Energy metabolism and contractility in ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature

Driedzic, William R.; Gesser, H.

doi:10.1152/physrev.1994.74.1.221

Cited by 215 publications

(127 citation statements)

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“…As a consequence, animals display a large variation in cardiac function according to the mode of life and the activity level (Costa et al, 2008). The ability of the cardiac muscle to maintain pump performance under different physiological conditions is one of the most important characteristics that enable vertebrates to survive under adverse conditions (Driedzic and Gesser, 1994). Consequently, efficient adjustments of cardiac output in response to xenobiotics, achieved by changes in stroke volume and/or heart rate are crucial.…”

Section: Discussionmentioning

confidence: 99%

Effects of the organophosphorus pesticide Folisuper 600 (methyl parathion) on the heart function of bullfrog tadpoles, Lithobates catesbeianus (Shaw, 1802)

et al. 2015

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The aim of this work was to evaluate whether the heart function of bullfrog tadpoles (25 Gosner stage) is affected by their acute exposure (48 h) to a sub-lethal concentration (10 µg.L -1 ) of the active principle of the organophosphorus pesticide Folisuper 600R (methyl parathion -MP). Our results demonstrated that MP causes not only a reduction in tadpoles' cardiac ventricular mass, resulting in a marked reduction in their cardiac twitch force, but also impairs their swimming performance, irrespective of increasing their heart rate. Together, these findings indicate that low and realistic concentration of MP have a negative impact on tadpoles' performance, jeopardizing their survival. Keywords: methyl parathion, cardiac performance, bullfrog tadpoles, Lithobates catesbeianus (Rana catesbeiana).Efeitos do pesticida organofosforado Folisuper 600 (metil paration) sobre a função cardíaca de girinos de rã-touro, Lithobates catesbeianus (Shaw, 1802) ResumoO objetivo do presente estudo foi avaliar se a função cardíaca de girinos de rãs-touro (estágio 25 de Gosner) é afetada pela exposição aguda (48h) a uma concentração sub-letal (10 µg.L -1 ) do princípio ativo do pesticida organofosforado Folisuper 600R (metil paration -MP). Nossos resultados demonstraram que o MP ocasionou não apenas uma redução na massa ventricular cardíaca dos girinos, como também provocou uma redução na sua força de contração cardíaca e de seu desempenho natatório, a despeito de ter sido observado um aumento de sua freqüência cardíaca. Conjuntamente, os achados aqui obtidos indicam que uma baixa e realística concentração de MP exerce um impacto negativo sobre o desempenho dos girinos, ameaçando sua sobrevivência.Palavras-chave: metil paration, desempenho cardíaco, girinos de rã-touro, Lithobates catesbeianus (Rana Catesbeiana).

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Section: Discussionmentioning

confidence: 99%

Effects of the organophosphorus pesticide Folisuper 600 (methyl parathion) on the heart function of bullfrog tadpoles, Lithobates catesbeianus (Shaw, 1802)

et al. 2015

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“…Adjustments in mitochondrial properties and capacities are crucial for acclimation to the cold in some fishes as are increases in cardiac glycogen storage [47]. These data suggest that remodelling in cellular energetics may accompany the remodelling in cellular Ca 2þ flux in the bluefin tuna heart.…”

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confidence: 87%

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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“…However, the myocytes of cold-adapted fish developed adaptive mechanisms that lead to a relative temperature-insensitivity of sarcolemmal Ca 2+ -transporting systems (particularly L-channels and NCX), maximizing the proportional contribution of transarcolemmal Ca 2+ fluxes to the relaxation/contraction cycle Xue et al, 1999;Kim et al, 2000;Shiels et al, 2000;Elias et al, 2001). This allows Ca 2+ to be delivered to myosin at a rate and magnitude compatible with the low heart rates observed in cold-adapted fish (Farrell & Jones, 1992;Driedzic & Gesser, 1994;Lillywhite et al, 1999), assuring their survival in temperatures considered cardioplegic to endotherms, even without the direct participation of the SR in Ca 2+ management. In contrast, in very active temperate teleosts, as well as in tropical fish, which present considerably higher heart rates, a more direct participation of the SR in the E-C coupling in order to reduce the diffusion distances is predictable.…”

Section: Discussionmentioning

confidence: 99%

“…Although present, the role of the SR in the beat-to-beat regulation of contractions of the teleost heart requires further definition, as ryanodine, which impedes SR function, has a negative impact only at rates below the physiological range of frequencies in most species (Driedzic & Gesser, 1994). Ryanodine is a plant alkaloid that binds specifically and irreversibly to SR Ca 2+ -release channels, thereby reducing the functional importance of SR for the excitation-contraction (E-C) coupling (Nayler et al, 1970;Rousseau et al, 1987;Coronado et al, 1994;Bers, 2001).…”

Section: Introductionmentioning

confidence: 99%

Differences in Ca2+-management between the ventricle of two species of neotropical teleosts: the jeju, Hoplerythrinus unitaeniatus (Spix & Agassiz, 1829), and the acara, Geophagus brasiliensis (Quoy & Gaimard, 1824)

2009

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This study analyzed the physiological role of the cardiac sarcoplasmic reticulum (SR) of two neotropical teleosts, the jeju, Hoplerythrinus unitaeniatus (Erythrinidae), and the acara, Geophagus brasiliensis (Cichlidae). While the in vivo heart frequency (f H -bpm) of acara (79.6 ± 6.6) was higher than that of the jeju (50.3 ± 2.7), the opposite was observed for the ventricular inotropism (Fc -mN/mm 2 ) at 12 bpm (acara = 28.66 ± 1.86 vs. jeju = 36.09 ± 1.67). A 5 min diastolic pause resulted in a strong potentiation of Fc (≅ 90%) of strips from jeju, which was completely abolished by ryanodine. Ryanodine also resulted in a ≅ 20% decrease in the Fc developed by strips from jeju at both subphysiological (12 bpm) and physiological (in vivo) frequencies. However, this effect of ryanodine reducing the Fc from jeju was completely compensated by adrenaline increments (10 -9 and 10 -6 M). In contrast, strips from acara were irresponsive to ryanodine, irrespective of the stimulation frequency, and increases in adrenaline concentration (to 10 -9 and 10 -6 M) further increased Fc. These results reinforce the hypothesis of the functionality of the SR as a common trait in neotropical ostariophysian (as jeju), while in acanthopterygians (as acara) it seems to be functional mainly in 'athletic' species.

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Energy metabolism and contractility in ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature

Cited by 215 publications

References 0 publications

Effects of the organophosphorus pesticide Folisuper 600 (methyl parathion) on the heart function of bullfrog tadpoles, Lithobates catesbeianus (Shaw, 1802)

Effects of the organophosphorus pesticide Folisuper 600 (methyl parathion) on the heart function of bullfrog tadpoles, Lithobates catesbeianus (Shaw, 1802)

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

Differences in Ca2+-management between the ventricle of two species of neotropical teleosts: the jeju, Hoplerythrinus unitaeniatus (Spix & Agassiz, 1829), and the acara, Geophagus brasiliensis (Quoy & Gaimard, 1824)

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