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In vivo X-ray diffraction and simultaneous EMG reveal the time course of myofilament lattice dilation and filament stretch.

ABSTRACT: Muscle function within an organism depends on the feedback between molecular and meter-scale processes. Although the motions of muscle's contractile machinery are well described in isolated preparations, only a handful of experiments have documented the kinematics of the lattice occurring when multi-scale interactions are fully intact. We used time-resolved X-ray diffraction to record the kinematics of the myofilament lattice within a normal operating context: the tethered flight of Manduca sexta As the primary flight muscles of M . sexta are synchronous, we used these results to reveal the timing of in vivo cross-bridge recruitment, which occurred 24 ms (s.d. 26) following activation. In addition, the thick filaments stretched an average of 0.75% (s.d. 0.32) and thin filaments stretched 1.11% (s.d. 0.65). In contrast to other in vivo preparations, lattice spacing changed an average of 2.72% (s.d. 1.47). Lattice dilation of this magnitude significantly affects shortening velocity and force generation, and filament stretching tunes force generation. While the kinematics were consistent within individual trials, there was extensive variation between trials. Using a mechanism-free machine learning model we searched for patterns within and across trials. Although lattice kinematics were predictable within trials, the model could not create predictions across trials. This indicates that the variability we see across trials may be explained by latent variables occurring in this naturally functioning system. The diverse kinematic combinations we documented mirror muscle's adaptability and may facilitate its robust function in unpredictable conditions.

SUBMITTER: Malingen SA

PROVIDER: S-EPMC7490515 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:During muscle contraction, myosin motors anchored to thick filaments bind to and slide actin thin filaments. These motors rely on energy derived from ATP, supplied, in part, by diffusion from the sarcoplasm to the interior of the lattice of actin and myosin filaments. The radial spacing of filaments in this lattice may change or remain constant during contraction. If the lattice is isovolumetric, it must expand when the muscle shortens. If, however, the spacing is constant or has a different pattern of axial and radial motion, then the lattice changes volume during contraction, driving fluid motion and assisting in the transport of molecules between the contractile lattice and the surrounding intracellular space. We first create an advective-diffusive-reaction flow model and show that the flow into and out of the sarcomere lattice would be significant in the absence of lattice expansion. Advective transport coupled to diffusion has the potential to substantially enhance metabolite exchange within the crowded sarcomere. Using time-resolved x-ray diffraction of contracting muscle, we next show that the contractile lattice is neither isovolumetric nor constant in spacing. Instead, lattice spacing is time varying, depends on activation, and can manifest as an effective time-varying Poisson ratio. The resulting fluid flow in the sarcomere lattice of synchronous insect flight muscles is even greater than expected for constant lattice spacing conditions. Lattice spacing depends on a variety of factors that produce radial force, including cross-bridges, titin-like molecules, and other structural proteins. Volume change and advective transport varies with the phase of muscle stimulation during periodic contraction but remains significant at all conditions. Although varying in magnitude, advective transport will occur in all cases in which the sarcomere is not isovolumetric. Akin to "breathing," advective-diffusive transport in sarcomeres is sufficient to promote metabolite exchange and may play a role in the regulation of contraction itself.

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In vivo X-ray diffraction and simultaneous EMG reveal the time course of myofilament lattice dilation and filament stretch.

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