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Energetic optimization of ion conduction rate by the K+ selectivity filter

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  • João H. Morais-Cabral

    (Howard Hughes Medical Institute, Laboratory of Molecular Neurobiology and Biophysics, Rockefeller University
    Yale University)

  • Yufeng Zhou

    (Howard Hughes Medical Institute, Laboratory of Molecular Neurobiology and Biophysics, Rockefeller University)

  • Roderick MacKinnon

    (Howard Hughes Medical Institute, Laboratory of Molecular Neurobiology and Biophysics, Rockefeller University)

Abstract

The K+ selectivity filter catalyses the dehydration, transfer and rehydration of a K+ ion in about ten nanoseconds. This physical process is central to the production of electrical signals in biology. Here we show how nearly diffusion-limited rates are achieved, by analysing ion conduction and the corresponding crystallographic ion distribution in the selectivity filter of the KcsA K+ channel. Measurements with K+ and its slightly larger analogue, Rb+, lead us to conclude that the selectivity filter usually contains two K+ ions separated by one water molecule. The two ions move in a concerted fashion between two configurations, K+-water-K+-water (1,3 configuration) and water-K+-water-K+ (2,4 configuration), until a third ion enters, displacing the ion on the opposite side of the queue. For K+, the energy difference between the 1,3 and 2,4 configurations is close to zero, the condition of maximum conduction rate. The energetic balance between these configurations is a clear example of evolutionary optimization of protein function.

Suggested Citation

  • João H. Morais-Cabral & Yufeng Zhou & Roderick MacKinnon, 2001. "Energetic optimization of ion conduction rate by the K+ selectivity filter," Nature, Nature, vol. 414(6859), pages 37-42, November.
    • Handle: RePEc:nat:nature:v:414:y:2001:i:6859:d:10.1038_35102000
    DOI: 10.1038/35102000
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    Cited by:

    1. 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.
    2. Shigetoshi Oiki & Masayuki Iwamoto & Takashi Sumikama, 2011. "Cycle Flux Algebra for Ion and Water Flux through the KcsA Channel Single-File Pore Links Microscopic Trajectories and Macroscopic Observables," PLOS ONE, Public Library of Science, vol. 6(1), pages 1-13, January.

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