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Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands

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  • Sergei Yu. Noskov

    (Weill Medical College of Cornell University
    Russian Academy of Sciences)

  • Simon Bernèche

    (University of Basel)

  • Benoît Roux

    (Weill Medical College of Cornell University)

Abstract

Potassium channels are essential for maintaining a normal ionic balance across cell membranes. Central to this function is the ability of such channels to support transmembrane ion conduction at nearly diffusion-limited rates while discriminating for K+ over Na+ by more than a thousand-fold. This selectivity arises because the transfer of the K+ ion into the channel pore is energetically favoured, a feature commonly attributed to a structurally precise fit between the K+ ion and carbonyl groups lining the rigid and narrow pore1. But proteins are relatively flexible structures2,3 that undergo rapid thermal atomic fluctuations larger than the small difference in ionic radius between K+ and Na+. Here we present molecular dynamics simulations for the potassium channel KcsA, which show that the carbonyl groups coordinating the ion in the narrow pore are indeed very dynamic (‘liquid-like’) and that their intrinsic electrostatic properties control ion selectivity. This finding highlights the importance of the classical concept of field strength4. Selectivity for K+ is seen to emerge as a robust feature of a flexible fluctuating pore lined by carbonyl groups.

Suggested Citation

  • Sergei Yu. Noskov & Simon Bernèche & Benoît Roux, 2004. "Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands," Nature, Nature, vol. 431(7010), pages 830-834, October.
  • Handle: RePEc:nat:nature:v:431:y:2004:i:7010:d:10.1038_nature02943
    DOI: 10.1038/nature02943
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    Cited by:

    1. Weiwen Xin & Jingru Fu & Yongchao Qian & Lin Fu & Xiang-Yu Kong & Teng Ben & Lei Jiang & Liping Wen, 2022. "Biomimetic KcsA channels with ultra-selective K+ transport for monovalent ion sieving," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Carus H. Y. Lau & Emelie Flood & Mark J. Hunter & Billy J. Williams-Noonan & Karen M. Corbett & Chai-Ann Ng & James C. Bouwer & Alastair G. Stewart & Eduardo Perozo & Toby W. Allen & Jamie I. Vandenbe, 2024. "Potassium dependent structural changes in the selectivity filter of HERG potassium channels," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Lilia Leisle & Kin Lam & Sepehr Dehghani-Ghahnaviyeh & Eva Fortea & Jason D. Galpin & Christopher A. Ahern & Emad Tajkhorshid & Alessio Accardi, 2022. "Backbone amides are determinants of Cl− selectivity in CLC ion channels," Nature Communications, Nature, vol. 13(1), pages 1-11, December.

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