Elevated Ca2+ ATPase (SERCA2) activity in tuna hearts: Comparative aspects of temperature dependence

Castilho, Pedro C.; Landeira-Fernandez, Ana M.; Morrissette, Jeffery M.; Block, Barbara A.

doi:10.1016/j.cbpa.2007.03.033

Cited by 29 publications

(40 citation statements)

References 53 publications

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“…[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].…”

Section: Discussionsupporting

confidence: 66%

“…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.…”

Section: Introductionmentioning

confidence: 99%

“…Q 10 ) effects on the ion channels and pumps that underlie the cardiac action potential [21,22] and that cycle Ca 2þ during e-c coupling (e.g. I Ca : [22,23,24]; ryanodine receptor: [25][26][27]; SERCA: [17,18,26]; Na þ -Ca 2þ exchanger: [28]). In an attempt to compensate for the direct effects of temperature on e-c coupling pathways, some animals adjust their phenotype during chronic temperature exposure.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2010

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Bluefin tuna have a unique physiology. Elevated metabolic rates coupled with heat exchangers enable bluefin tunas to conserve heat in their locomotory muscle, viscera, eyes and brain, yet their hearts operate at ambient water temperature. This arrangement of a warm fish with a cold heart is unique among vertebrates and can result in a reduction in cardiac function in the cold despite the elevated metabolic demands of endothermic tissues. In this study, we used laser scanning confocal microscopy and electron microscopy to investigate how acute and chronic temperature change affects tuna cardiac function. We examined the temporal and spatial properties of the intracellular Ca ] i , indicating that temperature change limits cardiac myocyte performance. Importantly, we show that thermal acclimation offered partial compensation for these direct effects of temperature. Prolonged cold exposure (more than four weeks) increased the amplitude and kinetics of D[Ca 2þ ] i by increasing intracellular Ca 2þ cycling through the sarcoplasmic reticulum (SR). These functional findings are supported by electron microscopy, which revealed a greater volume fraction of ventricular SR in cold-acclimated tuna myocytes. The results indicate that SR function is crucial to the performance of the bluefin tuna heart in the cold. We suggest that SR Ca 2þ cycling is the malleable unit of cellular Ca 2þ flux, offering a mechanism for thermal plasticity in fish hearts. These findings have implications beyond endothermic fish and may help to delineate the key steps required to protect vertebrate cardiac function in the cold.

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Section: Discussionsupporting

confidence: 66%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2010

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“…In the fish heart, both the presence of PLN in myocyte SR and the role of PLN phosphorylation in SERCA2a activation have been reported (Will et al 1985;Castilho et al 2007), but the role of PLN S-nitrosylation in the pump activation is heretofore completely unknown. As in mammals, also in fish, the amino acid sequence of PLN (see GenBank accession numbers for zebrafish: XM_701636.1 and puffer fish: CAG06667, DeWitt et al 2006) includes cysteine residues, which are a potential target for S-nitrosylation.…”

Section: Discussionmentioning

confidence: 99%

Phospholamban S-nitrosylation modulates Starling response in fish heart

et al. 2009

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The Frank -Starling mechanism is a fundamental property of the vertebrate heart, which allows the myocardium to respond to increased filling pressure with a more vigorous contraction of its lengthened fibres. In mammals, myocardial stretch increases cardiac nitric oxide (NO) release from both vascular endothelium and cardiomyocytes. This facilitates myocardial relaxation and ventricular diastolic distensibility, thus influencing the Frank -Starling mechanism.In the in vitro working heart of the eel Anguilla anguilla, we previously showed that an endogenous NO release affects the Frank -Starling response making the heart more sensitive to preload. Using the same bioassay, we now demonstrate that this effect is confirmed in the presence of the exogenous NO donor S-nitroso-N-acetyl penicillamine, is independent from endocardial endothelium and guanylate cyclase/ cGMP/protein kinase G and cAMP/protein kinase A pathways, involves a PI(3)kinase-mediated activation of endothelial NO synthase and a modulation of the SR-CA 2þ ATPase (SERCA2a) pumps. Furthermore, we show that NO influences cardiac response to preload through S-nitrosylation of phospholamban and consequent activation of SERCA2a. This suggests that in the fish heart NO modulates the Frank -Starling response through a beat-to-beat regulation of calcium reuptake and thus of myocardial relaxation.We propose that this mechanism represents an important evolutionary step for the stretch-induced intrinsic regulation of the vertebrate heart, providing, at the same time, a stimulus for mammalian-oriented studies.

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“…With regards to scombrids, recent physiological and electron microscopy work has demonstrated that the bluefin ventricle and atrium, the bigeye tuna ventricle and the yellowfin tuna atrium have evolved a more advanced 'mammalian-like' form of E-C coupling, with a significant proportion (40-50%) of activator Ca 2+ used for contraction originating in the SR (DiMaio and Block, 2008;Galli et al, 2008;Shiels et al, 1999;Shiels et al, 2011). Furthermore, biochemical studies indicate bluefin tuna have increased SR Ca 2+ ATPase (SERCA-2) activity and expression over a range of temperatures when compared with other scombrids Castilho et al, 2007). Lastly, Ca 2+ entry through the L-type Ca 2+ channel is greater and inactivation kinetics are faster in atrial myocytes of bluefin tuna than of Pacific mackerel (Shiels et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Temperature effects on Ca2+ cycling in scombrid cardiomyocytes: a phylogenetic comparison

Galli

Lipnick

Shiels

et al. 2011

Journal of Experimental Biology

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SUMMARYSpecialisations in excitation-contraction coupling may have played an important role in the evolution of endothermy and high cardiac performance in scombrid fishes. We examined aspects of Ca 2+ handling in cardiomyocytes from Pacific bonito (Sarda chiliensis), Pacific mackerel (Scomber japonicus), yellowfin tuna (Thunnus albacares) and Pacific bluefin tuna (Thunnus orientalis). The whole-cell voltage-clamp technique was used to measure the temperature sensitivity of the L-type Ca 2+ channel current (I Ca ), density, and steady-state and maximal sarcoplasmic reticulum (SR) Ca 2+ content (ssSR load and maxSR load ). Current-voltage relations, peak I Ca density and charge density of I Ca were greatest in mackerel and yellowfin at all temperatures tested. I Ca density and kinetics were temperature sensitive in all species studied, and the magnitude of this response was not related to the thermal preference of the species. SR load was greater in atrial than in ventricular myocytes in the Pacific bluefin tuna, and in species that are more cold tolerant (bluefin tuna and mackerel). I Ca and SR load were particularly small in bonito, suggesting the Na + /Ca 2+ exchanger plays a more pivotal role in Ca 2+ entry into cardiomyocytes of this species. Our comparative approach reveals that the SR of cold-tolerant scombrid fishes has a greater capacity for Ca 2+ storage. This specialisation may contribute to the temperature tolerance and thermal niche expansion of the bluefin tuna and mackerel.

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Elevated Ca2+ ATPase (SERCA2) activity in tuna hearts: Comparative aspects of temperature dependence

Cited by 29 publications

References 53 publications

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

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

Phospholamban S-nitrosylation modulates Starling response in fish heart

Temperature effects on Ca2+ cycling in scombrid cardiomyocytes: a phylogenetic comparison

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