Comparison of sarcoplasmic reticulum calcium content in atrial and ventricular myocytes of three fish species

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.

Section: +supporting

confidence: 91%

Section: G L J Galli and Othersmentioning

confidence: 99%

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

Galli

Lipnick

Shiels

et al. 2011

“…Collectively, the current evidence suggests that the relatively sluggish SR Ca 2+ handling of crucian carp ventricular myocytes is further depressed in winter. It should be noted, however, that the Ca 2+ -storing capacity of cardiac SR is strikingly large in both warm-and cold-acclimated crucian carp (Haverinen and Vornanen, 2009a), and therefore may play a significant role in intracellular Ca 2+ buffering throughout the year despite depressed Ca 2+ kinetics in winter fish. As leakage of SR Ca 2+ stores and malfunction of SR Ca 2+ cycling can be origins for several forms of cardiac arrhythmia (Volders et al, 2000;Zhao et al, 2012), the reduced intracellular Ca 2+ cycling in winter-acclimatised fish may be protective against dysfunction in the cold and oxygen-deficient conditions (see 'Avoidance of cardiac arrhythmia', below).…”

Section: Discussionmentioning

confidence: 99%

Effects of prolonged anoxia on electrical activity of the heart in Crucian carp (Carassius carassius)

Tikkanen

Haverinen

Egginton

et al. 2016

Self Cite

The effects of sustained anoxia on cardiac electrical excitability were examined in the anoxia-tolerant crucian carp (Carassius carassius). The electrocardiogram (ECG) and expression of excitationcontraction coupling genes were studied in fish acclimatised to normoxia in summer (+18°C) or winter (+2°C), and in winter fish after 1, 3 and 6 weeks of anoxia. Anoxia induced a sustained bradycardia from a heart rate of 10.3±0.77 beats min −1 to 4.1±0.29 beats min −1 (P<0.05) after 5 weeks, and heart rate slowly recovered to control levels when oxygen was restored. Heart rate variability greatly increased under anoxia, and completely recovered under reoxygenation. The RT interval increased from 2.8±0.34 s in normoxia to 5.8±0.44 s under anoxia (P<0.05), which reflects a doubling of the ventricular action potential (AP) duration. Acclimatisation to winter induced extensive changes in gene expression relative to summer-acclimatised fish, including depression in those genes coding for the sarcoplasmic reticulum calcium pump (Serca2a_q2) and ATP-sensitive K + channels (Kir6.2) (P<0.05). Genes of delayed rectifier K + (kcnh6) and Ca 2+ channels (cacna1c) were up-regulated in winter fish (P<0.05). In contrast, the additional challenge of anoxia caused only minor changes in gene expression, e.g. depressed expression of Kir2.2b K + channel gene (kcnj12b), whereas expression of Ca 2+ (cacna1a, cacna1c and cacna1g) and Na + channel genes (scn4a and scn5a) was not affected. These data suggest that low temperature pre-conditions the crucian carp heart for winter anoxia, whereas sustained anoxic bradycardia and prolongation of AP duration are directly induced by oxygen shortage without major changes in gene expression.

“…Consistent with this, cell-type-specific differences in SR Ca 2+ uptake rate have been detected in intact atrial and ventricular myocytes of the fish heart. In voltage-clamped myocytes of rainbow trout and burbot (Lota lota) hearts, the rate of caffeine-sensitive Ca 2+ uptake was 60-80% faster in atrial than ventricular myocytes (Haverinen and Vornanen, 2009a). Similar to the chamber-related differences, the faster kinetics of contraction following cold acclimation can be partially attributed to the coldinduced enhancement of SR function, which is expressed as faster rate of SR Ca 2+ uptake in crude homogenates of the trout heart (Aho and Vornanen, 1998;Aho and Vornanen, 1999).…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, temperature has no effect on the expression of RyR (Tiitu and Vornanen, 2003), nor are there any chamberrelated differences in RyR expression of the trout heart (Birkedal et al, 2009). Similarly, the amount of main SR luminal Ca 2+ store protein, calsequestrin (Korajoki and Vornanen, 2009), and the size of the SR Ca 2+ stores of the rainbow trout atrial and ventricular myocytes remain unaltered in thermal acclimation (Haverinen and Vornanen, 2009a). Evidently, expression level and activity of the SERCA pump are the main means to produce chamber-and temperature-specific changes in the rate of Ca 2+ cycling through the fish cardiac SR.…”

Section: Physiological Significance Of Serca Expressionmentioning

confidence: 93%

Expression of SERCA and phospholamban in rainbow trout (Oncorhynchus mykiss) heart: comparison of atrial and ventricular tissue and effects of thermal acclimation

Korajoki

Vornanen

2012

Self Cite

2+uptake in cardiac homogenates of the cold-acclimated (CA) trout (Aho and Vornanen, 1998;Aho and Vornanen, 1999). These findings strongly suggest that temperature-induced changes in cardiac contractility in the CA trout are partly due to increases in the activity of the SR Ca 2+ pump. However, the molecular basis of these changes is still poorly elucidated.The interplay between cardiac SERCA2 and phospholamban (PLN) is crucial for Ca 2+ cycling through the SR and therefore for Accepted 5 December 2011 SUMMARY In the heart of rainbow trout (Oncorhynchus mykiss), the rate of contraction and Ca 2+ uptake into the sarcoplasmic reticulum (SR) are faster in atrial than ventricular muscle, and contraction force relies more on SR Ca 2+ stores after acclimation to cold. This study tested the hypothesis that differences in contractile properties and Ca 2+ regulation between atrial and ventricular muscle, and between warm-(WA) and cold-acclimated (CA) trout hearts, are associated with differences in expression of sarco(endo)plasmic reticulum Ca 2+ ATPase (SERCA) and/or phospholamban (PLN), an inhibitor of the cardiac SERCA. Quantitative PCR (SERCA only) and antibodies raised against SERCA and PLN were used to determine abundances of SERCA2 transcripts and SERCA and PLN proteins, respectively, in atrium and ventricle of trout acclimated to cold (+4°C, CA) and warm (+18°C, WA) temperatures. Expression of SERCA2 transcripts was 1.6 and 2.1 times higher in atrium than ventricle of WA and CA trout, respectively (P<0.05). At the protein level, differences in SERCA expression between atrium and ventricle were 6.1-and 23-fold for WA and CA trout, respectively (P<0.001). Acclimation to cold increased SERCA2 transcripts 2.6-and 2.0-fold in atrial and ventricular muscle, respectively (P<0.05). At the protein level, cold-induced elevation of SERCA (4.6-fold) was noted only in atrial (P<0.05) but not in ventricular tissue (P>0.05). The expression pattern of PLN was similar to that of the SERCA protein, but chamber-specific and temperature-induced differences were much smaller than in the case of SERCA. In the ventricle, PLN/SERCA ratio was 2.1 and 7.0 times higher than in the atrium for WA and CA fish, respectively. These findings are consistent with the hypothesis that low PLN/SERCA ratio in atrial tissue enables faster SR Ca 2+ reuptake and thus contributes to faster kinetics of contraction in comparison with ventricular muscle. Similarly, cold-induced decrease in PLN/SERCA ratio may be associated with faster contraction kinetics of the CA trout heart, in particular in the atrial muscle.