Thermal Activation of Thin Filaments in Striated Muscle

Ishii, Shuya; Oyama, Kotaro; Shintani, Seine A.; Kobirumaki-Shimozawa, Fuyu; Ishiwata, Shin’ichi; Fukuda, Norio

doi:10.3389/fphys.2020.00278

Cited by 6 publications

(7 citation statements)

References 66 publications

(79 reference statements)

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“…Moreover, studies taking advantage of an in vitro motility assay showed that increasing temperature induces sliding movements of reconstituted thin filaments in the absence of Ca 2+ (pCa 9), above 35°C with human cardiac Tm and bovine cardiac Tn ( Ishii et al, 2019a ) and above 43°C with human cardiac Tm and human cardiac Tn ( Brunet et al, 2012 ). These findings obtained under various experimental conditions are in agreement with the supposition that crossbridge cycling is accelerated by heating in a Ca 2+ -independent manner (see Ishii et al, 2019a , 2020 for details).…”

Section: Introductionsupporting

confidence: 88%

“…Ambient temperature is an important factor that affects myofibrillar Ca 2+ sensitivity in both skeletal and cardiac muscles (e.g., Mühlrad and Hegyi, 1965 ; Murphy and Hasselbach, 1968 ; Hartshorne et al, 1972 ; Stephenson and Williams, 1981 ; Harrison and Bers, 1989 ). It has been reported that heating elicits myofibrilar force generation in a Ca 2+ -independent manner (for review see Ranatunga, 2018 ; Ishii et al, 2020 ). For example, heating has been shown to increase active force in intact frog sartorius muscle ( Hill, 1970 ) and skinned rabbit psoas fibers ( Ranatunga, 1994 ) in a relaxing solution.…”

Section: Introductionmentioning

confidence: 99%

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Myosin and tropomyosin–troponin complementarily regulate thermal activation of muscles

Ishii,

Oyama,

Kobirumaki-Shimozawa

et al. 2023

Journal of General Physiology

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Contraction of striated muscles is initiated by an increase in cytosolic Ca2+ concentration, which is regulated by tropomyosin and troponin acting on actin filaments at the sarcomere level. Namely, Ca2+-binding to troponin C shifts the “on–off” equilibrium of the thin filament state toward the “on” state, promoting actomyosin interaction; likewise, an increase in temperature to within the body temperature range shifts the equilibrium to the on state, even in the absence of Ca2+. Here, we investigated the temperature dependence of sarcomere shortening along isolated fast skeletal myofibrils using optical heating microscopy. Rapid heating (25 to 41.5°C) within 2 s induced reversible sarcomere shortening in relaxing solution. Further, we investigated the temperature-dependence of the sliding velocity of reconstituted fast skeletal or cardiac thin filaments on fast skeletal or β-cardiac myosin in an in vitro motility assay within the body temperature range. We found that (a) with fast skeletal thin filaments on fast skeletal myosin, the temperature dependence was comparable to that obtained for sarcomere shortening in fast skeletal myofibrils (Q10 ∼8), (b) both types of thin filaments started to slide at lower temperatures on fast skeletal myosin than on β-cardiac myosin, and (c) cardiac thin filaments slid at lower temperatures compared with fast skeletal thin filaments on either type of myosin. Therefore, the mammalian striated muscle may be fine-tuned to contract efficiently via complementary regulation of myosin and tropomyosin–troponin within the body temperature range, depending on the physiological demands of various circumstances.

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Section: Introductionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Myosin and tropomyosin–troponin complementarily regulate thermal activation of muscles

Ishii,

Oyama,

Kobirumaki-Shimozawa

et al. 2023

Journal of General Physiology

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“…This was probably because the activation of myosin movement by increasing the temperature increased the number of myosins forming crossbridges [ 28 , 29 , 37 , 38 ]. It is considered that the probability of crossbridge formation was also increased because troponin and tropomyosin became less likely to inhibit myosin crossbridge formation due to thermal fluctuation [ 28 , 29 , 37 , 38 ]. In addition, the thermal fluctuation of the actin filament itself may have increased the probability of proximity to the myosin head and increased the probability of crossbridge formation.…”

Section: Discussionmentioning

confidence: 99%

Effects of high-pressure treatment on the structure and function of myofibrils

Shintani

2021

BIOPHYSICS

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The effects of high pressure (40–70 MPa) on the structure and function of myofibrils were investigated by high pressure microscopy. When this pressure was applied to myofibrils immersed in relaxing solution, the sarcomere length remained almost unchanged, and the A band became shorter and wider. The higher the applied pressure, the faster the change. However, shortening and widening of the A band were not observed when pressure was applied to myofibrils immersed in a solution obtained by omitting ATP from the relaxing solution. However, even under these conditions, structural loss, such as loss of the Z-line structure, occurred. In order to evaluate the consequences of this pressure-treated myofibril, the oscillatory movement of sarcomere (sarcomeric oscillation) was evoked and observed. It was possible to induce sarcomeric oscillation even in pressure-treated myofibrils whose structure was destroyed. The pressurization reduced the total power of the sarcomeric oscillation, but did not change the average frequency. The average frequency did not change even when a pressure of about 40 MPa was applied during sarcomeric oscillation. The average frequency returned to the original when the pressure was returned to the original value after applying stronger pressure to prevent the sarcomere oscillation from being observed. This result suggests that the decrease in the number of myosin molecules forming the crossbridge does not affect the average frequency of sarcomeric oscillation. This fact will help build a mechanical hypothesis for sarcomeric oscillation. The pressurization treatment is a unique method for controlling the structure of myofibrils as described above.

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“…Heat-induced contraction without [Ca 2+ ] i increase could be explained from the perspective of Ca 2+ -independent thermal activation of thin filaments (Ishii et al 2020). In an in vitro motility assay, reconstituted cardiac thin filaments slid on myosin in Ca 2+ -free solution when the temperature was increased over ~ 43 °C (Brunet et al 2012).…”

Section: Muscle Contractions Induced By Heat Pulsesmentioning

confidence: 99%

Opto-thermal technologies for microscopic analysis of cellular temperature-sensing systems

2021

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Could enzymatic activities and their cooperative functions act as cellular temperature-sensing systems? This review introduces recent opto-thermal technologies for microscopic analyses of various types of cellular temperature-sensing system. Optical microheating technologies have been developed for local and rapid temperature manipulations at the cellular level. Advanced luminescent thermometers visualize the dynamics of cellular local temperature in space and time during microheating. An optical heater and thermometer can be combined into one smart nanomaterial that demonstrates hybrid function. These technologies have revealed a variety of cellular responses to spatial and temporal changes in temperature. Spatial temperature gradients cause asymmetric deformations during mitosis and neurite outgrowth. Rapid changes in temperature causes imbalance of intracellular Ca2+ homeostasis and membrane potential. Among those responses, heat-induced muscle contractions are highlighted. It is also demonstrated that the short-term heating hyperactivates molecular motors to exceed their maximal activities at optimal temperatures. We discuss future prospects for opto-thermal manipulation of cellular functions and contributions to obtain a deeper understanding of the mechanisms of cellular temperature-sensing systems.

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Thermal Activation of Thin Filaments in Striated Muscle

Cited by 6 publications

References 66 publications

Myosin and tropomyosin–troponin complementarily regulate thermal activation of muscles

Myosin and tropomyosin–troponin complementarily regulate thermal activation of muscles

Effects of high-pressure treatment on the structure and function of myofibrils

Opto-thermal technologies for microscopic analysis of cellular temperature-sensing systems

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