A nanosecond time-resolved XFEL analysis of structural changes associated with CO release from cytochrome C oxidase

Atsuhiro Shimada, Minoru Kubo, Seiki Baba, Keitaro Yamashita, Kunio Hirata, Go Ueno, Takashi Nomura, Tetsunari Kimura, Kyoko Shinzawa-Itoh, Junpei Baba, Keita Hatano, Yuki Eto, Akari Miyamoto, Hironori Murakami, Takashi Kumasaka, Shigeki Owada, Kensuke Tono, Makina Yabashi, Yoshihiro Yamaguchi, Sachiko YanagisawaMiyuki Sakaguchi, Takashi Ogura, Ryo Komiya, Jiwang Yan, Eiki Yamashita, Masaki Yamamoto, Hideo Ago, Shinya Yoshikawa, Tomitake Tsukihara

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Abstract

Bovine cytochrome c oxidase (CcO), a 420-kDa membrane protein, pumps protons using electrostatic repulsion between protons transferred through a water channel and net positive charges created by oxidation of heme a (Fea) for reduction of O2 at heme a3 (Fea3). For this process to function properly, timing is essential: The channelmust be closed after collection of the protons to be pumped and before Fea oxidation. If the channel were to remain open, spontaneous backflow of the collected protons would occur. For elucidation of the channel closure mechanism, the opening of the channel, which occurs upon release of COfrom CcO, is investigated by newly developed time-resolved x-ray freeelectron laser and infrared techniqueswith nanosecond time resolution. The opening process indicates that CuB senses completion of proton collection and binds O2 before binding to Fea3 to close the water channel using a conformational relay system, which includes CuB, heme a3, and a transmembrane helix, to block backflow of the collected protons.

Original languageEnglish
Article numbere1603042
JournalScience advances
Volume3
Issue number7
DOIs
Publication statusPublished - 2017 Jul 5

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ASJC Scopus subject areas

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Shimada, A., Kubo, M., Baba, S., Yamashita, K., Hirata, K., Ueno, G., Nomura, T., Kimura, T., Shinzawa-Itoh, K., Baba, J., Hatano, K., Eto, Y., Miyamoto, A., Murakami, H., Kumasaka, T., Owada, S., Tono, K., Yabashi, M., Yamaguchi, Y., ... Tsukihara, T. (2017). A nanosecond time-resolved XFEL analysis of structural changes associated with CO release from cytochrome C oxidase. Science advances, 3(7), [e1603042]. https://doi.org/10.1126/sciadv.1603042