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

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.

1992 ◽  
Vol 70 (6) ◽  
pp. 1218-1229 ◽  
Author(s):  
Odile Mathieu-Costello ◽  
Peter J. Agey ◽  
Richard B. Logemann ◽  
Richard W. Brill ◽  
Peter W. Hochachka

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.


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.


1998 ◽  
Vol 201 (23) ◽  
pp. 3211-3220 ◽  
Author(s):  
O. Mathieu-Costello ◽  
P. J. Agey ◽  
E. S. Quintana ◽  
K. Rousey ◽  
L. Wu ◽  
...  

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.


1996 ◽  
Vol 80 (3) ◽  
pp. 904-909 ◽  
Author(s):  
O. Mathieu-Costello ◽  
P. J. Agey ◽  
L. Wu ◽  
J. Hang ◽  
T. H. Adair

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.


2021 ◽  
Vol 12 ◽  
Author(s):  
Alyssa D. Brown ◽  
Leah A. Davis ◽  
Matthew J. Fogarty ◽  
Gary C. Sieck

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.


1992 ◽  
Vol 262 (6) ◽  
pp. R955-R965 ◽  
Author(s):  
O. Mathieu-Costello ◽  
J. M. Szewczak ◽  
R. B. Logemann ◽  
P. J. Agey

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.


1996 ◽  
Vol 81 (1) ◽  
pp. 419-425 ◽  
Author(s):  
B. Kayser ◽  
H. Hoppeler ◽  
D. Desplanches ◽  
C. Marconi ◽  
B. Broers ◽  
...  

Muscle ultrastructure and biochemistry in vastus lateralis muscle biopsies and the response to exercise of 8 lowland Tibetans (T) were compared with those of 8 Nepalese lowlanders (N). Blood hemoglobin was lower in T than in N (119 +/- 3 vs. 131 +/- 2 g/l; P < 0.05). Peak O2 consumption per kilogram of body mass was similar [37.9 +/- 2.2 (T) vs. 40.1 +/- 1.36 ml.min-1.kg body mass-1 (N)]. Maximum exercise blood lactate was the same [11.4 (T) +/- 0.5 vs. 11.3 +/- 0.6 mM (N)]. Muscle fiber type distribution was similar [type I, 58.6 +/- 3.4 (N) vs. 57.0 +/- 3.4% (T); type IIa, 24.1 +/- 3.5 vs. 27.1 +/- 1.6%; type IIb, 17.4 +/- 1.4 vs. 15.9 +/- 2.9%]. T had smaller fiber cross-sectional areas [3,413 +/- 677 (T) vs. 3,895 +/- 447 microns 2 (N); P < 0.05] but had similar number of capillaries per muscle fiber [1.35 +/- 0.23 (T) vs. 1.46 +/- 0.08 (N)] and muscle fiber area supplied per capillary [399 +/- 29 (T) vs. 382 +/- 65 mm2 (N)]. Total mitochondrial volume density was much lower in T (3.99 +/- 0.17%) than in N (5.51 +/- 0.19%) (P < 0.025). Mirroring mitochondrial volume density, citrate synthase and 3-hydroxyacyl-CoA dehydrogenase activities were lower in T than in N (P < 0.05). The activities of L-lactate dehydrogenase and hexokinase were the same in both groups. T had significantly less muscle fiber lipid droplets than did N, which correlated with the low activity of 3-hydroxyacyl-CoA dehydrogenase (r = 0.57, P = 0.02). In conclusion, lowland-born T have a low mitochondrial volume-to-specific peak O2 consumption ratio, which, based on previous measurements on altitude-born Sherpas (B. Kayser, H. Hoppeler, H. Claassen and P. Cerretelli. J. Appl. Physiol. 70: 1938-1942, 1991), appears to be an inborn feature.


2020 ◽  
Vol 98 (Supplement_4) ◽  
pp. 120-121
Author(s):  
Chloey P Guy ◽  
Catherine L Wellman ◽  
David G Riley ◽  
Charles R Long ◽  
Ron D Randel ◽  
...  

Abstract We previously determined that prenatal stress (PNS) differentially affected methylation of DNA from leukocytes of 28-d-old calves. Specifically, COX14 (cytochrome c oxidase (COX) assembly factor) and CKMT1B (mitochondrial creatine kinase U-type) were hypomethylated and COA5 (COX assembly factor 5), COX5A (COX subunit 5A), NRF1 (nuclear respiratory factor 1), and GSST1 (glutathione S-transferase theta-1) were hypermethylated in PNS compared to non-PNS calves (P ≤ 0.05). Our current objective was to test the hypothesis that PNS exhibit impaired mitochondrial function and greater oxidative stress than non-PNS calves. Blood and longissimus dorsi muscle samples were collected from yearling Brahman calves whose mothers were stressed by 2 h transportation at 60, 80, 100, 120, and 140 days of gestation (PNS; 8 bulls, 6 heifers) and non-PNS calves (4 bulls, 6 heifers). Serum was evaluated for the stress hormone, cortisol, and muscle damage marker, creatine kinase; muscle was analyzed for mitochondrial volume density and function by citrate synthase (CS) and COX activities, respectively, concentration of malondialdehyde, a lipid peroxidation marker, and activity of the antioxidant, superoxide dismutase (SOD). Data were analyzed using mixed linear models with treatment and sex as fixed effects. Serum cortisol was numerically higher in PNS than non-PNS calves but was not statistically different. Muscle CS and COX activities relative to protein were greater in PNS than non-PNS calves (P ≤ 0.03), but COX relative to CS activity was similar between groups. Activity of COX was greater in bulls than heifers (P = 0.03), but no other measure was affected by sex. All other measures were unaffected by PNS. Prenatal stress did not affect markers of muscle damage and oxidative stress in yearling Brahman calves at rest but mitochondrial volume density and function were greater in PNS calves. Acute stressors induce oxidative stress, so implications of differences in mitochondria in PNS calves following a stressor should be investigated.


2021 ◽  
Vol 99 (Supplement_3) ◽  
pp. 127-127
Author(s):  
Chloey P Guy ◽  
Lauren T Wesolowski ◽  
Audrey L Earnhardt ◽  
Dustin Law ◽  
Don A Neuendorff ◽  
...  

Abstract Temperament impacts skeletal muscle mitochondria in Brahman heifers, but this has not been investigated in steers or between cattle breeds. We hypothesized mitochondrial measures would be greater in Angus than Brahman, temperamental than calm steers, and the trapezius (TRAP) than the longissimus thoracis (LT) muscle. Samples from calm (n = 13 per breed), intermediate (n = 12 per breed), and temperamental (n=13 per breed) Angus and Brahman steers (mean±SD 10.0±0.8 mo) were evaluated for mitochondrial enzyme activities via colorimetry. Calm and temperamental LT samples were evaluated for oxidative phosphorylation (P) and electron transfer (E) capacities by high-resolution respirometry. Data were analyzed using linear models with fixed effects of breed, muscle, temperament, and all interactions. Brahman tended to have greater mitochondrial volume density (citrate synthase activity; CS) than Angus (P = 0.08), while intrinsic (relative to CS) mitochondrial function (cytochrome c oxidase activity) was greater in Angus than Brahman (P = 0.001) and greater in TRAP than LT (P = 0.008). Angus exhibited greater integrative (per mg tissue) and intrinsic P with complex I (PCI), P with complexes I+II (PCI+II), maximum noncoupled E, and E with complex II (ECII; P ≤ 0.04) and tended to have greater intrinsic leak (P = 0.1) than Brahman. Contribution of PCI to total E was greater in Angus than Brahman (P = 0.01), while contribution of ECII to total E was greater in Brahman than Angus (P = 0.05). A trend for the interaction of breed and temperament (P = 0.07) indicated calm Angus had the greatest intrinsic ECII (P ≤ 0.03) while intrinsic ECII was similar between temperamental Angus and calm and temperamental Brahman. Integrative PCI+II and ECII, and the contribution of PCI and PCI+II to overall E tended to be greater in temperamental than calm steers (P ≤ 0.09), while intrinsic ECII tended to be greater in calm than temperamental steers (P = 0.07). The impact of these mitochondrial differences on meat quality measures remains to be determined.


2017 ◽  
Vol 222 (1) ◽  
pp. e12905 ◽  
Author(s):  
A.-K. Meinild Lundby ◽  
R. A. Jacobs ◽  
S. Gehrig ◽  
J. de Leur ◽  
M. Hauser ◽  
...  

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