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Kv3.1 uses a timely resurgent K+ current to secure action potential repolarization

Author

Listed:
  • Alain J. Labro

    (University of Chicago, GCIS Building, Room W244, 929 East 57th Street, Chicago, Illinois 60637, USA
    University of Antwerp)

  • Michael F. Priest

    (University of Chicago, GCIS Building, Room W244, 929 East 57th Street, Chicago, Illinois 60637, USA)

  • Jérôme J. Lacroix

    (University of Chicago, GCIS Building, Room W244, 929 East 57th Street, Chicago, Illinois 60637, USA)

  • Dirk J. Snyders

    (University of Antwerp)

  • Francisco Bezanilla

    (University of Chicago, GCIS Building, Room W244, 929 East 57th Street, Chicago, Illinois 60637, USA)

Abstract

High-frequency action potential (AP) transmission is essential for rapid information processing in the central nervous system. Voltage-dependent Kv3 channels play an important role in this process thanks to their high activation threshold and fast closure kinetics, which reduce the neuron’s refractory period. However, premature Kv3 channel closure leads to incomplete membrane repolarization, preventing sustainable AP propagation. Here, we demonstrate that Kv3.1b channels solve this problem by producing resurgent K+ currents during repolarization, thus ensuring enough repolarizing power to terminate each AP. Unlike previously described resurgent Na+ and K+ currents, Kv3.1b’s resurgent current does not originate from recovery of channel block or inactivation but results from a unique combination of steep voltage-dependent gating kinetics and ultra-fast voltage-sensor relaxation. These distinct properties are readily transferrable onto an orthologue Kv channel by transplanting the voltage-sensor’s S3–S4 loop, providing molecular insights into the mechanism by which Kv3 channels contribute to high-frequency AP transmission.

Suggested Citation

  • Alain J. Labro & Michael F. Priest & Jérôme J. Lacroix & Dirk J. Snyders & Francisco Bezanilla, 2015. "Kv3.1 uses a timely resurgent K+ current to secure action potential repolarization," Nature Communications, Nature, vol. 6(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms10173
    DOI: 10.1038/ncomms10173
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    Cited by:

    1. Qiansheng Liang & Gamma Chi & Leonardo Cirqueira & Lianteng Zhi & Agostino Marasco & Nadia Pilati & Martin J. Gunthorpe & Giuseppe Alvaro & Charles H. Large & David B. Sauer & Werner Treptow & Manuel , 2024. "The binding and mechanism of a positive allosteric modulator of Kv3 channels," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Gamma Chi & Qiansheng Liang & Akshay Sridhar & John B. Cowgill & Kasim Sader & Mazdak Radjainia & Pu Qian & Pablo Castro-Hartmann & Shayla Venkaya & Nanki Kaur Singh & Gavin McKinley & Alejandra Ferna, 2022. "Cryo-EM structure of the human Kv3.1 channel reveals gating control by the cytoplasmic T1 domain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Martin J. Gunthorpe, 2022. "Timing is everything: structural insights into the disease-linked Kv3 channels controlling fast action-potential firing in the brain," Nature Communications, Nature, vol. 13(1), pages 1-4, December.
    4. Yeon Jin Kim & Beth B. Peterson & Joanna D. Crook & Hannah R. Joo & Jiajia Wu & Christian Puller & Farrel R. Robinson & Paul D. Gamlin & King-Wai Yau & Felix Viana & John B. Troy & Robert G. Smith & O, 2022. "Origins of direction selectivity in the primate retina," Nature Communications, Nature, vol. 13(1), pages 1-20, December.

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