Temperature-induced cardiac remodelling in fish

Abstract

Thermal acclimation causes the heart of some fish species to undergo significant remodelling. This includes changes in electrical activity, energy utilization and structural properties at the gross and molecular level of organization. The purpose of this Review is to summarize the current state of knowledge of temperature-induced structural remodelling in the fish ventricle across different levels of biological organization, and to examine how such changes result in the modification of the functional properties of the heart. The structural remodelling response is thought to be responsible for changes in cardiac stiffness, the Ca²⁺ sensitivity of force generation and the rate of force generation by the heart. Such changes to both active and passive properties help to compensate for the loss of cardiac function caused by a decrease in physiological temperature. Hence, temperature-induced cardiac remodelling is common in fish that remain active following seasonal decreases in temperature. This Review is organized around the ventricular phases of the cardiac cycle - specifically diastolic filling, isovolumic pressure generation and ejection - so that the consequences of remodelling can be fully described. We also compare the thermal acclimation-associated modifications of the fish ventricle with those seen in the mammalian ventricle in response to cardiac pathologies and exercise. Finally, we consider how the plasticity of the fish heart may be relevant to survival in a climate change context, where seasonal temperature changes could become more extreme and variable.

Keywords: Cardiac function; Cardiac histology; Cardiac remodelling; Connective tissue; Thermal acclimation.

Fig. 1.

Ca²⁺ sensitivity of force generation by skinned ventricular fibres over a range of temperatures. pCa₅₀ is the Ca²⁺ concentration required to generate half-maximum force. When compared at the same temperature, trout ventricular fibres require 10 times less Ca²⁺ than those from the rat to generate the same amount of force. Figure adapted from Churcott et al. (1994).

Fig. 2.

Trans-sarcolemmal Ca²⁺ flux varies in trout cardiac myocytes with acute temperature changes. Acute reductions in temperature reduce Ca²⁺ flux through L-type Ca²⁺ channels in rainbow trout atrial myocytes. All values are means±s.e.m. The values for I_Ca (pA) are normalized from the measured cell capacitance to give the value in pA pF⁻¹. Figure adapted from Shiels et al. (2000).

Fig. 3.

Thermal remodelling of ventricular compliance in the rainbow trout. Ex vivo pressure–volume relationships show increased passive stiffness of the whole ventricle following cold acclimation (5°C) compared with controls (10°C), and increased compliance following warm acclimation (18°C). Data points show the means±s.e. All lines are significantly different from each other, assessed via GLM. Figure is adapted from Keen et al. (2016).

Fig. 4.

Thermal remodelling of ventricular collagen in rainbow trout and zebrafish. Representative bright-field (left) and polarised-light (right) micrographs of control (A) rainbow trout and (B) zebrafish ventricular tissue sections stained with PicroSirius Red, which allows semi-quantification of fibrillar collagen content. Cold acclimation causes an increase in ventricular collagen content in (C) rainbow trout, but (D) a decrease in thick collagen fibres in the zebrafish ventricle. (E) Increased ventricular collagen content in rainbow trout is associated with increased mRNA expression of collagen-promoting genes (5°C; blue), compared with control (10°C; green), whereas warm acclimation (18°C; red) is associated with an increase in mRNA expression of collagen-degrading genes. (F) Following cold acclimation, zebrafish ventricles show an increase in mRNA expression of collagen-regulatory genes, suggesting increased collagen turnover. In the zebrafish experiment fish were maintained at 27°C (Control) or acclimated to 20°C (cold). All data are means±s.e. Letters and symbols indicate significant differences. Figures modified from Johnson et al. (2014) and Keen et al. (2016). Scale bars: 100 μm.

Fig. 5.

Cardiac contractile properties of trout acclimated to 4°C, 11°C and 17°C. (A) The maximal activity of actomyosin Mg²⁺-ATPase isolated from ventricles is higher in preparations from cold-acclimated trout than those from warm-acclimated trout when measured at 17°C. (B) The Ca²⁺ sensitivity of force generation by cardiac trabeculae from trout acclimated to 4°C (blue line) is greater than that of trabeculae from trout acclimated to 11°C (black line) or 17°C (red line) when measured at 15°C. pCa₅₀ is the pCa at half-maximum force. SL, sarcomere length. (C) Developed pressures at ventricle volumes greater than baseline are higher for the 4°C acclimated (blue symbols) fish than those for the 11°C (black symbols) and 17°C (red symbols) acclimated fish. Circles indicate ventricular developed pressures, while squares indicate diastolic pressures. All data are means± s.e. Figures modified from Klaiman et al. (2011) and Klaiman et al. (2014). The images on the right of the panels are: (A) a schematic of a thick and thin filament inside a cardiac myofilament; (B) a micrograph of a trout cardiac myofilament preparation attached to a force transducer and servo motor via aluminium clips; and (C) a schematic of a trout heart.

Fig. 6.

Thermal remodelling of the rainbow trout heart. A summary of the effects of chronic cooling (5°C) and chronic warming (18°C) on the rainbow trout heart, compared with those of fish kept at control temperature (10°C). ¹Klaiman et al., 2011; ²Klaiman et al., 2014; ³Keen et al., 2016; ⁴Vornanen et al., 2005; ⁵Driedzic et al., 1996; ⁶Driedzic and Gesser, 1994.