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Taurine depresses cardiac contractility and enhances systemic heart glucose utilization in the cuttlefish, Sepia officinalis

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Abstract

Taurine is the most abundant amino acid in the blood of the cuttlefish, Sepia officinalis, where levels can exceed 200 mmol L−1. In mammals, intracellular taurine modulates cardiac Ca2+ handling and carbohydrate metabolism at much lower concentrations but it is not clear if it exerts similar actions in cephalopods. Blood Ca2+ levels are high in cephalopods and we hypothesized that taurine would depress cardiac Ca2+ flux and modulate contractility in systemic and branchial hearts of cuttlefish. Heart performance was assessed with an in situ perfused systemic heart preparation and contractility was evaluated using isometrically contracting systemic and branchial heart muscle rings. Stroke volume, cardiac output, and Ca2+ sensitivity were significantly lower in systemic hearts perfused with supplemental taurine (100 mmol L−1) than in controls. In muscle ring preparations, taurine impaired relaxation at high contraction frequencies, an effect abolished by supra-physiological Ca2+ levels. Taurine did not affect oxygen consumption in non-contracting systemic heart muscle, but extracellular glucose utilization was twice that of control preparations. Collectively, our results suggest that extracellular taurine depresses cardiac Ca2+ flux and potentiates glucose utilization in cuttlefish. Variations in taurine levels may represent an important mechanism for regulating cardiovascular function and metabolism in cephalopods.

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Acknowledgments

The authors thank Dr. Juan Fuentes, Mr. João Reis and the students and staff at Ramalhete Station for valuable input and logistical assistance with the study. TJM and WRD were supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grants. WRD holds the Canada Research Chair in Marine Bioscience. AVS was supported by Fundação para a Ciência e a Tecnologia through Programa Investigador FCT 2014 (IF/00576/2014) and project SEPIATECH (31-03-05-FEP-2) funded by the Portuguese Government Program PROMAR. NIC was supported by an NSERC CGS-M award and a New Brunswick Innovation Foundation graduate fellowship.

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Authors and Affiliations

  1. Department of Chemistry and Biochemistry, Mount Allison University, Sackville, NB, E4L1G8, Canada

    Tyson J. MacCormack & N. I. Callaghan

  2. C.C.Mar, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, Faro, Portugal

    A. V. Sykes

  3. Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, Canada

    W. R. Driedzic

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  1. Tyson J. MacCormack
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  2. N. I. Callaghan
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  3. A. V. Sykes
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  4. W. R. Driedzic
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Correspondence to Tyson J. MacCormack.

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Communicated by G. Heldmaier.

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MacCormack, T.J., Callaghan, N.I., Sykes, A.V. et al. Taurine depresses cardiac contractility and enhances systemic heart glucose utilization in the cuttlefish, Sepia officinalis . J Comp Physiol B 186, 215–227 (2016). https://doi.org/10.1007/s00360-015-0946-0

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  • DOI: https://doi.org/10.1007/s00360-015-0946-0

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