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Microscopic heat pulses activate cardiac thin filaments.

Abstract

During the excitation-contraction coupling of the heart, sarcomeres are activated via thin filament structural changes (i.e., from the "off" state to the "on" state) in response to a release of Ca2+ from the sarcoplasmic reticulum. This process involves chemical reactions that are highly dependent on ambient temperature; for example, catalytic activity of the actomyosin ATPase rises with increasing temperature. Here, we investigate the effects of rapid heating by focused infrared (IR) laser irradiation on the sliding of thin filaments reconstituted with human α-tropomyosin and bovine ventricular troponin in an in vitro motility assay. We perform high-precision analyses measuring temperature by the fluorescence intensity of rhodamine-phalloidin-labeled F-actin coupled with a fluorescent thermosensor sheet containing the temperature-sensitive dye Europium (III) thenoyltrifluoroacetonate trihydrate. This approach enables a shift in temperature from 25°C to ∼46°C within 0.2 s. We find that in the absence of Ca2+ and presence of ATP, IR laser irradiation elicits sliding movements of reconstituted thin filaments with a sliding velocity that increases as a function of temperature. The heating-induced acceleration of thin filament sliding likewise occurs in the presence of Ca2+ and ATP; however, the temperature dependence is more than twofold less pronounced. These findings could indicate that in the mammalian heart, the on-off equilibrium of the cardiac thin filament state is partially shifted toward the on state in diastole at physiological body temperature, enabling rapid and efficient myocardial dynamics in systole.

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  • Authors+Show Affiliations

    ,

    Department of Physics, School of Advanced Science and Engineering, Waseda University, Tokyo, Japan.

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    Department of Physics, School of Advanced Science and Engineering, Waseda University, Tokyo, Japan. Department of Cell Physiology, The Jikei University School of Medicine, Tokyo, Japan. Quantum Beam Science Research Directorate, National Institutes for Quantum and Radiological Science and Technology, Gunma, Japan. PRESTO, Japan Science and Technology Agency, Saitama, Japan.

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    Department of Physics, School of Advanced Science and Engineering, Waseda University, Tokyo, Japan. Department of Cell Physiology, The Jikei University School of Medicine, Tokyo, Japan.

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    Department of Physics, School of Advanced Science and Engineering, Waseda University, Tokyo, Japan. Epithelial Biology Laboratory, Institute of Medical Biology, Agency for Science, Technology and Research, Singapore, Singapore.

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    Department Biomedical Sciences, Chubu University, Aichi, Japan.

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    PRESTO, Japan Science and Technology Agency, Saitama, Japan. Institute for Protein Research, Osaka University, Osaka, Japan.

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    Department of Cell Physiology, The Jikei University School of Medicine, Tokyo, Japan.

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    Department of Cell Physiology, The Jikei University School of Medicine, Tokyo, Japan. Department of Anesthesiology, The Jikei University School of Medicine, Tokyo, Japan.

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    Department of Cell Physiology, The Jikei University School of Medicine, Tokyo, Japan noriof@jikei.ac.jp.

    Department of Physics, Faculty of Science and Engineering, Waseda University, Tokyo, Japan ishiwata@waseda.jp.

    Source

    The Journal of general physiology 151:6 2019 Jun 03 pg 860-869

    Pub Type(s)

    Journal Article

    Language

    eng

    PubMed ID

    31010810

    Citation

    Ishii, Shuya, et al. "Microscopic Heat Pulses Activate Cardiac Thin Filaments." The Journal of General Physiology, vol. 151, no. 6, 2019, pp. 860-869.
    Ishii S, Oyama K, Arai T, et al. Microscopic heat pulses activate cardiac thin filaments. J Gen Physiol. 2019;151(6):860-869.
    Ishii, S., Oyama, K., Arai, T., Itoh, H., Shintani, S. A., Suzuki, M., ... Ishiwata, S. (2019). Microscopic heat pulses activate cardiac thin filaments. The Journal of General Physiology, 151(6), pp. 860-869. doi:10.1085/jgp.201812243.
    Ishii S, et al. Microscopic Heat Pulses Activate Cardiac Thin Filaments. J Gen Physiol. 2019 Jun 3;151(6):860-869. PubMed PMID: 31010810.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Microscopic heat pulses activate cardiac thin filaments. AU - Ishii,Shuya, AU - Oyama,Kotaro, AU - Arai,Tomomi, AU - Itoh,Hideki, AU - Shintani,Seine A, AU - Suzuki,Madoka, AU - Kobirumaki-Shimozawa,Fuyu, AU - Terui,Takako, AU - Fukuda,Norio, AU - Ishiwata,Shin'ichi, Y1 - 2019/04/22/ PY - 2018/09/14/received PY - 2019/02/20/revised PY - 2019/03/31/accepted PY - 2019/12/03/pmc-release PY - 2019/4/24/pubmed PY - 2019/4/24/medline PY - 2019/4/24/entrez SP - 860 EP - 869 JF - The Journal of general physiology JO - J. Gen. Physiol. VL - 151 IS - 6 N2 - During the excitation-contraction coupling of the heart, sarcomeres are activated via thin filament structural changes (i.e., from the "off" state to the "on" state) in response to a release of Ca2+ from the sarcoplasmic reticulum. This process involves chemical reactions that are highly dependent on ambient temperature; for example, catalytic activity of the actomyosin ATPase rises with increasing temperature. Here, we investigate the effects of rapid heating by focused infrared (IR) laser irradiation on the sliding of thin filaments reconstituted with human α-tropomyosin and bovine ventricular troponin in an in vitro motility assay. We perform high-precision analyses measuring temperature by the fluorescence intensity of rhodamine-phalloidin-labeled F-actin coupled with a fluorescent thermosensor sheet containing the temperature-sensitive dye Europium (III) thenoyltrifluoroacetonate trihydrate. This approach enables a shift in temperature from 25°C to ∼46°C within 0.2 s. We find that in the absence of Ca2+ and presence of ATP, IR laser irradiation elicits sliding movements of reconstituted thin filaments with a sliding velocity that increases as a function of temperature. The heating-induced acceleration of thin filament sliding likewise occurs in the presence of Ca2+ and ATP; however, the temperature dependence is more than twofold less pronounced. These findings could indicate that in the mammalian heart, the on-off equilibrium of the cardiac thin filament state is partially shifted toward the on state in diastole at physiological body temperature, enabling rapid and efficient myocardial dynamics in systole. SN - 1540-7748 UR - https://www.unboundmedicine.com/medline/citation/31010810/Microscopic_heat_pulses_activate_cardiac_thin_filaments L2 - http://jgp.rupress.org/cgi/pmidlookup?view=long&pmid=31010810 DB - PRIME DP - Unbound Medicine ER -