scholarly journals Differential regulation of the fiber type-specific gene expression of the sarcoplasmic reticulum calcium-ATPase isoforms induced by exercise training

2014 ◽  
Vol 117 (5) ◽  
pp. 544-555 ◽  
Author(s):  
Marc P. Morissette ◽  
Shanel E. Susser ◽  
Andrew N. Stammers ◽  
Kimberley A. O'Hara ◽  
Phillip F. Gardiner ◽  
...  

The regulatory role of adenosine monophosphate-activated protein kinase (AMPK)-α2 on sarcoplasmic reticulum calcium-ATPase (SERCA) 1a and SERCA2a in different skeletal muscle fiber types has yet to be elucidated. Sedentary (Sed) or exercise-trained (Ex) wild-type (WT) and AMPKα2-kinase dead (KD) transgenic mice, which overexpress a mutated and inactivated AMPKα2 subunit, were utilized to characterize how genotype or exercise training influenced the regulation of SERCA isoforms in gastrocnemius. As expected, both Sed and Ex KD mice had >40% lower AMPK phosphorylation and 30% lower SERCA1a protein than WT mice ( P < 0.05). In contrast, SERCA2a protein was not different among KD and WT mice. Exercise increased SERCA1a and SERCA2a protein content among WT and KD mice, compared with their Sed counterparts. Maximal SERCA activity was lower in KD mice, compared with WT. Total phospholamban protein was higher in KD mice than in WT and lower in Ex compared with Sed mice. Exercise training increased phospholamban Ser16 phosphorylation in WT mice. Laser capture microdissection and quantitative PCR indicated that SERCA1a mRNA expression among type I fibers was not altered by genotype or exercise, but SERCA2a mRNA was increased 30-fold in WT+Ex, compared with WT+Sed. In contrast, the exercise-stimulated increase for SERCA2a mRNA was blunted in KD mice. Exercise upregulated SERCA1a and SERCA2a mRNA among type II fibers, but was not altered by genotype. Collectively, these data suggest that exercise differentially influences SERCA isoform expression in type I and type II fibers. Additionally, AMPKα2 influences the regulation of SERCA2a mRNA in type I skeletal muscle fibers following exercise training.

2016 ◽  
Vol 121 (2) ◽  
pp. 483-492 ◽  
Author(s):  
C. R. Lamboley ◽  
V. L. Wyckelsma ◽  
B. D. Perry ◽  
M. J. McKenna ◽  
G. D. Lamb

Inactivity negatively impacts on skeletal muscle function mainly through muscle atrophy. However, recent evidence suggests that the quality of individual muscle fibers is also altered. This study examined the effects of 23 days of unilateral lower limb suspension (ULLS) on specific force and sarcoplasmic reticulum (SR) Ca2+ content in individual skinned muscle fibers. Muscle biopsies of the vastus lateralis were taken from six young healthy adults prior to and following ULLS. After disuse, the endogenous SR Ca2+ content was ∼8% lower in type I fibers and maximal SR Ca2+ capacity was lower in both type I and type II fibers (−11 and −5%, respectively). The specific force, measured in single skinned fibers from three subjects, decreased significantly after ULLS in type II fibers (−23%) but not in type I fibers (−9%). Western blot analyses showed no significant change in the amounts of myosin heavy chain (MHC) I and MHC IIa following the disuse, whereas the amounts of sarco(endo)plasmic reticulum Ca2+-ATPase 1 (SERCA1) and calsequestrin increased by ∼120 and ∼20%, respectively, and the amount of troponin I decreased by ∼21%. These findings suggest that the decline in force and power occurring with muscle disuse is likely to be exacerbated in part by reductions in maximum specific force in type II fibers, and in the amount of releasable SR Ca2+ in both fiber types, the latter not being attributable to a reduced calsequestrin level. Furthermore, the ∼3-wk disuse in human elicits change in SR properties, in particular a more than twofold upregulation in SERCA1 density, before any fiber-type shift.


1989 ◽  
Vol 257 (5) ◽  
pp. E736-E742 ◽  
Author(s):  
W. H. Martin ◽  
A. R. Coggan ◽  
R. J. Spina ◽  
J. E. Saffitz

The density and distribution of beta-adrenergic receptors in type I and II fibers of human gastrocnemius and quadriceps muscles were characterized in ten healthy sedentary subjects and in a subgroup of six subjects before and after 12 wk of endurance exercise training. Total tissue content of beta-receptors was measured in frozen sections of skeletal muscle biopsies incubated with 125I-labeled cyanopindolol in the presence and absence of 10(-5) M L-propranolol. The relative beta-receptor densities of type I and II fibers were delineated autoradiographically. Muscle fiber types were identified in adjacent serial sections by histochemical staining of myofibrillar adenosine-triphosphatase (ATPase) activity. Type I fibers had a threefold greater beta-receptor density than type II fibers of the same muscle [P less than 0.001; type I-to-type II fiber ratio of beta-receptor density was 3.06 +/- 0.43 (SD)]. Exercise training elicited a change in muscle fiber subtype composition (+34% type IIa and -42% type IIb; P less than 0.05 and P = 0.066, respectively), a 40% increase in citrate synthase activity of skeletal muscle (P = 0.01), and a 23% rise in peak oxygen uptake (P less than 0.001). However, no change in total tissue content of beta-receptors was observed after exercise training, even when receptor density was adjusted for preconditioning fiber type composition. Thus beta-receptor density of type I fibers of human skeletal muscle is threefold greater than that of type II fibers. Enhanced capacity for aerobic metabolism after endurance exercise training is not associated with upregulation of total beta-receptor density.


2015 ◽  
Vol 593 (11) ◽  
pp. 2499-2514 ◽  
Author(s):  
C. R. Lamboley ◽  
V. L. Wyckelsma ◽  
T. L. Dutka ◽  
M. J. McKenna ◽  
R. M. Murphy ◽  
...  

1989 ◽  
Vol 66 (1) ◽  
pp. 465-475 ◽  
Author(s):  
R. H. Fitts ◽  
D. L. Costill ◽  
P. R. Gardetto

This study examined the effect of a typical collegiate swim-training program and an intensified 10-day training period on the peak tension (Po), negative log molar Ca2+ concentration (pCa)-force, and maximal shortening speed (Vmax) of the slow-twitch type I and fast-twitch type II fibers of the deltoid muscle. Over a 10-wk period, the swimmers averaged 4,266 +/- 264 m/day swimming intermittent bouts of front crawl, kicking, or pulling. The training program induced an almost twofold increase in the mitochondrial marker enzyme citrate synthase. Po of the single fibers was not altered by either the training or 10-day intensive training programs, and no significant differences were observed in the Po (kg/cm2) of type I compared with the type II fibers. The type II fiber diameters were significantly larger than the type I fibers (94 +/- 4 vs. 80 +/- 2 microns), and although fiber diameters were unaffected by the training, the 10-day intensive training significantly reduced the type II fiber diameter. The type I fibers from the trained swimmers showed pCa-force curves shifted to the right such that higher free Ca2+ levels were required to elicit a given percent of Po (for values less than 0.5 Po). The activation threshold (pCa) for the onset of tension and the pCa required to elicit one-half maximal tension were not altered by the training in either fiber type. Fiber Vmax (measured by the slack test) was fivefold higher in type II compared with type I fibers (4.85 +/- 0.50 vs. 0.86 +/- 0.04 fiber lengths/s). The exercise-training program significantly increased and decreased the Vmax of the slow and fast fibers, respectively. The 10 days of intensified training produced a further significant decrease in the Vmax of the type II fibers. After a period of detraining, the Vmax of both fiber types returned to the control level. The force-velocity relation was not significantly altered in either fiber type by the swim training; however, the intensified training significantly depressed the velocity of the type II fiber at all loads studied. The Vmax changes with exercise training are likely explained by an exercise-induced expression of fast myosin in slow fibers and slow myosin in fast fibers.


2009 ◽  
Vol 107 (4) ◽  
pp. 1138-1143 ◽  
Author(s):  
Martijn A. Bekedam ◽  
Brechje J. van Beek-Harmsen ◽  
Willem van Mechelen ◽  
Anco Boonstra ◽  
Willem J. van der Laarse

The purpose of this study was to determine the myoglobin concentration in skeletal muscle fibers of chronic heart failure (CHF) patients and to calculate the effect of myoglobin on oxygen buffering and facilitated diffusion. Myoglobin concentration, succinate dehydrogenase (SDH) activity, and cross-sectional area of individual muscle fibers from the vastus lateralis of five control and nine CHF patients were determined using calibrated histochemistry. CHF patients compared with control subjects were similar with respect to myoglobin concentration: type I fibers 0.69 ± 0.11 mM (mean ± SD), type II fibers 0.52 ± 0.07 mM in CHF vs. type I fibers 0.70 ± 0.09 mM, type II fibers 0.49 ± 0.07 mM in control, whereas SDH activity was significantly lower in CHF in both fiber types ( P < 0.01). The myoglobin concentration in type I fibers was higher than in type II fibers ( P < 0.01). Consequently, the oxygen buffering capacity, calculated from myoglobin concentration/SDH activity was increased in CHF: type I fibers 11.4 ± 2.1 s, type II fibers 13.6 ± 3.9 s in CHF vs. type I fibers 7.8 ± 0.9 s, type II fibers 7.5 ± 1.0 s in control, all P < 0.01). The calculated extracellular oxygen tension required to prevent core anoxia (Po2crit) in muscle fibers was similar when controls were compared with patients in type I fibers 10.3 ± 0.9 Torr in CHF and 11.5 ± 3.3 Torr in control, but was lower in type II fibers of patients 6.1 ± 2.8 Torr in CHF and 14.7 ± 6.2 Torr in control, P < 0.01. The lower Po2crit of type II fibers may facilitate oxygen extraction from capillaries. Reduced exercise tolerance in CHF is not due to myoglobin deficiency.


2014 ◽  
Vol 117 (7) ◽  
pp. 797-805 ◽  
Author(s):  
T. L. Dutka ◽  
C. R. Lamboley ◽  
R. M. Murphy ◽  
G. D. Lamb

Taurine occurs in high concentrations in muscle and is implicated in numerous physiological processes, yet its effects on many aspects of contractility remain unclear. Using mechanically skinned segments of human vastus lateralis muscle fibers, we characterized the effects of taurine on sarcoplasmic reticulum (SR) Ca2+ accumulation and contractile apparatus properties in type I and type II fibers. Prolonged myoplasmic exposure (>10 min) to taurine substantially increased the rate of accumulation of Ca2+ by the SR in both fiber types, with no change in the maximum amount accumulated; no such effect was found with carnosine. SR Ca2+ accumulation was similar with 10 or 20 mM taurine, but was significantly slower at 5 mM taurine. Cytoplasmic taurine (20 mM) had no detectable effects on the responsiveness of the Ca2+ release channels in either fiber type. Taurine caused a small increase in Ca2+ sensitivity of the contractile apparatus in type I fibers, but type II fibers were unaffected; maximum Ca2+-activated force was unchanged in both cases. The effects of taurine on SR Ca2+ accumulation 1) only became apparent after prolonged cytoplasmic exposure, and 2) persisted for some minutes after complete removal of taurine from the cytoplasm, consistent with the hypothesis that the effects were due to an action of taurine from inside the SR. In summary, taurine potentiates the rate of SR Ca2+ uptake in both type I and type II human fibers, possibly via an action from within the SR lumen, with the degree of potentiation being significantly reduced at low physiological taurine levels.


2020 ◽  
Vol 128 (4) ◽  
pp. 795-804 ◽  
Author(s):  
Tatiana Moro ◽  
Camille R. Brightwell ◽  
Elena Volpi ◽  
Blake B. Rasmussen ◽  
Christopher S. Fry

Aging induces physiological decline in human skeletal muscle function and morphology, including type II fiber atrophy and an increase in type I fiber frequency. Resistance exercise training (RET) is an effective strategy to overcome muscle mass loss and improve strength, with a stronger effect on type II fibers. In the present study, we sought to determine the effect of a 12-wk progressive RET program on the fiber type-specific skeletal muscle hypertrophic response in older adults. Nineteen subjects [10 men and 9 women (71.1 ± 4.3 yr)] were studied before and after the 12-wk program. Immunohistochemical analysis was used to quantify myosin heavy chain (MyHC) isoform expression, cross-sectional area (CSA), satellite cell abundance, myonuclear content, and lipid droplet density. RET induced an increase in MyHC type II fiber frequency and a concomitant decrease in MyHC type I fiber frequency. Mean CSA increased significantly only in MyHC type II fibers (+23.3%, P < 0.05), but myonuclear content increased only in MyHC type I fibers ( P < 0.05), with no change in MyHC type II fibers. Satellite cell content increased ~40% in both fiber types ( P > 0.05). RET induced adaptations to the capillary supply to satellite cells, with the distance between satellite cells and the nearest capillary increasing in type I fibers and decreasing in type II fibers. Both fiber types showed similar decrements in intramuscular lipid density with training ( P < 0.05). Our data provide intriguing evidence for a fiber type-specific response to RET in older adults and suggest flexibility in the myonuclear domain of type II fibers during a hypertrophic stimulus. NEW & NOTEWORTHY In older adults, progressive resistance exercise training (RET) increased skeletal muscle fiber volume and cross-sectional area independently of myonuclear accretion, leading to an expansion of the myonuclear domain. Fiber type-specific analyses illuminated differential adaptation; type II fibers underwent hypertrophy and exhibited myonuclear domain plasticity, whereas myonuclear accretion occurred in type I fibers in the absence of a robust hypertrophic response. RET also augmented satellite cell-capillary interaction and reduced intramyocellular lipid density to improve muscle quality.


1988 ◽  
Vol 25 (1) ◽  
pp. 77-82 ◽  
Author(s):  
K. G. Braund ◽  
K. A. Amling

Skeletal muscle samples from two healthy dogs were stored in ice at 0 C for up to 30 hours to examine the influence of time on cell morphology and morphometry. Cytochemical and histochemical properties of muscle to 18 hours were not markedly different from fresh frozen tissue. Samples stored to 30 hours were still satisfactory, despite a decline and unevenness in depth of staining. Morphometry from samples stored at 0 C for 6 hours or longer is not recommended, due to the statistically significant increase in diameter (from 21 to 25%) of type I and type II fibers.


1996 ◽  
Vol 270 (1) ◽  
pp. H115-H120 ◽  
Author(s):  
H. N. Sabbah ◽  
H. Shimoyama ◽  
V. G. Sharov ◽  
T. Kono ◽  
R. C. Gupta ◽  
...  

The proportion of slow-twitch, fatigue-resistant type 1 skeletal muscle (SM) fibers is often reduced in heart failure (HF), while the proportion of fatigue-sensitive type-II fibers increases. This maladaptation may be partially responsible for the exercise intolerance that characterize HF. In this study, we examined the effects of early monotherapy with the angiotensin-converting enzyme inhibor, enalapril, and the beta-blocker, metoprolol, on SM fiber type composition in 18 dogs with moderate HF produced by intracoronary microembolizations. HF dogs were randomized to 3 mo therapy with enalapril (10 mg twice daily), metoprolol (25 mg twice daily), or no treatment. Triceps muscle biopsies were obtained at baseline, before randomization, and at the end of 30 mo of therapy. Type I and type II SM fibers were differentiated by myofibrillar adenosinetriphosphatase (pH 9.4). In untreated dogs, the proportion of type I fibers was 27 +/- 1% before randomization and decreased to 23 +/- 1% (P < 0.05) at the end of 3 mo of follow up. In dogs treated with enalapril or metoprolol, the proportion of type I fibers was 30 +/- 4 and 28 +/- 2% before randomization and 33 +/- 4 and 33 +/- 1%, respectively, after 3 mo of therapy. In conclusion, in dogs with moderate HF, early therapy with enalapril or metoprolol prevents the progressive decline in the proportion of type I SM fibers.


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