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Reduced passive force in skeletal muscles lacking protein arginylation.

ABSTRACT: Arginylation is a posttranslational modification that plays a global role in mammals. Mice lacking the enzyme arginyltransferase in skeletal muscles exhibit reduced contractile forces that have been linked to a reduction in myosin cross-bridge formation. The role of arginylation in passive skeletal myofibril forces has never been investigated. In this study, we used single sarcomere and myofibril measurements and observed that lack of arginylation leads to a pronounced reduction in passive forces in skeletal muscles. Mass spectrometry indicated that skeletal muscle titin, the protein primarily linked to passive force generation, is arginylated on five sites located within the A band, an important area for protein-protein interactions. We propose a mechanism for passive force regulation by arginylation through modulation of protein-protein binding between the titin molecule and the thick filament. Key points are as follows: 1) active and passive forces were decreased in myofibrils and single sarcomeres isolated from muscles lacking arginyl-tRNA-protein transferase (ATE1). 2) Mass spectrometry revealed five sites for arginylation within titin molecules. All sites are located within the A-band portion of titin, an important region for protein-protein interactions. 3) Our data suggest that arginylation of titin is required for proper passive force development in skeletal muscles.

SUBMITTER: Leite FS

PROVIDER: S-EPMC4719035 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Reduced passive force in skeletal muscles lacking protein arginylation.

Leite Felipe S FS Minozzo Fábio C FC Kalganov Albert A Cornachione Anabelle S AS Cheng Yu-Shu YS Leu Nicolae A NA Han Xuemei X Saripalli Chandra C Yates John R JR Granzier Henk H Kashina Anna S AS Rassier Dilson E DE

American journal of physiology. Cell physiology 20151028 2

Arginylation is a posttranslational modification that plays a global role in mammals. Mice lacking the enzyme arginyltransferase in skeletal muscles exhibit reduced contractile forces that have been linked to a reduction in myosin cross-bridge formation. The role of arginylation in passive skeletal myofibril forces has never been investigated. In this study, we used single sarcomere and myofibril measurements and observed that lack of arginylation leads to a pronounced reduction in passive force ...[more]

PMID: 26511365

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Project description:ObjectiveWe reviewed and appraised the existing evidence of in vivo manifestations of residual force enhancement in human skeletal muscles and assessed, through a meta-analysis, the effect of an immediate history of eccentric contraction on the subsequent torque capacity of voluntary and electrically evoked muscle contractions.MethodsOur search was conducted from database inception to May 2020. Descriptive information was extracted from, and quality was assessed for, 45 studies. Meta-analyses and metaregressions were used to analyze residual torque enhancement and its dependence on the angular amplitude of the preceding eccentric contraction.ResultsProcedures varied across studies with regards to muscle group tested, angular stretch amplitude, randomization of contractions, time window analyzed, and verbal command. Torque capacity in isometric (constant muscle tendon unit length and joint angle) contractions preceded by an eccentric contraction was typically greater compared to purely isometric contractions, and this effect was greater for electrically evoked muscle contractions than voluntary contractions. Residual torque enhancement differed across muscle groups for the voluntary contractions, with a significant enhancement in torque observed for the adductor pollicis, ankle dorsiflexors, ankle plantar flexors, and knee extensors, but not for the elbow and knee flexors. Meta-regressions revealed that the angular amplitude of the eccentric contraction (normalized to the respective joint's full range of motion) was not associated with the residual torque enhancement observed.ConclusionThere is evidence of residual torque enhancement for most, but not all, muscle groups, and residual torque enhancement is greater for electrically evoked than for voluntary contractions. Contrary to our hypothesis, and contrary to generally accepted findings on isolated muscle preparations, residual torque enhancement in voluntary and electrically evoked contractions does not seem to depend on the angular amplitude of the preceding eccentric contraction.

Dataset Information

Reduced passive force in skeletal muscles lacking protein arginylation.

Publications

Reduced passive force in skeletal muscles lacking protein arginylation.

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