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Structural snapshots of V/A-ATPase reveal the rotary catalytic mechanism of rotary ATPases

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  • J. Kishikawa

    (Kyoto Sangyo University, Kamigamo-Motoyama
    Osaka University)

  • A. Nakanishi

    (Kyoto Sangyo University, Kamigamo-Motoyama
    Osaka University)

  • A. Nakano

    (Kyoto Sangyo University, Kamigamo-Motoyama)

  • S. Saeki

    (Kyoto Sangyo University, Kamigamo-Motoyama)

  • A. Furuta

    (Kyoto Sangyo University, Kamigamo-Motoyama)

  • T. Kato

    (Osaka University)

  • K. Mistuoka

    (Osaka University)

  • K. Yokoyama

    (Kyoto Sangyo University, Kamigamo-Motoyama)

Abstract

V/A-ATPase is a motor protein that shares a common rotary catalytic mechanism with FoF1 ATP synthase. When powered by ATP hydrolysis, the V1 domain rotates the central rotor against the A3B3 hexamer, composed of three catalytic AB dimers adopting different conformations (ABopen, ABsemi, and ABclosed). Here, we report the atomic models of 18 catalytic intermediates of the V1 domain of V/A-ATPase under different reaction conditions, determined by single particle cryo-EM. The models reveal that the rotor does not rotate immediately after binding of ATP to the V1. Instead, three events proceed simultaneously with the 120˚ rotation of the shaft: hydrolysis of ATP in ABsemi, zipper movement in ABopen by the binding ATP, and unzipper movement in ABclosed with release of both ADP and Pi. This indicates the unidirectional rotation of V/A-ATPase by a ratchet-like mechanism owing to ATP hydrolysis in ABsemi, rather than the power stroke model proposed previously for F1-ATPase.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28832-5
    DOI: 10.1038/s41467-022-28832-5
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    References listed on IDEAS

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    1. Meghna Sobti & Hiroshi Ueno & Hiroyuki Noji & Alastair G. Stewart, 2021. "The six steps of the complete F1-ATPase rotary catalytic cycle," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. Hiroyuki Noji & Ryohei Yasuda & Masasuke Yoshida & Kazuhiko Kinosita, 1997. "Direct observation of the rotation of F1-ATPase," Nature, Nature, vol. 386(6622), pages 299-302, March.
    3. Rikiya Watanabe & Hiroyuki Noji, 2014. "Timing of inorganic phosphate release modulates the catalytic activity of ATP-driven rotary motor protein," Nature Communications, Nature, vol. 5(1), pages 1-7, May.
    4. Matteo Allegretti & Niklas Klusch & Deryck J. Mills & Janet Vonck & Werner Kühlbrandt & Karen M. Davies, 2015. "Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase," Nature, Nature, vol. 521(7551), pages 237-240, May.
    5. Hongyun Wang & George Oster, 1998. "Energy transduction in the F1 motor of ATP synthase," Nature, Nature, vol. 396(6708), pages 279-282, November.
    6. Mohammad T. Mazhab-Jafari & Alexis Rohou & Carla Schmidt & Stephanie A. Bueler & Samir Benlekbir & Carol V. Robinson & John L. Rubinstein, 2016. "Atomic model for the membrane-embedded VO motor of a eukaryotic V-ATPase," Nature, Nature, vol. 539(7627), pages 118-122, November.
    7. Atsuko Nakanishi & Jun-ichi Kishikawa & Masatada Tamakoshi & Kaoru Mitsuoka & Ken Yokoyama, 2018. "Cryo EM structure of intact rotary H+-ATPase/synthase from Thermus thermophilus," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    8. Timothy Elston & Hongyun Wang & George Oster, 1998. "Energy transduction in ATP synthase," Nature, Nature, vol. 391(6666), pages 510-513, January.
    9. 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.
    10. Shou Furuike & Masahiro Nakano & Kengo Adachi & Hiroyuki Noji & Kazuhiko Kinosita & Ken Yokoyama, 2011. "Resolving stepping rotation in Thermus thermophilus H+-ATPase/synthase with an essentially drag-free probe," Nature Communications, Nature, vol. 2(1), pages 1-9, September.
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