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An iris diaphragm mechanism to gate a cyclic nucleotide-gated ion channel

Author

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  • Arin Marchesi

    (INSERM U1006, Aix-Marseille Université, Parc Scientifique et Technologique de Luminy
    Parc Scientifique et Technologique de Luminy)

  • Xiaolong Gao

    (Weill Cornell Medical College)

  • Ricardo Adaixo

    (University of Basel)

  • Jan Rheinberger

    (Weill Cornell Medical College)

  • Henning Stahlberg

    (University of Basel)

  • Crina Nimigean

    (Weill Cornell Medical College
    Weill Cornell Medical College
    Weill Cornell Medical College)

  • Simon Scheuring

    (INSERM U1006, Aix-Marseille Université, Parc Scientifique et Technologique de Luminy
    Weill Cornell Medical College
    Weill Cornell Medical College)

Abstract

Cyclic nucleotide-gated (CNG) ion channels are non-selective cation channels key to signal transduction. The free energy difference of cyclic-nucleotide (cAMP/cGMP) binding/unbinding is translated into mechanical work to modulate the open/closed probability of the pore, i.e., gating. Despite the recent advances in structural determination of CNG channels, the conformational changes associated with gating remain unknown. Here we examine the conformational dynamics of a prokaryotic homolog of CNG channels, SthK, using high-speed atomic force microscopy (HS-AFM). HS-AFM of SthK in lipid bilayers shows that the CNBDs undergo dramatic conformational changes during the interconversion between the resting (apo and cGMP) and the activated (cAMP) states: the CNBDs approach the membrane and splay away from the 4-fold channel axis accompanied by a clockwise rotation with respect to the pore domain. We propose that these movements may be converted by the C-linker to pull the pore helices open in an iris diaphragm-like mechanism.

Suggested Citation

  • Arin Marchesi & Xiaolong Gao & Ricardo Adaixo & Jan Rheinberger & Henning Stahlberg & Crina Nimigean & Simon Scheuring, 2018. "An iris diaphragm mechanism to gate a cyclic nucleotide-gated ion channel," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-06414-8
    DOI: 10.1038/s41467-018-06414-8
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    Cited by:

    1. Vishal R. Patel & Arturo M. Salinas & Darong Qi & Shipra Gupta & David J. Sidote & Marcel P. Goldschen-Ohm, 2021. "Single-molecule imaging with cell-derived nanovesicles reveals early binding dynamics at a cyclic nucleotide-gated ion channel," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. Xiaolong Gao & Philipp A. M. Schmidpeter & Vladimir Berka & Ryan J. Durham & Chen Fan & Vasanthi Jayaraman & Crina M. Nimigean, 2022. "Gating intermediates reveal inhibitory role of the voltage sensor in a cyclic nucleotide-modulated ion channel," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Zhongjie Ye & Nicola Galvanetto & Leonardo Puppulin & Simone Pifferi & Holger Flechsig & Melanie Arndt & Cesar Adolfo Sánchez Triviño & Michael Palma & Shifeng Guo & Horst Vogel & Anna Menini & Clemen, 2024. "Structural heterogeneity of the ion and lipid channel TMEM16F," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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