Cold acclimation increases cardiac myofilament function and ventricular pressure generation in trout

Abstract

Reducing temperature below the optimum of most vertebrate hearts impairs contractility and reduces organ function. However, a number of fish species, including the rainbow trout, can seasonally acclimate to low temperature. Such ability requires modification of physiological systems to compensate for the thermodynamic effects of temperature on biological processes. The current study tested the hypothesis that rainbow trout compensate for the direct effect of cold temperature by increasing cardiac contractility during cold acclimation. We examined cardiac contractility, following thermal acclimation (4, 11 and 17°C), by measuring the Ca 2+ sensitivity of force generation by chemically skinned cardiac trabeculae as well as ventricular pressure generation using a modified Langendorff preparation. We demonstrate, for the first time, that the Ca 2+ sensitivity of force generation was significantly higher in cardiac trabeculae from 4°C-acclimated trout compared with those acclimated to 11 or 17°C, and that this functional change occurred in parallel with a decrease in the level of cardiac troponin T phosphorylation. In addition, we show that the magnitude and rate of ventricular pressure generation was greater in hearts from trout acclimated to 4°C compared with those from animals acclimated to 11 or 17°C. Taken together, these results suggest that enhanced myofilament function, caused by modification of existing contractile proteins, is at least partially responsible for the observed increase in pressure generation after acclimation to 4°C. In addition, by examining the phenotypic plasticity of a comparative model we have identified a strategy, used in vivo, by which the force-generating capacity of cardiac muscle can be increased.

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

“…The fish heart remodels with seasonal temperature change [23, 36, 39, 40, 11, 13, 19, 43, 42, 30]. Here, we focused on the passive properties of the rainbow trout atrium across multiple levels of biological organisation following chronic cooling and warming.…”

Transforming growth factor beta-1 (TGF-β1) stimulates collagen synthesis in cultured rainbow trout cardiac fibroblasts

“…It is thought that these changes help to compensate for the effects of temperature on the heart's capacity to support the oxygen requirements of the animal. For example, Klaiman et al (2014) demonstrated that the magnitude and rate of ventricular pressure generation was greater in hearts from trout acclimated to 4°C than in those from animals acclimated to 11 or 17°C. In addition, cold acclimation has been demonstrated to cause cardiac hypertrophy and to increase cardiac connective tissue, while warm acclimation causes the opposite response (Keen et al, 2017;Klaiman et al, 2011).…”

Calcium response of KCl-excited populations of ventricular myocytes from the European sea bass (Dicentrarchus labrax): a promising approach to integrate cell-to-cell heterogeneity in studying the cellular basis of fish cardiac performance

“…These seemingly inconsistent observations must, however, be considered carefully as Farrell et al (1996) investigated the integrated response of in situ perfused heart preparations while our own experiment targeted a single cellular mechanism i.e., intracellular Ca 2+ mobilization. The possibility cannot be excluded that acclimation conditions influence other components of the contractile machinery such as the Ca 2+ sensitivity of force generation, the rate of cardiac actomyosin ATPase or the phosphorylation of cardiac troponins (Klaiman et al 2014), resulting in a different integrated response.…”