IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-44847-6.html
   My bibliography  Save this article

Cochaperones convey the energy of ATP hydrolysis for directional action of Hsp90

Author

Listed:
  • Leonie Vollmar

    (University of Freiburg
    University of Freiburg)

  • Julia Schimpf

    (University of Freiburg
    University of Freiburg)

  • Bianca Hermann

    (University of Freiburg)

  • Thorsten Hugel

    (University of Freiburg
    University of Freiburg)

Abstract

The molecular chaperone and heat shock protein Hsp90 is part of many protein complexes in eukaryotic cells. Together with its cochaperones, Hsp90 is responsible for the maturation of hundreds of clients. Although having been investigated for decades, it still is largely unknown which components are necessary for a functional complex and how the energy of ATP hydrolysis is used to enable cyclic operation. Here we use single-molecule FRET to show how cochaperones introduce directionality into Hsp90’s conformational changes during its interaction with the client kinase Ste11. Three cochaperones are needed to couple ATP turnover to these conformational changes. All three are therefore essential for a functional cyclic operation, which requires coupling to an energy source. Finally, our findings show how the formation of sub-complexes in equilibrium followed by a directed selection of the functional complex can be the most energy efficient pathway for kinase maturation.

Suggested Citation

  • Leonie Vollmar & Julia Schimpf & Bianca Hermann & Thorsten Hugel, 2024. "Cochaperones convey the energy of ATP hydrolysis for directional action of Hsp90," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44847-6
    DOI: 10.1038/s41467-024-44847-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-44847-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-44847-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ryohei Yasuda & Hiroyuki Noji & Masasuke Yoshida & Kazuhiko Kinosita & Hiroyasu Itoh, 2001. "Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase," Nature, Nature, vol. 410(6831), pages 898-904, April.
    2. Fabio D. Steffen & Mokrane Khier & Danny Kowerko & Richard A. Cunha & Richard Börner & Roland K. O. Sigel, 2020. "Metal ions and sugar puckering balance single-molecule kinetic heterogeneity in RNA and DNA tertiary contacts," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. C. Ratzke & B. Hellenkamp & T. Hugel, 2014. "Four-colour FRET reveals directionality in the Hsp90 multicomponent machinery," Nature Communications, Nature, vol. 5(1), pages 1-9, September.
    4. Maru Jaime-Garza & Carlos A. Nowotny & Daniel Coutandin & Feng Wang & Mariano Tabios & David A. Agard, 2023. "Hsp90 provides a platform for kinase dephosphorylation by PP5," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yan Kuai & Junxue Chen & Zetao Fan & Gang Zou & Joseph. R. Lakowicz & Douguo Zhang, 2021. "Planar photonic chips with tailored angular transmission for high-contrast-imaging devices," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    2. J. Kishikawa & A. Nakanishi & A. Nakano & S. Saeki & A. Furuta & T. Kato & K. Mistuoka & K. Yokoyama, 2022. "Structural snapshots of V/A-ATPase reveal the rotary catalytic mechanism of rotary ATPases," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Atsuki Nakano & Jun-ichi Kishikawa & Kaoru Mitsuoka & Ken Yokoyama, 2023. "Mechanism of ATP hydrolysis dependent rotation of bacterial ATP synthase," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    4. Paul David Harris & Alessandra Narducci & Christian Gebhardt & Thorben Cordes & Shimon Weiss & Eitan Lerner, 2022. "Multi-parameter photon-by-photon hidden Markov modeling," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-44847-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.