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  3. Understanding the cardiac toxicity of the anthropogenic pollutant phenanthrene on the freshwater indicator species, the brown trout (Salmo trutta): From whole heart to cardiomyocytes

Understanding the cardiac toxicity of the anthropogenic pollutant phenanthrene on the freshwater indicator species, the brown trout (Salmo trutta): From whole heart to cardiomyocytes

  • Chemosphere. 2020 Jan;239:124608. doi: 10.1016/j.chemosphere.2019.124608.
Martins Oshioriamhe Ainerua 1,  Jake Tinwell 2,  Shiva Nag Kompella 2,  Elin Sørhus 3,  Keith N White 4,  Bart E van Dongen 5,  Holly A Shiels 6
Affiliations

Affiliations

  • 1 Cardiovascular Division, School of Medicine, Faculty of Biology, Medicine and Health, University of Manchester, Core Technology Facility Building, Manchester, M13 9NT, United Kingdom; Department of Animal and Environmental Biology, Faculty of Life Sciences, University of Benin, PMB 1154, Benin City, Nigeria.
  • 2 Cardiovascular Division, School of Medicine, Faculty of Biology, Medicine and Health, University of Manchester, Core Technology Facility Building, Manchester, M13 9NT, United Kingdom.
  • 3 Institute of Marine Research, P.O. Box 1870, Nordnes, NO-5817, Bergen, Norway.
  • 4 School of Earth Atmospheric and Environmental Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester, M13 9GB, United Kingdom.
  • 5 School of Earth Atmospheric and Environmental Sciences, Williamson Research Centre for Molecular Science, University of Manchester, Williamson Building, Oxford Road, Manchester, M13 9PL, United Kingdom.
  • 6 Cardiovascular Division, School of Medicine, Faculty of Biology, Medicine and Health, University of Manchester, Core Technology Facility Building, Manchester, M13 9NT, United Kingdom. Electronic address: Holly.shiels@manchester.ac.uk.
PMID: 31499312 DOI: 10.1016/j.chemosphere.2019.124608
Abstract

Freshwater systems are faced with a myriad of stressors including geomorphological alterations, nutrient overloading and pollution. Previous studies in marine fish showed polyaromatic hydrocarbons (PAHs) to be cardiotoxic. However, the cardiotoxicity of anthropogenic pollutants in freshwater fishes is unclear and has not been examined across multiple levels of cardiac organization. Here we investigated the effect of phenanthrene (Phe), a pervasive anthropogenic pollutant on a sentinel freshwater species, the brown trout (Salmo trutta). We first examined the electrical activity of the whole heart and found prolongation (∼8.6%) of the QT interval (time between ventricular depolarization and repolarization) of the electrocardiogram (ECG) and prolongation (∼13.2%) of the monophasic action potential duration (MAPD) following ascending doses of Phe. At the tissue level, Phe significantly reduced trabecular force generation by ∼24% at concentration 15 μM and above, suggesting Phe reduces cellular calcium cycling. This finding was supported by florescent microscopy showing a reduction (∼39%) in the intracellular calcium transient amplitude following Phe exposure in isolated brown trout ventricular myocytes. Single-cell electrophysiology was used to reveal the mechanism underlying contractile and electrical dysfunction following Phe exposure. A Phe-dependent reduction (∼38%) in the L-type CA2+ current accounts, at least in part, for the lowered CA2+ transient and force production. Prolongation of the MAPD and QT interval was explained by a reduction (∼70%) in the repolarising delayed rectifier K+ current following Phe exposure. Taken together, our study shows a direct impact of Phe across multiple levels of cardiac organization in a key freshwater salmonid.

Keywords

AP; Cardiac action potential; ECG; Electrophysiology; Fish; PAHs; Poly aromatic hydrocarbons; Toxicology; brown trout.

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