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Three-dimensional structure of the basketweave Z-band in midshipman fish sonic muscle

Burgoyne, T; Heumann, JM; Morris, EP; Knupp, C; Liu, J; Reedy, MK; Taylor, KA; ... Luther, PK; + view all (2019) Three-dimensional structure of the basketweave Z-band in midshipman fish sonic muscle. Proceedings of the National Academy of Sciences (PNAS) , 116 (31) pp. 15534-15539. 10.1073/pnas.1902235116. Green open access

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Abstract

Striated muscle enables movement in all animals by the contraction of myriads of sarcomeres joined end to end by the Z-bands. The contraction is due to tension generated in each sarcomere between overlapping arrays of actin and myosin filaments. At the Z-band, actin filaments from adjoining sarcomeres overlap and are cross-linked in a regular pattern mainly by the protein α-actinin. The Z-band is dynamic, reflected by the 2 regular patterns seen in transverse section electron micrographs; the so-called small-square and basketweave forms. Although these forms are attributed, respectively, to relaxed and actively contracting muscles, the basketweave form occurs in certain relaxed muscles as in the muscle studied here. We used electron tomography and subtomogram averaging to derive the 3D structure of the Z-band in the swimbladder sonic muscle of type I male plainfin midshipman fish (Porichthys notatus), into which we docked the crystallographic structures of actin and α-actinin. The α-actinin links run diagonally between connected pairs of antiparallel actin filaments and are oriented at an angle of about 25° away from the actin filament axes. The slightly curved and flattened structure of the α-actinin rod has a distinct fit into the map. The Z-band model provides a detailed understanding of the role of α-actinin in transmitting tension between actin filaments in adjoining sarcomeres.

Type: Article
Title: Three-dimensional structure of the basketweave Z-band in midshipman fish sonic muscle
Open access status: An open access version is available from UCL Discovery
DOI: 10.1073/pnas.1902235116
Publisher version: https://doi.org/10.1073/pnas.1902235116
Language: English
Additional information: This version is the author accepted manuscript. For information on re-use, please refer to the publisher’s terms and conditions.
Keywords: Science & Technology, Multidisciplinary Sciences, Science & Technology - Other Topics, Z-line, Z-disc, alpha-actinin, electron tomography, subtomogram averaging, ALPHA-ACTININ, STRIATED-MUSCLE, Z-DISK, TITIN, ULTRASTRUCTURE, VISUALIZATION, ORGANIZATION, ARCHITECTURE, SARCOMERE, SYMMETRY
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > Institute of Ophthalmology
URI: https://discovery.ucl.ac.uk/id/eprint/10081656
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