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    Voltage sensor movements of Ca1.1 during an action potential in skeletal muscle fibers

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    Author
    Banks, Quinton cc
    Bibollet, Hugo
    Contreras, Minerva
    Bennett, Daniel F
    Bannister, Roger A
    Schneider, Martin F
    Hernández-Ochoa, Erick O
    Date
    2021-10-05
    Journal
    Proceedings of the National Academy of Sciences of the United States of America
    Publisher
    National Academy of Sciences of the United States of America
    Type
    Article
    
    Metadata
    Show full item record
    See at
    https://doi.org/10.1073/pnas.2026116118
    Abstract
    The skeletal muscle L-type Ca2+ channel (CaV1.1) works primarily as a voltage sensor for skeletal muscle action potential (AP)-evoked Ca2+ release. CaV1.1 contains four distinct voltage-sensing domains (VSDs), yet the contribution of each VSD to AP-evoked Ca2+ release remains unknown. To investigate the role of VSDs in excitation-contraction coupling (ECC), we encoded cysteine substitutions on each S4 voltage-sensing segment of CaV1.1, expressed each construct via in vivo gene transfer electroporation, and used in cellulo AP fluorometry to track the movement of each CaV1.1 VSD in skeletal muscle fibers. We first provide electrical measurements of CaV1.1 voltage sensor charge movement in response to an AP waveform. Then we characterize the fluorescently labeled channels' VSD fluorescence signal responses to an AP and compare them with the waveforms of the electrically measured charge movement, the optically measured free myoplasmic Ca2+, and the calculated rate of Ca2+ release from the sarcoplasmic reticulum for an AP, the physiological signal for skeletal muscle fiber activation. A considerable fraction of the fluorescence signal for each VSD occurred after the time of peak Ca2+ release, and even more occurred after the earlier peak of electrically measured charge movement during an AP, and thus could not directly reflect activation of Ca2+ release or charge movement, respectively. However, a sizable fraction of the fluorometric signals for VSDs I, II, and IV, but not VSDIII, overlap the rising phase of charge moved, and even more for Ca2+ release, and thus could be involved in voltage sensor rearrangements or Ca2+ release activation.
    Keyword
    CaV1.1
    action potential
    excitation–contraction coupling
    skeletal muscle
    voltage sensor domain
    Identifier to cite or link to this item
    http://hdl.handle.net/10713/16763
    ae974a485f413a2113503eed53cd6c53
    10.1073/pnas.2026116118
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