Effects of temperature acclimation on muscle relaxation in the carp: A mechanical, biochemical, and ultrastructural study

Abstract

Common carp (Cyprinus carpio L.) were acclimated to either 5-8°C or 20-25°C for a minimum of 1 month, and the twitch contraction kinetics of a myotomal nerve-muscle preparation were investigated. A significant compensation for the acute effects of temperature was achieved in twitch kinetics by acclimation to 8°C. An acute drop in temperature from 20 to 8°C in preparations from warm-acclimated fish led to approximately two-to three-fold increases in the half-times for activation and relaxation. At 8"C, values were 50% faster in 8°C-than in 20°C-acclimated fish, indicating a partial capacity adaptation in rates of both twitch activation and relaxation.The mechanisms underlying temperature compensation of twitch contraction kinetics were investigated. A quantitative ultrastructural study was performed on the sarcoplasmic reticulum (S.R.) of fast and slow myotomal muscles. No differences were found in the surface and volume densities of the S.R. in fast-twitch fibres between cold-and warm-acclimated fish. The surface densities of terminal cisternae and S.R. were higher in slow-twitch fibres from the warmacclimated fish. Parvalbumin concentration in fast fibres was found to be independent of acclimation temperature (0.61-0.68 mmolikg wet weight). Although the relative proportions of parvalbumin isoforms (I-IV) showed considerable individual variation this was not correlated with environmental temperature. The Ca" -ATPase activity of S.R.-enriched microsomes prepared from fast myotomal muscle was 60% higher a t 8°C in cold-than warm-acclimated carp. This suggests that changes in the kinetics and/or density of Ca2+ pumps contribute to the observed capacity adaptation in relaxation rate with temperature acclimation. Other possible mechanisms underlying the plasticity of twitch contraction kinetics in carp are briefly discussed.

How well do muscle biomechanics predict whole-animal locomotor performance? The role of Ca2+ handling

“…Ca 2+ handling dynamics within the muscle cell are one of the most (Berchtold et al, 2000). Differences in expression and activity of the Ca 2+ release channels dihydropyridine receptor (DHPR) and ryanodine receptor (RyR), and Ca 2+ re-sequestration by sarco(endo)plasmic reticulum ATPase (SERCA) can affect power output and fatigue resistance of isolated muscle (Fleming et al, 1990;Syme and Tonks, 2004;James et al, 2011). However, the impact of these molecules on whole-animal performance remains unresolved, although the increase in densities of DHPR and RyR with endurance training in some fish (Antilla et al, 2006) indicates that these molecules are important for whole-animal locomotion.…”

Environment and plasticity of myogenesis in teleost fish

“…These species show a classical trade-off in swimming performance between seasonal high and low temperatures with acclimatization (Fry and Hart, 1948;Johnson and Bennett, 1995), involving changes in myofibrillar ATPase activity (Johnston et al, 1975a;Johnson and Bennett, 1995), muscle shorting speed (Johnston et al, 1985), twitch duration (Fleming et al, 1990) and power output (Wakeling et al, 2000). Microarray studies indicate hundreds of protein targets (Gracey et al, 2004), including the class II myosins (Imai et al, 1997 isoforms being expressed at some acclimation temperatures, but not others (Nihei et al, 2006).…”

Variation in expression of calcium-handling proteins is associated with inter-individual differences in mechanical performance of rat (Rattus norvegicus) skeletal muscle

“…An increased density of dihydropyridine and ryanodine receptors in muscle is correlated with increased shortening velocity and force in isolated muscle (Kandarian et al, 1992;Golden et al, 2003;Mänttäri and Järvilehto, 2005), and their density is increased following endurance training in trout (Anttila et al, 2008). SERCA is responsible for calcium reuptake from the cytoplasm to the sarcoplasmic reticulum, and its activity can therefore determine muscle relaxation rate (Fleming et al, 1990;Wilson et al, 1998). SERCA activity is regulated by phosphorylation of phospholamban, which in its unphosphorylated form inhibits SERCA activity (Verboomen et al, 1992;Periasamy and Kalyanasundaram, 2007).…”