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X-ray structural analyses of azide-bound cytochrome c oxidases reveal that the H-pathway is critically important for the proton-pumping activity.

Shimada A, Hatano K, Tadehara H, Yano N, Shinzawa-Itoh K, Yamashita E, Muramoto K, Tsukihara T, Yoshikawa S
J Biol Chem 293 14868-14879 (2018)
Related entries: 5z84, 5z85, 5zco, 5zcp, 5zcq, 8gvm

Cited: 11 times
EuropePMC logo PMID: 30077971

Abstract

Cytochrome c oxidase (CcO) is the terminal oxidase of cellular respiration, reducing O2 to water and pumping protons. X-ray structural features have suggested that CcO pumps protons via a mechanism involving electrostatic repulsions between pumping protons in the hydrogen-bond network of a proton-conducting pathway (the H-pathway) and net positive charges created upon oxidation of an iron site, heme a (Fe a2+), for reduction of O2 at another iron site, heme a3 (Fe a32+). The protons for pumping are transferred to the hydrogen-bond network from the N-side via the water channel of the H-pathway. Back-leakage of protons to the N-side is thought to be blocked by closure of the water channel. To experimentally test this, we examined X-ray structures of the azide-bound, oxidized bovine CcO and found that an azide derivative (N3--Fe a33+, CuB2+-N3-) induces a translational movement of the heme a3 plane. This was accompanied by opening of the water channel, revealing that Fe a3 and the H-pathway are tightly coupled. The channel opening in the oxidized state is likely to induce back-leakage of pumping protons, which lowers the proton level in the hydrogen-bond network during enzymatic turnover. The proton level decrease weakens the electron affinity of Fe a , if Fe a electrostatically interacts with protons in the hydrogen-bond network. The previously reported azide-induced redox-potential decrease in Fe a supports existence of the electrostatic interaction. In summary, our results indicate that the H-pathway is critical for CcO's proton-pumping function.

Articles - 5z86 mentioned but not cited (2)

  1. Multiscale Simulations of Biological Membranes: The Challenge To Understand Biological Phenomena in a Living Substance. Enkavi G, Javanainen M, Kulig W, Róg T, Vattulainen I. Chem Rev 119 5607-5774 (2019)
  2. X-ray structural analyses of azide-bound cytochrome c oxidases reveal that the H-pathway is critically important for the proton-pumping activity. Shimada A, Hatano K, Tadehara H, Yano N, Shinzawa-Itoh K, Yamashita E, Muramoto K, Tsukihara T, Yoshikawa S. J Biol Chem 293 14868-14879 (2018)


Reviews citing this publication (2)

  1. Complex Interplay of Heme-Copper Oxidases with Nitrite and Nitric Oxide. Chen J, Xie P, Huang Y, Gao H. Int J Mol Sci 23 979 (2022)
  2. Recent progress in experimental studies on the catalytic mechanism of cytochrome c oxidase. Shimada A, Tsukihara T, Yoshikawa S. Front Chem 11 1108190 (2023)

Articles citing this publication (7)

  1. Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase. Ishigami I, Lewis-Ballester A, Echelmeier A, Brehm G, Zatsepin NA, Grant TD, Coe JD, Lisova S, Nelson G, Zhang S, Dobson ZF, Boutet S, Sierra RG, Batyuk A, Fromme P, Fromme R, Spence JCH, Ros A, Yeh SR, Rousseau DL. Proc Natl Acad Sci U S A 116 3572-3577 (2019)
  2. X-ray structures of catalytic intermediates of cytochrome c oxidase provide insights into its O2 activation and unidirectional proton-pump mechanisms. Shimada A, Etoh Y, Kitoh-Fujisawa R, Sasaki A, Shinzawa-Itoh K, Hiromoto T, Yamashita E, Muramoto K, Tsukihara T, Yoshikawa S. J Biol Chem 295 5818-5833 (2020)
  3. Critical roles of the CuB site in efficient proton pumping as revealed by crystal structures of mammalian cytochrome c oxidase catalytic intermediates. Shimada A, Hara F, Shinzawa-Itoh K, Kanehisa N, Yamashita E, Muramoto K, Tsukihara T, Yoshikawa S. J Biol Chem 297 100967 (2021)
  4. Structural basis for safe and efficient energy conversion in a respiratory supercomplex. Kao WC, Ortmann de Percin Northumberland C, Cheng TC, Ortiz J, Durand A, von Loeffelholz O, Schilling O, Biniossek ML, Klaholz BP, Hunte C. Nat Commun 13 545 (2022)
  5. Crystallographic studies of cytochrome c and cytochrome c oxidase. Tsukihara T. J Biochem 171 13-15 (2022)
  6. Characterisation of the Cyanate Inhibited State of Cytochrome c Oxidase. Kruse F, Nguyen AD, Dragelj J, Schlesinger R, Heberle J, Mroginski MA, Weidinger IM. Sci Rep 10 3863 (2020)
  7. Crystallographic cyanide-probing for cytochrome c oxidase reveals structural bases suggesting that a putative proton transfer H-pathway pumps protons. Shimada A, Baba J, Nagao S, Shinzawa-Itoh K, Yamashita E, Muramoto K, Tsukihara T, Yoshikawa S. J Biol Chem 299 105277 (2023)


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