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Kinetics and mapping of Ca-driven calmodulin conformations on skeletal and cardiac muscle ryanodine receptors

Author

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  • Robyn T. Rebbeck

    (University of Minnesota)

  • Bengt Svensson

    (University of Minnesota)

  • Jingyan Zhang

    (University of Minnesota)

  • Montserrat Samsó

    (Virginia Commonwealth University)

  • David D. Thomas

    (University of Minnesota)

  • Donald M. Bers

    (University of California at Davis)

  • Razvan L. Cornea

    (University of Minnesota)

Abstract

Calmodulin transduces [Ca2+] information regulating the rhythmic Ca2+ cycling between the sarcoplasmic reticulum and cytoplasm during contraction and relaxation in cardiac and skeletal muscle. However, the structural dynamics by which calmodulin modulates the sarcoplasmic reticulum Ca2+ release channel, the ryanodine receptor, at physiologically relevant [Ca2+] is unknown. Using fluorescence lifetime FRET, we resolve different structural states of calmodulin and Ca2+-driven shifts in the conformation of calmodulin bound to ryanodine receptor. Skeletal and cardiac ryanodine receptor isoforms show different calmodulin-ryanodine receptor conformations, as well as binding and structural kinetics with 0.2-ms resolution, which reflect different functional roles of calmodulin. These FRET methods provide insight into the physiological calmodulin-ryanodine receptor structural states, revealing additional distinct structural states that complement cryo-EM models that are based on less physiological conditions. This technology will drive future studies on pathological calmodulin-ryanodine receptor interactions and dynamics with other important ryanodine receptor bound modulators.

Suggested Citation

  • Robyn T. Rebbeck & Bengt Svensson & Jingyan Zhang & Montserrat Samsó & David D. Thomas & Donald M. Bers & Razvan L. Cornea, 2024. "Kinetics and mapping of Ca-driven calmodulin conformations on skeletal and cardiac muscle ryanodine receptors," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48951-5
    DOI: 10.1038/s41467-024-48951-5
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    References listed on IDEAS

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    1. Ran Zalk & Oliver B. Clarke & Amédée des Georges & Robert A. Grassucci & Steven Reiken & Filippo Mancia & Wayne A. Hendrickson & Joachim Frank & Andrew R. Marks, 2015. "Structure of a mammalian ryanodine receptor," Nature, Nature, vol. 517(7532), pages 44-49, January.
    2. Deshun Gong & Ximin Chi & Jinhong Wei & Gewei Zhou & Gaoxingyu Huang & Lin Zhang & Ruiwu Wang & Jianlin Lei & S. R. Wayne Chen & Nieng Yan, 2019. "Modulation of cardiac ryanodine receptor 2 by calmodulin," Nature, Nature, vol. 572(7769), pages 347-351, August.
    3. Kellie A. Woll & Omid Haji-Ghassemi & Filip Van Petegem, 2021. "Pathological conformations of disease mutant Ryanodine Receptors revealed by cryo-EM," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Rouslan G. Efremov & Alexander Leitner & Ruedi Aebersold & Stefan Raunser, 2015. "Architecture and conformational switch mechanism of the ryanodine receptor," Nature, Nature, vol. 517(7532), pages 39-43, January.
    5. Zhen Yan & Xiao-chen Bai & Chuangye Yan & Jianping Wu & Zhangqiang Li & Tian Xie & Wei Peng & Chang-cheng Yin & Xueming Li & Sjors H. W. Scheres & Yigong Shi & Nieng Yan, 2015. "Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution," Nature, Nature, vol. 517(7532), pages 50-55, January.
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