Concentric intermediate filament lattice links to specialized Z-band junctional complexes in sonic muscle fibers of the type I male midshipman fish.
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 ( approximately 1.2 microm) 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 approximately 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.
Lewis
Michael K
MK
Muscle Proteomics and Nanotechnology Section, Laboratory of Muscle Biology, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, DHHS, Bethesda, MD 20892, USA.
Nahirney
Patrick C
PC
Chen
Victor
V
Adhikari
Bishow B
BB
Wright
John
J
Reedy
Michael K
MK
Bass
Andrew H
AH
Wang
Kuan
K
D000818:Animals; D024541:Batrachoidiformes; D003599:Cytoskeleton / Q000378:metabolism; D003893:Desmin / Q000737:chemistry; D003896:Desmosomes / Q000378:metabolism; D015151:Immunoblotting; D007381:Intermediate Filament Proteins / Q000737:chemistry; D008297:Male; D018613:Microscopy, Confocal; D008854:Microscopy, Electron; D008856:Microscopy, Fluorescence; D016253:Microscopy, Immunoelectron; D008953:Models, Anatomic; D018485:Muscle Fibers, Skeletal / Q000737:chemistry*; D009124:Muscle Proteins / Q000737:chemistry; D051190:Plectin; D013010:Sonication
D003893:Desmin; D007381:Intermediate Filament Proteins; D009124:Muscle Proteins; D051190:Plectin