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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
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    References listed on IDEAS

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    1. 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.
    2. 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.
    3. 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.
    4. 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.
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