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Chemistry of ion coordination and hydration revealed by a K+ channel–Fab complex at 2.0 Å resolution

Author

Listed:
  • Yufeng Zhou

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

  • João H. Morais-Cabral

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

  • Amelia Kaufman

    (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

Ion transport proteins must remove an ion's hydration shell to coordinate the ion selectively on the basis of its size and charge. To discover how the K+ channel solves this fundamental aspect of ion conduction, we solved the structure of the KcsA K+ channel in complex with a monoclonal Fab antibody fragment at 2.0 Å resolution. Here we show how the K+ channel displaces water molecules around an ion at its extracellular entryway, and how it holds a K+ ion in a square antiprism of water molecules in a cavity near its intracellular entryway. Carbonyl oxygen atoms within the selectivity filter form a very similar square antiprism around each K+ binding site, as if to mimic the waters of hydration. The selectivity filter changes its ion coordination structure in low K+ solutions. This structural change is crucial to the operation of the selectivity filter in the cellular context, where the K+ ion concentration near the selectivity filter varies in response to channel gating.

Suggested Citation

  • Yufeng Zhou & João H. Morais-Cabral & Amelia Kaufman & Roderick MacKinnon, 2001. "Chemistry of ion coordination and hydration revealed by a K+ channel–Fab complex at 2.0 Å resolution," Nature, Nature, vol. 414(6859), pages 43-48, November.
    • Handle: RePEc:nat:nature:v:414:y:2001:i:6859:d:10.1038_35102009
    DOI: 10.1038/35102009
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    Cited by:

    1. Rongming Xu & Yuan Kang & Weiming Zhang & Bingcai Pan & Xiwang Zhang, 2023. "Two-dimensional MXene membranes with biomimetic sub-nanochannels for enhanced cation sieving," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. 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.
    3. Adam C. Oken & Nicolas E. Lisi & Ipsita Krishnamurthy & Alanna E. McCarthy & Michael H. Godsey & Arthur Glasfeld & Steven E. Mansoor, 2024. "High-affinity agonism at the P2X7 receptor is mediated by three residues outside the orthosteric pocket," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. 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.
    5. Marcos Matamoros & Xue Wen Ng & Joshua B. Brettmann & David W. Piston & Colin G. Nichols, 2023. "Conformational plasticity of NaK2K and TREK2 potassium channel selectivity filters," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Ri-Jian Mo & Shuang Chen & Li-Qiu Huang & Xin-Lei Ding & Saima Rafique & Xing-Hua Xia & Zhong-Qiu Li, 2024. "Regulating ion affinity and dehydration of metal-organic framework sub-nanochannels for high-precision ion separation," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    7. Ahmed Rohaim & Bram J. A. Vermeulen & Jing Li & Felix Kümmerer & Federico Napoli & Lydia Blachowicz & João Medeiros-Silva & Benoît Roux & Markus Weingarth, 2022. "A distinct mechanism of C-type inactivation in the Kv-like KcsA mutant E71V," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Yue Wang & Yixiao Hu & Jian-Ping Guo & Jun Gao & Bo Song & Lei Jiang, 2024. "A physical derivation of high-flux ion transport in biological channel via quantum ion coherence," Nature Communications, Nature, vol. 15(1), pages 1-8, December.
    9. Purushotham Selvakumar & Ana I. Fernández-Mariño & Nandish Khanra & Changhao He & Alice J. Paquette & Bing Wang & Ruiqi Huang & Vaughn V. Smider & William J. Rice & Kenton J. Swartz & Joel R. Meyerson, 2022. "Structures of the T cell potassium channel Kv1.3 with immunoglobulin modulators," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Xingya Li & Gengping Jiang & Meipeng Jian & Chen Zhao & Jue Hou & Aaron W. Thornton & Xinyi Zhang & Jefferson Zhe Liu & Benny D. Freeman & Huanting Wang & Lei Jiang & Huacheng Zhang, 2023. "Construction of angstrom-scale ion channels with versatile pore configurations and sizes by metal-organic frameworks," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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