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Cardiac contractility of the African sharptooth catfish, Clarias gariepinus: role of extracellular Ca2+, sarcoplasmic reticulum, and β-adrenergic stimulation

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Abstract

This study investigated the dependence of contraction from extracellular Ca2+, the presence of a functional sarcoplasmic reticulum (SR), and the effects of β-adrenergic stimulation using isometric cardiac muscle preparations. Moreover, the expression of Ca2+-handling proteins such as SR-Ca2+-ATPase (SERCA), phospholamban (PLN), and Na+/Ca2+ exchanger (NCX) were also evaluated in the ventricular tissue of adult African sharptooth catfish, Clarias gariepinus, a facultative air-breathing fish. In summary, we observed that (1) contractility was strongly regulated by extracellular Ca2+; (2) inhibition of SR Ca2+-release by application of ryanodine reduced steady-state force production; (3) ventricular myocardium exhibited clear post-rest decay, even in the presence of ryanodine, indicating a decrease in SR Ca2+ content and NCX as the main pathway for Ca2+ extrusion; (4) a positive force-frequency relationship was observed above 60 bpm (1.0 Hz); (5) ventricular tissue was responsive to β-adrenergic stimulation, which caused significant increases in twitch force, kept a linear force-frequency relationship from 12 to 96 bpm (0.2 to Hz), and improved the cardiac pumping capacity (CPC); and (6) African catfish myocardium exhibited similar expression patterns of NCX, SERCA, and PLN, corroborating our findings that both mechanisms for Ca2+ transport across the SR and sarcolemma contribute to Ca2+ activator. In conclusion, this fish species displays great physiological plasticity of E-C coupling, able to improve the ability to maintain cardiac performance under physiological conditions to ecological and/or adverse environmental conditions, such as hypoxic air-breathing activity.

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Acknowledgements

The authors are grateful to the Polletini Fish Farm, which provided the fish. They are also grateful to Mr. Angelo Carnelosi for the technical assistance.

Funding

This study was supported by FAPESP (São Paulo Research Foundation – N.U.J. Scientific Initiation Fellowship, Grant Number 11/07645-1), CAPES (Coordination for the Improvement of Higher Education Personnel - A.G.L. and E.S.V. Doctoral Fellowships), and INCT-FisComp (National Institute of Science and Technology in Comparative Physiology - Grant Numbers CNPq 573921/2008-3, FAPESP 08/57712-4).

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Authors and Affiliations

  1. Department of Physiological Sciences, Federal University of São Carlos (UFSCar), Via Washington Luís km 235, 13565-905 São Carlos, São Paulo, Brazil

    Diana Amaral Monteiro, André Guelli Lopes, Nathalia Usun Jejcic, Eliton da Silva Vasconcelos, Ana Lúcia Kalinin & Francisco Tadeu Rantin

  2. Joint Graduate Program in Physiological Sciences, Federal University of São Carlos – UFSCar/São Paulo State University, UNESP Campus Araraquara, São Paulo, Brazil

    André Guelli Lopes & Eliton da Silva Vasconcelos

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  1. Diana Amaral Monteiro
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Contributions

A.G.L. and N.U.J.: performed the experiment and collected the data, analyzed and interpreted the data, writing—original draft preparation. D.A.M.: analyzed and interpreted the data, writing—original draft preparation, writing—reviewing and editing, and conceptualization. A.L.K.: conceptualization, funding acquisition. F.T.R.: supervised the research and critically revised the final version of the manuscript, funding acquisition. All authors provided intellectual feedback on the manuscript and approved its final version.

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Correspondence to Diana Amaral Monteiro.

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Monteiro, D.A., Lopes, A.G., Jejcic, N.U. et al. Cardiac contractility of the African sharptooth catfish, Clarias gariepinus: role of extracellular Ca2+, sarcoplasmic reticulum, and β-adrenergic stimulation. Fish Physiol Biochem 47, 1969–1982 (2021). https://doi.org/10.1007/s10695-021-01023-7

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