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

• Published in: Journal of structural biology Vol. 143; no. 1; pp. 56 - 71
• Main Authors: Lewis, Michael K., Nahirney, Patrick C., Chen, Victor, Adhikari, Bishow B., Wright, John, Reedy, Michael K., Bass, Andrew H., Wang, Kuan
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.07.2003
• Subjects: Animals; Batrachoidiformes; Confocal microscopy; Cytoskeleton; Cytoskeleton - metabolism; Desmin; Desmin - chemistry; Desmosomes - metabolism; Immunoblotting; Intermediate Filament Proteins - chemistry; Male; Microscopy, Confocal; Microscopy, Electron; Microscopy, Fluorescence; Microscopy, Immunoelectron; Midshipman fish; Models, Anatomic; Muscle Fibers, Skeletal - chemistry; Muscle Proteins - chemistry; Plectin; Sonic muscle fiber; Sonication; Superfast muscle; Wide Z band; Z bar; Z corset; α-Actinin; Sonic muscle fiber; Z corset; Plectin; Superfast muscle; Cytoskeleton; Z bar; Confocal microscopy; α-Actinin; Midshipman fish; Wide Z band; Desmin
• ISSN: 1047-8477; 1095-8657
• DOI: 10.1016/S1047-8477(03)00121-7

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 (∼1.2 μm) 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 (3–4 nm) 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.