potential angiogenesis regulatory factors in human skeletal muscle Acclimatization to 4100 m does not change capillary density or mRNA expression of (PDF (original) (raw)
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Increased fiber capillarization in flight muscle of finch at altitude
Respiration Physiology, 1998
We examined fiber capillarization and ultrastructure in the highly aerobic flight muscle of six gray crowned rosy finches (Leucosticte arctoa; mass 22.99 0.5 (SE) g) living at altitude (A; White Mountains of Eastern California; 4000 m) compared to eight sea-level (SL) house finches (Carpodacus mexicanus, mass, 19.8 9 0.6 g) of the same subfamily, Carduelinae. Capillary length per fiber volume (A, 10 400 9 409 mm − 2 ; SL, 75139 423; P B0.001) and capillary-tofiber ratio (A, 2.32 90.07; SL, 1.85 90.06; PB0.001) were significantly greater in A, with no difference in fiber cross-sectional area compared to SL. Capillary geometry was significantly different in A, yielding a greater contribution of tortuosity and branching to capillary length than in SL. Capillary-to-fiber surface ratio and fiber mitochondrial volume were both greater in A, but their ratio was similar to SL, indicating a proportional increase in the size of the capillary to fiber interface and fiber mitochondrial volume in A to sustain high levels of aerobic capacity while living at altitude.
Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle
Respiration physiology, 1992
We investigated structural characteristics for high O2 flux in hummingbird flight muscle, i.e. the most O2 demanding skeletal muscle per unit tissue mass among vertebrates. Pectoralis and supracoracoideus muscles of 3-4 g hummingbirds (Selaphorus rufus) were perfusion fixed in situ, processed for electron microscopy and analyzed by morphometry. Small fiber size (group mean +/- SE, 201 +/- 14 microns 2 at 2.1 microns sarcomere length), large capillary length per fiber volume (8947 +/- 869 mm-2) and high mitochondrial volume density per volume of muscle fiber (34.5 +/- 0.9%) were characteristic features of the muscles. Considering capillary supply and mitochondrial volume on an individual fiber basis showed that the size of the capillary-to-fiber interface (i.e. capillary surface per fiber surface) was also high in the muscles. Comparison with mammalian hindlimb pointed to a major role of the size of the capillary-to-fiber interface in providing a great potential for O2 flux rate from...
Fiber capillarization relative to mitochondrial volume in diaphragm of shrew
Journal of Applied …, 2002
Mathieu-Costello, O., S. Morales, J. Savolainen, and M. Vornanen. Fiber capillarization relative to mitochondrial volume in diaphragm of shrew. was to examine fiber capillarization in relation to fiber mitochondrial volume in the highly aerobic diaphragm of the shrew, the smallest mammal. The diaphragms of four common shrews [Sorex araneus; body mass, 8.2 Ϯ 1.3 (SE) g] and four lesser shrews (Sorex minutus, 2.6 Ϯ 0.1 g) were perfusion fixed in situ, processed for electron microscopy, and analyzed by morphometry. Capillary length per fiber volume was extremely high, at values of 8,008 Ϯ 1,054 and 12,332 Ϯ 625 mm Ϫ2 in S. araneus and S. minutus, respectively (P ϭ 0.012), with no difference in capillary geometry between the two species. Fiber mitochondrial volume density was 28.5 Ϯ 2.3% (S. araneus) and 36.5 Ϯ 1.4% (S. minutus; P ϭ 0.025), yielding capillary length per milliliter mitochondria values (S. araneus, 27.8 Ϯ 1.5 km; S. minutus, 33.9 Ϯ 2.2 km; P ϭ 0.06) as high as in the flight muscle of the hummingbird and small bats. The size of the capillary-fiber interface (i.e., capillary surface per fiber surface ratio) per fiber mitochondrial volume in shrew diaphragm was also as high as in bird and bat flight muscles, and it was about two times greater than in rat hindlimb muscle. Thus, whereas fiber capillary and mitochondrial volume densities decreased with increased body mass in S. araneus compared with S. minutus Soricinae shrews, fiber capillarization per milliliter mitochondria in both species was much higher than previously reported for shrew diaphragm, and it matched that of the intensely aerobic flight muscles of birds and mammals. capillary-fiber interface; capillary anisotropy; capillary shape; ultrastructure; morphometry
European journal of applied …, 1992
The effects of changes in oxygen supply and oxygen demands on fiber cross-sectional areas, capillary dersities and capillary to fiber ratios were determined in three skeletal muscles of rat. The muscles examined were the vastus lateralis, soleus, and diaphragm. Reduced oxygen supply was produced by subjecting rats to ambient hypoxia, and increased oxygen demands were produced by subjecting rats to low ambient temperatures or treatment with thyroxin. Capillaries were visualized by injecting fluorescent dyes into the circulation. Muscles were quick frozen at resting lengths to preserve normal fiber geometry and were subsequently sectioned on a cryostat. All of the muscles sampled from animals in the experimental groups had elevated capillary densities. However, capillary to fiber ratios were not increased significantly in any muscle, for any experimental condition. Thus, all of the observed differences in capillarity were due to changes in the intrinsic rate of muscle fiber growth. Further, the relations of capillary density and capillary to fiber ratio to fiber area were the same as those obtained during normal maturation, suggesting that capillary growth is closely linked to the intrinsic rate of fiber growth.
Descriptive and functional morphometry of skeletal muscle fibres in wild birds
Canadian Journal of Zoology, 1999
The fibre types of four forelimb and two hind-limb muscles involved in locomotion were morphometrically analyzed in three species of wild birds: the mallard (Anas platyrhynchos), common coot (Fulica atra), and yellowlegged gull (Larus cachinnans). Fibre cross-sectional area and perimeter, maximal diffusion distance, and number of capillaries per fibre were measured and the functional implications and physiological demands of the muscles of each species were inferred. In general, all morphometric values were lower in oxidative fibres than in anaerobic fibres, indicating that the supply of oxygen and metabolites available to aerobically working muscles is enhanced. The lower level of activity required during gliding as opposed to flapping flight, and the need to maintain the wings in an outstretched position, presumably by means of isometric contractions, may explain the greater size of the oxidative fibres of the pectoralis and scapulotriceps muscles of the gull. In contrast, the high oxidative demand imposed on mallards and coots by sustained flapping flight is met by small oxidative fibres, possibly at the expense of a reduction in the ability of each fibre to generate force. Anaerobic fibres of the gastrocnemius muscle had greater cross-sectional areas in the mallard and coot than in the gull. This is interpreted as an adaptive response to force generation during burst locomotion, which is usually performed by both mallards and coots, in sharp contrast to the buoyant swimming and postural activities undertaken by gull's legs. The fast oxidative fibres of the gastrocnemius muscle were, in general, larger than those of the iliotibialis muscle in the three species, which matches the different mechanical and functional roles of these muscles during swimming. Résumé : Les types de fibres dans les muscles responsables de la locomotion, quatre muscles des membres antérieurs et deux muscles des membres postérieurs, ont fait l'objet d'une analyse morphométrique chez trois espèces d'oiseaux en nature, le Canard colvert (Anas platyrhynchos), la Foulque macroule (Fulica atra) et le Goéland leucophée (Larus cachinnans). La surface des fibres en coupe transversale, leur périmètre, les distances maximales de diffusion et le nombre de capillaires par fibre ont été mesurés et ces mesures ont permis de déduire les conditions de fonctionnement, de même que les besoins physiologiques des muscles de chaque espèce. En général, toutes les mesures morphométriques se sont avérées plus basses dans les fibres oxydatives que dans les fibres anaérobies, ce qui indique que la quantité d'oxygène et de métabolites fournie aux muscles à fonctionnement aérobie est supérieure. L'activité moins importante reliée au vol plané par opposition au vol avec battements d'ailes et la nécessité de maintenir les ailes étendues, probablement par l'intermédiaire de contractions isométriques, explique probablement la taille plus grande des fibres oxydatives du pectoralis et des scapulotriceps chez le goéland. En revanche, le besoin important d'oxygène pour assurer le battement des ailes chez le colvert et la foulque est fourni par les fibres oxydatives de petite taille, ce qui se traduit probablement par une diminution de la force que peut générer chaque fibre. Chez le Canard colvert et chez la foulque, les fibres anaérobies du gastrocnémien ont une surface plus grande en coupe transversale que celles du goéland. Il semble qu'il s'agisse là d'une adaptation au déploiement d'une force au cours d'un déplacement subit, une tactique utilisée couramment par le colvert et la foulque, tactique totalement différente de la nage par flottaison et des activités reliées à la posture associées aux pattes du goéland. Les fibres oxydatives rapides du gastrocnémien sont en général plus grosses que celles du muscle iliotibialis chez les trois espèces, ce qui correspond aux rôles mécanique et fonctionnel de ces muscles au cours de la nage.
Comparative skeletal muscle fibre morphometry among wild birds with different locomotor behaviour
Journal of Anatomy, 1998
Six muscles of the mallard duck (Anas platyrhynchos), the common coot (Fulica atra) and the yellow-legged gull (Larus cachinnans) were analysed morphometrically, with special emphasis on their functional implications and physiological needs. Oxidative fibres always had significantly smaller size than anaerobic fibres, although no differences in the number of capillaries per fibre were found. This resulted in greater capillary counts per unit of fibre area and perimeter in oxidative than anaerobic fibres, which indicates that the greater demand for oxygen supply may be achieved by decreasing the size of the muscle fibre rather than by increasing the number of associated capillaries. Fast oxidative fibres of the pectoralis and the triceps of the gull had greater sizes than the fast oxidative fibres of the mallard and the coot, which correlates with the difference in energetic demands between flapping and gliding flight. Greater fibre cross-sectional areas and perimeters seem suited to afford the long-lasting activity with low metabolic demands required during gliding. By contrast, mallards and coots attain a high oxidative metabolism, during sustained flapping flight, by reducing fibre size at the expense of a diminished ability for force generation. Between-species comparisons of the hindlimb muscles only yielded differences for the anaerobic fibres of the gastrocnemius, as an important adaptive response to force generation during burst locomotion. The need to manage sustained swimming abilities effectively may result in similar FOG fibre morphometry of the hindlimb muscles studied, indicating that a compromise between the oxygen flux to the muscle cell and the development of power is highly optimised in oxidative fibres of the bird species studied.
Journal of Experimental Biology, 2009
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, b0.1 to 0.8) over a body mass range of ~20-1500g, but only creatine phosphokinase showed positive scaling in lateral red muscle (b0.5). Although oxidative enzymes showed negative allometry in red muscle (b-0.01 to-0.02), mass-specific myoglobin content scaled positively (b0.7). 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 2962±305mm-2) as a result of larger fibre size (658±31 vs 307±24m 2 in 1595g and 22.9g 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 ~40% fibre volume in the smallest to ~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 (b0.085) may enhance specific force generation in larger fish. Modelling intracellular P O2 distribution suggests such integrated structural modifications are required to maintain adequate oxygen delivery (calculated P O2 5.15±0.02kPa and 5.21±0.01kPa in small and large fish, respectively).
Mitochondrial function in sparrow pectoralis muscle
Journal of Experimental Biology, 2012
Flying birds couple a high daily energy turnover with double-digit millimolar blood glucose concentrations and insulin resistance. Unlike mammalian muscle, flight muscle predominantly relies on lipid oxidation during locomotion at high fractions of aerobic capacity, and birds outlive mammals of similar body mass by a factor of three or more. Despite these intriguing functional differences, few data are available comparing fuel oxidation and free radical production in avian and mammalian skeletal muscle mitochondria. Thus we isolated mitochondria from English sparrow pectoralis and rat mixed hindlimb muscles. Maximal O 2 consumption and net H 2 O 2 release were measured in the presence of several oxidative substrate combinations. Additionally, NADand FAD-linked electron transport chain (ETC) capacity was examined in sonicated mitochondria. Sparrow mitochondria oxidized palmitoyl-L-carnitine 1.9-fold faster than rat mitochondria and could not oxidize glycerol-3-phosphate, while both species oxidized pyruvate, glutamate and malate-aspartate shuttle substrates at similar rates. Net H 2 O 2 release was not significantly different between species and was highest when glycolytic substrates were oxidized. Sonicated sparrow mitochondria oxidized NADH and succinate over 1.8 times faster than rat mitochondria. The high ETC catalytic potential relative to matrix substrate dehydrogenases in sparrow mitochondria suggests a lower matrix redox potential is necessary to drive a given O 2 consumption rate. This may contribute to preferential reliance on lipid oxidation, which may result in lower in vivo reactive oxygen species production in birds compared with mammals. . Relation between plasma lactate concentration and fat oxidation rates over a wide range of exercise intensities. Int. J. Sports Med. 25, 32-37. Ahlborg, G., Felig, P., Hagenfeldt, L., Hendler, R. and Wahren, J. (1974). Substrate turnover during prolonged exercise in man. Splanchnic and leg metabolism of glucose, free fatty acids, and amino acids. . (2009). Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. . Enzymic and metabolic adaptations in the gastrocnemius, plantaris and soleus muscles of hypocaloric rats. Biochem. J. 261, 219-225. Armstrong, R. B. and Phelps, R. O. (1984). Muscle fiber type composition of the rat hindlimb. Am. J. Anat. 171, 259-272. Baldwin, K. M., Klinkerfuss, G. H., Terjung, R. L., Mole, P. A. and Holloszy, J. O. (1972). Respiratory capacity of white, red, and intermediate muscle: adaptative response to exercise. . Localization at complex I and mechanism of the higher free radical production of brain nonsynaptic mitochondria in the short-lived rat than in the longevous pigeon. J. Bioenerg. Biomembr. 30, 235-243. Barja, G., Cadenas, S., Rojas, C., Perez-Campo, R. and Lopez-Torres, M. (1994).
Maximal diffusion-distance within skeletal muscle can be estimated from mitochondrial distributions
Respiration Physiology, 1990
Mitochondrial volume density (V,[mit]) distributions were measured with a test pattern of concentric rings centered upon randomly chosen capillaries in oxidative skeletal muscle ceils of two Antarctic fishes, Trematomus newnesi and Notothenia gibberifrons. Vv(mit) in both species was highest in the ring closest to the capillary, minimal further from the capillary (at a distance that was characteristic for each species), and rose in the annuli furthest from the capillary. Plots of Vv(mit) against total area between each ring and the central capillary fit the form of a second-order polynomial (r2> 0.9). If Po2 or blood-borne metabolite concentration predicates the pattern of Vv(mit) distribution, minimal Vv(mit) is at the same position as the minimum in concentration or gaseous partial pressure of capillary-supplied commodities. This minimum is the boundary between cylinders of tissue being supplied by adjacent capillaries, and thus delineates the maximal diffusion-distance for capillary-supplied commodities. Maximal diffusion-distance (#m) for T. newnesi-26.23 + 1.64; N. gibberifrons = 21.45 + 0.51. For 02, maximal diffusion-distance conventionally is referred to as Krogh's radius, R. With an easily obtained estimate of numerical capillary density, these R values can be used to calculate a capillary tortuosity constant (c[k,0]) and capillary length density (Jr [c,f]). c(k,0) values were also determined using an established method, and R and Jv(c,f) values calculated from these values did not significantly differ from values determined from mitochondrial distributions. Mitochondrial distribution analysis may more accurately reflect changes in capillary blood flow and heterogeneity of diffusion and solubility constants within muscle than currently existing techniques. Similar distributions of V,,(mit) reported for several species of vertebrates suggest wide applicability of the method. Animal, antarctic fish; Capillaries, density in skeletal muscle, tortuosity; Diffusion, of 02 in tissue; Mitochondria, distribution of-in skeletal muscle; Skeletal muscle, diffusion distance, capillary supply Several methods exists to estimate maximal diffusion-distances for capillary-supplied commodities within skeletal muscle, including the capillary-domains method (Hoofd et al., 1985), the closest individual method (Kayar et al., 1982), and the concentric circle method (Kayar and Banchero, 1982). All of these techniques are based upon August Krogh's pioneering model of oxygen delivery to striated muscle cells (Krogh, 1919).
Capillary blood transit time in muscles in relation to body size and aerobic capacity. J Exp Biol
Journal of Experimental Biology
The mean minimal transit time for blood in muscle capillaries (tc) was estimated in six species, spanning two orders of magnitude in body mass and aerobic capacity: horse, steer, dog, goat, fox and agouti. Arterial (CaO∑) and mixed venous (Cv -O∑) blood O2 concentrations, blood hemoglobin concentrations ([Hb]) and oxygen uptake rates were measured while the animals ran on a treadmill at a speed that elicited the maximal oxygen consumption rate (V · O∑max) from each animal. Blood flow to the muscles (Q · m) was assumed to be 85 % of cardiac output, which was calculated using the Fick relationship. Total muscle capillary blood volume (Vc) and total muscle mitochondrial volume were estimated by morphometry, using a whole-body muscle sampling scheme. The tc was computed as Vc/Q · m. The tc was 0.3-0.5 s in the 4 kg foxes and agoutis, 0.7-0.8 s in the 25 kg dogs and goats, and 0.8-1.0 s in the 400 kg horses and steers. The tc was positively correlated with body mass and negatively correlated with transcapillary O2 release rate per unit capillary length. Mitochondrial content was positively correlated with V · O∑max and with the product of Q · m and [Hb]. These data suggested that Q · m, Vc, maximal hemoglobin flux, and consequently tc, are co-adjusted to result in muscle O2 supply conditions that are matched to the O2 demands of the muscles at V ·