Reversible vacuolation of T-tubules in skeletal muscle: Mechanisms and implications for cell biology

Krolenko, S. A.; Lucy, J. A.

doi:10.1016/s0074-7696(01)02006-x

Cited by 32 publications

(32 citation statements)

References 138 publications

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“…The latter property underscores the role of the t-system in compartmentalizing its luminal solutes that would otherwise affect its excitability. The t-system is also a dynamic structure, changing its volume or vacuolating with osmotic stress or other factors (Krolenko et al, 1995;Krolenko and Lucy, 2001;Launikonis and Stephenson, 2002a;Launikonis and Stephenson, 2004).…”

Section: Introductionmentioning

confidence: 99%

Three-dimensional reconstruction and analysis of the tubular system of vertebrate skeletal muscle

Jayasinghe

Launikonis

2013

Journal of Cell Science

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SummarySkeletal muscle fibres are very large and elongated. In response to excitation there must be a rapid and uniform release of Ca 2+ throughout for contraction. To ensure a uniform spread of excitation throughout the fibre to all the Ca 2+ release sites, the muscle internalizes the plasma membrane, to form the tubular (t-) system. Hence the t-system forms a complex and dense network throughout the fibre that is responsible for excitation-contraction coupling and other signalling mechanisms. However, we currently do not have a very detailed view of this membrane network because of limitations in previously used imaging techniques to visualize it. In this study we serially imaged fluorescent dye trapped in the t-system of fibres from rat and toad muscle using the confocal microscope, and deconvolved and reconstructed these images to produce the first three-dimensional reconstructions of large volumes of the vertebrate tsystem. These images showed complex arrangements of tubules that have not been described previously and also allowed the association of the t-system with cellular organelles to be visualized. There was a high density of tubules close to the nuclear envelope because of the close and parallel alignment of the long axes of the myofibrils and the nuclei. Furthermore local fluorescence intensity variations from sub-resolution tubules were converted to tubule diameters. Mean diameters of tubules were 85.966.6 and 91.268.2 nm, from rat and toad muscle under isotonic conditions, respectively. Under osmotic stress the distribution of tubular diameters shifted significantly in toad muscle only, with change specifically occurring in the transverse but not longitudinal tubules.

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Section: Introductionmentioning

confidence: 99%

Three-dimensional reconstruction and analysis of the tubular system of vertebrate skeletal muscle

Jayasinghe

Launikonis

2013

Journal of Cell Science

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“…Such osmotic shock can convert the T-tubule network into many membrane-bound vacuoles, which can either remain interconnected by normal T-tubules, or become separated (Figure 2) [9,10]. Surprisingly, this vacuolation which results in 5-15 fold increase in the relative volume of T-tubule system is reversed spontaneously [11,12].…”

Section: Introductionmentioning

confidence: 99%

“…A single frog skeletal muscle fiber stained with a lipophilic fluorescence probe is shown. Shown are serial confocal microscopic images of the same fiber (a) 5 minutes, (b) 12 minutes and (c) 30 minutes after the fiber was transferred from a solution containing 110 mM glycerol to a solution without glycerol (reprinted from [10]; © 2001 with permission from Elsevier).…”

Section: Introductionmentioning

confidence: 99%

“…In addition to this artificial condition, this vacuolation phenomenon is observed upon muscle fatigue or diseases [10,13]. Based on this plasticity and on the large membrane surface of the T-tubules network which corresponds to about 80% of the sarcolemma surface, several functions non-related to EC coupling are proposed for the T-tubules system [10,13].…”

Section: Introductionmentioning

confidence: 99%

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T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases

2011

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In skeletal muscle, the excitation-contraction (EC) coupling machinery mediates the translation of the action potential transmitted by the nerve into intracellular calcium release and muscle contraction. EC coupling requires a highly specialized membranous structure, the triad, composed of a central T-tubule surrounded by two terminal cisternae from the sarcoplasmic reticulum. While several proteins located on these structures have been identified, mechanisms governing T-tubule biogenesis and triad formation remain largely unknown. Here, we provide a description of triad structure and plasticity and review the role of proteins that have been linked to T-tubule biogenesis and triad formation and/or maintenance specifically in skeletal muscle: caveolin 3, amphiphysin 2, dysferlin, mitsugumins, junctophilins, myotubularin, ryanodine receptor, and dihydhropyridine Receptor. The importance of these proteins in triad biogenesis and subsequently in muscle contraction is sustained by studies on animal models and by the direct implication of most of these proteins in human myopathies.

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“…71,72 Commonly-described t-tubule abnormalities in skeletal muscle include widening of triads 73,74 and micron-scale dilatation (vacuolation). 75,76 Such abnormalities have been observed in connection to pathologies such as human myotubular myopathies 73 , myotonic muscular dystrophy, 77 rippling muscle disease 78 and a range of genetic myopathies (see review 79 ). Vacuolation is often seen in non-pathological conditions as fatigue 75 or in muscle damage due to eccentric contractions.…”

Section: Altered T-tubule Structure In Health and Disease: Motivatingmentioning

confidence: 99%

Revealing t-tubules in striated muscle with new optical super-resolution microscopy techniques

et al. 2014

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The t-tubular system plays a central role in the synchronisation of calcium signalling and excitation-contraction coupling in most striated muscle cells. Light microscopy has been used for imaging t-tubules for well over 100 years and together with electron microscopy (EM), has revealed the three-dimensional complexities of the t-system topology within cardiomyocytes and skeletal muscle fibres from a range of species. The emerging super-resolution single molecule localisation microscopy (SMLM) techniques are offering a near 10-fold improvement over the resolution of conventional fluorescence light microscopy methods, with the ability to spectrally resolve nanometre scale distributions of multiple molecular targets. In conjunction with the next generation of electron microscopy, SMLM has allowed the visualisation and quantification of intricate t-tubule morphologies within large areas of muscle cells at an unprecedented level of detail. In this paper, we review recent advancements in the ttubule structural biology with the utility of various microscopy techniques. We outline the technical considerations in adapting SMLM to study t-tubules and its potential to further our understanding of the molecular processes that underlie the sub-micron scale structural alterations observed in a range of muscle pathologies.

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Reversible vacuolation of T-tubules in skeletal muscle: Mechanisms and implications for cell biology

Cited by 32 publications

References 138 publications

Three-dimensional reconstruction and analysis of the tubular system of vertebrate skeletal muscle

Three-dimensional reconstruction and analysis of the tubular system of vertebrate skeletal muscle

T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases

Revealing t-tubules in striated muscle with new optical super-resolution microscopy techniques

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