signaling
J. Biol. Chem., June 16, 2006; 281(24): 16361 - 16369.
[Abstract] [Full Text] [PDF]

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 Hum Mol GenetHome page
M. Thomas, J. M. Harrell, Y. Morishima, H.-M. Peng, W. B. Pratt, and A. P. Lieberman
Pharmacologic and genetic inhibition of hsp90-dependent trafficking reduces aggregation and promotes degradation of the expanded glutamine androgen receptor without stress protein induction
Hum. Mol. Genet., June 1, 2006; 15(11): 1876 - 1883.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
R. Li, J. Soosairajah, D. Harari, A. Citri, J. Price, H. L. Ng, C. J. Morton, M. W. Parker, Y. Yarden, and O. Bernard
Hsp90 increases LIM kinase activity by promoting its homo-dimerization
FASEB J, June 1, 2006; 20(8): 1218 - 1220.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Citri, D. Harari, G. Shohat, P. Ramakrishnan, J. Gan, S. Lavi, M. Eisenstein, A. Kimchi, D. Wallach, S. Pietrokovski, et al.
Hsp90 Recognizes a Common Surface on Client Kinases
J. Biol. Chem., May 19, 2006; 281(20): 14361 - 14369.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
L. T. Gooljarsingh, C. Fernandes, K. Yan, H. Zhang, M. Grooms, K. Johanson, R. H. Sinnamon, R. B. Kirkpatrick, J. Kerrigan, T. Lewis, et al.
A biochemical rationale for the anticancer effects of Hsp90 inhibitors: Slow, tight binding inhibition by geldanamycin and its analogues
PNAS, May 16, 2006; 103(20): 7625 - 7630.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
K. Terasawa, K. Yoshimatsu, S.-i. Iemura, T. Natsume, K. Tanaka, and Y. Minami
Cdc37 interacts with the glycine-rich loop of hsp90 client kinases.
Mol. Cell. Biol., May 1, 2006; 26(9): 3378 - 3389.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Richter, S. Moser, F. Hagn, R. Friedrich, O. Hainzl, M. Heller, S. Schlee, H. Kessler, J. Reinstein, and J. Buchner
Intrinsic Inhibition of the Hsp90 ATPase Activity
J. Biol. Chem., April 21, 2006; 281(16): 11301 - 11311.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. D. Westerheide, T. L. A. Kawahara, K. Orton, and R. I. Morimoto
Triptolide, an Inhibitor of the Human Heat Shock Response That Enhances Stress-induced Cell Death
J. Biol. Chem., April 7, 2006; 281(14): 9616 - 9622.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
X. Cen, A. Nitta, S. Ohya, Y. Zhao, N. Ozawa, A. Mouri, D. Ibi, L. Wang, M. Suzuki, K. Saito, et al.
An analog of a dipeptide-like structure of FK506 increases glial cell line-derived neurotrophic factor expression through cAMP response element-binding protein activated by heat shock protein 90/Akt signaling pathway.
J. Neurosci., March 22, 2006; 26(12): 3335 - 3344.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Cell. Biol.Home page
A. Chadli, J. D. Graham, M. G. Abel, T. A. Jackson, D. F. Gordon, W. M. Wood, S. J. Felts, K. B. Horwitz, and D. Toft
GCUNC-45 Is a Novel Regulator for the Progesterone Receptor/hsp90 Chaperoning Pathway.
Mol. Cell. Biol., March 1, 2006; 26(5): 1722 - 1730.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
A. Tsapara, K. Matter, and M. S. Balda
The Heat-Shock Protein Apg-2 Binds to the Tight Junction Protein ZO-1 and Regulates Transcriptional Activity of ZONAB
Mol. Biol. Cell, March 1, 2006; 17(3): 1322 - 1330.
[Abstract] [Full Text] [PDF]

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 BloodHome page
C. Cohen-Saidon, I. Carmi, A. Keren, and E. Razin
Antiapoptotic function of Bcl-2 in mast cells is dependent on its association with heat shock protein 90beta
Blood, February 15, 2006; 107(4): 1413 - 1420.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
S. J. H. Arlander, S. J. Felts, J. M. Wagner, B. Stensgard, D. O. Toft, and L. M. Karnitz
Chaperoning Checkpoint Kinase 1 (Chk1), an Hsp90 Client, with Purified Chaperones
J. Biol. Chem., February 3, 2006; 281(5): 2989 - 2998.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
L. Shang and T. B. Tomasi
The Heat Shock Protein 90-CDC37 Chaperone Complex Is Required for Signaling by Types I and II Interferons
J. Biol. Chem., January 27, 2006; 281(4): 1876 - 1884.
[Abstract] [Full Text] [PDF]


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