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

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 sarcomer...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 116; no. 31; pp. 15534 - 15539
Main Authors Burgoyne, Thomas, Heumann, John M., Morris, Edward P., Knupp, Carlo, Liu, Jun, Reedy, Michael K., Taylor, Kenneth A., Wang, Kuan, Luther, Pradeep K.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 30.07.2019
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Summary: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.
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Author contributions: M.K.R., K.W., and P.K.L. designed research; T.B., C.K., J.L., and P.K.L. performed research; M.K.R., K.A.T., and K.W. contributed new reagents/analytic tools; T.B., J.M.H., E.P.M., and P.K.L. analyzed data; and E.P.M. and P.K.L. wrote the paper.
Edited by James A. Spudich, Stanford University School of Medicine, Stanford, CA, and approved June 24, 2019 (received for review February 7, 2019)
2Present address: Institute of Ophthalmology, University College London, London, EC1V 9EL.
4Deceased 18 June 2019.
3Present address: Department of Microbial Pathogenesis, Yale School of Medicine, New Haven, CT 06510.
1T.B., J.M.H., E.P.M., and C.K. contributed equally to this work.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1902235116