Superfast contractions without superfast energetics: ATP usage by SR‐Ca²⁺ pumps and crossbridges in toadfish swimbladder muscle

Abstract

Powering the large variety of motor activities in which animals engage has required the evolution of different muscle types with widely varying contraction speeds. Hill showed as early as 1938 that the rate at which an active muscle uses energy is proportional to its isometric twitch speed (Hill, 1938(Hill, , 1950. The mechanisms underlying this relationship appear to be that both the rates of SR-Ca¥ pumping and crossbridge cycling increase to permit faster twitch speeds. Because both processes require ATP, there must be an increase in the rate of ATP utilization. Researchers have been able to partition the energy used during contraction into its two constituent parts by stretching muscle beyond myofilament overlap. In muscles from diverse species representing a large range of twitch speeds, it was found that a constant proportion (•25-40%) of the total energy during contraction is used by SR-Ca¥ pumps and nearly all of the remainder by the crossbridges (reviewed in Homsher & Kean, 1978). This finding is consistent with the notion that, as twitch speed of the muscle increases, the crossbridge kinetics and the Ca¥ pumping rate increase in unison. However, it is unclear if this must necessarily be the case. If the Ca¥ transient duration were the rate limiting step of relaxation, it seems possible that, in muscles adapted for very high frequency contractions, the SR-Ca¥ pumping rate might have increased far more dramatically than the crossbridge cycling rate. This in turn would increase the proportion of energy used by SR-Ca¥ pumps. Also, in these high frequency contraction muscles, the relative myofibrillar volume is known to be reduced (e.g. to 50% in toadfish swimbladder) as the space is taken up by increasing volume of SR (Rome & Lindstedt, 1998). This should increase further the proportion of the total energy utilization by the SR-Ca¥ pumps. To test this hypothesis, we determined the ATP utilization rate and partitioned it between SR-Ca¥ pumps and crossbridges in the swimbladder muscle of toadfish. The swimbladder has the fastest isometric relaxation rate of any vertebrate muscle (e.g. at 15°C it takes only •10 ms for force to fall from 90 to 10% in swimbladder compared with 1. The rate at which an isometrically contracting muscle uses energy is thought to be proportional to its twitch speed. In both slow and fast muscles, however, a constant proportion (25-40%) of the total energy has been found to be used by SR-Ca¥ pumps and the remainder by crossbridges. We examined whether SR-Ca¥ pumps account for a larger proportion of the energy in the fastest vertebrate muscle known (the toadfish swimbladder), and whether the swimbladder muscle utilizes energy at the superfast rate one would predict from its mechanics. 2. The ATP utilization rates of the SR-Ca¥ pumps and crossbridges were measured using a coupled assay system on fibres skinned with saponin. Surprisingly, despite its superfast twitch speed, the ATP utilization rate of swimbladder was no higher than that of much slower fast-twitch amphibian muscles. 3. Th...

Electrical and mechanical properties and mode of innervation in scorpionfish sound-producing muscle fibres

“…This may indicate that only a small fraction of cross-bridges within the SBM fibres can be activated to interact with the thin filament during brief twitches evoked by motor nerve impulses, while a much larger fraction of cross-bridges can be effectively activated by transverse a.c. stimulation. This view is supported by the report of Rome and Klimov (2000), who measured rates of ATP utilization by the SR and cross-bridges in toadfish sound-producing muscle fibres.…”

The scaling of myofibrillar actomyosin ATPase activity in apid bee flight muscle in relation to hovering flight energetics

“…The rate of ATP hydrolysis was determined in glycerinated muscle fibres by a NADH-linked assay (Loxdale, 1976;Glyn and Sleep, 1985;Stienen et al, 1996;Potma and Stienen, 1996;Reggiani et al, 1997;Syme et al, 1997;Rome and Klimov, 2000) in which resynthesis of ATP utilised by the muscle fibre (Eqn 1) was coupled to the oxidation of NADH. In this assay, ADP is rephosphorylated by PEP, catalysed by PK (Eqn 2).…”

DESIGN AND FUNCTION OF SUPERFAST MUSCLES: New Insights into the Physiology of Skeletal Muscle

“…We used standard partitioning techniques (i.e., knocking out the Ca 2+ pumps as discussed in Reference 27) and also exploited the right-shifted force-pCa curve to measure SR-Ca 2+ ATP utilization directly (i.e., at pCa below which force generation starts) to partition and measure directly the rate of ATP usage by the cross-bridges and SR-Ca 2+ pumps (28). The means by which the swimbladder achieves the superfast g needed for rapid relaxation with a modest ATP utilization per myosin head can be understood by the mechanism described above: The swimbladder muscle has very few attached cross-bridges at any one time [=f/(f + g)]; thus the cross-bridge cycling rate (ATPase = number of attached bridges * g) is modest.…”