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

Thomas Burgoyne, John M. Heumann, Edward P. Morris, Carlo Knupp, Jun Liu, Michael K. Reedy, Kenneth A. Taylor, Kuan Wang, Pradeep K. Luther

Research output: Contribution to journalArticle

1 Citation (Scopus)

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.

Original languageEnglish
Pages (from-to)15534-15539
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number31
DOIs
Publication statusPublished - Jul 30 2019

Fingerprint

Actinin
Actin Cytoskeleton
Sarcomeres
Fishes
Muscles
Batrachoidiformes
Electron Microscope Tomography
Air Sacs
Striated Muscle
Myosins
Actins
Electrons
Proteins

Keywords

  • electron tomography
  • subtomogram averaging
  • Z-disc
  • Z-line
  • α-actinin

ASJC Scopus subject areas

  • General

Cite this

Three-dimensional structure of the basketweave Z-band in midshipman fish sonic muscle. / Burgoyne, Thomas; Heumann, John M.; Morris, Edward P.; Knupp, Carlo; Liu, Jun; Reedy, Michael K.; Taylor, Kenneth A.; Wang, Kuan; Luther, Pradeep K.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 31, 30.07.2019, p. 15534-15539.

Research output: Contribution to journalArticle

Burgoyne, Thomas ; Heumann, John M. ; Morris, Edward P. ; Knupp, Carlo ; Liu, Jun ; Reedy, Michael K. ; Taylor, Kenneth A. ; Wang, Kuan ; Luther, Pradeep K. / Three-dimensional structure of the basketweave Z-band in midshipman fish sonic muscle. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 31. pp. 15534-15539.
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