Force and Kinetics of Fast and Slow Muscle Myosin Determined with a Synthetic Sarcomere-like Nanomachine

Overview

Journal Commun Biol

Specialty Biology

Date 2024 Mar 24

PMID 38521889

Authors

Valentina Buonfiglio

Irene Pertici

Matteo Marcello

Ilaria Morotti

Marco Caremani

Massimo Reconditi

Marco Linari

Duccio Fanelli

Vincenzo Lombardi

Pasquale Bianco

Affiliations

Soon will be listed here.

Abstract

Myosin II is the muscle molecular motor that works in two bipolar arrays in each thick filament of the striated (skeletal and cardiac) muscle, converting the chemical energy into steady force and shortening by cyclic ATP-driven interactions with the nearby actin filaments. Different isoforms of the myosin motor in the skeletal muscles account for the different functional requirements of the slow muscles (primarily responsible for the posture) and fast muscles (responsible for voluntary movements). To clarify the molecular basis of the differences, here the isoform-dependent mechanokinetic parameters underpinning the force of slow and fast muscles are defined with a unidimensional synthetic nanomachine powered by pure myosin isoforms from either slow or fast rabbit skeletal muscle. Data fitting with a stochastic model provides a self-consistent estimate of all the mechanokinetic properties of the motor ensemble including the motor force, the fraction of actin-attached motors and the rate of transition through the attachment-detachment cycle. The achievements in this paper set the stage for any future study on the emergent mechanokinetic properties of an ensemble of myosin molecules either engineered or purified from mutant animal models or human biopsies.

References

Kron S, Toyoshima Y, Uyeda T, Spudich J . Assays for actin sliding movement over myosin-coated surfaces. Methods Enzymol. 1991; 196:399-416. DOI: 10.1016/0076-6879(91)96035-p. View

Potma E, van Graas I, Stienen G . Effects of pH on myofibrillar ATPase activity in fast and slow skeletal muscle fibers of the rabbit. Biophys J. 1994; 67(6):2404-10. PMC: 1225625. DOI: 10.1016/S0006-3495(94)80727-1. View

Wendt I, Gibbs C . Energy production of mammalian fast- and slow-twitch muscles during development. Am J Physiol. 1974; 226(3):642-7. DOI: 10.1152/ajplegacy.1974.226.3.642. View

Reggiani C, Potma E, Bottinelli R, Canepari M, Pellegrino M, Stienen G . Chemo-mechanical energy transduction in relation to myosin isoform composition in skeletal muscle fibres of the rat. J Physiol. 1997; 502 ( Pt 2):449-60. PMC: 1159562. DOI: 10.1111/j.1469-7793.1997.449bk.x. View

Smith D, Geeves M . Strain-dependent cross-bridge cycle for muscle. Biophys J. 1995; 69(2):524-37. PMC: 1236278. DOI: 10.1016/S0006-3495(95)79926-X. View

Ishijima A, Kojima H, Higuchi H, Harada Y, Funatsu T, Yanagida T . Multiple- and single-molecule analysis of the actomyosin motor by nanometer-piconewton manipulation with a microneedle: unitary steps and forces. Biophys J. 1996; 70(1):383-400. PMC: 1224937. DOI: 10.1016/S0006-3495(96)79582-6. View

Stienen G, Kiers J, Bottinelli R, Reggiani C . Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J Physiol. 1996; 493 ( Pt 2):299-307. PMC: 1158918. DOI: 10.1113/jphysiol.1996.sp021384. View

Hill A . The heat of activation and the heat of shortening in a muscle twitch. Proc R Soc Lond B Biol Sci. 1949; 136(883):195-211. DOI: 10.1098/rspb.1949.0019. View

HUXLEY A . Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957; 7:255-318. View

10.

Woledge R, Curtin N, Homsher E . Energetic aspects of muscle contraction. Monogr Physiol Soc. 1985; 41:1-357. View

11.

Reggiani C, Bottinelli R, Stienen G . Sarcomeric Myosin Isoforms: Fine Tuning of a Molecular Motor. News Physiol Sci. 2001; 15:26-33. DOI: 10.1152/physiologyonline.2000.15.1.26. View

12.

Uyeda T, Kron S, Spudich J . Myosin step size. Estimation from slow sliding movement of actin over low densities of heavy meromyosin. J Mol Biol. 1990; 214(3):699-710. DOI: 10.1016/0022-2836(90)90287-V. View

13.

Suzuki N, Miyata H, Ishiwata S, Kinosita Jr K . Preparation of bead-tailed actin filaments: estimation of the torque produced by the sliding force in an in vitro motility assay. Biophys J. 1996; 70(1):401-8. PMC: 1224938. DOI: 10.1016/S0006-3495(96)79583-8. View

14.

Finer J, Simmons R, Spudich J . Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature. 1994; 368(6467):113-9. DOI: 10.1038/368113a0. View

15.

Linari M, Piazzesi G, Pertici I, Dantzig J, Goldman Y, Lombardi V . Straightening Out the Elasticity of Myosin Cross-Bridges. Biophys J. 2020; 118(5):994-1002. PMC: 7063436. DOI: 10.1016/j.bpj.2020.01.002. View

16.

Bottinelli R, Betto R, Schiaffino S, Reggiani C . Unloaded shortening velocity and myosin heavy chain and alkali light chain isoform composition in rat skeletal muscle fibres. J Physiol. 1994; 478 ( Pt 2):341-9. PMC: 1155690. DOI: 10.1113/jphysiol.1994.sp020254. View

17.

Barclay C, Woledge R, Curtin N . Is the efficiency of mammalian (mouse) skeletal muscle temperature dependent?. J Physiol. 2010; 588(Pt 19):3819-31. PMC: 2998229. DOI: 10.1113/jphysiol.2010.192799. View

18.

Wendt I, Gibbs C . Energy production of rat extensor digitorum longus muscle. Am J Physiol. 1973; 224(5):1081-6. DOI: 10.1152/ajplegacy.1973.224.5.1081. View

19.

Percario V, Boncompagni S, Protasi F, Pertici I, Pinzauti F, Caremani M . Mechanical parameters of the molecular motor myosin II determined in permeabilised fibres from slow and fast skeletal muscles of the rabbit. J Physiol. 2017; 596(7):1243-1257. PMC: 5878222. DOI: 10.1113/JP275404. View

20.

He Z, Bottinelli R, Pellegrino M, Ferenczi M, Reggiani C . ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys J. 2000; 79(2):945-61. PMC: 1300991. DOI: 10.1016/S0006-3495(00)76349-1. View