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Ca2+ cycling in cardiomyocytes from a high-performance reptile, the varanid lizard (Varanus exanthematicus).

Galli GL, Warren DE, Shiels HA - Am. J. Physiol. Regul. Integr. Comp. Physiol. (2009)

Bottom Line: Specializations in excitation-contraction coupling may also contribute to the varanids superior cardiovascular performance.Lizard ventricular myocytes were found to be spindle-shaped, lack T-tubules, and were approximately 190 microm in length and 5-7 microm in width and depth.In aggregate, our results suggest varanids have an enhanced capacity to transport Ca(2+) through the Na(+)/Ca(2+) exchanger, and sarcoplasmic reticulum suggesting specializations in excitation-contraction coupling may provide a means to support high cardiovascular performance.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, The University of Manchester, Core Technology Facility, Manchester, United Kingdom. ggalli@interchange.ubc.ca

ABSTRACT
The varanid lizard possesses one of the largest aerobic capacities among reptiles with maximum rates of oxygen consumption that are twice that of other lizards of comparable sizes at the same temperature. To support this aerobic capacity, the varanid heart possesses morphological adaptations that allow the generation of high heart rates and blood pressures. Specializations in excitation-contraction coupling may also contribute to the varanids superior cardiovascular performance. Therefore, we investigated the electrophysiological properties of the l-type Ca(2+) channel and the Na(+)/Ca(2+) exchanger (NCX) and the contribution of the sarcoplasmic reticulum to the intracellular Ca(2+) transient (Delta[Ca(2+)](i)) in varanid lizard ventricular myocytes. Additionally, we used confocal microscopy to visualize myocytes and make morphological measurements. Lizard ventricular myocytes were found to be spindle-shaped, lack T-tubules, and were approximately 190 microm in length and 5-7 microm in width and depth. Cardiomyocytes had a small cell volume ( approximately 2 pL), leading to a large surface area-to-volume ratio (18.5), typical of ectothermic vertebrates. The voltage sensitivity of the l-type Ca(2+) channel current (I(Ca)), steady-state activation and inactivation curves, and the time taken for recovery from inactivation were also similar to those measured in other reptiles and teleosts. However, transsarcolemmal Ca(2+) influx via reverse mode Na(+)/Ca(2+) exchange current was fourfold higher than most other ectotherms. Moreover, pharmacological inhibition of the sarcoplasmic reticulum led to a 40% reduction in the Delta[Ca(2+)](i) amplitude, and slowed the time course of decay. In aggregate, our results suggest varanids have an enhanced capacity to transport Ca(2+) through the Na(+)/Ca(2+) exchanger, and sarcoplasmic reticulum suggesting specializations in excitation-contraction coupling may provide a means to support high cardiovascular performance.

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Effects of sarcoplasmic reticulum (SR) inhibitors ryanodine (10 μM) and thapsigargin (1 μM) on the intracellular Ca2+ transient (Δ[Ca2+]i) in isolated ventricular cardiomyocytes from the varanid lizard field stimulated at 0.2 Hz and room temperature. A: representative recording. B: baseline intracellular Ca2+ concentration. C: Ca2+ rise slope. D: Tau (τ), the first-order decay constant of cytosolic Ca2+ clearance during relaxation. E: amplitude of the Δ[Ca2+]i. *Statistically significant difference between controls and SR-inhibited treatments (n = 12).
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Figure 2: Effects of sarcoplasmic reticulum (SR) inhibitors ryanodine (10 μM) and thapsigargin (1 μM) on the intracellular Ca2+ transient (Δ[Ca2+]i) in isolated ventricular cardiomyocytes from the varanid lizard field stimulated at 0.2 Hz and room temperature. A: representative recording. B: baseline intracellular Ca2+ concentration. C: Ca2+ rise slope. D: Tau (τ), the first-order decay constant of cytosolic Ca2+ clearance during relaxation. E: amplitude of the Δ[Ca2+]i. *Statistically significant difference between controls and SR-inhibited treatments (n = 12).

Mentions: To determine the relative importance of the SR to Δ[Ca2+]i in varanid ventricular cardiomyocytes, Δ[Ca2+]i was measured in field-stimulated cardiomyocytes with and without SR inhibition by ryanodine (10 μmol/l) and thapsigargin (1 μmol/l) (Fig. 2A). While no effect of the drug application on baseline Δ[Ca2+]i was observed (Fig. 2B), SR inhibition significantly decreased the rate of rise of the Ca2+ transient (Fig. 2C) and its peak amplitude (Fig. 2D), the latter by 40%. The decay constant τ increased with SR inhibition (Fig. 2E).


Ca2+ cycling in cardiomyocytes from a high-performance reptile, the varanid lizard (Varanus exanthematicus).

Galli GL, Warren DE, Shiels HA - Am. J. Physiol. Regul. Integr. Comp. Physiol. (2009)

Effects of sarcoplasmic reticulum (SR) inhibitors ryanodine (10 μM) and thapsigargin (1 μM) on the intracellular Ca2+ transient (Δ[Ca2+]i) in isolated ventricular cardiomyocytes from the varanid lizard field stimulated at 0.2 Hz and room temperature. A: representative recording. B: baseline intracellular Ca2+ concentration. C: Ca2+ rise slope. D: Tau (τ), the first-order decay constant of cytosolic Ca2+ clearance during relaxation. E: amplitude of the Δ[Ca2+]i. *Statistically significant difference between controls and SR-inhibited treatments (n = 12).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2803631&req=5

Figure 2: Effects of sarcoplasmic reticulum (SR) inhibitors ryanodine (10 μM) and thapsigargin (1 μM) on the intracellular Ca2+ transient (Δ[Ca2+]i) in isolated ventricular cardiomyocytes from the varanid lizard field stimulated at 0.2 Hz and room temperature. A: representative recording. B: baseline intracellular Ca2+ concentration. C: Ca2+ rise slope. D: Tau (τ), the first-order decay constant of cytosolic Ca2+ clearance during relaxation. E: amplitude of the Δ[Ca2+]i. *Statistically significant difference between controls and SR-inhibited treatments (n = 12).
Mentions: To determine the relative importance of the SR to Δ[Ca2+]i in varanid ventricular cardiomyocytes, Δ[Ca2+]i was measured in field-stimulated cardiomyocytes with and without SR inhibition by ryanodine (10 μmol/l) and thapsigargin (1 μmol/l) (Fig. 2A). While no effect of the drug application on baseline Δ[Ca2+]i was observed (Fig. 2B), SR inhibition significantly decreased the rate of rise of the Ca2+ transient (Fig. 2C) and its peak amplitude (Fig. 2D), the latter by 40%. The decay constant τ increased with SR inhibition (Fig. 2E).

Bottom Line: Specializations in excitation-contraction coupling may also contribute to the varanids superior cardiovascular performance.Lizard ventricular myocytes were found to be spindle-shaped, lack T-tubules, and were approximately 190 microm in length and 5-7 microm in width and depth.In aggregate, our results suggest varanids have an enhanced capacity to transport Ca(2+) through the Na(+)/Ca(2+) exchanger, and sarcoplasmic reticulum suggesting specializations in excitation-contraction coupling may provide a means to support high cardiovascular performance.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, The University of Manchester, Core Technology Facility, Manchester, United Kingdom. ggalli@interchange.ubc.ca

ABSTRACT
The varanid lizard possesses one of the largest aerobic capacities among reptiles with maximum rates of oxygen consumption that are twice that of other lizards of comparable sizes at the same temperature. To support this aerobic capacity, the varanid heart possesses morphological adaptations that allow the generation of high heart rates and blood pressures. Specializations in excitation-contraction coupling may also contribute to the varanids superior cardiovascular performance. Therefore, we investigated the electrophysiological properties of the l-type Ca(2+) channel and the Na(+)/Ca(2+) exchanger (NCX) and the contribution of the sarcoplasmic reticulum to the intracellular Ca(2+) transient (Delta[Ca(2+)](i)) in varanid lizard ventricular myocytes. Additionally, we used confocal microscopy to visualize myocytes and make morphological measurements. Lizard ventricular myocytes were found to be spindle-shaped, lack T-tubules, and were approximately 190 microm in length and 5-7 microm in width and depth. Cardiomyocytes had a small cell volume ( approximately 2 pL), leading to a large surface area-to-volume ratio (18.5), typical of ectothermic vertebrates. The voltage sensitivity of the l-type Ca(2+) channel current (I(Ca)), steady-state activation and inactivation curves, and the time taken for recovery from inactivation were also similar to those measured in other reptiles and teleosts. However, transsarcolemmal Ca(2+) influx via reverse mode Na(+)/Ca(2+) exchange current was fourfold higher than most other ectotherms. Moreover, pharmacological inhibition of the sarcoplasmic reticulum led to a 40% reduction in the Delta[Ca(2+)](i) amplitude, and slowed the time course of decay. In aggregate, our results suggest varanids have an enhanced capacity to transport Ca(2+) through the Na(+)/Ca(2+) exchanger, and sarcoplasmic reticulum suggesting specializations in excitation-contraction coupling may provide a means to support high cardiovascular performance.

Show MeSH
Related in: MedlinePlus