Effects of MgATP and MgADP on the cross-bridge kinetics of rabbit soleus slow-twitch muscle fibers

Wang, Brant G.; Kawai, Masataka

doi:10.1016/s0006-3495(96)79346-3

Cited by 39 publications

(81 citation statements)

References 51 publications

(68 reference statements)

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“…The slow EMB-fiber data, on the other hand, fit a configuration in which the rate-limiting step is an isomerization of myosin before MgADP release ( Fig. 3 A and C), consistent with reaction schemes proposed for other slow striated muscles (11,12,21).…”

Section: Resultssupporting

confidence: 85%

“…For both IFI and EMB, elevating [MgATP] increased the frequency of optimum work production ( fw max ) to a saturating level (Fig. 1 A), a result qualitatively similar to that observed in other muscle types (11,12,21). However, Ϸ15 mM MgATP was required to reach maximal fw max in IFI compared with Ϸ2 mM for EMBexpressing fibers, which suggests that the affinity of MgATP for myosin is much lower in IFI than in EMB.…”

supporting

confidence: 80%

“…In IFI fibers at saturating levels of MgATP (15-20 mM), fw max was insensitive to changes in [Pi]; at 10 mM MgATP, fw max showed a slight tendency to decrease with increasing [Pi]; at 5 mM MgATP, fw max decreased significantly with increasing [Pi]. These trends are opposite to the Pi-dependent rise in fw max observed in EMB fibers and all other striated muscle fiber types studied by using this technique (10)(11)(12)21). The lack of IFI fw max sensitivity to [Pi] at saturating [MgATP] strongly suggests a departure from the typical myosin cross-bridge scheme, where, with MgADP rate limiting for oscillatory work production, fw max is not independent of [Pi] in working muscle (9)(10)(11)(12)(21)(22)(23).…”

mentioning

confidence: 87%

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An exceptionally fast actomyosin reaction powers insect flight muscle

Swank

Vishnudas

Maughan

2006

Proc. Natl. Acad. Sci. U.S.A.

115

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Insects, as a group, have been remarkably successful in adapting to a great range of physical and biological environments, in large part because of their ability to fly. The evolution of flight in small insects was accompanied by striking adaptations of the thoracic musculature that enabled very high wing beat frequencies. At the cellular and protein filament level, a stretch activation mechanism evolved that allowed high-oscillatory work to be achieved at very high frequencies as contraction and nerve stimulus became asynchronous. At the molecular level, critical adaptations occurred within the motor protein myosin II, because its elementary interactions with actin set the speed of sarcomere contraction. Here, we show that the key myosin enzymatic adaptations required for powering the very fast flight muscles in the fruit fly Drosophila melanogaster include the highest measured detachment rate of myosin from actin (forward rate constant, 3,698 s ؊1 ), an exceptionally weak affinity of MgATP for myosin (association constant, 0.2 mM ؊1 ), and a unique rate-limiting step in the cross-bridge cycle at the point of inorganic phosphate release. The latter adaptations are constraints imposed by the overriding requirement for exceptionally fast release of the hydrolytic product MgADP. Otherwise, as in Drosophila embryonic muscle and other slow muscle types, a step associated with MgADP release limits muscle contraction speed by delaying the detachment of myosin from actin.cross-bridge cycle ͉ Drosophila ͉ kinetics ͉ myosin I n Drosophila melanogaster two sets of antagonistic, asynchronous flight muscles oscillate at Ϸ200 beats per second, powering the wings indirectly by deforming the thoracic cuticle into which the muscles and wings insert. Although the myofibrillar basis of oscillatory work and power production is known (1-5), the molecular adaptations that allow the indirect flight muscles (IFM) to operate at very high frequencies are less well understood. In muscles of slow-to-moderate speed, muscle velocity is thought to be limited by prolonging the time myosin spends strongly bound to actin before detachment (6, 7). The prolongation is essential for coupling enzyme chemical kinetics, which normally occur rapidly, to the slower movements of the sarcomere during normal muscle function. In most vertebrate striated muscle types, the comparatively slow release of MgADP (one of the products of MgATP hydrolysis) is thought to be the ratelimiting step (8-13). However, recent studies suggest MgADP release may not be rate limiting for faster muscle types (14-16). If so, we reasoned that a shift in rate-limiting step to another part of the cross-bridge cycle should be most readily apparent in working indirect insect flight muscle, the fastest known muscle type.We had directly shown that myosin isoforms determine Drosophila IFM speed by using genetic engineering methods to substitute a relatively slow embryonic myosin (EMB) for the native fast myosin (IFI) in the IFM (Fig. 1A Inset) (17,18). This substitution transformed the ...

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Section: Resultssupporting

confidence: 85%

supporting

confidence: 80%

mentioning

confidence: 87%

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An exceptionally fast actomyosin reaction powers insect flight muscle

Swank

Vishnudas

Maughan

2006

Proc. Natl. Acad. Sci. U.S.A.

115

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“…The MgATP-dependent cross-bridge detachment rates from skinned rat soleus fibers at 17 C (Fig. 4 K) are consistent with the 2pc-MgATP relationships measured in skinned rabbit soleus fibers at 20 C (37,38). Specifically, we show that the myosin detachment rate increased from 8. soleus fibers at 20 C (37) compared to rat soleus fibers at 17 C (Fig.…”

Section: Discussionsupporting

confidence: 87%

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Fenwick

Leighton

Tanner

2016

Biophysical Journal

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Actin-myosin cross-bridges use chemical energy from MgATP hydrolysis to generate force and shortening in striated muscle. Previous studies show that increases in sarcomere length can reduce thick-to-thin filament spacing in skinned muscle fibers, thereby increasing force production at longer sarcomere lengths. However, it is unclear how changes in sarcomere length and lattice spacing affect cross-bridge kinetics at fundamental steps of the cross-bridge cycle, such as the MgADP release rate. We hypothesize that decreased lattice spacing, achieved through increased sarcomere length or osmotic compression of the fiber via dextran T-500, could slow MgADP release rate and increase cross-bridge attachment duration. To test this, we measured cross-bridge cycling and MgADP release rates in skinned soleus fibers using stochastic length-perturbation analysis at 2.5 and 2.0 mm sarcomere lengths as pCa and [MgATP] varied. In the absence of dextran, the force-pCa relationship showed greater Ca 2þ sensitivity for 2.5 vs. 2.0 mm sarcomere length fibers (pCa 50 ¼ 5.68 5 0.01 vs. 5.60 5 0.01). When fibers were compressed with 4% dextran, the length-dependent increase in Ca 2þ sensitivity of force was attenuated, though the Ca 2þ sensitivity of the force-pCa relationship at both sarcomere lengths was greater with osmotic compression via 4% dextran compared to no osmotic compression. Without dextran, the cross-bridge detachment rate slowed by~15% as sarcomere length increased, due to a slower MgADP release rate (11.2 5 0.5 vs. 13.5 5 0.7 s À1 ). In the presence of dextran, cross-bridge detachment was~20% slower at 2.5 vs. 2.0 mm sarcomere length due to a slower MgADP release rate (10.1 5 0.6 vs. 12.9 5 0.5 s À1 ). However, osmotic compression of fibers at either 2.5 or 2.0 mm sarcomere length produced only slight (and statistically insignificant) slowing in the rate of MgADP release. These data suggest that skeletal muscle exhibits sarcomere-length-dependent changes in cross-bridge kinetics and MgADP release that are separate from, or complementary to, changes in lattice spacing.

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“…The Km estimated from the rigor stiffness was 0·04 mÒ in soleus and 0·14 mÒ in psoas fibres. According to Wang & Kawai (1996), Km derived in the 'sinusoidal analysis' on rabbit fibres was 0·06 mÒ in soleus and 0·4 mÒ in psoas fibres. The high affinity for ADP of the muscles for slow contraction probably results from a slow dissociation of ADP from the cross-bridges (step 1 in Fig.…”

Section: Discussionmentioning

confidence: 99%

Mechanical study of rat soleus muscle using caged ATP and X‐ray diffraction: high ADP affinity of slow cross‐bridges

Horiuti

Yagi

Takemori

1997

The Journal of Physiology

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The cross‐bridges in slow‐ and fast‐twitch fibres (taken, respectively, from soleus and psoas muscles of rats) were examined in mechanical experiments using caged ATP and X‐ray diffraction, to compare their binding of ATP and ADP. Caged ATP was photolysed in rigor fibres. When ADP was removed from pre‐photolysis fibres, the initial relaxation (±Ca2+) in soleus was as fast as that in psoas fibres, whereas the subsequent contraction (+Ca2+) was slower in soleus than in psoas. The ATPase rate during the steady‐state contraction was also slower in soleus fibres. When ADP was added to pre‐photolysis fibres (±Ca2+), tension developed even in the initial phase, the overall tension development being biphasic. Both initial and late components of the Ca2+‐free contraction were enhanced when ADP was added before photolysis, although pre‐photolysis ADP was not a prerequisite for the late component. The effect of ADP was greater in soleus than in psoas fibres. Static experiments on rigor fibres revealed a higher ADP affinity in soleus fibres. The intensity of the actin layer‐line from ADP rigor soleus fibres decreased rapidly on photorelease of ATP. We conclude that, despite the tight ADP binding of the soleus cross‐bridge, its isometric reaction is not rate limited by the ‘off’ rate of ADP.

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Effects of MgATP and MgADP on the cross-bridge kinetics of rabbit soleus slow-twitch muscle fibers

Cited by 39 publications

References 51 publications

An exceptionally fast actomyosin reaction powers insect flight muscle

An exceptionally fast actomyosin reaction powers insect flight muscle

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Mechanical study of rat soleus muscle using caged ATP and X‐ray diffraction: high ADP affinity of slow cross‐bridges

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