Concentric intermediate filament lattice links to specialized Z-band junctional complexes in sonic muscle fibers of the type I male midshipman fish

Michael K. Lewis, Patrick C. Nahirney, Victor Chen, Bishow B. Adhikari, John Wright, Michael K. Reedy, Andrew H. Bass, Kuan Wang

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Type I male midshipman fish produce high-frequency hums for prolonged durations using sonic muscle fibers, each of which contains a hollow tube of radially oriented thin and flat myofibrils that display extraordinarily wide (∼1.2μm) Z bands. We have revealed an elaborate cytoskeletal network of desmin filaments associated with the contractile cylinder that form interconnected concentric ring structures in the core and periphery at the level of the Z bands. Stretch and release of single fibers revealed reversible length changes in the elastic desmin lattice. This lattice is linked to Z bands via novel intracellular desmosome-like junctional complexes that collectively form a ring, termed the "Z corset," around the periphery and within the core of the cylinder. The junctional complex consists of regularly spaced parallel ∼900-nm-long cytoskeletal rods, or "Z bars," interconnected with slender (3-4nm) plectin-positive filaments. Z bars are linked to the Z band by plectin filaments and on the opposite side to a dense mesh of desmin filaments. Adjacent Z bands are linked by slender filaments that appear to suspend sarcotubules. We propose that the highly reinforced elastic desmin cytoskeleton and the unique Z band junctions are structural adaptations that enable the muscles' high-frequency and high-endurance activity.

Original languageEnglish
Pages (from-to)56-71
Number of pages16
JournalJournal of Structural Biology
Volume143
Issue number1
DOIs
Publication statusPublished - Jul 1 2003
Externally publishedYes

Keywords

  • Confocal microscopy
  • Cytoskeleton
  • Desmin
  • Midshipman fish
  • Plectin
  • Sonic muscle fiber
  • Superfast muscle
  • Wide Z band
  • Z bar
  • Z corset
  • α-Actinin

ASJC Scopus subject areas

  • Structural Biology

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