Japan Agency for Medical Research and Development (AMED)
JP21wm0525018
Japan
Japan Society for the Promotion of Science (JSPS)
22H04742
Japan
Japan Society for the Promotion of Science (JSPS)
JP20K21383
Japan
Japan Society for the Promotion of Science (JSPS)
JP21H01875
Japan
Japan Society for the Promotion of Science (JSPS)
21H05142
Japan
Japan Society for the Promotion of Science (JSPS)
22H00400
Japan
Japan Society for the Promotion of Science (JSPS)
22K19265
Japan
Citation
Journal: Cell / Year: 2023 Title: Structural basis for ion selectivity in potassium-selective channelrhodopsins. Authors: Seiya Tajima / Yoon Seok Kim / Masahiro Fukuda / YoungJu Jo / Peter Y Wang / Joseph M Paggi / Masatoshi Inoue / Eamon F X Byrne / Koichiro E Kishi / Seiwa Nakamura / Charu Ramakrishnan / ...Authors: Seiya Tajima / Yoon Seok Kim / Masahiro Fukuda / YoungJu Jo / Peter Y Wang / Joseph M Paggi / Masatoshi Inoue / Eamon F X Byrne / Koichiro E Kishi / Seiwa Nakamura / Charu Ramakrishnan / Shunki Takaramoto / Takashi Nagata / Masae Konno / Masahiro Sugiura / Kota Katayama / Toshiki E Matsui / Keitaro Yamashita / Suhyang Kim / Hisako Ikeda / Jaeah Kim / Hideki Kandori / Ron O Dror / Keiichi Inoue / Karl Deisseroth / Hideaki E Kato / Abstract: KCR channelrhodopsins (K-selective light-gated ion channels) have received attention as potential inhibitory optogenetic tools but more broadly pose a fundamental mystery regarding how their K ...KCR channelrhodopsins (K-selective light-gated ion channels) have received attention as potential inhibitory optogenetic tools but more broadly pose a fundamental mystery regarding how their K selectivity is achieved. Here, we present 2.5-2.7 Å cryo-electron microscopy structures of HcKCR1 and HcKCR2 and of a structure-guided mutant with enhanced K selectivity. Structural, electrophysiological, computational, spectroscopic, and biochemical analyses reveal a distinctive mechanism for K selectivity; rather than forming the symmetrical filter of canonical K channels achieving both selectivity and dehydration, instead, three extracellular-vestibule residues within each monomer form a flexible asymmetric selectivity gate, while a distinct dehydration pathway extends intracellularly. Structural comparisons reveal a retinal-binding pocket that induces retinal rotation (accounting for HcKCR1/HcKCR2 spectral differences), and design of corresponding KCR variants with increased K selectivity (KALI-1/KALI-2) provides key advantages for optogenetic inhibition in vitro and in vivo. Thus, discovery of a mechanism for ion-channel K selectivity also provides a framework for next-generation optogenetics.
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