Ultrastructure of the sarcoplasmic reticulum in cardiac myocytes from Pacific bluefin tuna

Abstract

Pacific bluefin tuna are active teleost fish with a large capacity for heat conservation and endothermy. They have a high metabolism, and hence the myocardium must be capable of sustaining elevated levels of cardiac output over a wide range of temperatures. To examine the way that the myocardial cells of bluefin tuna respond to their unique cardiac physiology, we have studied the ultrastructure of the internal membrane system and mitochondria of atrial and ventricular myocytes by light and electron microscopy. Our results reveal that cardiomyocytes of juvenile bluefin tuna posses a relatively high content of sarcoplasmic reticulum (SR), together with a large volume of mitochondria within the two (compact and spongy) ventricular compartments and in the atrial myocardium. The mitochondrial structure and distribution in bluefin tuna myocardium follow specific metabolic zonation resulting in a higher volume and lower cristae density in the compact ventricular layer than in atrium and spongy layer. The presence of junctional SR profiles and an extensive network of free SR within cells may ensure a rapid delivery of Ca(2+) to the myofibrils. This, in conjunction with transarcolemmal Ca(2+) entry, might contribute to a faster excitation-contraction-relaxation cycle and thus enhance cardiac performance, cardiac output, and the maintenance of excitability at low temperatures. We propose that the mitochondrial configuration together with the developed SR ultrastructure of bluefin tunas myocardium are important evolutionary steps for the maintenance of high heart rates and endothermy in this teleost fish.

Warm fish with cold hearts: thermal plasticity of excitation–contraction coupling in bluefin tuna

“…[33]). Our functional model is supported by morphological evidence for Ca 2þ -induced Ca 2þ -release in bluefin tuna myocytes [19], recent electrophysiological studies [21,34], and biochemical studies on isolated SR vesicles [17,18].…”

“…However, isolated tissue studies have revealed that elevated cardiac performance in fishes is associated with increased use of SR Ca 2þ cycling [9,11 -16]. Biochemical studies with isolated SR vesicles clearly show that bluefin tuna have more SR Ca 2þ ATPase (SERCA) than their warmer sister taxa [17,18] and structural studies demonstrate that an extensive SR is present in bluefin tuna hearts [19]. However, to date, only one study [20] has directly investigated the physiological role of SR Ca 2þ during e -c coupling in fish heart, and this study did not examine the effect of temperature.…”

Phospholamban S-nitrosylation modulates Starling response in fish heart

“…This mechanism, which involves membrane caveolae (regarding their occurrence in fish heart, see Di Maio & Block 2008) and cytoskeleton , causes a sustained increase in enzyme activity, probably by reducing the dissociation of calmodulin from activated eNOS (McCabe et al 2000), thus enhancing NO production. To verify our hypothesis, i.e.…”

“…In the teleost heart, the presence of caveolae, junctional SR profiles and the network of free SR has been described in detail by Di Maio & Block (2008). It is known that the serinethreonine kinase Akt phosphorylates eNOS in vitro as well as in vivo (Dimmeler et al 1999), thereby causing a sustained increase in the enzyme activity (McCabe et al 2000).…”

“…This elevated sensitivity of the fish hearts to the Starling response, well documented in both temperate eurytherm and cold-adapted teleosts (gilthead seabream, Icardo et al 2005;eel, Imbrogno et al 2001;icefish, Tota et al 1991), has been in part attributed to a greater myocardial extensibility of the highly trabeculate fish heart, coupled to a maintained increase in myofilament Ca 2þ sensitivity over a large range of sarcomere lengths (Di Maio & Block 2008;Shiels & White 2008).…”