Muscle Fine Structure Research Articles

Allometry of skeletal muscle fine structure allows maintenance of aerobic capacity during ontogenetic growth

Controversy exists over the scaling of oxygen consumption with body mass in vertebrates. A combination of biochemical and structural analyses were used to examine whether individual elements influencing oxygen delivery and demand within locomotory muscle respond similarly during ontogenetic growth of striped bass. Mass-specific metabolic enzyme activity confirmed that glycolytic capacity scaled positively in deep white muscle (regression slope, b=0.1 to 0.8) over a body mass range of approximately 20-1500 g, but only creatine phosphokinase showed positive scaling in lateral red muscle (b=0.5). Although oxidative enzymes showed negative allometry in red muscle (b=-0.01 to -0.02), mass-specific myoglobin content scaled positively (b=0.7). Capillary to fibre ratio of red muscle was higher in larger (1.42+/-0.15) than smaller (1.20+/-0.15) fish, suggesting progressive angiogenesis. By contrast, capillary density decreased (1989+/-161 vs 2,962+/-305 mm(-2)) as a result of larger fibre size (658+/-31 vs 307+/-24 microm(2) in 1595 g and 22.9 g fish, respectively). Thus, facilitated and convective delivery of O(2) show opposite allometric trends. Relative mitochondrial content of red muscle (an index of O(2) demand) varied little with body mass overall, but declined from approximately 40% fibre volume in the smallest to approximately 30% in the largest fish. However, total content per fibre increased, suggesting that mitochondrial biogenesis supported aerobic capacity during fibre growth. Heterogeneous fibre size indicates both hypertrophic and hyperplastic growth, although positive scaling of fibre myofibrillar content (b=0.085) may enhance specific force generation in larger fish. Modelling intracellular P(O(2)) distribution suggests such integrated structural modifications are required to maintain adequate oxygen delivery (calculated P(O(2)) 5.15+/-0.02 kPa and 5.21+/-0.01 kPa in small and large fish, respectively).

Muscle microanatomy and its changes during contraction: the legacy of William Bowman (1816–1892)

Striated muscle fine structure began to be really understood following a comprehensive survey of the matter carried out by William Bowman in the late 1830s. The publications resulting from such a study, the first of which earned for the author a precocious election as Fellow of the Royal Society, are herewith examined in the context of contemporary views on the subject as well as of their subsequent repercussion and current knowledge today. It is shown that not only Bowman succeeded in establishing the true architecture of striated muscle fibres to the extent possible with the most advanced technology available in his day--explaining and eradicating alternative erroneous concepts in the process--but also in correctly describing the basic microstructural changes associated with contraction. In addition, although unrecognized by him or others at the time, his experiments with muscle provided direct evidence for the existence of a selectively permeable cell membrane--in the present meaning of the word--over half a century before its officially accepted discovery. Yet, in spite of these remarkable advances, Bowman arrived at the conclusion that the structure of striated muscle fibres is essentially irrelevant for the mechanism of contraction. Possible reasons behind Bowman's breakthrough accomplishments as a pioneer of modern muscle research, and his failure to understand their significance for muscle physiology, are discussed.

Muscle fine structure reflects ecotype in two nototheniids

The fine structure of swimming (pectoral) and myotomal (axial) skeletal muscle and myocardium of two species of Antarctic nototheniid fishes were studied by electron microscopy, comparing the cryopelagic Pagothenia borchgrevinki and the benthic Trematomus bernacchii. Mean fibre size varied by a factor of four among muscles within each species and may have reflected the locomotory power available, being larger in pectoral oxidative (red) and axial glycolytic (white) muscle of P. borchgrevinki. Both species use labriform locomotion, and the more active P. borchgrevinki had a greater capillary supply, expressed as a capillary to fibre ratio, than T. bernacchii to both red (3·48 ± 0·36 v. 1·63 ± 0·14, mean ± s.e.; P < 0·01) and white (2·70 ± 0·20 v. 1·53 ± 0·18, mean ± s.e.; P < 0·01) regions of the pectoral musculature. The greater aerobic scope of P. borchgrevinki was strikingly demonstrated in the higher mitochondrial content of all skeletal muscle types sampled, and the ventricular myocardium (0·269 ± 0·011 v. 0·255 ± 0·012 mean ± s.e.; P < 0·05). Minor differences were found in other elements of fibre composition, with the exception of a five‐fold greater lipid content in pectoral red fibres of P. borchgrevinki(0·074 ± 0·014 mean ± s.e.)v. T. bernacchii(0·010 ± 0·003; P < 0·05). Differences in muscle fine structure among species clearly reflected differences in their ecotype.

Muscle fine structure may maintain the function of oxidative fibres in haemoglobinless Antarctic fishes.

Muscle fine structure and metabolism were examined in four species of Antarctic fishes that vary in their expression of haemoglobin (Hb). To determine how locomotory pectoral muscles maintain function, metabolic capacity, capillary supply and fibre ultrastructure were examined in two nototheniid species that express Hb (Notothenia coriiceps and Gobionotothen gibberifrons) and two species of channichthyid icefish that lack Hb (Chaenocephalus aceratus and Chionodraco rastrospinosus). Surprisingly, icefish have higher densities of mitochondria than red-blooded species (C. aceratus, 53+/-3% of cell volume; C. rastrospinosus, 39+/-3%; N. coriiceps, 29+/-3%; G. gibberifrons, 25+/-1%). Despite higher mitochondrial densities the aerobic metabolic capacities per g wet mass, estimated from measurements of maximal activities of key metabolic enzymes, are lower in icefish compared to red-blooded species. This apparent incongruity can be explained by the significantly lower mitochondrial cristae surface area per unit mitochondrion volume in icefishes (C. aceratus, 20.8+/-1.6 microm(-1); C. rastrospinosus, 25.5+/-1.8 microm(-1)) compared to red-blooded species (N. coriiceps, 33.6+/-3.0 microm(-1); G. gibberifrons, 37.7+/-3.6 microm(-1)). Consequently, the cristae surface area per unit muscle mass is conserved at approximately 9 m(2)g(-1). Although high mitochondrial densities in icefish muscle do not enhance aerobic metabolic capacity, they may facilitate intracellular oxygen movement because oxygen is more soluble in lipid, including the hydrocarbon core of intracellular membrane systems, than in aqueous cytoplasm. This may be particularly vital in icefish, which have larger oxidative muscle fibres compared to red-blooded nototheniods (C. aceratus, 2932+/-428 microm(2); C. rastrospinosus, 9352+/-318 microm(2); N. coriiceps, 1843+/-312 microm(2); G. gibberifrons, 2103+/-194 microm(2)). These large fibres contribute to a relatively low capillary density, which is partially compensated for in icefish by a high index of tortuosity in the capillary bed (C. aceratus=1.4, N. coriiceps=1.1).

Peripheral oxygen transport in skeletal muscle of Antarctic and sub-Antarctic notothenioid fish.

Transcellular oxygen flux was modelled mathematically in the aerobic skeletal muscles of perciform fish species living at widely different temperatures (Antarctica, sub-Antarctica and the Mediterranean Sea). Using structural data derived from stereological analysis of electron micrographs, mean fibre P(O(2)) was calculated on the basis of temperature-corrected rates of mitochondrial respiration and oxygen diffusion. The mean muscle fibre diameter (MFD) among Antarctic notothenioids was in the range 17-61 microm and mitochondrial volume density, Vv(mit,f), was 0.27-0.53, but capillary-to-fibre ratio varied only between 1.2 and 1.5. For a mean capillary P(O(2)) of 6 kPa, the model predicted a mean tissue P(O(2)) in the range 0.7-5.8 kPa at the estimated maximum aerobic capacity (M(O(2)max)). The lowest levels of tissue oxygenation were found in the pectoral muscle fibres of the icefish Chaenocephalus aceratus, which lacks the respiratory pigments haemoglobin and myoglobin. Red-blooded notothenioids found in the sub-Antarctic had a similar muscle fine structure to those caught south of the Antarctic Convergence, with an MFD of 20-41 microm and Vv(mit,f) of 0.27-0.33, resulting in an estimated mean P(O(2)) of 4-5 kPa at M(O(2)max). Mean tissue P(O(2)) in the sub-Antarctic icefish Champsocephalus esox, with greater MFD and Vv(mit,f), 56 microm and 0.51, respectively, was calculated to exceed 1 kPa at winter temperatures (4 degrees C), although oxidative metabolism was predicted to be impaired at the summer maximum of 10 degrees C. At the high end of the thermal range, related perciform species from the Mediterranean had a negligible drop in intracellular P(O(2)) across their small-diameter fibres, to a minimum of 5.4 kPa, comparable with that predicted for Trematomus newnesi from the Antarctic (5.6 kPa) with a similar MFD. These data suggest that, within a single phylogenetic group, integrative structural adaptations potentially enable a similar degree of tissue oxygenation over a 20 degrees C range of environmental temperature in the red-blooded notothenioids, and that this is compromised by the lack of respiratory pigments in the icefishes. The mean capillary radius was 1.5 times greater in the two icefish than in the other notothenioids, and the model simulations indicate that the evolution of wide-bore capillaries is essential to maintain tissue oxygenation in the absence of respiratory pigments.

The possible role of intracellular lipid in determining oxygen delivery to fish skeletal muscle

Transcellular oxygen flux in skeletal muscle fibres was modelled mathematically. In eels at the same environmental temperature (15°C), changes in muscle structure associated with increased levels of activity elevated mean fibre P O 2 by 30% to 5.2 kPa, despite greater fibre radius and V ̇ O 2 , due to more capillaries and intracellular lipid. The latter results in a 68% increase in oxygen permeability ( P O 2 ). While cold acclimation of striped bass (5 vs. 25°C) led to a modest (12%) fibre hypertrophy, V ̇ O 2 fell proportionately more (by 60%). A 50% increase in capillary supply again aids oxygen flux, while the presence of intracellular lipid effectively reverses the cold-induced decrease in P O 2 . The combined effect is to increase mean fibre P O 2 from 1.9 to 4.6 kPa and minimum P O 2 from 0.57 to 4.2 kPa, respectively. These data suggest little selection pressure exists to alter fibre composition in order to increase peripheral oxygen transport, while the magnitude of change in intracellular P O 2 is likely in excess of that required to maintain locomotory activity. Hence, there may be some other factor than P O 2 regulating structural reorganisation of muscle fine structure.

Muscle fine structure and microtubule birefringence measured with a new pol-scope.

Previous articleNext article No AccessCELL DIVISION, CELL MOTILITY, AND DEVELOPMENTMuscle Fine Structure and Microtubule Birefringence Measured with a New Pol-ScopeP. T. Tran, S. Inoué, E. D. Salmon, and R. OldenbourgP. T. Tran Search for more articles by this author , S. Inoué Search for more articles by this author , E. D. Salmon Search for more articles by this author , and R. Oldenbourg Search for more articles by this author PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The Biological Bulletin Volume 187, Number 2October 1994 Published in association with the Marine Biological Laboratory Article DOIhttps://doi.org/10.1086/BBLv187n2p244 Views: 13Total views on this site Citations: 2Citations are reported from Crossref Copyright © 1994 by Marine Biological LaboratoryPDF download Crossref reports the following articles citing this article:P. Tran, E. D. Salmon, and R. Oldenbourg Mitotic Spindle Fine Structures Observed With Polarized Light, The Biological Bulletin 191, no.22 (Sep 2016): 271–272.https://doi.org/10.1086/BBLv191n2p271E. L. Bearer, J. Liu, A. Hsu, and T. S. Reese Method for Visualizing Filaments in Axoplasm by Electron Microscopy, The Biological Bulletin 191, no.22 (Sep 2016): 272–273.https://doi.org/10.1086/BBLv191n2p272

Microscopic anatomy of pycnogonida: I. Cuticle, epidermis, and muscle

The integument of Pycnogonida (Arthropoda) consists of an epicuticle decorated with tubercles and a filamentous coat, an exocuticle with a small number of ill-defined layers, and an endocuticle whose numerous layers are composed of conspicuously cross-banded fibrils. This cuticular periodicity, attributable to cross-linked chitin, has been observed previously in uncalcified and untanned cuticle of many lower crustaceans, especially branchiopods and copepods, and in scattered examples of thin respiratory or excretory cuticles of other arthropods. It is uniformly present in all representatives of all nine pycnogonid families examined to date. Stomodeal, proctodeal, and arthrodial cuticles are devoid of the endocuticular periodicity. The cuticle is decorated with sensory filaments and setae, but is more noteworthy for a dense coverage by glands, up to 1,400/mm2. Myocuticular junctions have desmosomal fine structure previously found only in chelicerates. Muscle fine structure is that of slow fibers with long sarcomeres and a high actin to myosin filament ratio, except for cardiac muscle, which has short sarcomeres. Among the arthropods, only merostomates resemble the pycnogonids in the lack of fast somatic muscle fibers. Pycnogonids display a hybrid array of fine structural features that variously serve to relate them to some arthropod subphyla and distance them from others.

Developmental autonomy of muscle fine structure in muscle lineage cells of ascidian embryos

We have observed ultrastructural features of muscle differentiation in the muscle lineage cells of cleavage-arrested whole embryos and partial embryos of ascidians. Whole embryos of Ciona intestinalis and Ascidia ceratodes were cleavage-arrested with cytochalasin B at the 8-cell stage and reared to an age equivalent to several hours after hatching; these embryos formed extensive myofilaments which were often further organized into myofibrils of different sizes and densities in the peripheral cytoplasm of the two muscle lineage blastomeres (B4.1 pair). Developing myofibrils in cleavage-arrested embryos resembled the muscle elements observed in normal hatched larvae, but were less uniformly organized. A similar development of myofilaments and myofibrils occurred in the muscle lineage cells of multicellular partial embryos reared to “hatching” age. These partial embryos resulted from the isolated muscle lineage pair (B4.1) of blastomeres of the 8-cell stage ( Ciona and Ascidia), and from a muscle lineage blastomere pair (B5.2) isolated at the 16-cell stage ( Ascidia). Muscle lineage cells in the partial embryos were readily identified by the dense aggregates of mitochondria in their cytoplasm. Taken together, these results from the two kinds of partial embryo effectively eliminate inductive interactions with embryonic tissues other than mesodermal as a necessary factor in the onset of self-differentiation in muscle lineage cells. The relative complexity of muscle phenotype expressed in cleavage-arrested and partial embryos attests to an unusually strong developmental autonomy in the ascidian muscle lineages. This autonomy lends further support to the theory that a localized and segregated egg cytoplasmic determinant is responsible for larval muscle development in ascidian embryos.

Trophic reactions of crayfish muscle fibers and neuromuscular synapses after denervation, tenotomy, and immobilization

Severed motor nerve terminals remain morphologically intact and functionally competent for several months following transection of the motor nerve to the claw opener muscle of crayfish ( Procambarus clarki). However, severed motor axons are not entirely normal in that excitatory synapses produce junctional potentials that are somewhat smaller than control values. Tenotomy or immobilization often produce little change in synaptic potentials for at least 180 days. Opener muscle fibers with severed motor axons or immobilized muscle fibers show little ultrastructural change for at least 100 days, provided the nerve terminals remain intact. However, after tenotomy, muscle fibers atrophy within 20 to 30 days. This atrophy is more rapid and more severe if nerve terminals on that muscle fiber have degenerated. These atrophic changes in muscle fine structure include disorganization of myofibrils and disruption or loss of the sarcomere Z bands. In summary, our data show that drastic changes in crayfish muscle structure can proceed after tentomy without concomitant changes in function of the motor nerve terminals; and conversely, although transecting the motor nerve has some effect on motor nerve terminals, decentralization has little effect on muscle fiber structure as long as nerve terminals remain intact. These data are in agreement with the hypothesis that crustacean muscle fibers are trophically dependent on the presence of functional nerve terminals and on passive fiber tension (or resting length).

Molluscan visceral muscle fine structure. General structure and sarcolemmal organization in the smooth muscle of the intestinal wall of Buccinum undatum L.

Fine structure of intestinal muscle in the gastropod Buccinum undatum is described. Myofibrillar organization is typical of non-pseudostriated molluscan muscles. The dense body system is poorly developed but there are extensive attachment plaques. The sarcolemma is elaborately modified. Deep infoldings of the membrane give the cells an irregular outline. Such infoldings enclose extracellular matrix and are associated with attachment plaques. Arising from these and from the general sarcolemma are numerous tubular membranous invaginations ending blindly at varying depth in the sarcoplasm. These structures have a helical coat of particles on the cytoplasmic face. Associated with both types of invagination are subsarcolemmal vesicles. The possibility that the tubular invaginations are analogues of vertebrate smooth muscle caveolae or striated muscle T-tubules and that the vesicles are the corresponding sarcoplasmic reticulum is discussed. The occurrence of such structures in molluscan muscle and elsewhere is reviewed.

Intermembrane inclusions induced by anoxia in heart and skeletal muscle mitochondria.

Heart and skeletal muscle from rats of different ages were incubated in vitro in an oxygen-free medium supplied with substrates in order to investigate the effect of anoxia on muscle fine structure, particulary on the mitochondria. In skeletal muscle fibers anoxia has been found to induce changes similar to those previously described in ischemic muscles in vivo namely giant mitochondria, apparently derived by mitochondrial fusion, and intermembrane inclusions with a paracrystalline structure. The plate-like inclusions are mostly located in the intracristal spaces and are closely associated to cristal membranes even in markedly swollen mitochondria. Identical inclusions have been observed in cardiac muscle cells following anoxic injury, whereas they are never found in non-muscle cells such as endothelia, fibroblasts and nerve fibers. Cardiac and skeletal muscle fibers from newborn rats maintained in an oxygen-free medium show mitochondrial swelling but no intermembrane inclusions. The different response of mitochondria from developing vs adult striated muscle to anoxia may be due to changes during postnatal development in the quality or quantity of the protein component(s) involved in paracrystal formation.

An ultrastructural study of tettigoniid muscle in relation to function

The modian dorsal longitudinal indirect flight muscles from the mesothorax and metathorax of Homorocoryphus nitidulus vicinus have been studied to determine whether structural differences might offer an explanation for reports that the mesothoracic musculature effects a wing-beat rate of 140 beats/sec during stridulation, whereas during flight, it, like that of the metathorax, effects wing-beat frequencies of 14 to 20 beats/sec. No differences were observed and it is concluded that the high wing-beat rate, reported during stridulation, is not reflected in any specific modification of mesothoracic muscle fine structure. In addition, the fine structure of these muscles has been examined in order to determine changes associated with ageing; particular attention has been paid to variations in the chondriome.

MUSCLE FINE STRUCTURE IN THE KUGELBERG-WELANDER SYNDROME (CHRONIC SPINAL MUSCULAR ATROPHY)

Journal Article Muscle Fine Structure in the Kugelberg-Welander Syndrome (Chronic Spinal Muscular Atrophy) Get access Robert G. Roth, M.D., Robert G. Roth, M.D. New York, N.Y. Search for other works by this author on: Oxford Academic PubMed Google Scholar Leonard J. Graziani, M.D., Leonard J. Graziani, M.D. New York, N.Y. Search for other works by this author on: Oxford Academic PubMed Google Scholar Robert D. Terry, M.D., Robert D. Terry, M.D. New York, N.Y. Search for other works by this author on: Oxford Academic PubMed Google Scholar Labe C. Scheinberg, M.D. Labe C. Scheinberg, M.D. New York, N.Y. ‡Health Research Council Invesitgator. Search for other works by this author on: Oxford Academic PubMed Google Scholar Journal of Neuropathology & Experimental Neurology, Volume 24, Issue 3, July 1965, Pages 444–454, https://doi.org/10.1097/00005072-196507000-00006 Published: 01 July 1965

SARCOLEMMAL INVAGINATIONS CONSTITUTING THE T SYSTEM IN FISH MUSCLE FIBERS.

Striated muscle fibers from the body and tail myotomes of a fish, the black Mollie, have been examined with particular attention to the sarcoplasmic reticulum (SR) and transverse tubular (or T) system. The material was fixed in osmium tetroxide and in glutaraldehyde, and the images provided by the two kinds of fixatives were compared. Glutaraldehyde fixes a fine structure that is broadly comparable with that preserved by osmium tetroxide alone but differs in some significant details. Especially significant improvements were obtained in the preservation of the T system, that is, the system of small tubules that pervades the fiber at every Z line or A-I junction level. As a result of this improved glutaraldehyde fixation, the T system is now clearly defined as an entity of fine structure distinct from the SR but uniquely associated with the SR and myofibrils. Glutaraldehyde fixation also reveals that the T system is a sarcolemmal derivative that retains its continuity with the sarcolemma and limits a space that is in direct communication with the extracellular environment. These structural features favor the conclusion that the T system plays a prominent role in the fast intracellular conduction of the excitatory impulse. The preservation of other elements of muscle fine structure, including the myofibrils, seems for reasons discussed, to be substantially improved by glutaraldehyde.