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Department of Zoology, La Trobe University, Bundoora, Victoria 3086, Australia

Address correspondence to Bradley S. Launikonis at his present address: Department of Molecular Biophysics and Physiology, Rush University Medical Centre, 1750 W. Harrison St., Chicago, IL 60612. Fax: (312) 942-8711; email: zoobl{at}zoo.latrobe.edu.au

A method was developed that allows conversion of changes in maximum Ca²⁺-dependent fluorescence of a fixed amount of fluo-3 into volume changes of the fluo-3–containing solution. This method was then applied to investigate by confocal microscopy the osmotic properties of the sealed tubular (t-) system of toad and rat mechanically skinned fibers in which a certain amount of fluo-3 was trapped. When the osmolality of the myoplasmic environment was altered by simple dilution or addition of sucrose within the range 190–638 mosmol kg^-1, the sealed t-system of toad fibers behaved almost like an ideal osmometer, changing its volume inverse proportionally to osmolality. However, increasing the osmolality above 638 to 2,550 mosmol kg^-1 caused hardly any change in t-system volume. In myoplasmic solutions made hypotonic to 128 mosmol kg^-1, a loss of Ca²⁺ from the sealed t-system of toad fibers occurred, presumably through either stretch-activated cationic channels or store-operated Ca²⁺ channels. In contrast to the behavior of the t-system in toad fibers, the volume of the sealed t-system of rat fibers changed little (by <20%) when the osmolality of the myoplasmic environment changed between 210 and 2,800 mosmol kg^-1. Results were also validated with calcein. Clear differences between rat and toad fibers were also found with respect to the t-system permeability for glycerol. Thus, glycerol equilibrated across the rat t-system within seconds to minutes, but was not equilibrated across the t-system of toad fibers even after 20 min. These results have broad implications for understanding osmotic properties of the t-system and reversible vacuolation in muscle fibers. Furthermore, we observed for the first time in mammalian fibers an orderly lateral shift of the t-system networks whereby t-tubule networks to the left of the Z-line crossover to become t-tubule networks to the right of the Z-line in the adjacent sarcomere (and vice versa). This orderly rearrangement can provide a pathway for longitudinal continuity of the t-system along the fiber axis.

Key Words: t-system • skeletal muscle • osmotic gradient • skinned fibers • glycerol

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