Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation

Caremani, Marco; Brunello, Elisabetta; Linari, Marco; Fusi, Luca; Irving, Thomas C.; Gore, David; Piazzesi, Gabriella; Irving, Malcolm; Lombardi, Vincenzo; Reconditi, Massimo

doi:10.1085/jgp.201912424

Title: Low temperature traps myosin motors of mammalian muscle in a refractory state that prevents activation

Journal Article · 25 September 2019 · Journal of General Physiology

DOI: https://doi.org/10.1085/jgp.201912424 · OSTI ID:1566274

Caremani, Marco;

;

; Fusi, Luca;

; Gore, David;

; Irving, Malcolm;

;

Myosin motors in the thick filament of resting striated (skeletal and cardiac) muscle are trapped in an OFF state, in which the motors are packed in helical tracks on the filament surface, inhibiting their interactions with actin and utilization of ATP. To investigate the structural changes induced in the thick filament of mammalian skeletal muscle by changes in temperature, we collected x-ray diffraction patterns from the fast skeletal muscle extensor digitorum longus of the mouse in the temperature range from near physiological (35°C) to 10°C, in which the maximal isometric force (T0) shows a threefold decrease. In resting muscle, x-ray reflections signaling the OFF state of the thick filament indicate that cooling produces a progressive disruption of the OFF state with motors moving away from the ordered helical tracks on the surface of the thick filament. We find that the number of myosin motors in the OFF state at 10°C is half of that at 35°C. At T0, changes in the x-ray signals that report the fraction and conformation of actin-attached motors can be explained if the threefold decrease in force associated with lowering temperature is due not only to a decrease in the force-generating transition in the actin-attached motors but also to a twofold decrease in the number of such motors. Thus, lowering the temperature reduces to the same extent the fraction of motors in the OFF state at rest and the fraction of motors attached to actin at T0, suggesting that motors that leave the OFF state accumulate in a disordered refractory state that makes them unavailable for interaction with actin upon stimulation. This regulatory effect of temperature on the thick filament of mammalian skeletal muscle could represent an energetically convenient mechanism for hibernating animals.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1566274

Journal Information:: Journal of General Physiology, Journal Name: Journal of General Physiology Journal Issue: 11 Vol. 151; ISSN 0022-1295

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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