Abstract
Phenanthrene (Phen) is one of the widespread species of polyaromatic hydrocarbons, a tricyclic compound, component of crude oil and diesel fuel. Earlier studies have shown its negative effects on fish heart function that may explain the toxicity of this pollutant. The present study aimed to elucidate the cardiac electrophysiological effects of Phen in shorthorn sculpin, the widespread and common fish of the Arctic region using the patch-clamp technique. We have found pronounced effects of Phen on the duration and upstroke velocity of action potentials (APs) in sculpin ventricular myocytes. 1 µM Phen produced almost two-fold prolongation of AP duration measured at 90% repolarization level and significant reduction of maximal upstroke velocity of AP. These effects are attributed to suppression of K+ rapid delayed rectifier current IKr (IC50 = 144 nM) and fast Na+ current INa (IC50 = 5.85 µM). Resting membrane potential and K+ inward rectifier current IK1 were not affected by Phen even in the maximal concentration of 30 µM. Thus, low concentrations of Phen induce changes in cellular electrical activity of sculpin ventricular myocytes which might lead to proarrhythmic effects such as slowing of repolarization and decrease in excitation conduction velocity at the tissue level.
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REFERENCES
Le Bihanic F, Clérandeau C, Le Menach K, Morin B, Budzinski H, Cousin X, Cachot J (2014) Developmental toxicity of PAH mixtures in fish early life stages. Part II: adverse effects in Japanese medaka. Environ Sci Pollut Res 21: 13732–13743. https://doi.org/10.1007/s11356-014-2676-3
Lucas J, Perrichon P, Nouhaud M, Audras A, Leguen I, Lefrancois C (2014) Aerobic metabolism and cardiac activity in the descendants of zebrafish exposed to pyrolytic polycyclic aromatic hydrocarbons. Environ Sci Pollut Res 21: 13888–13897. https://doi.org/10.1007/s11356-014-3116-0
Brette F, Machado B, Cros C, Incardona JP, Scholz NL, Block BA (2014) Crude oil impairs cardiac excitation-contraction coupling in fish. Science 343: 772–726. https://doi.org/10.1126/science.1242747
Brette F, Shiels HA, Galli GL, Cros C, Incardona JP, Scholz NL, Block BA (2017) A Novel Cardiotoxic Mechanism for a Pervasive Global Pollutant. Sci Rep 7: 41476. https://doi.org/10.1038/srep41476
Vehniäinen ER, Haverinen J, Vornanen M (2019) Polycyclic Aromatic Hydrocarbons Phenanthrene and Retene Modify the Action Potential via Multiple Ion Currents in Rainbow Trout Oncorhynchus mykiss Cardiac Myocytes. Environ Toxicol Chem 38: 2145–2153. https://doi.org/10.1002/etc.4530
Ainerua MO, Tinwell J, Kompella SN, Sorhus E, White KN, van Dongen BE, Shiels HA (2020) 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 239: 124608. https://doi.org/10.1016/j.chemosphere.2019.124608
Abramochkin DV, Kompella SN, Shiels HA (2021) Phenanthrene alters the electrical activity of atrial and ventricular myocytes of a polar fish, the Navaga cod. Aquat Toxicol 235: 105823. https://doi.org/10.1016/j.aquatox.2021.105823
Kompella SN, Brette F, Hancox JC, Shiels HA (2021) Phenanthrene impacts zebrafish cardiomyocyte excitability by inhibiting IKr and shortening action potential duration. J Gen Physiol 153: e202012733. https://doi.org/10.1085/jgp.202012733
Hassinen M, Haverinen J, Vornanen M (2008) Electrophysiological properties and expression of the delayed rectifier potassium (ERG) channels in the heart of thermally acclimated rainbow trout. Am J Physiol Regul Integr Comp Physiol 295: R297–R308. https://doi.org/10.1152/ajpregu.00612.2007
Abramochkin DV, Filatova TS, Pustovit KB, Voronina YA, Kuzmin VS, Vornanen M (2022) Ionic currents underlying different patterns of electrical activity in working cardiac myocytes of mammals and non-mammalian vertebrates. Comp Biochem Physiol A 268: 111204. https://doi.org/10.1016/j.cbpa.2022.111204
Luksenburg JA, Pedersen T (2002) Sexual and geographical variation in life history parameters of the shorthorn sculpin. J Fish Biol 61: 1453–1464. https://doi.org/10.1111/j.1095-8649.2002.tb02489.x
Luksenburg JA, Pedersen T, Falk-Petersen IB (2004) Reproduction of the shorthorn sculpin Myoxocephalus scorpius in northern Norway. J Sea Res 51: 157–166. https://doi.org/10.1016/j.seares.2003.09.001
Abramochkin DV, Vornanen M (2015) Seasonal acclimatization of the cardiac potassium currents (IK1 and IKr) in an arctic marine teleost, the navaga cod (Eleginus navaga). J Comp Physiol B 185: 883–890. https://doi.org/10.1007/s00360-015-0925-5
Filatova TS, Abramochkin DV, Shiels HA (2019) Thermal acclimation and seasonal acclimatization: a comparative study of cardiac response to prolonged temperature change in shorthorn sculpin. J Exp Biol 222: jeb202242. https://doi.org/10.1242/jeb.202242
Hove-Madsen L, Tort L (1998) L-type Ca2+ current and excitation-contraction coupling in single atrial myocytes from rainbow trout. Am J Physiol 275: 2061–2069. https://doi.org/10.1152/ajpregu.1998.275.6.R2061
Abramochkin DV, Vornanen M (2017) Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga). J Comp Physiol B 187: 329–338. https://doi.org/10.1007/s00360-016-1032-y
Vornanen M, Hassinen M, Haverinen J (2011) Tetrodotoxin sensitivity of the vertebrate cardiac Na+ current. Mar Drugs 9: 2409–2422. https://doi.org/10.3390/md9112409
Heuer RM, Galli GLJ, Shiels HA, Fieber LA, Cox GK, Mager EM, Stieglitz JD, Benetti DD, Grosell M, Crossley DA (2019) Impacts of Deepwater Horizon Crude Oil on Mahi-Mahi (Coryphaena hippurus) Heart Cell Function. Environ Sci Technol 53: 9895–9904. https://doi.org/10.1021/acs.est.9b03798
Abramochkin DV, Haverinen J, Mitenkov YA, Vornanen M (2019) Temperature and external K(+) dependence of electrical excitation in ventricular myocytes of cod-like fishes. J Exp Biol 222: jeb193607. https://doi.org/10.1242/jeb.193607
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This work was supported by Russian Science Foundation (grant no. 22-14-00075) to DVA.
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Translated by A. Polyanovsky
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Filatova, T.S., Mikhailova, V.B., Guskova, V.O. et al. The Effects of Phenanthrene on the Electrical Activity in the Heart of Shorthorn Sculpin (Myoxocephalus scorpio). J Evol Biochem Phys 58 (Suppl 1), S44–S51 (2022). https://doi.org/10.1134/S0022093022070055
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DOI: https://doi.org/10.1134/S0022093022070055