Can increases in capillarization explain the early adaptations in metabolic regulation in human muscle to short-term training?

2012 ◽  
Vol 90 (5) ◽  
pp. 557-566 ◽  
Author(s):  
Howard J. Green ◽  
Margaret Burnett ◽  
Helen Kollias ◽  
Jing Ouyang ◽  
Ian Smith ◽  
...  

To investigate the hypothesis that increases in fibre capillary density would precede increases in oxidative potential following training onset, tissue was extracted from the vastus lateralis prior to (0 days) and following 3 and 6 consecutive days of submaximal cycle exercise (2 h·day–1). Participants were untrained males (age = 21.4 ± 0.58 years; peak oxygen consumption = 46.2 ± 1.6 mL·kg–1·min–1; mean ± standard error (SE)). Tissue was assessed for succinic dehydrogenase activity (SDH) by microphotometry and indices of capillarization based on histochemically assessed area and capillary counts (CC) in specific fibre types. Three days of training (n = 13) resulted in a generalized decrease (p < 0.05) in fibre area (–14.2% ± 3.0%; mean ± SE) and increase (p < 0.05) in CC/Area (20.4% ± 2.7%) and no change in either CC or SDH activity. Following 6 days of treatment (n = 6), increases (p < 0.05) in CC (18.2% ± 4.2%), CC/Area (28.9% ± 3.2%), and SDH activity (22.9% ± 6.0%) occurred that was not specific to major fibre type. No changes in either fibre area or fibre-type distribution were observed with additional training. We conclude that increases in angiogenic-based capillary density and oxidative potential occur coincidentally following training onset, while increases in capillary density, mediated by reductions in fibre area, represent an initial isolated response, the significance of which may be linked to the metabolic alterations that also result.

2009 ◽  
Vol 297 (5) ◽  
pp. R1383-R1391 ◽  
Author(s):  
H. J. Green ◽  
E. Bombardier ◽  
M. E. Burnett ◽  
I. C. Smith ◽  
S. M. Tupling ◽  
...  

In this study, we investigated the hypothesis that the metabolic adaptations observed during steady-state exercise soon after the onset of training would be displayed during the nonsteady period of moderate exercise and would occur in the absence of increases in peak aerobic power (V̇o2peak) and in muscle oxidative potential. Nine untrained males [age = 20.8 ± 0.70 (SE) yr] performed a cycle task at 62% V̇o2peak before (Pre-T) and after (Post-T) training for 2 h/day for 5 days at task intensity. Tissue samples extracted from the vastus lateralis at 0 min (before exercise) and at 10, 60, and 180 s of exercise, indicated that at Pre-T, reductions ( P < 0.05) in phosphocreatine and increases ( P < 0.05) in creatine, inorganic phosphate, calculated free ADP, and free AMP occurred at 60 and 180 s but not at 10 s. At Post-T, the concentrations of all metabolites were blunted ( P < 0.05) at 60 s. Training also reduced ( P < 0.05) the increase in lactate and the lactate-to-pyruvate ratio observed during exercise at Pre-T. These adaptations occurred in the absence of change in V̇o2peak (47.8 ± 1.7 vs. 49.2 ± 1.7 ml·kg−1·min−1) and in the activities (mol·kg protein−1·h−1) of succinic dehydrogenase (3.48 ± 0.21 vs. 3.77 ± 0.35) and citrate synthase (7.48 ± 0.61 vs. 8.52 ± 0.65) but not cytochrome oxidase (70.8 ± 5.1 vs. 79.6 ± 6.6 U/g protein; P < 0.05). It is concluded that the tighter metabolic control observed following short-term training is initially expressed during the nonsteady state, probably as a result of increases in oxidative phosphorylation that is not dependent on changes in V̇o2peak while the role of oxidative potential remains uncertain.


1995 ◽  
Vol 78 (1) ◽  
pp. 138-145 ◽  
Author(s):  
H. J. Green ◽  
S. Jones ◽  
M. Ball-Burnett ◽  
B. Farrance ◽  
D. Ranney

In previous research we established using a short-term (5–7 days) training model that increases in muscle oxidative potential are not a prerequisite for the characteristic energy metabolic adaptations (lower lactate, glycogen depletion, and phosphocreatine hydrolysis) observed during prolonged exercise. To investigate whether increased muscle aerobic potential further potentiates the metabolic adaptive response, seven healthy male volunteers [maximal O2 uptake (VO2max) = 45.1 +/- 1.1 (SE) ml.kg-1.min-1] engaged in an 8-wk training program consisting of 2 h of cycle exercise at 62% of pretraining VO2max 5–6 times/wk. Analysis of tissue samples obtained from the vastus lateralis after 60 min of exercise revealed that by 4 wk of training muscle lactate concentration, phosphocreatine hydrolysis, and glycogen depletion were depressed (all P < 0.05). Further training for 4 wk had no additional effect (P < 0.05). The ratio of fructose 6-phosphate to fructose 1,6-phosphate, an index of phosphofructokinase activity, was not altered with training. Muscle oxidative potential as estimated from the maximal activity of succinic dehydrogenase increased by 31% by 4 wk of training (P <0.05) before plateauing during the final 4 wk of training. The increase in VO2max of 15.6% (P < 0.05) noted with training was also primarily expressed during the initial 4 wk. O2 uptake during submaximal exercise was unchanged. Because the metabolic response was similar in magnitude to that previously observed with short-term training, we conclude that, at least for the conditions of this study, the development of increased muscle aerobic potential is of minimal consequence on the magnitude of the energy metabolic adaptations examined.


1999 ◽  
Vol 276 (2) ◽  
pp. R591-R596 ◽  
Author(s):  
H. Green ◽  
C. Goreham ◽  
J. Ouyang ◽  
M. Ball-Burnett ◽  
D. Ranney

To examine the hypothesis that increases in fiber cross-sectional area mediated by high-resistance training (HRT) would result in a decrease in fiber capillarization and oxidative potential, regardless of fiber type, we studied six untrained males (maximum oxygen consumption, 45.6 ± 2.3 ml ⋅ kg−1 ⋅ min−1; mean ± SE) participating in a 12-wk program designed to produce a progressive hypertrophy of the quadriceps muscle. The training sessions, which were conducted 3 times/wk, consisted of three sets of three exercises, each performed for 6–8 repetitions maximum (RM). Measurements of fiber-type distribution obtained from tissue extracted from the vastus lateralis at 0, 4, 7, and 12 wk indicated reductions ( P < 0.05) in type IIB fibers (15.1 ± 2.1% vs. 7.2 ± 1.3%) by 4 wk in the absence of changes in the other fiber types (types I, IIA, and IIAB). Training culminated in a 17% increase ( P < 0.05) in cross-sectional area by 12 wk with initial increases observed at 4 wk. The increase was independent of fiber type-specific changes. The number of capillaries in contact with each fiber type increased by 12 wk, whereas capillary contacts-to-fiber area ratios remained unchanged. In a defined cross-sectional field, HRT also increased the capillaries per fiber at 12 wk. Training failed to alter cellular oxidative potential, as measured by succinic dehydrogenase (SDH) activity, regardless of fiber type and training duration. It is concluded that modest hypertrophy induced by HRT does not compromise cellular tissue capillarization and oxidative potential regardless of fiber type.


2012 ◽  
Vol 90 (5) ◽  
pp. 567-578 ◽  
Author(s):  
Howard J. Green ◽  
Aziz Batada ◽  
Bill Cole ◽  
Margaret E. Burnett ◽  
Helen Kollias ◽  
...  

In this study, we hypothesized that athletes involved in 5–6 months of sprint-type training would display higher levels of proteins and processes involved in muscle energy supply and utilization. Tissue was sampled from the vastus lateralis of 13 elite ice hockey players (peak oxygen consumption = 51.8 ± 1.3 mL·kg–1·min–1; mean ± standard error) at the end of a season (POST) and compared with samples from 8 controls (peak oxygen consumption = 45.5 ± 1.4 mL·kg–1·min–1) (CON). Compared with CON, higher activities were observed in POST (p < 0.05) only for succinic dehydrogenase (3.32 ± 0.16 mol·(mg protein)–1·min–1 vs. 4.10 ± 0.11 mol·(mg protein)–1·min–1) and hexokinase (0.73 ± 0.05 mol·(mg protein)–1·min–1 vs. 0.90 ± 0.05mol·(mg protein)–1·min–1) but not for phosphorylase, phosphofructokinase, and creatine phosphokinase. No differences were found in Na+,K+-ATPase concentration (βmax: 262 ± 36 pmol·(g wet weight)–1 vs. 275 ± 27 pmol·(g wet weight)–1) and the maximal activity of the sarcoplasmic reticulum Ca2+-ATPase (98.1 ± 6.1 µmol·(g protein)–1·min–1 vs. 102 ± 3.3 µmol·(g protein)–1·min–1). Cross-sectional area was lower (p < 0.05) in POST but only for the type IIA fibres (6312 ± 684 μm2 vs. 5512 ± 335 μm2), while the number of capillary counts per fibre and the capillary to fibre area ratio were generally higher (p < 0.05). These findings suggest that elite trained ice hockey players display elevations only in support of glucose-based aerobic metabolism that occur in the absence of alterations in excitation–contraction processes.


2020 ◽  
Vol 45 (4) ◽  
pp. 368-375 ◽  
Author(s):  
Joshua P. Nederveen ◽  
George Ibrahim ◽  
Stephen A. Fortino ◽  
Tim Snijders ◽  
Dinesh Kumbhare ◽  
...  

The percutaneous muscle biopsy procedure is an invaluable tool for characterizing skeletal muscle and capillarization. Little is known about methodological or biological variation stemming from the technique in heterogeneous muscle. Five muscle biopsies were taken from the vastus lateralis of a group of young men (n = 29, 22 ± 1 years) over a 96-h period. We investigated the repeatability of fibre distribution, indices of muscle capillarization and perfusion, and myofibre characteristics. No differences between the biopsies were reported in myofibre type distribution, cross-sectional area (CSA), and perimeter. Capillary-to-fibre perimeter exchange index and individual capillary-fibre contacts were unchanged with respect to the location of the muscle biopsy and index of capillarization. The variability in the sampling distribution of fibre type specific muscle CSA increased when fewer than 150 muscle fibres were quantified. Variability in fibre type distribution increased when fewer than 150 muscle fibres were quantified. Myofibre characteristics and indices of capillarization are largely consistent throughout the vastus lateralis when assessed via the skeletal muscle biopsy technique. Novelty Markers of muscle capillarization and perfusion were unchanged across multiple sites of the human vastus lateralis. Myofibre characteristics such as muscle cross-sectional area, perimeter, and fibre type distribution were also unchanged. Variation of muscle CSA was higher when fewer than 150 muscle fibres were quantified.


2009 ◽  
Vol 106 (4) ◽  
pp. 1181-1186 ◽  
Author(s):  
Jennifer L. Robbins ◽  
Brian D. Duscha ◽  
Daniel R. Bensimhon ◽  
Karlman Wasserman ◽  
James E. Hansen ◽  
...  

Although both capillary density and peak oxygen consumption (V̇o2) improve with exercise training, it is difficult to find a relationship between these two measures. It has been suggested that peak V̇o2 may be more related to central hemodynamics than to the oxidative potential of skeletal muscle, which may account for this observation. We hypothesized that change in a measure of submaximal performance, anaerobic threshold, might be related to change in skeletal muscle capillary density, a marker of oxidative potential in muscle, with training. Due to baseline differences among these variables, we also hypothesized that relationships might be sex specific. A group of 21 subjects completed an inactive control period, whereas 28 subjects (17 men and 11 women) participated in a 6-mo high-intensity exercise program. All subjects were sedentary, overweight, and dyslipidemic. Potential relationships were assessed between change in capillary density with both change in V̇o2 at peak and at anaerobic threshold with exercise training. All variables and relationships were assessed for sex-specific effects. Change in peak V̇o2 was not related to change in capillary density after exercise training in either sex. Men had a positive correlation between change in V̇o2 at anaerobic threshold and change in capillary density with exercise training ( r = 0.635; P < 0.01), whereas women had an inverse relationship ( r = −0.636; P < 0.05) between the change in these variables. These findings suggest that, although enhanced capillary density is associated with training-induced improvements in submaximal performance in men, this relationship is different in women.


2014 ◽  
Vol 92 (4) ◽  
pp. 315-323 ◽  
Author(s):  
Howard J. Green ◽  
Don Ranney ◽  
Margaret Burnett ◽  
Patti Galvin ◽  
Natasha Kyle ◽  
...  

To investigate fibre-type abnormalities in women with work-related myalgia (WRM), tissue samples were extracted from their trapezius (TRAP) and the extensor carpi radialis brevis (ECRB) muscles and compared with healthy controls (CON). For the ECRB samples (CON, n = 6; WRM, n = 11), no differences (P > 0.05) were found between groups for any of the properties examined, namely fibre-type (I, IIA, IIX, IIAX) distribution, cross-sectional fibre area, capillary counts (CC), capillary to fibre area ratio, and succinic dehydrogenase activity. For the TRAP samples (CON, n = 6; WRM, n = 8), the only difference (P < 0.05) observed between groups was for CC (CON > WRM), which was not statistically significant (P > 0.05) when age was used a covariant. A comparison of the properties of these 2 muscles in the CON group indicated a higher (P < 0.05) and lower (P < 0.05) percentage of type I and type IIA fibres, respectively, in the TRAP as well as higher (P < 0.05) CC, which was not specific to fibre type. These preliminary results suggest that the properties employed to characterize fibre types do not differentiate CON from WRM for either the TRAP or ECRB. As a consequence, the role of inherent fibre-type differences between these muscles in the pathogenesis of WRM remains uncertain.


1993 ◽  
Vol 71 (8) ◽  
pp. 615-618 ◽  
Author(s):  
E. R. Chin ◽  
H. J. Green

To investigate the relationship among fibre type, oxidative potential, and Na+–K+ ATPase concentration in skeletal muscle, adult male Wistar rats weighing 259 ± 8 g [Formula: see text] were sacrificed and the soleus (SOL), extensor digitoram longus (EDL), red vastus lateralis (RV), and white vastus lateralis (WV) removed. These muscles were chosen as being representative of the two major fibre type populations: slow twitch (SOL) and fast twitch (EDL, RV, WV) and exhibiting either a high (SOL, EDL, RV) or low (WV) oxidative potential. Na+–K+ ATPase concentration (pmol∙g−1 wet weight), measured by the [3H]ouabain binding technique, differed (p < 0.01) only between the WV (238 ± 7.9) and the SOL (359 ± 9.6), EDL (365 ± 10), and RV (403 ± 12). Similarly, muscle oxidative potential as measured by the maximal activity of citrate synthase was different (p < 0.01) only between the WV and the other three muscles. Citrate synthase activity (μmol∙min−1∙g−1 wet weight) was 4.0 ± 0.7, 12.3 ± 0.9, 9.1 ± 0.7, and 11.3 ± 1.0 in the WV, SOL, EDL, and RV, respectively. These results indicate that Na+–K+ ATPase concentration is not related to the speed of contraction but to the oxidative potential of the muscle. Since chronic activity is a primary determinant of oxidative potential, it would be expected that increases in Na+–K+ ATPase would accompany increases in muscle utilization.Key words: Na+–K+ ATPase, citrate synthase, type I and type II fibres.


1995 ◽  
Vol 73 (4) ◽  
pp. 474-482 ◽  
Author(s):  
H. J. Green ◽  
M. Ball-Burnett ◽  
G. Jamieson ◽  
J. Cadefau ◽  
R. Cussó

In previous studies we have been able to demonstrate tighter metabolic control of muscle metabolism during prolonged steady-state exercise 5 to 6 days after the initiation of training and well before changes in oxidative potential. To examine whether the metabolic adaptations are manifested during the non-steady-state adjustment to submaximal exercise, 11 male subjects ([Formula: see text] peak, 45 ± 2.4 mL∙kg−1∙min−1, [Formula: see text]) performed 98 min of cycle exercise at 67% of [Formula: see text] peak prior to and following 3 to 4 days of training for 2 h per day. Analysis of lactate concentration (mmol/kg dry weight) in samples rapidly extracted from vastus lateralis indicated reductions (p < 0.05) of 44% at 3 min (42.1 ± 7.1 vs. 23.6 ± 7.7), 29% at 15 min (35.4 ± 6.4 vs. 25.0 ± 6.0), and 32% at 98 min (22.9 ± 6.9 vs. 15.6 ± 3.2) with training. Training also resulted in higher phosphocreatine and lower creatine and Pi values that were not specific to any exercise time point. In addition, [Formula: see text] was not altered either during the non-steady state or during the steady-state phases of exercise. These results suggest that at least part of the tightening of the metabolic control and the apparent reduction in glycogenolysis and glycolysis in response to short-term training occurs during the adjustment phase to steady-state exercise.Key words: training, metabolic control, nonsteady state.


2000 ◽  
Vol 88 (2) ◽  
pp. 634-640 ◽  
Author(s):  
Howard Green ◽  
Brian Roy ◽  
Susan Grant ◽  
Margaret Burnett ◽  
Russ Tupling ◽  
...  

To investigate the hypothesis that acclimatization to altitude would result in a downregulation in muscle Na+-K+-ATPase pump concentration, tissue samples were obtained from the vastus lateralis muscle of six volunteers (5 males and 1 female), ranging in age from 24 to 35 yr, both before and within 3 days after a 21-day expedition to the summit of Mount Denali, Alaska (6,194 m). Na+-K+-ATPase, measured by the [3H]ouabain-binding technique, decreased by 13.8% [348 ± 12 vs. 300 ± 7.6 (SE) pmol/g wet wt; P< 0.05]. No changes were found in the maximal activities (mol ⋅ kg protein− 1 ⋅ h− 1) of the mitochondrial enzymes, succinic dehydrogenase (3.63 ± 0.20 vs. 3.25 ± 0.23), citrate synthase (4.76 ± 0.44 vs. 4.94 ± 0.44), and malate dehydrogenase (12.6 ± 1.8 vs. 12.7 ± 1.2). Similarly, the expedition had no effect on any of the histochemical properties examined, namely fiber-type distribution (types I, IIA, IIB, IC, IIC, IIAB), area, capillarization, and succinic dehydrogenase activity. Peak aerobic power (52.3 ± 2.1 vs. 50.6 ± 1.9 ml ⋅ kg− 1 ⋅ min− 1) and body mass (76.9 ± 3.7 vs. 75.5 ± 2.9 kg) were also unaffected. We concluded that acclimatization to altitude results in a downregulation in muscle Na+-K+-ATPase pump concentration, which occurs without changes in oxidative potential and other fiber-type histochemical properties.


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