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Structural insights into functional properties of the oxidized form of cytochrome c oxidase

Author

Listed:
  • Izumi Ishigami

    (Albert Einstein College of Medicine)

  • Raymond G. Sierra

    (SLAC National Accelerator Laboratory)

  • Zhen Su

    (SLAC National Accelerator Laboratory
    Stanford University)

  • Ariana Peck

    (SLAC National Accelerator Laboratory)

  • Cong Wang

    (SLAC National Accelerator Laboratory)

  • Frederic Poitevin

    (SLAC National Accelerator Laboratory)

  • Stella Lisova

    (SLAC National Accelerator Laboratory)

  • Brandon Hayes

    (SLAC National Accelerator Laboratory)

  • Frank R. Moss

    (SLAC National Accelerator Laboratory
    Altos Labs)

  • Sébastien Boutet

    (SLAC National Accelerator Laboratory)

  • Robert E. Sublett

    (SLAC National Accelerator Laboratory)

  • Chun Hong Yoon

    (SLAC National Accelerator Laboratory)

  • Syun-Ru Yeh

    (Albert Einstein College of Medicine)

  • Denis L. Rousseau

    (Albert Einstein College of Medicine)

Abstract

Cytochrome c oxidase (CcO) is an essential enzyme in mitochondrial and bacterial respiration. It catalyzes the four-electron reduction of molecular oxygen to water and harnesses the chemical energy to translocate four protons across biological membranes. The turnover of the CcO reaction involves an oxidative phase, in which the reduced enzyme (R) is oxidized to the metastable OH state, and a reductive phase, in which OH is reduced back to the R state. During each phase, two protons are translocated across the membrane. However, if OH is allowed to relax to the resting oxidized state (O), a redox equivalent to OH, its subsequent reduction to R is incapable of driving proton translocation. Here, with resonance Raman spectroscopy and serial femtosecond X-ray crystallography (SFX), we show that the heme a3 iron and CuB in the active site of the O state, like those in the OH state, are coordinated by a hydroxide ion and a water molecule, respectively. However, Y244, critical for the oxygen reduction chemistry, is in the neutral protonated form, which distinguishes O from OH, where Y244 is in the deprotonated tyrosinate form. These structural characteristics of O provide insights into the proton translocation mechanism of CcO.

Suggested Citation

  • Izumi Ishigami & Raymond G. Sierra & Zhen Su & Ariana Peck & Cong Wang & Frederic Poitevin & Stella Lisova & Brandon Hayes & Frank R. Moss & Sébastien Boutet & Robert E. Sublett & Chun Hong Yoon & Syu, 2023. "Structural insights into functional properties of the oxidized form of cytochrome c oxidase," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41533-x
    DOI: 10.1038/s41467-023-41533-x
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    References listed on IDEAS

    as
    1. Guillaume Tetreau & Anne-Sophie Banneville & Elena A. Andreeva & Aaron S. Brewster & Mark S. Hunter & Raymond G. Sierra & Jean-Marie Teulon & Iris D. Young & Niamh Burke & Tilman A. Grünewald & Joël B, 2020. "Serial femtosecond crystallography on in vivo-grown crystals drives elucidation of mosquitocidal Cyt1Aa bioactivation cascade," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. F. Kolbe & S. Safarian & Ż. Piórek & S. Welsch & H. Müller & H. Michel, 2021. "Cryo-EM structures of intermediates suggest an alternative catalytic reaction cycle for cytochrome c oxidase," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    3. Jacques-Philippe Colletier & Michael R. Sawaya & Mari Gingery & Jose A. Rodriguez & Duilio Cascio & Aaron S. Brewster & Tara Michels-Clark & Robert H. Hice & Nicolas Coquelle & Sébastien Boutet & Gart, 2016. "De novo phasing with X-ray laser reveals mosquito larvicide BinAB structure," Nature, Nature, vol. 539(7627), pages 43-47, November.
    4. Michael I. Verkhovsky & Audrius Jasaitis & Marina L. Verkhovskaya & Joel E. Morgan & Mårten Wikström, 1999. "Proton translocation by cytochrome c oxidase," Nature, Nature, vol. 400(6743), pages 480-483, July.
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