Ultrastructure of Aerobic Muscle in Antarctic Fishes may Contribute to Maintenance Of Diffusive Fluxes

1990 ◽  
Vol 150 (1) ◽  
pp. 205-220 ◽  
Author(s):  
RICHARD L. LONDRAVILLE ◽  
BRUCE D. SIDELL

Quantitative ultrastructural analyses were performed on red (oxidative) and white (glycolytic) skeletal muscles from two species of antarctic fish to identify features of subcellular structure that may be related to muscle metabolism at cold body temperature. Trematomus newnesi (Boulenger) is an active pelagic species and Notothenia gibberifrons (Lönnberg) is a sluggish bottom-dweller. White fibres of both species are poorly vascularized [capillary density, NA(c,f), for T. newnesi 73.9±11.3mm−2; for N. gibberifrons is 76.0±14.1mm−2], and have low percentages of cell volume occupied by mitochondria [volume density, Vv(mit,f), for T. newnesi is 0.014±0.005; for N. gibberifrons is 0.006±0.003]. Ultrastructure of oxidative fibres in both species resembles that of cold-acclimated temperate-zone fishes. Mitochondrial volume densities of red fibres reflect differences in ecotype between species [Vv(mit,f) for T. newnesi is 0.348±0.012; for N. gibberifrons is 0.249±0.007]. The less clustered array of mitochondria in oxidative fibres of T. newnesi compared with N. gibberifrons may support an equivalent flux of aqueous metabolites between mitochondrial and cytoplasmic compartments, despite a greater mean intracellular diffusion distance (τh) between these compartments in T. newnesi than in N. gibberifrons (τh=1.05±0.07μm and 0.77±0.06μm, respectively). Although Vv(mit.)) is higher in red fibres of the active species, capillary supply is less extensive [capillary length density, Jv(c,f), for T. newnesi is 481.3±49.0mm mm−3; N. gibberifrons is 696.3±33.7mm mm−3] and the maximal diffusion-distance for oxygen is greater in T. newnesi than in N. gibberifrons (Krogh's radius, R=26.3±1.64μm and 21.5±0.51μm, respectively). A mismatch appears to exist between oxygen supply [Jv(c,f)] and oxygen demand [Vv(mit,f)] in T. newnesi red fibres in view of published data for other fishes. The twofold higher volume density of lipid [Vv(lip,f)] in T. newnesi compared with N. gibberifrons may resolve this paradox [Vv(lip,f) is 0.026±0.002 and 0.012±0.004, respectively]. Because oxygen is at least four times more soluble in lipid than in aqueous cytoplasm, lipid may enhance oxygen flux through oxidative muscle and play a role similar to myoglobin in these myoglobin-poor fishes.

2005 ◽  
Vol 99 (1) ◽  
pp. 281-289 ◽  
Author(s):  
O. Mathieu-Costello ◽  
Y. Ju ◽  
M. Trejo-Morales ◽  
L. Cui

The objective was to examine whether muscle structural capacity for O2 flux (i.e., capillary-to-fiber surface ratio) relative to fiber mitochondrial volume deteriorates with the muscle atrophy of aging in predominantly slow- (soleus, S) and fast-twitch (extensor digitorum longus, EDL) muscles of old (24 mo) and very old (35 mo) F344BN rats compared with adult (12 mo old). Wet muscle mass decreased 29% (196 ± 4 to 139 ± 5 mg) in S and 22% (192 ± 3 to 150 ± 3 mg) in EDL between 12 and 35 mo of age, without decline in body mass. Capillary density increased 65% (1,387 ± 54 to 2,291 ± 238 mm−2) in S and 130% (964 ± 95 to 2,216 ± 311 mm−2) in EDL, because of the muscle fiber atrophy, whereas capillary per fiber number remained unchanged. Altered capillary geometry, i.e., lesser contribution of tortuosity and branching to capillary length, was found in S at 35 compared with 12 and 24 mo, and not in EDL. Accounting for capillary geometry revealed 55% (1,776 ± 78 to 2,750 ± 271 mm−2) and 113% (1,194 ± 112 to 2,540 ± 343 mm−2) increases in capillary length-to-fiber volume ratio between 12 and 35 mo of age in S and EDL, respectively. Fiber mitochondrial volume density was unchanged over the same period, causing mitochondrial volume per micrometer fiber length to decrease in proportion to the fiber atrophy in both muscles. As a result of the smaller fiber mitochondrial volume in the face of the unchanged capillary-to-fiber number ratio, capillary-to-fiber surface ratio relative to fiber mitochondrial volume not only did not deteriorate, but in fact increased twofold in both muscles between 12 and 35 mo of age, independent of their different fiber type.


1986 ◽  
Vol 120 (1) ◽  
pp. 189-199 ◽  
Author(s):  
S. R. Kayar ◽  
K. E. Conley ◽  
H. Claassen ◽  
H. Hoppeler

Rats were subjected to a laddermill running programme either once per week for 6 weeks, or daily for 6 weeks. Heart mass and maximal oxygen consumption rate increased relative to controls and with the frequency of the running programme. Mitochondrial distribution, measured in seven regions within fibres, was similar in all hearts, with a peak volume density of 0.42 +/− 0.01 occurring 4–5 microns from the centre of a capillary. Capillary density decreased with increasing heart mass, but total capillary length and capillary-to-fibre ratio were constant. Thus the higher metabolic demands of the running programmes did not alter the volume density or distribution of mitochondria, despite significant increases in heart mass and decreases in capillarity.


1999 ◽  
Vol 277 (2) ◽  
pp. H756-H762 ◽  
Author(s):  
A. M. Lewis ◽  
O. Mathieu-Costello ◽  
P. J. McMillan ◽  
R. D. Gilbert

To determine the effect of chronic hypoxia on myocardial capillarity, we exposed pregnant ewes to an altitude of 3,820 m from day 30 to day 139 of gestation and compared the fetus to low-altitude (∼300 m) controls. We hypothesized that capillarity would increase in the hypoxic myocardium to optimize oxygen and metabolite flux to hypoxic tissues. Fetal hearts were fixed by retrograde aortic perfusion and processed for microscopy and stereological evaluation. Fiber cross-sectional area and capillary density were measured and standardized to sarcomere length. Capillary volume density and capillary diameter were measured, capillary-to-fiber ratio and capillary length density were calculated, and the capillary anisotropy coefficient was obtained from a table of known values. Capillary-to-fiber ratio, capillary volume density, and the capillary anisotropy coefficient were not different between hypoxia and control groups. Capillary diameter was significantly larger in the right compared with the left ventricle of hypoxic but not control hearts; fiber cross-sectional area tended to be larger in the right ventricle of both groups, but this was not significant. As a result of larger fiber size, capillary density and capillary length density were significantly smaller in the right ventricle of hypoxic but not control fetal hearts. Contrary to our hypothesis, the ovine fetus does not show morphological adaptation in the myocardium after ∼109 days of high-altitude hypoxic stress.


2000 ◽  
Vol 88 (2) ◽  
pp. 560-566 ◽  
Author(s):  
Russell T. Hepple ◽  
Michael C. Hogan ◽  
Creed Stary ◽  
Donald E. Bebout ◽  
Odile Mathieu-Costello ◽  
...  

Although evidence for muscle O2 diffusion limitation of maximal O2 uptake has been found in the intact organism and isolated muscle, its relationship to diffusion distance has not been examined. Thus we studied six sets of three purpose-bred littermate dogs (aged 10–12 mo), with 1 dog per litter allocated to each of three groups: control (C), exercise trained for 8 wk (T), or left leg immobilized for 3 wk (I). The left gastrocnemius muscle from each animal was surgically isolated, pump-perfused, and electrically stimulated to peak O2 uptake at three randomly applied levels of arterial oxygenation [normoxia, arterial[Formula: see text]([Formula: see text]) 77 ± 2 (SE) Torr; moderate hypoxia, [Formula: see text]: 33 ± 1 Torr; and severe hypoxia, [Formula: see text]: 22 ± 1 Torr]. O2 delivery (ml ⋅ min−1 ⋅ 100 g− 1) was kept constant among groups for each level of oxygenation, with O2 delivery decreasing with decreasing [Formula: see text]. O2extraction (%) was lower in I than T or C for each condition, but calculated muscle O2 diffusing capacity (Dm[Formula: see text]) per 100 grams of muscle was not different among groups. After the experiment, the muscle was perfusion fixed in situ, and a sample from the midbelly was processed for microscopy. Immobilized muscle showed a 45% reduction of muscle fiber cross-sectional area ( P < 0.05), and a resulting 59% increase in capillary density ( P < 0.05) but minimal reduction in capillary-to-fiber ratio (not significant). In contrast, capillarity was not significantly different in T vs. C muscle. The results show that a dramatically increased capillary density (and reduced diffusion distance) after short-term immobilization does not improve Dm[Formula: see text] in heavily working skeletal muscle.


1989 ◽  
Vol 257 (1) ◽  
pp. H1-H9 ◽  
Author(s):  
J. J. Smolich ◽  
A. M. Walker ◽  
G. R. Campbell ◽  
T. M. Adamson

This study has examined left (LV) and right ventricular (RV) myocardial morphometry in perfusion-fixed hearts of late-gestation sheep fetuses, neonatal lambs, and adult sheep. During development, myocyte size, intercapillary distance, and myocyte myofibrillar and mitochondrial volume densities increased, whereas capillary density, the myocyte-to-capillary ratio, and the myocyte matrix volume density decreased. RV myocytes were larger than LV myocytes in cross section in fetuses and 4-day-old lambs. LV and RV myocytes were of similar size in 7-day-old lambs. LV and RV myocytes were of larger in older lambs and adult sheep. Differences between LV and RV myocyte volume densities of myofibrils, mitochondria, and matrix were also observed in fetuses and young lambs. As well, variation in capillary size and density was apparent between ventricles in the fetal and neonatal periods. We conclude that, in the sheep heart, 1) LV and RV morphometric differences exist during fetal and postnatal development, 2) fetal LV and RV myocardial morphometry is consistent with an RV dominance in utero, 3) rapid growth of LV and RV myocytes occurs in the perinatal period, and 4) the relative size of LV and RV myocytes does not reflect a postnatal LV dominance until between 1 and 4 wk after birth.


1998 ◽  
Vol 9 (6) ◽  
pp. 1018-1022 ◽  
Author(s):  
K Amann ◽  
M Breitbach ◽  
E Ritz ◽  
G Mall

Experiments indicate that capillary density is reduced in the hypertrophied left ventricle of rats with subtotal nephrectomy compared to control rats with similar BP and left ventricular hypertrophy, suggesting that in uremia, hypertrophying cardiomyocytes outgrow their capillary supply. No information on myocardial capillary supply in humans is currently available. The hearts of nine dialyzed patients, nine patients with essential hypertension, and 10 normotensive control subjects at postmortem were obtained. Subjects with stenosing coronary lesions and left ventricular pump failure were excluded. Special sampling procedures were used to exclude stereologic artefacts. Capillaries were specifically stained with ulex lectin and analyzed by stereologic techniques. Length density of myocardial capillaries (Lv; mm/mm3) was significantly (P < 0.001) lower in dialyzed patients (1483 +/- 238) than in patients with essential hypertension (1872 +/- 243) or in normotensive control patients (2898 +/- 456). In parallel, myocyte diameter and volume density of myocardial interstitial tissue were significantly (P < 0.001) increased in uremic patients compared to patients with essential hypertension and control patients, respectively. Diminished left ventricular capillary supply in renal failure must increase critical oxygen diffusion distance in the myocardium, thus exposing cardiomyocytes to the risk of hypoxia. It is unknown whether such reduced ischemia tolerance can be reversed by increasing oxygen supply (e.g., by reversing anemia).


2002 ◽  
Vol 205 (6) ◽  
pp. 829-840 ◽  
Author(s):  
Durmus Deveci ◽  
Stuart Egginton

SUMMARY The physiological, metabolic and anatomical adaptations of skeletal muscle to chronic cold exposure were investigated in Wistar rats (Rattus norvegicus), a species that defends core temperature, and Syrian hamsters (Mesocricetus auratus), which may adopt a lower set point under unfavourable conditions. Animals were exposed to a simulated onset of winter in an environmental chamber, progressively shortening photoperiod and reducing temperature from 12 h:12 h L:D and 22°C to 1 h:23 h L:D and 5°C over 4 weeks. The animals were left at 4°C for a further 4 weeks to complete the process of cold-acclimation. M. tibialis anterior from control (euthermic) and cold-acclimated animals of similar mass showed a significant hyperactivity-induced hypertrophy in the rat, but a small disuse atrophy in the hamster. Little evidence was found for interconversion among fibre types in skeletal muscle on cold-acclimation, and only modest differences were seen in activity of oxidative or glycolytic enzymes in either species. However, adjustments in Type II fibre size paralleled the muscle hypertrophy in rat and atrophy in hamster. Cold-induced angiogenesis was present in the rat, averaging a 28 % increase in capillary-to-fibre ratio (C:F) but, as this was balanced by fibre hypertrophy across the whole muscle, there was no change in capillary density (CD). In contrast, the C:F was similar in both groups of hamsters, whereas CD rose by 33 % in line with fibre atrophy. Within distinct regions of the m. tibialis anterior, there was a correlation between angiogenesis and fibre size in rats, in which oxygen diffusion distance increased, but not in hamsters, in which there was a reduced oxygen diffusion distance. Consequently, the change in C:F was greatest (39 %) in the glycolytic cortex region of the m. tibialis anterior in rats. We conclude that non-hibernator and hibernator rodents improve peripheral oxygen transport following cold-acclimation by different mechanisms. In rats, an increase in fibre girth was accompanied by a true angiogenesis, while the improved apparent capillary supply in hamsters was due to smaller fibre diameters. These responses are consistent with the strategies of resisting and accommodating, respectively, an annual fall in environmental temperature.


1979 ◽  
Vol 237 (6) ◽  
pp. E548 ◽  
Author(s):  
A P Shepherd

It has been postulated that local circulatory control mechanisms regulate the O2 flux to parenchymal cells by two vascular mechanisms: changes in blood flow that minimize capillary PO2 variations and changes in the density of the perfused capillary bed through which O2 extraction is regulated. To test this prediction, isolated loops of canine jejenum and ileum were perfused at either constant blood flow or constant pressure, and intraluminal glucose was used to increase metabolic rate. In the constant-flow series, glucose increased O2 extraction, O2 uptake, and rubidium extraction. Resistance fell when the metabolic rate was elevated. In the constant-pressure series, glucose increased blood flow, O2 extraction, O2 uptake, and capillary filtration coefficients. These results show that vascular resistance falls and that capillary density increases following an increase in oxygen demand. Thus, the glucose-stimulated gut loop seems to be a valid model of metabolic hyperemia, and its behavior would be difficult to reconcile with a purely myogenic theory of intestinal blood flow autoregulation.


2002 ◽  
Vol 93 (1) ◽  
pp. 346-353 ◽  
Author(s):  
O. Mathieu-Costello ◽  
S. Morales ◽  
J. Savolainen ◽  
M. Vornanen

The objective 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 ± 1.3 (SE) g] and four lesser shrews ( Sorex minutus, 2.6 ± 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 ± 1,054 and 12,332 ± 625 mm−2 in S. araneus and S. minutus, respectively ( P= 0.012), with no difference in capillary geometry between the two species. Fiber mitochondrial volume density was 28.5 ± 2.3% ( S. araneus) and 36.5 ± 1.4% ( S. minutus; P = 0.025), yielding capillary length per milliliter mitochondria values ( S. araneus, 27.8 ± 1.5 km; S. minutus, 33.9 ± 2.2 km; P = 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. minutusSoricinae 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.


1988 ◽  
Vol 133 (2) ◽  
pp. 89-95 ◽  
Author(s):  
Laurence Mermod ◽  
Hans Hoppeler ◽  
Susan R. Kayar ◽  
Reto Straub ◽  
Ewald R. Weibel

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