15
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      The unified myofibrillar matrix for force generation in muscle

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Human movement occurs through contraction of the basic unit of the muscle cell, the sarcomere. Sarcomeres have long been considered to be arranged end-to-end in series along the length of the muscle into tube-like myofibrils with many individual, parallel myofibrils comprising the bulk of the muscle cell volume. Here, we demonstrate that striated muscle cells form a continuous myofibrillar matrix linked together by frequently branching sarcomeres. We find that all muscle cells contain highly connected myofibrillar networks though the frequency of sarcomere branching goes down from early to late postnatal development and is higher in slow-twitch than fast-twitch mature muscles. Moreover, we show that the myofibrillar matrix is united across the entire width of the muscle cell both at birth and in mature muscle. We propose that striated muscle force is generated by a singular, mesh-like myofibrillar network rather than many individual, parallel myofibrils.

          Abstract

          Skeletal muscle cells have long been considered to be made primarily of many individual, parallel myofibrils. Here, the authors show that the striated muscle contractile machinery forms a highly branched, mesh-like myofibrillar matrix connected across the entire length and width of the muscle cell.

          Related collections

          Most cited references38

          • Record: found
          • Abstract: not found
          • Article: not found

          Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation.

            Bookmark
            • Record: found
            • Abstract: not found
            • Article: not found

            Structural changes in muscle during contraction; interference microscopy of living muscle fibres.

              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Force generation by skeletal muscle is controlled by mechanosensing in myosin filaments.

              Contraction of both skeletal muscle and the heart is thought to be controlled by a calcium-dependent structural change in the actin-containing thin filaments, which permits the binding of myosin motors from the neighbouring thick filaments to drive filament sliding. Here we show by synchrotron small-angle X-ray diffraction of frog (Rana temporaria) single skeletal muscle cells that, although the well-known thin-filament mechanism is sufficient for regulation of muscle shortening against low load, force generation against high load requires a second permissive step linked to a change in the structure of the thick filament. The resting (switched 'OFF') structure of the thick filament is characterized by helical tracks of myosin motors on the filament surface and a short backbone periodicity. This OFF structure is almost completely preserved during low-load shortening, which is driven by a small fraction of constitutively active (switched 'ON') myosin motors outside thick-filament control. At higher load, these motors generate sufficient thick-filament stress to trigger the transition to its long-periodicity ON structure, unlocking the major population of motors required for high-load contraction. This concept of the thick filament as a regulatory mechanosensor provides a novel explanation for the dynamic and energetic properties of skeletal muscle. A similar mechanism probably operates in the heart.
                Bookmark

                Author and article information

                Contributors
                brian.glancy@nih.gov
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                24 July 2020
                24 July 2020
                2020
                : 11
                : 3722
                Affiliations
                [1 ]ISNI 0000 0001 2297 5165, GRID grid.94365.3d, National Heart, Lung and Blood Institute, , National Institutes of Health, ; Bethesda, MD 20892 USA
                [2 ]ISNI 0000 0001 2297 5165, GRID grid.94365.3d, National Institute of Arthritis and Musculoskeletal and Skin Diseases, , National Institutes of Health, ; Bethesda, MD 20892 USA
                Author information
                http://orcid.org/0000-0001-6038-4358
                http://orcid.org/0000-0003-1029-3444
                http://orcid.org/0000-0002-8571-244X
                Article
                17579
                10.1038/s41467-020-17579-6
                7381600
                32709902
                9b55ae11-7337-4f56-9a7b-7add62b59e2d
                © This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 3 December 2019
                : 7 July 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000050, U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (NHLBI);
                Award ID: 1ZIAHL006221-03
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                physiology,electron microscopy,skeletal muscle
                Uncategorized
                physiology, electron microscopy, skeletal muscle

                Comments

                Comment on this article