Cited by 220Heat shock proteins researchProtein Structure and DynamicsUbiquitin and proteasome pathways

The DOI matches its Crossref record; 99 of the 99 references it cites were found in a registry or an index; 37 of the 49 sources its claims cite were checked for support.

Structure of Hsp90–Hsp70–Hop–GR reveals the Hsp90 client-loading mechanism

Open access

Published version of a preprint

Abstract

Maintaining a healthy proteome is fundamental for the survival of all organisms 1. Integral to this are Hsp90 and Hsp70, molecular chaperones that together facilitate the folding, remodelling and maturation of the many 'client proteins' of Hsp90 2. The glucocorticoid receptor (GR) is a model client protein that is strictly dependent on Hsp90 and Hsp70 for activity 3-7. Chaperoning GR involves a cycle of inactivation by Hsp70; formation of an inactive GR-Hsp90-Hsp70-Hop 'loading' complex; conversion to an active GR-Hsp90-p23 'maturation' complex; and subsequent GR release 8. However, to our knowledge, a molecular understanding of this intricate chaperone cycle is lacking for any client protein. Here we report the cryo-electron microscopy structure of the GR-loading complex, in which Hsp70 loads GR onto Hsp90, uncovering the molecular basis of direct coordination by Hsp90 and Hsp70. The structure reveals two Hsp70 proteins, one of which delivers GR and the other scaffolds the Hop cochaperone. Hop interacts with all components of the complex, including GR, and poises Hsp90 for subsequent ATP hydrolysis. GR is partially unfolded and recognized through an extended binding pocket composed of Hsp90, Hsp70 and Hop, revealing the mechanism of GR loading and inactivation. Together with the GR-maturation complex structure 9, we present a complete molecular mechanism of chaperone-dependent client remodelling, and establish general principles of client recognition, inhibition, transfer and activation.

Overview

Integrity signals

Registry

Crossref · 10.1038/s41586-021-04252-1

Cites

99 of 99 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

45 Own result · 33 Own interpretation · 13 Supported · 11 Partly supported · 3 Supported so far · 3 No full text of the sources · 3 Own method · 1 No basis given · accuracy not yet measured

Show all 51 claims

  • It may state two separate claims as one. 52
  • Probably not a substantial claim. 12
  • The quote only partly states this claim. 1
61 of 61
  • The paper relies on this without support.

    The reconstituted loading complex containing Hsp90(D93N) and excess ADP represents the native client-loading intermediate of the GR chaperone cycle.

    “The client-loading complex was prepared by reconstitution using excess ADP to enhance client binding by Hsp70 and an ATP-binding deficient Hsp90 (Hsp90(D93N)) to stall the cycle at this intermediate step”
  • The paper relies on this without support.

    The structural features observed in the cryo-EM map reflect the solution conformation of the complex and are not artifacts of glutaraldehyde stabilization or cryo-EM sample preparation.

    “followed by glutaraldehyde stabilization”
    “A cryo-EM reconstruction at around 3.6 Å resolution was obtained from about 4 million particles”
  • The paper relies on this without support.

    The GR ligand-binding domain used in the reconstitution behaves as full-length GR in the chaperone cycle.

    “the active GR ligand-binding domain (hereafter, GR for simplicity)”
  • The paper relies on this without support.

    Most proteins interact with Hsp70 at least during initial folding, and only a subset are Hsp90 clients.

    “Although most, if not all, proteins engage with Hsp70 at least during initial folding, only a subset are Hsp90 clients.”
  • The paper relies on this without support.

    Hop is absent from bacteria and organellar compartments, while Hsp70s are present everywhere.

    “Although Hop is absent in bacteria and organellar compartments, Hsp70s are ubiquitously present and the client binding provided by HopDP2 is probably substituted by the Hsp90amphi-α.”
5 of 5

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Self-check

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Citations

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Metadata

Authors
Wang, R. Y.-R., Noddings, C. M., Kirschke, E., Myasnikov, A. G., Johnson, J. L., & Agard, D. A.
Affiliations
  • University of California, San Francisco (US)
  • University of Idaho (US)
Corresponding author
Agard, David A.
Venue
Nature
Published
2021-12-22
Volume
601
Issue
7893
Pages
460-464
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W4200487611
Cited by
220
References
77
Citations by year
2026: 43 · 2025: 45 · 2024: 49 · 2023: 42 · 2022: 33 · 2021: 7
FWCI
9.25
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • Research Square (submittedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (submittedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • W. M. Keck Foundation
  • Life Sciences Research Foundation
  • National Institutes of Health (1s10od021741-01, 1s10od020054-01)
  • University of California, San Francisco
  • National Cancer Institute (F31CA265084)
  • National Institute of General Medical Sciences (R35GM118099, P20GM104420, R01GM127675)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
Keywords
HSP90, HSP70, glucocorticoid receptor, protein maturation, Hsp90 client proteins, protein unfolding, ATP hydrolysis, chaperone cycle, cryo-EM structure
MeSH terms
Humans, Protein Binding, Receptors, Glucocorticoid, Protein Folding, Homeodomain Proteins, Molecular Chaperones, HSP70 Heat-Shock Proteins, HSP90 Heat-Shock Proteins, Cryoelectron Microscopy

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