ADP binds similarly to rigor muscle myofibrils and to actomyosin‐subfragment one

Johnson, Robert E.; Adams, Patricia H.

doi:10.1016/0014-5793(84)81067-4

Cited by 30 publications

(12 citation statements)

References 21 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Therefore, the kinetic mechanism observed for actomyosin-Si may be a reasonable approximation for the mechanism that occurs in muscle undergoing unloaded shortening. The dissociation constant for ADP binding to rabbit psoas and bovine cardiac myofibrils has been measured to be 200 and 7 ,uM, respectively (33). These values are comparable to those for rabbit fast skeletal and bovine cardiac muscle actomyosin-Si in solution, 160 /iM (8,34) and 10 AtM (9), respectively.…”

Section: Discussionsupporting

confidence: 57%

ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle.

Siemankowski¹,

Wiseman²,

White³

1985

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

413

318

View full text Add to dashboard Cite

The rate constant for dissociation of ADP from actomyosin subfragment 1 (Si) has been measured in this laboratory and elsewhere for a variety of vertebrate muscle types. We have made the following observations: (i) In solution, the dissociation of ADP from actomyosin-Sl limits the rate of dissociation of actomyosin-Sl-ADP by ATP and, presumably, also limits the rate of crossbridge detachment in contracting muscle. (it) For muscle types in which the rate of ADP dissociation from actomyosin-Sl is slow enough to measure using stopped-flow methods, the rate constants are nearly the same as the theoretical value for the minimum allowable rate constant for dissociation of an attached crossbridge. Therefore, ADP dissociation is sufficiently slow to be the molecular step that limits the maximum shortening velocity of these muscles. (i) Variation with muscle type of the rate constant for ADP dissociation may be a general phylogenetic mechanism for regulating shortening velocity.that one or more of the rate constants of the ATP hydrolysis mechanism limits the muscle contraction rate. For a molecular step to limit the shortening velocity of muscle, it must have the following attributes:(i) The rate constant for such a step must be consistent with both the maximum working length of an individual crossbridge and the rate of axial displacement of the thick and thin filaments observed in contracting muscle. The minimum allowable rate constant, kmin, for the conversion of an attached crossbridge state in muscle (corresponding to the AM states in the top line of Eq. 1) to other attached or detached states (corresponding to the M states in the bottom line of Eq. 1) can be estimated from the maximum rate of contraction (the unloaded shortening velocity) and the distance over which a crossbridge can remain attached, using Eq. 2, Muscle contraction is thought to occur as the result of a cyclic association and dissociation of crossbridges formed between myosin molecules in the thick filaments and F-actin molecules in the thin filament, involving concomitant hydrolysis of ATP. This cycle can lead to relative sliding of the actin and myosin filaments and result in the production of work. A rationale for studying the kinetic mechanism of ATP hydrolysis by actomyosin-Sl in solution is that it may directly relate to the observed physiological properties of muscle. A condensed version of the kinetic mechanism, consistent with recent observations (1, 2), is shown in Eq. 1. The second-order reactions of nucleotide and phosphate binding have been shown to be two-step reactions (3-5), but they are condensed here to single steps:where M represents myosin subfragment-1 (Si) and AM represents actomyosin S1. Different types of vertebrate muscles have shortening velocities that vary by almost two orders of magnitude. Barany showed that the steady-state rate of hydrolysis of MgATP by actomyosin is correlated with muscle shortening velocity (6).However, it has not been demonstrated that the rate of ATP hydrolysis directly limits shortening ve...

show abstract

Section: Discussionsupporting

confidence: 57%

ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle.

Siemankowski¹,

Wiseman²,

White³

1985

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

413

318

View full text Add to dashboard Cite

show abstract

“…This result is similar to the difference between rabbit psoas and bovine myocardium studied in solutions and myofibrils. It was reported that the MgADP association constant of bovine myocardium is 16 to 29 times larger than that of rabbit psoas (White and Taylor, 1976;Greene and Eisenberg, 1980;Johnson and Adams, 1984;Siemankowski et al, 1985).…”

Section: Comparison With Cardiac Muscle Fibersmentioning

confidence: 96%

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

Wang

Kawai

1996

Biophysical Journal

View full text Add to dashboard Cite

The elementary steps surrounding the nucleotide binding step in the cross-bridge cycle were investigated with sinusoidal analysis in rabbit soleus slow-twitch muscle fibers. The single-fiber preparations were activated at pCa 4.40, ionic strength 180 mM, 20 degrees C, and the effects of MgATP (S) and MgADP (D) concentrations on three exponential processes B, C, and D were studied. Our results demonstrate that all apparent (measured) rate constants increased and saturated hyperbolically as the MgATP concentration was increased. These results are consistent with the following cross-bridge scheme: [cross-bridge scheme: see text] where A = actin, M = myosin, S = MgATP, and D = MgADP. AM+S is a collision complex, and AM*S is its isomerized form. From our studies, we obtained K0 = 18 +/- 4 mM-1 (MgADP association constant, N = 7, average +/- sem), K1a = 1.2 +/- 0.3 mM-1 (MgATP association constant, N = 8 hereafter), k1b = 90 +/- 20 s-1 (rate constant of ATP isomerization), k-1b = 100 +/- 9 s-1 (rate constant of reverse isomerization), K1b = 1.0 +/- 0.2 (equilibrium constant of isomerization), k2 = 21 +/- 3 s-1 (rate constant of cross-bridge detachment), k-2 = 14.1 +/- 1.0 s-1 (rate constant of reversal of detachment), and K2 = 1.6 +/- 0.3 (equilibrium constant of detachment). K0 is 8 times and K1a is 2.2 times those in rabbit psoas, indicating that nucleotides bind to cross-bridges more tightly in soleus slow-twitch muscle fibers than in psoas fast-twitch muscle fibers. These results indicate that cross-bridges of slow-twitch fibers are more resistant to ATP depletion than those of fast-twitch fibers. The rate constants of ATP isomerization and cross-bridge detachment steps are, in general, one-tenth to one-thirtieth of those in psoas.

show abstract

“…The Kd values obtained in the present study are much lower than reported before: 50/M (binding of [3H]ADP to turkey gizzard heavy meromyosin; Greene & Sellers, 1987); 100-300 /tM (inhibition of maximal shortening velocity in thiophosphorylated guinea-pig taenia coli fibre; Arner, Hellstrand & Ruiegg, 1987); 200,aM (in vitro motility assay using thiophosphorylated smooth muscle myosin; Warshaw & Trybus, 1991); 18-400 /tM (skeletal muscle;Marston, 1973;Cooke & Pate, 1985;Schoenberg & Eisenberg, 1987;Dantzig et al 1991). On the other hand, Kd values of ADP binding to cross-bridges are also low in cardiac myofibrils (7 AM; Johnson & Adams, 1984). It has been suggested that ADP dissociation from actomyosin S1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle (Siemankowski, Wiseman & White, 1985).…”

Section: High Affinity Mgadp Binding To Cross-bridges In Smooth Musclementioning

confidence: 99%

“…On the other hand, Kd values of ADP binding to cross-bridges are also low in cardiac myofibrils (7 AM; Johnson & Adams, 1984). It has been suggested that ADP dissociation from actomyosin S1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle (Siemankowski, Wiseman & White, 1985).…”

Section: High Affinity Mgadp Binding To Cross-bridges In Smooth Musclementioning

confidence: 99%

The effects of MgADP on cross‐bridge kinetics: a laser flash photolysis study of guinea‐pig smooth muscle.

Nishiye

Somlyo

Török

1993

The Journal of Physiology

View full text Add to dashboard Cite

SUMMARY1. The effects of AMgADP on cross-bridge kinetics were investigated using laser flash photolysis of caged ATP (P3-1(2-nitrophenyl) ethyladenosine 5'-triphosphate), in guinea-pig portal vein smooth muscle permeabilized with Staphylococcus aureus atoxin. Isometric tension and in-phase stiffness transitions from rigor state were monitored upon photolysis of caged ATP. The estimated concentration of ATP released from caged ATP by high-pressure liquid chromatography (HPLC) was 1P3 mM.2. The time course of relaxation initiated by photolysis of caged ATP in the absence of Ca2+ was well fitted during the initial 200 ms by two exponential functions with tine constants of. respectively, T1 = 34 ms and T2 = 1P2 s and relative amplitudes of 0 14 and 0 86. Multiple exponential functions were needed to fit longer intervals; the half-time of the overall relaxation was 0-8 s. The second order rate constant for cross-bridge detachment by ATP, estimated from the rate of initial relaxation, was 0A4-23 x 104 M-1 s-1.3. MgADP dose dependently reduced both the relative amplitude of the first component and the rate constant of the second component of relaxation. Conversely, treatment of muscles with apyrase. to deplete endogenous ADP, increased the relative amplitude of the first component. In the presence of MgADP, in-phase stiffness decreased during force maintenance, suggesting that the force per crossbridge increased. The apparent dissociation constant (Kd) of MgADP for the crossbridge binding site, estimated from its concentration-dependent effect on the relative amplitude of the first component. was 1P3/M. This affinity is much higher than the previously reported values (50-300 JtM for smooth muscle; 18-400 /tM for skeletal muscle: 7-10 /um for cardiac muscle). It is possible that the high affinity reflects the properties of a state generated during the co-operative reattachment cycle, rather than that of the rigor bridge.4. The rate constant of MgADP release from cross-bridges, estimated from its concentration-dependent effect on the rate constant of the second (T2) component, was 0'35-7'7 s-'. To the extent that reattachment of cross-bridges could slow relaxation even during the initial 200 ms. this rate constant may be an underestimate. § To whom all correspondence should be addressed.Ms 1080 2E. XISHIY-E AND OTHERS 5. Inorganic phosphate (Pi, 30 mM) did not affect the rate of relaxation during the initial -50 ms, but accelerated the slower phase of relaxation, consistent with a cyclic cross-bridge model in which Pi increases the proportion of cross-bridges in detached ('weakly bound') states. In the presence of 100 /tM MgADP, Pi (10-50 mM) predominantly accelerated the final slow phase of relaxation, rather than the initial (T1 and T2) components, and shortened the duration of the plateau phase that followed the initial rapid relaxation.6. Muscles, in which the myosin light chains were thiophosphorylated, relaxed during the initial 40-50 ms after photolysis of caged ATP at the same rate as muscles with non-thiophos...

show abstract

ADP binds similarly to rigor muscle myofibrils and to actomyosin‐subfragment one

Cited by 30 publications

References 21 publications

ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle.

ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle.

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

The effects of MgADP on cross‐bridge kinetics: a laser flash photolysis study of guinea‐pig smooth muscle.

Contact Info

Product

Resources

About