Transverse tubular system depolarization reduces tetanic force in rat skeletal muscle fibers by impairing action potential repriming

2007 ◽  
Vol 292 (6) ◽  
pp. C2112-C2121 ◽  
Author(s):  
T. L. Dutka ◽  
G. D. Lamb

When muscle fibers are repeatedly stimulated, they may become depolarized and force output decline. Excitation of the transverse tubular system (T-system) is critical for activation, but its role in muscle fatigue is poorly understood. Here, mechanically skinned fibers from rat fast-twitch muscle were used, because the sarcolemma is absent but the T-system retains normal excitability and its properties can be studied in isolation. The T-system membrane was fully polarized by bathing the skinned fiber in an internal solution with 126 mM K+ (control solution) or set at partially depolarized levels (approximately −63 and −58 mV) in solutions with 66 or 55 mM K+, respectively, and action potentials (APs) were triggered in the sealed T-system by field stimulation. Prolonged depolarization of the T-system reduced tetanic force proportionately more than twitch force, with greater effect at higher stimulation frequency (responses at 20 and 100 Hz reduced to 71 and 62% in 66 mM K+ and to 54 and 35% in 55 mM K+, respectively). Double-pulse stimulation showed that depolarization increased the repriming period (estimated minimum time before a second AP can be produced) from ∼4 ms to ∼7.5 and 15 ms in the 66 and 55 mM K+ solutions, respectively. These results demonstrate that T-system depolarization reduces tetanic force by impairing AP repriming, rather than by preventing AP generation per se or by inactivating the T-system voltage sensors. The findings also explain why it is advantageous to reduce the rate of motoneuron stimulation to muscles during repeated or prolonged periods of activity.

1965 ◽  
Vol 26 (2) ◽  
pp. 467-476 ◽  
Author(s):  
Arthur Hess

Twitch and slow muscle fibers, identified morphologically in the garter snake, have been examined in the electron microscope. The transverse tubular system and the sarcoplasmic reticulum are separate entities distinct from each other. In twitch fibers, the tubular system and the dilated sacs of the sarcoplasmic reticulum form triads at the level of junction of A and I bands. In the slow fibers, the sarcoplasmic reticulum is severely depleted in amount and the transverse tubular system is completely absent. The junctional folds of the postsynaptic membrane of the muscle fiber under an "en grappe" ending of a slow fiber are not so frequent or regular in occurrence or so wide or so long as under the "en plaque" ending of a twitch fiber. Some physiological implications of these differences in fine structure of twitch and slow fibers are discussed. The absence of the transverse tubular system and reduction in amount of sarcoplasmic reticulum, along with the consequent disposition of the fibrils, the occurrence of multiple nerve terminals, and the degree of complexity of the post junctional folds of the sarcolemma appear to be the morphological basis for the physiological reaction of slow muscle fibers.


2005 ◽  
Vol 289 (6) ◽  
pp. C1502-C1512 ◽  
Author(s):  
T. L. Dutka ◽  
L. Cole ◽  
G. D. Lamb

During vigorous exercise, Pi concentration levels within the cytoplasm of fast-twitch muscle fibers may reach ≥30 mM. Cytoplasmic Pi may enter the sarcoplasmic reticulum (SR) and bind to Ca2+ to form a precipitate (CaPi), thus reducing the amount of releasable Ca2+. Using mechanically skinned rat fast-twitch muscle fibers, which retain the normal action potential-mediated Ca2+ release mechanism, we investigated the consequences of Pi exposure on normal excitation-contraction coupling. The total amount of Ca2+ released from the SR by a combined caffeine/low-Mg2+ concentration stimulus was reduced by ∼20%, and the initial rate of force development slowed after 2-min exposure to 30 mM Pi (with or without the presence creatine phosphate). Peak (50 Hz) tetanic force was also reduced (by ∼25% and ∼45% after 10 and 30 mM Pi exposure, respectively). Tetanic force responses produced after 30 mM Pi exposure were nearly identical to those observed in the same fiber after depletion of total SR Ca2+ by ∼35%. Ca2+ content assays revealed that the total amount of Ca2+ in the SR was not detectably changed by exposure to 30 mM Pi, indicating that Ca2+ had not leaked from the SR but instead formed a precipitate with the Pi, reducing the amount of available Ca2+ for rapid release. These results suggest that CaPi precipitation that occurs within the SR could contribute to the failure of Ca2+ release observed in the later stages of metabolic muscle fatigue. They also demonstrate that the total amount of Ca2+ stored in the SR cannot drop substantially below the normal endogenous level without reducing tetanic force responses.


2017 ◽  
Vol 150 (1) ◽  
pp. 95-110 ◽  
Author(s):  
Bradley S. Launikonis ◽  
Tanya R. Cully ◽  
Laszlo Csernoch ◽  
D. George Stephenson

The complex membrane structure of the tubular system (t-system) in skeletal muscle fibers is open to the extracellular environment, which prevents measurements of H+ movement across its interface with the cytoplasm by conventional methods. Consequently, little is known about the t-system’s role in the regulation of cytoplasmic pH, which is different from extracellular pH. Here we describe a novel approach to measure H+-flux measurements across the t-system of fast-twitch fibers under different conditions. The approach involves loading the t-system of intact rat fast-twitch fibers with a strong pH buffer (20 mM HEPES) and pH-sensitive fluorescent probe (10 mM HPTS) before the t-system is sealed off. The pH changes in the t-system are then tracked by confocal microscopy after rapid changes in cytoplasmic ionic conditions. T-system sealing is achieved by removing the sarcolemma by microdissection (mechanical skinning), which causes the tubules to pinch off and seal tight. After this procedure, the t-system repolarizes to physiological levels and can be electrically stimulated when placed in K+-based solutions of cytosolic-like ionic composition. Using this approach, we show that the t-system of fast-twitch skeletal fibers displays amiloride-sensitive Na+/H+ exchange (NHE), which decreases markedly at alkaline cytosolic pH and has properties similar to that in mammalian cardiac myocytes. We observed mean values for NHE density and proton permeability coefficient of 339 pmol/m2 of t-system membrane and 158 µm/s, respectively. We conclude that the cytosolic pH in intact resting muscle can be quantitatively explained with respect to extracellular pH by assuming that these values apply to the t-system membrane and the sarcolemma.


1963 ◽  
Vol 47 (1) ◽  
pp. 189-214 ◽  
Author(s):  
Lucien Girardier ◽  
John P. Reuben ◽  
Philip W. Brandt ◽  
Harry Grundfest

Under certain conditions only, isolated crayfish skeletal muscle fibers change in appearance, becoming grainy, darkening, and seemingly losing their striations. These changes result from development of large vesicles on both sides of the Z-line. The longitudinal sarcoplasmic reticulum remains unaffected. The vesicles are due to swelling of a transverse tubular system (TTS) which is presumably homologous with the T-system tubules of other muscle fibers. The vesiculations occur during efflux of water or on reducing external K or Cl, but only when KCl can leave the fiber. They never result from osmotic, ionic, or electrical changes when KCl cannot leave. Inward currents, applied through a KCl-filled intracellular cathode, also cause the vesiculations. These are not produced when the cathode is filled with K-propionate, nor by outward or longitudinal currents. Thus the transverse tubules swell only when Cl leaves the cell. Accordingly, their membrane is largely or exclusively anion-permselective. These findings also indicate that the TTS forms part of a current loop, connecting with the exterior of the fiber probably through radial tubules (RT) possessing membrane of low conductivity. Thus, part of the current flowing inward across the sarcolemma during activity can return to the exterior through the membrane of the TTS. The structure and properties of the latter offer the possibility for an efficient electrical mechanism to initiate excitation-contraction coupling.


2018 ◽  
Vol Volume 13 ◽  
pp. 125-131 ◽  
Author(s):  
Mariko Matsubara ◽  
Haruka Tohara ◽  
Koji Hara ◽  
Hiromichi Shinozaki ◽  
Yasuhiro Yamazaki ◽  
...  

Cells ◽  
2018 ◽  
Vol 7 (12) ◽  
pp. 243 ◽  
Author(s):  
Manting Ma ◽  
Bolin Cai ◽  
Liang Jiang ◽  
Bahareldin Ali Abdalla ◽  
Zhenhui Li ◽  
...  

Emerging studies indicate important roles for non-coding RNAs (ncRNAs) as essential regulators in myogenesis, but relatively less is known about their function. In our previous study, we found that lncRNA-Six1 can regulate Six1 in cis to participate in myogenesis. Here, we studied a microRNA (miRNA) that is specifically expressed in chickens (miR-1611). Interestingly, miR-1611 was found to contain potential binding sites for both lncRNA-Six1 and Six1, and it can interact with lncRNA-Six1 to regulate Six1 expression. Overexpression of miR-1611 represses the proliferation and differentiation of myoblasts. Moreover, miR-1611 is highly expressed in slow-twitch fibers, and it drives the transformation of fast-twitch muscle fibers to slow-twitch muscle fibers. Together, these data demonstrate that miR-1611 can mediate the regulation of Six1 by lncRNA-Six1, thereby affecting proliferation and differentiation of myoblasts and transformation of muscle fiber types.


FEBS Letters ◽  
1986 ◽  
Vol 203 (1) ◽  
pp. 20-24 ◽  
Author(s):  
Aravind Babu ◽  
Suzanne Pemrick ◽  
Jagdish Gulati

2016 ◽  
Vol 2016 ◽  
pp. 1-6 ◽  
Author(s):  
Marija Meznaric ◽  
Erika Cvetko

Smaller diaphragmatic motor unit potentials (MUPs) compared to MUPs of limb muscles lead to the hypothesis that diaphragmatic muscle fibers, being the generators of MUPs, might be also smaller. We compared autopsy samples of costal diaphragm and vastus lateralis of healthy men with respect to fibers’ size and expression of slow myosin heavy chain isoform (MyHC-1) and fast 2A isoform (MyHC-2A). Diaphragmatic fibers were smaller than fibers in vastus lateralis with regard to the mean minimal fiber diameter of slow-twitch (46.8 versus 72.2 μm,p<0.001), fast-twitch (45.1 versus 62.4 μm,p<0.001), and hybrid fibers (47.3 versus 65.0 μm,p<0.01) as well as to the mean fiber cross-sectional areas of slow-twitch (2376.0 versus 5455.9 μm2,p<0.001), fast-twitch (2258.7 versus 4189.7 μm2,p<0.001), and hybrid fibers (2404.4 versus 4776.3 μm2,p<0.01). The numerical proportion of slow-twitch fibers was higher (50.2 versus 36.3%,p<0.01) in costal diaphragm and the numerical proportion of fast-twitch fibers (47.2 versus 58.7%,p<0.01) was lower. The numerical proportion of hybrid fibers did not differ. Muscle fibers of costal diaphragm have specific characteristics which support increased resistance of diaphragm to fatigue.


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