Capillary–fiber geometrical relationships in tuna red muscle

1992 ◽  
Vol 70 (6) ◽  
pp. 1218-1229 ◽  
Author(s):  
Odile Mathieu-Costello ◽  
Peter J. Agey ◽  
Richard B. Logemann ◽  
Richard W. Brill ◽  
Peter W. Hochachka
Keyword(s):  
Fiber Surface ◽  
Fish Muscle ◽  
Volume Density ◽  
Capillary Length ◽  
Fiber Volume ◽  
Cross Sectional ◽  
Red Muscle ◽  
Rat Soleus Muscle ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density

The aim of this study was to examine the size and geometry of the capillary network in tuna red muscle, one of the most aerobic muscles in fish. Deep red muscle of 1.5- to 2-kg skipjack tuna, Katsuwonus pelamis, was perfusion fixed in situ, processed for electron microscopy, and analyzed by morphometry. Fiber cross-sectional area was 560 ± 30 (SE) μm2 in the samples. Capillary length per fiber volume was 4143 ± 242 (SE) mm−2 and mitochondrial volume density 28.5 ± 1.0 (SE) %. Indexes of capillarity such as average number of capillaries around a fiber, capillary length and surface per fiber volume, and capillary surface per fiber surface were high for a fish muscle. In fact, the size of the capillary–fiber interface (i.e., capillary to fiber surface) at a given mitochondrial volume per fiber was not significantly different in tuna red muscle compared with rat soleus muscle. However, calculation of mitochondrial respiratory rates in tuna red muscle yielded a substantially lower value (approximately 1/20th) compared with muscles of mammals. Besides the possible effect of differences in operating temperatures and (or) mitochondrial function(s) in fish compared with mammals, this suggests that the large capillary–fiber interface in tuna may be related to functions other than oxygen delivery per se, such as substrate and (or) heat transfer between capillaries and muscle fiber.

Fiber capillarization relative to mitochondrial volume in diaphragm of shrew

2002 ◽  
Vol 93 (1) ◽  
pp. 346-353 ◽  
Author(s):  
O. Mathieu-Costello ◽  
S. Morales ◽  
J. Savolainen ◽  
M. Vornanen
Keyword(s):  
Body Mass ◽  
Fiber Surface ◽  
Volume Density ◽  
Capillary Length ◽  
Fiber Volume ◽  
Hindlimb Muscle ◽  
Mitochondrial Volume ◽  
Flight Muscles ◽  
Mitochondrial Volume Density ◽  
Sorex Minutus

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.

Geometry of blood-tissue exchange in bat flight muscle compared with bat hindlimb and rat soleus muscle

1992 ◽  
Vol 262 (6) ◽  
pp. R955-R965 ◽  
Author(s):  
O. Mathieu-Costello ◽  
J. M. Szewczak ◽  
R. B. Logemann ◽  
P. J. Agey
Keyword(s):  
Soleus Muscle ◽  
Sarcomere Length ◽  
Flight Muscle ◽  
Fiber Surface ◽  
Capillary Length ◽  
Fiber Volume ◽  
Cross Sectional ◽  
Fiber Size ◽  
Rat Soleus Muscle ◽  
Mitochondrial Volume

We investigated the relationship between capillary-to-fiber geometry and muscle aerobic capacity by comparing the bat flight muscle (pectoralis muscle), i.e., an ultimate case of extreme O2 demand in a mammalian skeletal muscle, with bat hindlimb and rat soleus muscles. At a given sarcomere length (2.1 microns), fiber cross-sectional area was considerably smaller in bat muscles (pectoralis 318 +/- 10 microns 2, hindlimb 447 +/- 35 microns 2) than in rat soleus muscle (2,027 +/- 125 microns 2). Capillary number per fiber cross-sectional area was much greater in bat pectoralis (6,394 +/- 380/mm2) than in bat hindlimb and rat soleus muscle (2,865 +/- 238 and 1,301 +/- 129/mm2, respectively; all values normalized to 2.1-microns sarcomere length). At the same sarcomere length (2.1 microns), the degree of tortuosity and branching of capillaries were significantly greater in bat pectoralis than in bat hindlimb and rat soleus muscle. In bat flight muscle, capillary length per fiber volume was very high (9,025 +/- 342/mm2). It was 2.2- and 5.4-fold larger than in bat hindlimb and rat soleus, respectively. Mitochondria occupied 35.3 +/- 1.2, 16.5 +/- 1.3, and 6.1 +/- 0.9% of the muscle fiber volume in bat pectoralis, hindlimb, and rat soleus muscles, respectively. There was a strong correlation between capillary length (as well as capillary surface) per fiber volume and mitochondrial volume density in all muscles. Considering capillary supply and mitochondrial volume on an individual fiber basis, we found that 1) the number of capillaries around a fiber was linearly related to mitochondrial volume per micron length of fiber in the muscles but that 2) capillary surface per fiber surface, at given mitochondrial volume per micron length of fiber, was about twice as large in bat pectoralis as in rat soleus muscle, whereas in bat hindlimb it was intermediate between that in bat pectoralis and that in rat soleus muscle. This was due to the differences in fiber size (rat soleus greater than bat muscles) and capillary-to-fiber ratio (bat pectoralis greater than hindlimb) between the muscles. It is notable that in the bat, the substantially greater O2 transfer capacity of the flight muscle compared with hindlimb was achieved by increasing the size of the capillary-to-fiber interface, i.e., capillary-to-fiber surface, via an increase in capillary number rather than by substantially reducing fiber size.

Rat soleus muscle ultrastructure after hindlimb suspension

1990 ◽  
Vol 69 (2) ◽  
pp. 504-508 ◽  
Author(s):  
D. Desplanches ◽  
S. R. Kayar ◽  
B. Sempore ◽  
R. Flandrois ◽  
H. Hoppeler
Keyword(s):  
Soleus Muscle ◽  
Capillary Density ◽  
Volume Density ◽  
Hindlimb Suspension ◽  
Tail Suspension ◽  
Cross Sectional ◽  
Muscle Ultrastructure ◽  
Rat Soleus Muscle ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density

The aim of the present investigation was to determine, by quantitative electron microscopy, the effects of a 5-wk tail-suspension period on rat soleus muscle ultrastructure. A marked decline (-60%) in muscle mass occurred. The mean fiber cross-sectional area decreased to a greater extent (-75%) than the capillary-to-fiber ratio (-37%), leading to a higher capillary density (+148%) after hypokinesia. The total mitochondrial volume density remained unchanged, whereas the volume density of myofibrils was slightly but significantly reduced (-6%). A shift from subsarcolemmal to interfibrillar mitochondria occurred. Interfibrillar mitochondrial volume density was highest near the fiber border and decreased toward the fiber center. An increase in volume density of satellite cells suggested muscle regenerative events. Soleus atrophy with tail suspension greatly decreases the muscular volume but leaves the ultrastructural composition of muscle fibers relatively unaffected.

Greater capillary-fiber interface per fiber mitochondrial volume in skeletal muscles of old rats

2005 ◽  
Vol 99 (1) ◽  
pp. 281-289 ◽  
Author(s):  
O. Mathieu-Costello ◽  
Y. Ju ◽  
M. Trejo-Morales ◽  
L. Cui
Keyword(s):  
Fiber Type ◽  
Fiber Surface ◽  
Volume Ratio ◽  
Capillary Density ◽  
Volume Density ◽  
Capillary Length ◽  
Fiber Volume ◽  
Fiber Number ◽  
Mitochondrial Volume ◽  
Fiber Atrophy

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.

Fiber capillarization and ultrastructure of pigeon pectoralis muscle after cold acclimation

1998 ◽  
Vol 201 (23) ◽  
pp. 3211-3220 ◽  
Author(s):  
O. Mathieu-Costello ◽  
P. J. Agey ◽  
E. S. Quintana ◽  
K. Rousey ◽  
L. Wu ◽  
...  
Keyword(s):  
Cold Acclimation ◽  
Fiber Type ◽  
Pectoralis Major Muscle ◽  
Central Area ◽  
Volume Density ◽  
Pectoralis Muscle ◽  
Capillary Length ◽  
Fiber Volume ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density

We investigated the effect of 2 months of exposure to cold conditions(0-5 C) on capillarization and on fiber size, distribution and ultrastructure in the pectoralis muscle of nine pigeons (Columbia livia;mean body mass 700 31 g) and compared the results with measurements from four control birds (mean mass 715 42 g) kept at normal ambient temperature(22-23 C) for the same period. Superficial and deep portions of the muscles, taken from the central area of the right or left pectoralis major muscle, were perfusion-fixed in situ, processed for electron microscopy and analyzed by morphometry. Aerobic fibers represented the vast majority of fibers (93 1 %, mean s.e.m.) in all samples. After cold-acclimation, fiber sectional area was reduced and capillary density increased proportionally. There was no change in the degree of orientation (anisotropy) of capillaries, capillary-to-fiber ratio or fiber type distribution compared with controls. The volume density of mitochondria and lipid droplets in aerobic fibers and capillary diameter increased in response to cold, while the linear relationship between capillary length per fiber volume and fiber mitochondrial volume density remained unchanged. Capillary surface area,intrafiber lipid deposition and fiber mitochondrial volume density were all correlated in cold-acclimated pigeons. The results indicate a close match between the aerobic capacity of the highly aerobic fibers of the pectoralis muscle and their vascularization to meet the increased energetic demand of shivering.

Capillary-to-fiber surface ratio in rat fast-twitch hindlimb muscles after chronic electrical stimulation

1996 ◽  
Vol 80 (3) ◽  
pp. 904-909 ◽  
Author(s):  
O. Mathieu-Costello ◽  
P. J. Agey ◽  
L. Wu ◽  
J. Hang ◽  
T. H. Adair
Keyword(s):  
Electrical Stimulation ◽  
Fiber Surface ◽  
Volume Density ◽  
Capillary Length ◽  
Surface Area Ratio ◽  
Hindlimb Muscles ◽  
Chronic Electrical Stimulation ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density ◽  
Fast Twitch

We examined the relative plasticity of capillaries and fiber mitochondria in rat fast-twitch hindlimb muscles in response to chronic electrical stimulation. Specifically we addressed whether the size of the capillary-fiber interface increases in proportion to fiber mitochondrial volume, inasmuch as fiber aerobic capacity increases severalfold with chronic stimulation. Tibialis anterior and extensor digitorum longus muscles of six rats [367 +/- 17 (SD) g body wt] were stimulated (10 Hz, 8 h/day, 7 days/wk) for 28 consecutive days. Subsequently they were perfusion fixed in situ and stimulated, and contralateral control samples from the midbelly were processed for electron microscopy and morphometry. Capillary length density, capillary-to-fiber ratio, and fiber mitochondrial volume density increased two- to threefold in stimulated muscles, with no change in fiber or capillary diameter. Capillary-to-fiber surface area ratio per fiber unit mitochondrial volume was unchanged in stimulated muscles compared with contralateral controls, indicating a proportional increase in the size of the capillary-fiber interface and fiber mitochondrial volume in the muscles after chronic electrical stimulation.

scholarly journals Mitochondrial Fragmentation and Dysfunction in Type IIx/IIb Diaphragm Muscle Fibers in 24-Month Old Fischer 344 Rats

2021 ◽  
Vol 12 ◽  
Author(s):  
Alyssa D. Brown ◽  
Leah A. Davis ◽  
Matthew J. Fogarty ◽  
Gary C. Sieck
Keyword(s):  
Muscle Fibers ◽  
Volume Density ◽  
Diaphragm Muscle ◽  
Type I ◽  
Mitochondrial Fragmentation ◽  
Fiber Volume ◽  
Respiratory Capacity ◽  
Dehydrogenase Reaction ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density

Sarcopenia is characterized by muscle fiber atrophy and weakness, which may be associated with mitochondrial fragmentation and dysfunction. Mitochondrial remodeling and biogenesis in muscle fibers occurs in response to exercise and increased muscle activity. However, the adaptability mitochondria may decrease with age. The diaphragm muscle (DIAm) sustains breathing, via recruitment of fatigue-resistant type I and IIa fibers. More fatigable, type IIx/IIb DIAm fibers are infrequently recruited during airway protective and expulsive behaviors. DIAm sarcopenia is restricted to the atrophy of type IIx/IIb fibers, which impairs higher force airway protective and expulsive behaviors. The aerobic capacity to generate ATP within muscle fibers depends on the volume and intrinsic respiratory capacity of mitochondria. In the present study, mitochondria in type-identified DIAm fibers were labeled using MitoTracker Green and imaged in 3-D using confocal microscopy. Mitochondrial volume density was higher in type I and IIa DIAm fibers compared with type IIx/IIb fibers. Mitochondrial volume density did not change with age in type I and IIa fibers but was reduced in type IIx/IIb fibers in 24-month rats. Furthermore, mitochondria were more fragmented in type IIx/IIb compared with type I and IIa fibers, and worsened in 24-month rats. The maximum respiratory capacity of mitochondria in DIAm fibers was determined using a quantitative histochemical technique to measure the maximum velocity of the succinate dehydrogenase reaction (SDHmax). SDHmax per fiber volume was higher in type I and IIa DIAm fibers and did not change with age. In contrast, SDHmax per fiber volume decreased with age in type IIx/IIb DIAm fibers. There were two distinct clusters for SDHmax per fiber volume and mitochondrial volume density, one comprising type I and IIa fibers and the second comprising type IIx/IIb fibers. The separation of these clusters increased with aging. There was also a clear relation between SDHmax per mitochondrial volume and the extent of mitochondrial fragmentation. The results show that DIAm sarcopenia is restricted to type IIx/IIb DIAm fibers and related to reduced mitochondrial volume, mitochondrial fragmentation and reduced SDHmax per fiber volume.

Mitochondrial metabolism of cardiac and skeletal muscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish

1992 ◽  
Vol 70 (6) ◽  
pp. 1246-1253 ◽  
Author(s):  
Christopher D. Moyes ◽  
Odile A. Mathieu-Costello ◽  
Richard W. Brill ◽  
Peter W. Hochachka
Keyword(s):  
Specific Activity ◽  
Mitochondrial Protein ◽  
Volume Density ◽  
Tissue Mass ◽  
Oxidation Rates ◽  
Muscle Tissues ◽  
Red Muscle ◽  
Rate Of Oxygen Consumption ◽  
Mitochondrial Volume ◽  
Mitochondrial Volume Density

Tuna cardiac (atrium, compact and spongy ventricle) and skeletal muscle (red and white) were compared with carp tissues to determine the importance of mitochondrial differences in supporting the high aerobic capacities in tuna. Mitochondria isolated from red muscle of both species oxidized each of the physiological fuels at similar rates per milligram of mitochondrial protein, when differences in assay temperature are considered. The highest rate of oxygen consumption by ventricle mitochondria was 2 times greater in tuna than carp. The maximal oxidation rates were 3–4 times higher in ventricle than red muscle in both species. Tuna tissues had as much as 30–80% more mitochondrial protein per gram of tissue than carp. Morphometrically this was manifested as extremely densely packed mitochondrial cristae, rather than increased mitochondrial volume densities. In general, higher aerobic capacities of tuna ventricle and red muscle are primarily attributable to greater tissue mass and, to a lesser extent, differences in the nature or quantity of mitochondria per gram of tissue. Unlike ventricle and red muscle, tissues with relatively low mitochondrial contents in carp (white muscle, atrium) demonstrated several-fold higher mitochondrial contents in tuna. Enzyme analyses of tissue and isolated mitochondria suggest a greater dependence of tuna tissues on fatty acids as fuels. Activities of carnitine palmitoyl transferase (CPT) per milligram of protein were 2–2.5 times higher in tuna red muscle and ventricle mitochondria than in carp mitochondria from the same tissues. Whole tissue activity ratios of hexokinase/CPT, which indicate the relative importance of glucose and fatty acid metabolism, were 5 times higher in carp spongy ventricle and 12 times higher in carp compact ventricle. These data suggest that muscle aerobic capacity can be increased at several levels: tissue mass, mitochondrial volume density, cristae surface density, and mitochondrial specific activity. Large differences observed between carp and tuna muscles are due to cumulative effects of several of these factors.

Whole body and muscle respiratory capacity with dobutamine and hindlimb suspension

1991 ◽  
Vol 71 (6) ◽  
pp. 2419-2424 ◽  
Author(s):  
D. Desplanches ◽  
R. Favier ◽  
B. Sempore ◽  
H. Hoppeler
Keyword(s):  
Soleus Muscle ◽  
Metabolic Response ◽  
Volume Density ◽  
Hindlimb Suspension ◽  
Whole Body ◽  
Capillary Length ◽  
Muscle Weight ◽  
Cross Sectional ◽  
Beneficial Effects ◽  
Mitochondrial Volume

The effects of repeated injections of dobutamine, a synthetic catecholamine, were studied in control and tail-suspended rats to determine whether this drug could improve the metabolic response to unweighting. Dobutamine prevented the decrease in maximal oxygen uptake (VO2max) induced by hindlimb suspension. Furthermore, VO2max was 12% greater in dobutamine-treated animals than in saline-treated control animals. Soleus muscle weight and mean fiber cross-sectional area were decreased by 60 and 75%, respectively, in saline- and dobutamine-treated suspended rats. Total capillary length was unaffected by unweighting and increased 21% in all animals receiving dobutamine. The drug prevented the increase in total mitochondrial volume density (+30%) induced by unweighting but did not change total mitochondrial volume. Our results suggest that 1) dobutamine is useful to prevent the decrease of total aerobic capacity during hindlimb suspension, 2) dobutamine increases VO2max in control rats, and 3) total capillary length in soleus muscle is increased by the drug in all groups, although no beneficial effects on mitochondria can be detected.

Relationship between mitochondrial volume density and capillarity in hamster muscles

1987 ◽  
Vol 252 (1) ◽  
pp. H149-H155 ◽  
Author(s):  
S. M. Sullivan ◽  
R. N. Pittman
Keyword(s):  
Muscle Fiber ◽  
Volume Density ◽  
Contact Length ◽  
Cross Sectional ◽  
Fiber Contact ◽  
Fiber Size ◽  
Mitochondrial Volume ◽  
O2 Diffusion ◽  
Mitochondrial Volume Density ◽  
O2 Supply

Mitochondrial volume density and lipid droplet-volume density were stereologically determined from electron micrographs of muscle fibers from three hamster muscles: retractor, sartorius, and soleus. The number of capillaries around a fiber, length of capillary-fiber contact, and muscle fiber area were also measured. Glycolytic fibers of the retractor and sartorius had larger cross-sectional areas, lower mitochondrial-volume densities, fewer subsarcolemmal aggregates of mitochondria, and lower capillary-fiber contact length in comparison to oxidative fibers of the retractor and soleus. Values for mitochondrial volume density in the different muscles correlated well (r = 0.97) with resting O2 consumption. The mitochondrial volume densities for each muscle correlated well (r = 0.99) with O2 diffusion coefficients of these muscles. Our results indicate that an analysis of the adequacy of O2 supply to an individual muscle fiber must take into account an interplay among fiber size, percent of the muscle fiber perimeter in contact with a capillary (capillary-fiber contact), and O2 demand of the fiber estimated by mitochondrial volume density.

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