The Effects of Phenanthrene on Electrical Activity in Ventricular Cardiomyocytes of Atlantic Cod (Gadus morhua)

Cover Page

Cite item

Full Text

Abstract

The production of oil on the Arctic shelf and its transport along the Northern Sea Route increase risks of pollution of the ecosystems in the Arctic seas with oil and oil products. Today, polyaromatic hydrocarbons are known as the most toxic oil components, and phenanthrene is predominant in terms of its concentration in oil and physiological effects. Phenanthrene affects the electrical activity of fish heart, but its effects are species-specific. At the same time, the effects of phenanthrene on cardiac function in Arctic fishes, including economically important commercial species, are studied not enough. This study examines the effects of phenanthrene on electrical activity and ionic currents in ventricular myocardium of Atlantic cod (Gadus morhua). The major ionic currents in cod myocardium were IKr, IK1, INa and ICa. Phenanthrene (1 μM) did not affect the duration of action potentials (APs) recorded in isolated cod ventricular cardiomyocytes using patch clamp method. Meanwhile, phenanthrene suppressed rapid delayed rectifier current IKr by 61.33 ± 3.94%, decreasing the repolarization reserve of the myocardium. Phenanthrene did not affect nor the level of resting membrane potential, not background inward rectifier current IK1. Also, application of phenanthrene decreased AP upstroke velocity in cod myocytes, which was due to the suppression of fast sodium current INa. Finally, phenanthrene slightly reduced the amplitude of calcium current ICa and accelerated its inactivation, which overall led to the decrease in ICa charge transfer. Thus, the effects of phenanthrene on cod myocardium at cellular level can be described as potentially proarrhythmic, which makes the populations of cod in Arctic seas vulnerable to pollution of the aquatic environment by oil components after oil spills due to technological disasters.

Full Text

Restricted Access

About the authors

T. S. Filatova

Department of Human and Animal Physiology, Lomonosov Moscow State University

Author for correspondence.
Email: filatova@mail.bio.msu.ru
Russian Federation, Moscow

A. V. Shamshura

Department of Human and Animal Physiology, Lomonosov Moscow State University

Email: filatova@mail.bio.msu.ru
Russian Federation, Moscow

D. V. Abramochkina

Department of Human and Animal Physiology, Lomonosov Moscow State University

Email: filatova@mail.bio.msu.ru
Russian Federation, Moscow

References

  1. Dmitrieva D, Romasheva N (2020) Sustainable Development of Oil and Gas Potential of the Arctic and Its Shelf Zone: The Role of Innovations. J Mar Sci Eng 8:1003. https://doi.org/10.3390/JMSE8121003
  2. Hose JE, McGurk MD, Marty GD, Hinton DE, Brown ED, Baker TT (1996) Sublethal effects of the (Exxon Valdez) oil spill on herring embryos and larvae: morphological, cytogenetic, and histopathological assessments, 1989-1991. Can J Fish Aquat Sci 53:2355–2365. https://doi.org/10.1139/F96-174
  3. McGurk MD, Brown ED (1996) Egg–larval mortality of Pacific herring in Prince William Sound, Alaska, after the Exxon Valdez oil spill. Can J Fish Aquat Sci 53:2343–2354. https://doi.org/10.1139/F96-172
  4. Gulas S, Downton M, D’Souza K, Hayden K, Walker TR (2017) Declining Arctic Ocean oil and gas developments: Opportunities to improve governance and environmental pollution control. Mar Policy 75:53–61. https://doi.org/10.1016/J.MARPOL.2016.10.014
  5. Walker TR, Crittenden PD, Young SD, Prystina T (2006) An assessment of pollution impacts due to the oil and gas industries in the Pechora basin, north-eastern European Russia. Ecol Indic 6:369–387. https://doi.org/10.1016/J.ECOLIND.2005.03.015
  6. Rajendran S, Sadooni FN, Al-Kuwari HAS, Oleg A, Govil H, Nasir S, Vethamony P (2021) Monitoring oil spill in Norilsk, Russia using satellite data. Sci Rep 11:1–20. https://doi.org/10.1038/s41598-021-83260-7
  7. Bambulyak A, Ehlers S (2020) Oil spill damage: a collision scenario and financial liability estimations for the Northern Sea Route area. Sh Technol Res 148–164. https://doi.org/10.1080/09377255.2020.1786932
  8. Carls MG, Rice SD, Hose JE (1999) Sensitivity of fish embryos to weathered crude oil: Part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval pacific herring (Clupea pallasi). Environ Toxicol Chem 18:481–493. https://doi.org/10.1002/ETC.5620180317
  9. Lawal AT (2017) Polycyclic aromatic hydrocarbons. A review. Cogent Environ Sci 3:1339841
  10. Xu K, Zhang Y, Zheng J, Wang C, Chen R (2023) Comparative Toxicity of 3–5 Ringed Polycyclic Aromatic Hydrocarbons to Skeletal Development in Zebrafish Embryos and the Possible Reason. Bull Environ Contam Toxicol 110:8. https://doi.org/10.1007/S00128-022-03644-X/TABLES/2
  11. Incardona JP, Collier TK, Scholz NL (2004) Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 196:191–205. https://doi.org/10.1016/J.TAAP.2003.11.026
  12. Incardona JP, Carls MG, Day HL, Sloan CA, Bolton JL, Collier TK, Schoiz NL (2009) Cardiac arrhythmia is the primary response of embryonic pacific herring (Clupea pallasi) exposed to crude oil during weathering. Environ Sci Technol 43:201–207. https://doi.org/10.1021/ES802270T/SUPPL_FILE/ES802270T_SI_004.PDF
  13. Ainerua MO, Tinwell J, Kompella SN, Sørhus 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
  14. Brette F, Shiels HA, Galli GLJ, 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
  15. Brette F, Machado B, Cros C, Incardona JP, Scholz NL, Block BA (2014) Crude oil impairs cardiac excitation-contraction coupling in fish. Science (80- ) 343:772–776. https://doi.org/10.1126/SCIENCE.1242747
  16. Filatova TS, Mikhailova VB, Guskova VO, Abramochkin DV (2023) The Effects of Phenanthrene on the Electrical Activity in the Heart of Shorthorn Sculpin (Myoxocephalus scorpio). J Evol Biochem Physiol 2022 581 58:S44–S51. https://doi.org/10.1134/S0022093022070055
  17. 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
  18. Abramochkin D V, 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
  19. Abramochkin D V., 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 Part A Mol Integr Physiol 268:111204. https://doi.org/10.1016/J.CBPA.2022.111204
  20. 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.202012733/211701
  21. Troell M, Eide A, Isaksen J, Hermansen Ø, Crépin AS (2017) Seafood from a changing Arctic. Ambio 46:368–386. https://doi.org/10.1007/S13280-017-0954-2/TABLES/5
  22. Gadus morhua, Atlantic cod : fisheries, aquaculture, gamefish. https://fishbase.mnhn.fr/summary/69. Accessed 15 Mar 2024
  23. Abramochkin DV, Vornanen M (2017) Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga). J Comp Physiol B Biochem Syst Environ Physiol 187:329–338. https://doi.org/10.1007/s00360-016-1032-y
  24. Hove-Madsen L, Tort L (1998) L-type Ca²⁺ current and excitation-contraction coupling in single atrial myocytes from rainbow trout. Am J Physiol Integr Comp Physiol 275:R2061–R2069. https://doi.org/10.1152/ajpregu.1998.275.6.R2061
  25. Spector PS, Curran ME, Zou A, Keating MT, Sanguinetti MC (1996) Fast inactivation causes rectification of the IKr channel. J Gen Physiol 107:611–619. https://doi.org/10.1085/JGP.107.5.611
  26. Abramochkin DV, Haverinen J, Mitenkov YAYA, 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.193607/259631/AM/TEMPERATURE-AND-EXTERNAL-K-DEPENDENCE-OF
  27. Link JS, Bogstad B, Sparholt H, Lilly GR (2009) Trophic role of Atlantic cod in the ecosystem. Fish Fish 10:58–87. https://doi.org/10.1111/j.1467-2979.2008.00295.x
  28. Shiels HA, Paajanen V, Vornanen M (2006) Sarcolemmal ion currents and sarcoplasmic reticulum Ca²⁺content in ventricular myocytes from the cold stenothermic fish, the burbot( Lota lota ). J Exp Biol 209:3091–3100. https://doi.org/10.1242/jeb.02321
  29. 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 Biochem Syst Environ Physiol 185:883–890. https://doi.org/10.1007/s00360-015-0925-5
  30. Shiels HA, Paajanen V, Vornanen M (2006) Sarcolemmal ion currents and sarcoplasmic reticulum Ca²⁺content in ventricular myocytes from the cold stenothermic fish, the burbot( Lota lota ). J Exp Biol 209:3091–3100. https://doi.org/10.1242/jeb.02321
  31. Haverinen J, Vornanen M (2009) Responses of Action Potential and K + Currents to Temperature Acclimation in Fish Hearts: Phylogeny or Thermal Preferences? Physiol Biochem Zool 82:468–482. https://doi.org/10.1086/590223
  32. Haverinen J, Vornanen M (2004) Temperature acclimation modifies Na+ current in fish cardiac myocytes. J Exp Biol 207:2823–2833. https://doi.org/10.1242/jeb.01103
  33. Abramochkin D V., Filatova TS, Kuzmin VS, Voronkov YI, Kamkin A, Shiels HA (2023) Tricyclic hydrocarbon fluorene attenuates ventricular ionic currents and pressure development in the navaga cod. Comp Biochem Physiol Part C Toxicol Pharmacol 273:109736. https://doi.org/10.1016/j.cbpc.2023.109736
  34. Mesirca P, Torrente AG, Mangoni ME (2015) Functional role of voltage gated Ca²⁺ channels in heart automaticity. Front Physiol 6:19. https://doi.org/10.3389/fphys.2015.00019
  35. Varró A, Baczkó I (2011) Cardiac ventricular repolarization reserve: a principle for understanding drug-related proarrhythmic risk. Br J Pharmacol 164:14–36. https://doi.org/10.1111/j.1476-5381.2011.01367.x

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Effect of phenanthrene on AP configuration in cod ventricular cardiomyocytes. (a) Representative AP recordings under control conditions and in the presence of 1 μM phenanthrene; (b) Representative recording showing slowing of the fast depolarization phase of AP in the presence of 1 μM phenanthrene, the black line below shows the electrical stimulus, the arrow marks the region of interest; (c) Effect of 1 μM phenanthrene on the maximum rate of AP leading edge rise (n = 6; p < 0.01, paired Student's t-test); (d) Effect of 1 μM phenanthrene on the resting membrane potential (n = 6; p = 0.11, paired Student's t-test). (e) – effect of 1 μM phenanthrene on the duration of AP at 90% repolarization (n = 6; p = 0.20, paired Student's t-test); (f) – effect of 1 μM phenanthrene on the duration of AP at 5% repolarization (n = 6; p = 0.07, paired Student's t-test).

Download (197KB)
Indexing metadata
3. Fig. 2. Effect of phenanthrene on the delayed rectifier fast potassium current IKr in cod ventricular cardiomyocytes. (a) Representative IKᵣ traces; (b) Current-voltage characteristics of IKr in cod ventricular cardiomyocytes under control conditions and in the presence of 1 μM phenanthrene (n = 6 for both groups; **p < 0.01, * p < 0.05, paired Student's t-test); (c) Representative IKᵣ traces (at 40 mV) under control conditions and in the presence of 1 μM phenanthrene.

Download (159KB)
Indexing metadata
4. Fig. 3. Effect of phenanthrene on the background potassium inward rectifier current IK1 in cod ventricular cardiomyocytes. (a) Current-voltage characteristic of IK1 current under control conditions and in the presence of 1 μM phenanthrene (n = 6 for both groups, p > 0.05 for all potentials, paired Student's t-test); (b) representative IK1 recordings under control conditions and in the presence of 1 μM phenanthrene.

Download (126KB)
Indexing metadata
5. Fig. 4. Effect of phenanthrene on the fast sodium current INₐ in cod ventricular cardiomyocytes. (a) Representative INₐ traces; (b) Current-voltage characteristics of INₐ in cod ventricular cardiomyocytes under control conditions and in the presence of 1 μM phenanthrene (n = 7 for both groups, p > 0.05 for all potentials, paired Student's t-test); (c) Representative INₐ traces (at –30 mV) under control conditions and in the presence of 1 μM phenanthrene.

Download (174KB)
Indexing metadata
6. Fig. 5. Effect of phenanthrene on the calcium current ICa in cod ventricular cardiomyocytes. (a) Representative ICa traces; (b) Current-voltage characteristics of ICa in cod ventricular cardiomyocytes under control conditions and in the presence of 1 μM phenanthrene (n = 5 for both groups, p > 0.05 for all potentials, paired Student's t-test); (c) Representative ICa traces (at –10 mV) under control conditions and in the presence of 1 μM phenanthrene; (d) Effect of 1 μM phenanthrene on the time constant of ICa inactivation at –10 mV (n = 5; p = 0.22, paired Student's t-test). (e) Effect of 1 μM phenanthrene on the net charge transferred by ICa at –10 mV (n = 5; p < 0.01, paired Student's t-test).

Download (242KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences

Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».