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Myosin flares and actin leptomeres as myofibril assembly/disassembly intermediates in sonic muscle fibers

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Abstract

The sonic muscle of type 1 male midshipman fish produces loud and enduring mating calls. Each sonic muscle fiber contains a tubular contractile apparatus with radially arranged myofibrillar plates encased in a desmin-rich cytoskeleton that is anchored to broad Z bands (~1.2 μm wide). Immunomicroscopy has revealed patches of myosin-rich “flares” emanating from the contractile tubes into the peripheral sarcoplasm along the length of the fibers. These flares contain swirls of thick filaments devoid of associated thin filaments. In other regions of the sarcoplasm at the inner surface of the sarcolemma and near Z bands, abundant ladder-like leptomeres occur with rungs every 160 nm. Leptomeres consist of dense arrays of filaments (~4 nm) with a structure that resembles myofibrillar Z band structure. We propose that flares and leptomeres are distinct filamentous arrays representing site-specific processing of myofibrillar components during the assembly and disassembly of the sarcomere. Recent reports that myosin assembles into filamentous aggregates before incorporating into the A band in the skeletal muscles of vertebrates and Caenorhabditis elegans suggest that sonic fibers utilize a similar pathway. Thus, sonic muscle fibers, with their tubular design and abundant sarcoplasmic space, may provide an attractive muscle model to identify myofibrillar intermediates by structural and molecular techniques.

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Authors and Affiliations

  1. Muscle Proteomics and Nanotechnology Section, Laboratory of Muscle Biology, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Building 50, Room 1140, 20892, Bethesda, MD 29892, USA

    Patrick C. Nahirney & Kuan Wang

  2. Department of Cell and Developmental Biology, Weill Medical College of Cornell University, New York, NY, 10021, USA

    Donald A. Fischman

Authors
  1. Patrick C. Nahirney
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  2. Donald A. Fischman
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  3. Kuan Wang
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Correspondence to Kuan Wang.

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This work was supported by the Intramural Research Program of the NIAMS, NIH, HHS (KW).

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Nahirney, P.C., Fischman, D.A. & Wang, K. Myosin flares and actin leptomeres as myofibril assembly/disassembly intermediates in sonic muscle fibers. Cell Tissue Res 324, 127–138 (2006). https://doi.org/10.1007/s00441-005-0110-3

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