scholarly journals Regional differences in Ca2+ entry along the proximal-middle-distal muscle axis during eccentric contractions in rat skeletal muscle

2019 ◽  
Vol 127 (3) ◽  
pp. 828-837 ◽  
Author(s):  
Ayaka Tabuchi ◽  
Hiroaki Eshima ◽  
Yoshinori Tanaka ◽  
Shunsuke Nogami ◽  
Naoki Inoue ◽  
...  

Eccentric (ECC) contraction-induced muscle damage is associated with calcium ion (Ca2+) influx from the extracellular milieu through stretch-activated channels. It remains unknown whether Ca2+ influx consequent to repetitive ECC contractions is nonuniform across different muscle regions. We tested the hypothesis that there are regional differences in Ca2+ entry along the proximal-middle-distal muscle axis. Tibialis anterior (TA) muscles of adult male Wistar rats were exposed by reflecting the overlying skin and fasciae and ECC contractions evoked by peroneal nerve stimulation paired with simultaneous ankle extension (50 times/set, 2 protocols: 1 set and 10 sets). During ECC in the proximal, middle, and distal TA, we determined 1) muscle fiber extension by high-speed camera (200 frames/s) and 2) Ca2+ accumulation by in vivo bioimaging (Ca2+-sensitive probe Fura-2-acetoxymethyl ester). Muscle fiber extension from resting was significantly different among regions (i.e., proximal, 4.0%: < middle, 11.2%: < distal, 17.0%; ECC phase length at 500th contraction). Intracellular Ca2+ accumulation after 1 set of ECC was higher in the distal (1.46 ± 0.04, P < 0.05) than the proximal (1.27 ± 0.04) or middle (1.26 ± 0.05) regions. However, this regional Ca2+ accumulation difference disappeared by 32.5 min after the 1 set protocol when the muscle was quiescent and by contraction set 5 for the 10-set protocol. The initial preferential ECC-induced Ca2+ accumulation observed distally was associated spatially with the greater muscle extension compared with that of the proximal and middle regions. Disappearance of the regional Ca2+ accumulation disparity in quiescent and ECC-contracting muscle might be explained, in part, by axial Ca2+ propagation and account for the uniformity of muscle damage across regions evident 3 days post-ECC. NEW & NOTEWORTHY After 1 set of 50 eccentric (ECC) contractions in the anterior tibialis muscle, intracellular Ca2+ ([Ca2+]i) accumulation evinces substantial regional heterogeneity that is spatially coherent with muscle length changes (i.e., distal [Ca2+]i > middle, proximal). However, irrespective of whether 50 or 500 ECC contractions are performed, this heterogeneity is subsequently abolished, at least in part, by axial intracellular Ca2+ propagation. This Ca2+ homogenization across regions is consistent with the absence of any interregional difference in muscle damage 3 days post-ECC.

1999 ◽  
Vol 202 (16) ◽  
pp. 2139-2150 ◽  
Author(s):  
R.E. Shadwick ◽  
S.L. Katz ◽  
K.E. Korsmeyer ◽  
T. Knower ◽  
J.W. Covell

Cyclic length changes in the internal red muscle of skipjack tuna (Katsuwonus pelamis) were measured using sonomicrometry while the fish swam in a water tunnel at steady speeds of 1.1-2.3 L s(−)(1), where L is fork length. These data were coupled with simultaneous electromyographic (EMG) recordings. The onset of EMG activity occurred at virtually the same phase of the strain cycle for muscle at axial locations between approximately 0.4L and 0.74L, where the majority of the internal red muscle is located. Furthermore, EMG activity always began during muscle lengthening, 40–50 prior to peak length, suggesting that force enhancement by stretching and net positive work probably occur in red muscle all along the body. Our results support the idea that positive contractile power is derived from all the aerobic swimming muscle in tunas, while force transmission is provided primarily by connective tissue structures, such as skin and tendons, rather than by muscles performing negative work. We also compared measured muscle length changes with midline curvature (as a potential index of muscle strain) calculated from synchronised video image analysis. Unlike contraction of the superficial red muscle in other fish, the shortening of internal red muscle in skipjack tuna substantially lags behind changes in the local midline curvature. The temporal separation of red muscle shortening and local curvature is so pronounced that, in the mid-body region, muscle shortening at each location is synchronous with midline curvature at locations that are 7–8 cm (i.e. 8–10 vertebral segments) more posterior. These results suggest that contraction of the internal red muscle causes deformation of the body at more posterior locations, rather than locally. This situation represents a unique departure from the model of a homogeneous bending beam, which describes red muscle strain in other fish during steady swimming, but is consistent with the idea that tunas produce thrust by motion of the caudal fin rather than by undulation of segments along the body.


1998 ◽  
Vol 274 (2) ◽  
pp. C472-C480 ◽  
Author(s):  
Shinji Naito ◽  
Shunichi Shimizu ◽  
Shigeto Maeda ◽  
Jianwei Wang ◽  
Richard Paul ◽  
...  

Ets-1 is a transcription factor that activates expression of matrix-degrading proteinases such as collagenase and stromelysin. To study the control of ets-1 gene expression in rat vascular smooth muscle cells (VSMC), cells were exposed to factors known to regulate VSMC migration and proliferation. Platelet-derived growth factor-BB (PDGF-BB), endothelin-1 (ET-1), and phorbol 12-myristate 13-acetate (PMA) induced a dose-dependent expression of ets-1 mRNA. These effects were abrogated by inhibition of protein kinase C (PKC) by H-7 or chronic PMA treatment. Ets-1 mRNA was superinduced by PDGF-BB and ET-1 in the presence of cycloheximide. The chelation of intracellular Ca2+ by 1,2-bis(2-aminophenoxy)ethane- N, N, N′, N′-tetraacetic acid-acetoxymethyl ester and the depletion of endoplasmic reticulum intracellular Ca2+concentration ([Ca2+]i) by thapsigargin inhibited PDGF-BB- and ET-1-induced ets-1 mRNA, whereas ethylene glycol-bis(β-aminoethyl ether)- N, N, N′, N′-tetraacetic acid had no effect. However, [Ca2+]irelease alone was not sufficient to increase ets-1 mRNA. Forskolin blocked ET-1-, PDGF-BB-, and PMA-induced ets-1 mRNA, as well as inositol phosphate formation, consistent with an effect through impairment of PKC activation. Inhibitors of ets-1 gene expression, such as H-7 and herbimycin A, inhibited the ET-1 induction of collagenase I mRNA. We propose that ets-1 may be an important element in the orchestration of matrix proteinase expression and of vascular remodeling after arterial injury.


2001 ◽  
Vol 281 (5) ◽  
pp. H2133-H2142 ◽  
Author(s):  
Yuji Wakayama ◽  
Masahito Miura ◽  
Yoshinao Sugai ◽  
Yutaka Kagaya ◽  
Jun Watanabe ◽  
...  

Rapid shortening of active cardiac muscle [quick release (QR)] dissociates Ca2+ from myofilaments. We studied, using muscle stretches and QR, whether Ca2+ dissociation affects triggered propagated contractions (TPCs) and Ca2+waves. The intracellular Ca2+ concentration was measured by a SIT camera in right ventricular trabeculae dissected from rat hearts loaded with fura 2 salt, force was measured by a silicon strain gauge, and sarcomere length was measured by laser diffraction while a servomotor controlled muscle length. TPCs ( n = 27) were induced at 28°C by stimulus trains (7.5 s at 2.65 ± 0.13 Hz) at an extracellular Ca2+ concentration ([Ca2+]o) = 2.0 mM or with 10 μM Gd3+ at [Ca2+]o = 5.2 ± 0.73 mM. QR during twitch relaxation after a 10% stretch for 100–200 ms reduced both the time between the last stimulus and the peak TPC (PeakTPC) and the time between the last stimulus and peak Ca2+ wave (PeakCW) and increased PeakTPC and PeakCW ( n= 13) as well as the propagation velocity ( V prop; n = 8). Active force during stretch also increased V prop( r = 0.84, n = 12, P < 0.01), but Gd3+ had no effect ( n = 5). These results suggest that Ca2+ dissociation by QR during relaxation accelerates the initiation and propagation of Ca2+ waves.


Author(s):  
Katarzyna Nowakowska ◽  
Robert Michnik ◽  
Katarzyna Jochymczyk-Woźniak ◽  
Jacek Jurkojć ◽  
Ilona Kopyta

1982 ◽  
Vol 242 (3) ◽  
pp. C146-C158 ◽  
Author(s):  
R. A. Meiss

Controlled length changes were imposed on mesotubarium superius and ovarian ligament smooth muscles from the reproductive tracts of female rabbits in constant estrus. Stretches of up to 35% of the muscle length were applied during isometric contraction, relaxation, and steady-state force levels. Force was continuously monitored and was plotted as a function of length. During constant velocity stretches there was an initial steep rise in force, a rapid downward deviation from the initial slope, and a long region with a constant upward slope. Stretches made during contraction showed smaller initial rises in force and steeper linear portions than did identical comparison stretches made during relaxation. The value of the slope was independent of the prior developed force, but it did depend on whether the muscle was contracting or relaxing. During contraction and steady-state force levels, the slope was independent of the stretch rate, but it was strongly rate dependent during relaxation. Changes in the stretch rate during stretch caused associated changes in muscle force; the relationship was curvilinear and was exaggerated during relaxation. The findings are placed in the context of a sliding-filament--cross-bridge hypothesis.


1979 ◽  
Vol 42 (2) ◽  
pp. 420-440 ◽  
Author(s):  
G. E. Loeb ◽  
J. Duysens

1. Chronically implanted microelectrode wires in the L7 and S1 dorsal root ganglia were used to record unit activity from cat hindlimb primary and secondary muscle spindle afferents. Units could be reliably recorded for several days, permitting comparison of their activity with homonymous muscle EMG and length during a variety of normal, unrestrained movements. 2. The general observation was that among both primary and secondary endings there was a broad range of different patterns of activity depending on the type of muscle involved and the type of movement performed. 3. During walking, the activity of a given spindle primary was usually consistent among similar step cycles. However, the activity was usually poorly correlated with absolute muscle length, apparently unrealted to velocity of muscle stretch, and could change markedly for similar movements performed under different conditions. 4. Spindle activity modulation not apparently related to muscle length changes was assumed to be influenced by fusimotor activity. In certain muscles, this presumption leads to the conclusion that gamma-motoneurons may be activated out of phase with homonymous alpha-motoneurons as well as by more conventional alpha-gamma-motoneuron coactivation. 5. Simultaneous recordings of two spindle primary afferents from extensor digitorum longus indicated that spindles within the same muscle may differ considerably with respect to this presumed gamma-motoneuron drive. 6. Spindle secondary endings appeared to be predominantly passive indicators of muscle length during walking, but could demonstrate apparently strong fusimotor modulation during other motor activities such as postural changes and paw shaking. 7. Both primary and secondary endings were observed to undergo very rapid modulation of firing rates in response to presumed reflexly induced intrafusal contractions. 8. It is suggested that the pattern of fusimotor control of spindles may be tailored to the specific muscle and task being performed, rather than necessarily dominated by rigid alpha-gamma coactivation.


1990 ◽  
Vol 68 (1) ◽  
pp. 209-219 ◽  
Author(s):  
M. Okazawa ◽  
P. Pare ◽  
J. Road

We applied the technique of sonomicrometry to directly measure length changes of the trachealis muscle in vivo. Pairs of small 1-mm piezoelectric transducers were placed in parallel with the muscle fibers in the posterior tracheal wall in seven anesthetized dogs. Length changes were recorded during mechanical ventilation and during complete pressure-volume curves of the lung. The trachealis muscle showed spontaneous fluctuations in base-line length that disappeared after vagotomy. Before vagotomy passive pressure-length curves showed marked hysteresis and length changed by 18.5 +/- 13.2% (SD) resting length at functional residual capacity (LFRC) from FRC to total lung capacity (TLC) and by 28.2 +/- 16.2% LFRC from FRC to residual volume (RV). After vagotomy hysteresis decreased considerably and length now changed by 10.4 +/- 3.7% LFRC from FRC to TLC and by 32.5 +/- 14.6% LFRC from FRC to RV. Bilateral supramaximal vagal stimulation produced a mean maximal active shortening of 28.8 +/- 14.2% resting length at any lung volume (LR) and shortening decreased at lengths above FRC. The mean maximal velocity of shortening was 4.2 +/- 3.9% LR.S-1. We conclude that sonomicrometry may be used to record smooth muscle length in vivo. Vagal tone strongly influences passive length change. In vivo active shortening and velocity of shortening are less than in vitro, implying that there are significant loads impeding shortening in vivo.


1982 ◽  
Vol 14 (2) ◽  
pp. 144 ◽  
Author(s):  
W. C. Whiting ◽  
R. J. Gregor ◽  
R. R. Roy
Keyword(s):  

2017 ◽  
Vol 122 (3) ◽  
pp. 559-570 ◽  
Author(s):  
Jonathan M. Peake ◽  
Oliver Neubauer ◽  
Paul A. Della Gatta ◽  
Kazunori Nosaka

Unaccustomed exercise consisting of eccentric (i.e., lengthening) muscle contractions often results in muscle damage characterized by ultrastructural alterations in muscle tissue, clinical signs, and symptoms (e.g., reduced muscle strength and range of motion, increased muscle soreness and swelling, efflux of myocellular proteins). The time course of recovery following exercise-induced muscle damage depends on the extent of initial muscle damage, which in turn is influenced by the intensity and duration of exercise, joint angle/muscle length, and muscle groups used during exercise. The effects of these factors on muscle strength, soreness, and swelling are well characterized. By contrast, much less is known about how they affect intramuscular inflammation and molecular aspects of muscle adaptation/remodeling. Although inflammation has historically been viewed as detrimental for recovery from exercise, it is now generally accepted that inflammatory responses, if tightly regulated, are integral to muscle repair and regeneration. Animal studies have revealed that various cell types, including neutrophils, macrophages, mast cells, eosinophils, CD8 and T-regulatory lymphocytes, fibro-adipogenic progenitors, and pericytes help to facilitate muscle tissue regeneration. However, more research is required to determine whether these cells respond to exercise-induced muscle damage. A large body of research has investigated the efficacy of physicotherapeutic, pharmacological, and nutritional interventions for reducing the signs and symptoms of exercise-induced muscle damage, with mixed results. More research is needed to examine if/how these treatments influence inflammation and muscle remodeling during recovery from exercise.


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