The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga)

The intensive development of oil and gas industries in the Arctic threatens Arctic aquatic ecosystems. The toxic and primarily lethal cardiotoxic effects of oil in living organisms are believed to be associated with polyaromatic hydrocarbons (PAHs), and previous works revealed the electrophysiologic...

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Main Authors: T. S. Filatova, A. S. Borodkov, A. M. Karkhov, I. H. Dzhumaniiazova, O. B. Pustovit, D. V. Abramochkin, Т. С. Филатова, А. С. Бородков, А. М. Кархов, И. Х. Джуманиязова, О. Б. Пустовит, Д. В. Абрамочкин
Other Authors: Работа выполнена при финансовой поддержке Российского научного фонда (проект № 22-14- 00075). В работе было использовано оборудование, приобретенное МГУ имени М.В. Ломоносова в рамках федерального проекта «Развитие инфраструктуры для научных исследований и подготовки кадров» национального проекта «Наука и университеты» от 29.12.2022г №15-пр/42 (соглашение №355 от 15.03.2024).
Format: Article in Journal/Newspaper
Language:Russian
Published: Lomonosov Moscow State University, School of Biology 2024
Subjects:
oil
Online Access:https://vestnik-bio-msu.elpub.ru/jour/article/view/1384
https://doi.org/10.55959/MSU0137-0952-16-79-2S-9
id ftjhmub:oai:oai.vestnik-bio-msu.elpub.ru:article/1384
record_format openpolar
institution Open Polar
collection Herald of Moscow University. Series 16. Biology
op_collection_id ftjhmub
language Russian
topic нефть
action potential
patch-clamp
polyaromatic hydrocarbons
ionic currents
oil
потенциал действия
пэтч-кламп
полиароматические углеводороды
ионные токи
spellingShingle нефть
action potential
patch-clamp
polyaromatic hydrocarbons
ionic currents
oil
потенциал действия
пэтч-кламп
полиароматические углеводороды
ионные токи
T. S. Filatova
A. S. Borodkov
A. M. Karkhov
I. H. Dzhumaniiazova
O. B. Pustovit
D. V. Abramochkin
Т. С. Филатова
А. С. Бородков
А. М. Кархов
И. Х. Джуманиязова
О. Б. Пустовит
Д. В. Абрамочкин
The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga)
topic_facet нефть
action potential
patch-clamp
polyaromatic hydrocarbons
ionic currents
oil
потенциал действия
пэтч-кламп
полиароматические углеводороды
ионные токи
description The intensive development of oil and gas industries in the Arctic threatens Arctic aquatic ecosystems. The toxic and primarily lethal cardiotoxic effects of oil in living organisms are believed to be associated with polyaromatic hydrocarbons (PAHs), and previous works revealed the electrophysiological mechanisms of action of individual oil-derived PAHs. However, the physiological effects of a complex PAHs mixture in oil water-soluble fraction (WSF) have not been previously studied. This study is focused on the effects of oil WSF on electrical activity and major ionic currents in the working myocardium of navaga (Eleginus nawaga), which is one of the most important commercial fish species in the Arctic. We found that 1% and 10% solutions of oil WSF cause a marked increase in the duration of action potentials (APs) in navaga cardiomyocytes. This effect appears to be due to the suppression of rapid delayed rectifying current IKr (IC50 about 3% in ventricular and atrial myocardium). At higher concentrations, oil WSF also suppressed calcium current ICaL (IC50 = 10.6%), which led to a decrease in the contractile activity in isolated myocardial preparations. Unlike individual tricyclic PAHs, oil WSF did not affect fast sodium current INa and AP upstroke velocity. An assessment of the content of tricyclic PAHs in 10% solution of oil WSF showed that their total concentration is relatively low and does not exceed 100 nM. Thus, oil WSF also has a powerful cardiotoxic effect in fish myocardium, but its effects differ from the previously studied effects of tricyclic PAHs and suggest the presence of yet unexplored oil compounds that have a more powerful toxic potential against ERG channels. Интенсивное развитие нефте- и газодобывающей отраслей в Арктике ставит под угрозу арктические водные экосистемы. Считается, что токсическое и, прежде всего, летальное кардиотоксическое действие нефти на живые организмы связано с полиароматическими углеводородами (ПАУ), и в предыдущих работах были рассмотрены электрофизиологические ...
author2 Работа выполнена при финансовой поддержке Российского научного фонда (проект № 22-14- 00075). В работе было использовано оборудование, приобретенное МГУ имени М.В. Ломоносова в рамках федерального проекта «Развитие инфраструктуры для научных исследований и подготовки кадров» национального проекта «Наука и университеты» от 29.12.2022г №15-пр/42 (соглашение №355 от 15.03.2024).
format Article in Journal/Newspaper
author T. S. Filatova
A. S. Borodkov
A. M. Karkhov
I. H. Dzhumaniiazova
O. B. Pustovit
D. V. Abramochkin
Т. С. Филатова
А. С. Бородков
А. М. Кархов
И. Х. Джуманиязова
О. Б. Пустовит
Д. В. Абрамочкин
author_facet T. S. Filatova
A. S. Borodkov
A. M. Karkhov
I. H. Dzhumaniiazova
O. B. Pustovit
D. V. Abramochkin
Т. С. Филатова
А. С. Бородков
А. М. Кархов
И. Х. Джуманиязова
О. Б. Пустовит
Д. В. Абрамочкин
author_sort T. S. Filatova
title The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga)
title_short The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga)
title_full The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga)
title_fullStr The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga)
title_full_unstemmed The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga)
title_sort mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (eleginus nawaga)
publisher Lomonosov Moscow State University, School of Biology
publishDate 2024
url https://vestnik-bio-msu.elpub.ru/jour/article/view/1384
https://doi.org/10.55959/MSU0137-0952-16-79-2S-9
long_lat ENVELOPE(162.106,162.106,59.229,59.229)
geographic Arctic
Navaga
geographic_facet Arctic
Navaga
genre Arctic
Arctic
genre_facet Arctic
Arctic
op_source Vestnik Moskovskogo universiteta. Seriya 16. Biologiya; Том 79, № 2S (2024); 89-97
Вестник Московского университета. Серия 16. Биология; Том 79, № 2S (2024); 89-97
0137-0952
op_relation https://vestnik-bio-msu.elpub.ru/jour/article/view/1384/685
Krupenio N.N., Parmuzin P.I., Zamoiskii V.L. Mapping of segments polluted by petroleum products in the Usinsk region of the Komi republic from remotemeasurement data. Hydrotechnical Construction. 1995;29(11):648–652.
Филатова Т.С., Абрамочкин Д.В. Физиологические эффекты полициклических ароматических углеводородов (ПАУ) в организме рыб. Вестн. Моск. ун-та. Сер. 16: Биол. 2023;78(3):127–138.
Marris C.R., Kompella S.N., Miller M.R., Incardona J.P., Brette F., Hancox J.C., Sorhus E., Shiels H.A. Polyaromatic hydrocarbons in pollution: a heart-breaking matter. J. Physiol. 2020;598(2):227–247.
Brette F., Machado B., Cros C., Incardona J.P., Scholz N.L., Block B.A. Crude oil impairs cardiac excitation-contraction coupling in fish. Biophys. J. 2014;106(2):732a.
Vehniäinen E.R., Haverinen J., Vornanen M. Polycyclic aromatic hydrocarbons phenanthrene and retene modify the action potential via multiple ion currents in rainbow trout oncorhynchus mykiss cardiac myocytes. Env. Toxicol. Chem. 2019;38(10):2145–2153.
Ainerua M.O., Tinwell J., Kompella S.N., Sorhus E., White K.N., van Dongen B.E., Shiels H.A. 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;239:124608.
Abramochkin D.V., Kompella S.N., Shiels H.A. Phenanthrene alters the electrical activity of atrial and ventricular myocytes of a polar fish, the Navaga cod. Aquat. Toxicol. 2021;235:105823.
Abramochkin D.V., Haverinen J., Mitenkov Y.A., Vornanen M. Temperature and external K+ dependence of electrical excitation in ventricular myocytes of cod-like fishes. J. Exp. Biol. 2019;222(5):193607.
Kompella S.N., Brette F., Hancox J.C, Shiels H.A. Phenanthrene impacts zebrafish cardiomyocyte excitability by inhibiting IKr and shortening action potential duration. J. Gen. Physiol. 2021;153(2):e202012733.
Abramochkin D.V., Filatova T.S., Kuzmin V.S., Voronkov Y.I., Kamkin A., Shiels H.A. Tricyclic hydrocarbon fluorene attenuates ventricular ionic currents and pressure development in the navaga cod. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2023;273:109736.
Abramochkin D.V., Vornanen M. Inhibition of the cardiac ATP-dependent potassium current by KB-R7943. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2014;175:38–45.
Filatova T.S., Abramochkin D.V., Shiels H.A. Thermal acclimation and seasonal acclimatization: a comparative study of cardiac response to prolonged temperature change in shorthorn sculpin. J. Exp. Biol. 2019;222(Pt. 16):jeb202242.
Abramochkin D.V., Borodinova A.A., Rosenshtraukh L.V. Effects of acetylcholinesterase inhibitor paraoxon denote the possibility of non-quantal acetylcholine release in myocardium of different vertebrates. J. Comp. Physiol. B. 2012;182(1):101–108.
Heuer R.M., Galli G.L.J., Shiels H.A., Fieber L.A., Cox G.K., Mager E.M., Stieglitz J.D., Benetti D.D., Grosell M., Crossley Ii. D.A. Impacts of Deepwater Horizon crude oil on Mahi-Mahi (Coryphaena hippurus) heart cell function. Environ. Sci. Technol. 2019;53(16):9895–9904.
Haverinen J., Abramochkin D.V., Kamkin A., Vornanen M. Maximum heart rate in brown trout (Salmo trutta fario) is not limited by firing rate of pacemaker cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2017;312(2):R165–R171.
Abramochkin D.V., Filatova T.S., Pustovit K.B., Voronina Y.A., Kuzmin V.S., Vornanen M. Ionic currents underlying different patterns of electrical activity in working cardiac myocytes of mammals and non-mammalian vertebrates. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2022;268:111204.
Filatova T.S., Abramochkin D.V., Pavlova N.S., Pustovit K.B., Konovalova O.P., Kuzmin V.S., Dobrzynski H. Repolarizing potassium currents in working myocardium of Japanese quail: a novel translational model for cardiac electrophysiology. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2021;255:110919.
Abramochkin D.V., Vornanen M. Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga). J. Comp. Physiol. B 2017;187(2):329–338.
Belles B., Malécot C.O., Hescheler J., Trautwein W. “Run-down” of the Ca current during long whole-cell recordings in guinea pig heart cells: role of phosphorylation and intracellular calcium. Pflugers. Arch. 1988;411(4):353–360.
https://vestnik-bio-msu.elpub.ru/jour/article/view/1384
doi:10.55959/MSU0137-0952-16-79-2S-9
op_rights Authors who publish with this journal agree to the following terms:Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Авторы, публикующие статьи в данном журнале, соглашаются на следующее:Авторы сохраняют за собой автороские права и предоставляют журналу право первой публикации работы, которая по истечении 6 месяцев после публикации автоматически лицензируется на условиях Creative Commons Attribution License , которая позволяет другим распространять данную работу с обязательным сохранением ссылок на авторов оригинальной работы и оригинальную публикацию в этом журнале.Авторы имеют право размещать их работу в сети Интернет (например, в институтском хранилище или на персональном сайте).
op_doi https://doi.org/10.55959/MSU0137-0952-16-79-2S-9
_version_ 1811634042576044032
spelling ftjhmub:oai:oai.vestnik-bio-msu.elpub.ru:article/1384 2024-09-30T14:28:18+00:00 The mechanisms of effects of oil-derived polyaromatic hydrocarbons on cardiac electrical activity in navaga cod (Eleginus nawaga) Механизмы воздействия полиароматических углеводородов нефти на электрическую активность сердца северной наваги (Eleginus nawaga) T. S. Filatova A. S. Borodkov A. M. Karkhov I. H. Dzhumaniiazova O. B. Pustovit D. V. Abramochkin Т. С. Филатова А. С. Бородков А. М. Кархов И. Х. Джуманиязова О. Б. Пустовит Д. В. Абрамочкин Работа выполнена при финансовой поддержке Российского научного фонда (проект № 22-14- 00075). В работе было использовано оборудование, приобретенное МГУ имени М.В. Ломоносова в рамках федерального проекта «Развитие инфраструктуры для научных исследований и подготовки кадров» национального проекта «Наука и университеты» от 29.12.2022г №15-пр/42 (соглашение №355 от 15.03.2024). 2024-08-27 application/pdf https://vestnik-bio-msu.elpub.ru/jour/article/view/1384 https://doi.org/10.55959/MSU0137-0952-16-79-2S-9 rus rus Lomonosov Moscow State University, School of Biology https://vestnik-bio-msu.elpub.ru/jour/article/view/1384/685 Krupenio N.N., Parmuzin P.I., Zamoiskii V.L. Mapping of segments polluted by petroleum products in the Usinsk region of the Komi republic from remotemeasurement data. Hydrotechnical Construction. 1995;29(11):648–652. Филатова Т.С., Абрамочкин Д.В. Физиологические эффекты полициклических ароматических углеводородов (ПАУ) в организме рыб. Вестн. Моск. ун-та. Сер. 16: Биол. 2023;78(3):127–138. Marris C.R., Kompella S.N., Miller M.R., Incardona J.P., Brette F., Hancox J.C., Sorhus E., Shiels H.A. Polyaromatic hydrocarbons in pollution: a heart-breaking matter. J. Physiol. 2020;598(2):227–247. Brette F., Machado B., Cros C., Incardona J.P., Scholz N.L., Block B.A. Crude oil impairs cardiac excitation-contraction coupling in fish. Biophys. J. 2014;106(2):732a. Vehniäinen E.R., Haverinen J., Vornanen M. Polycyclic aromatic hydrocarbons phenanthrene and retene modify the action potential via multiple ion currents in rainbow trout oncorhynchus mykiss cardiac myocytes. Env. Toxicol. Chem. 2019;38(10):2145–2153. Ainerua M.O., Tinwell J., Kompella S.N., Sorhus E., White K.N., van Dongen B.E., Shiels H.A. 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;239:124608. Abramochkin D.V., Kompella S.N., Shiels H.A. Phenanthrene alters the electrical activity of atrial and ventricular myocytes of a polar fish, the Navaga cod. Aquat. Toxicol. 2021;235:105823. Abramochkin D.V., Haverinen J., Mitenkov Y.A., Vornanen M. Temperature and external K+ dependence of electrical excitation in ventricular myocytes of cod-like fishes. J. Exp. Biol. 2019;222(5):193607. Kompella S.N., Brette F., Hancox J.C, Shiels H.A. Phenanthrene impacts zebrafish cardiomyocyte excitability by inhibiting IKr and shortening action potential duration. J. Gen. Physiol. 2021;153(2):e202012733. Abramochkin D.V., Filatova T.S., Kuzmin V.S., Voronkov Y.I., Kamkin A., Shiels H.A. Tricyclic hydrocarbon fluorene attenuates ventricular ionic currents and pressure development in the navaga cod. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2023;273:109736. Abramochkin D.V., Vornanen M. Inhibition of the cardiac ATP-dependent potassium current by KB-R7943. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2014;175:38–45. Filatova T.S., Abramochkin D.V., Shiels H.A. Thermal acclimation and seasonal acclimatization: a comparative study of cardiac response to prolonged temperature change in shorthorn sculpin. J. Exp. Biol. 2019;222(Pt. 16):jeb202242. Abramochkin D.V., Borodinova A.A., Rosenshtraukh L.V. Effects of acetylcholinesterase inhibitor paraoxon denote the possibility of non-quantal acetylcholine release in myocardium of different vertebrates. J. Comp. Physiol. B. 2012;182(1):101–108. Heuer R.M., Galli G.L.J., Shiels H.A., Fieber L.A., Cox G.K., Mager E.M., Stieglitz J.D., Benetti D.D., Grosell M., Crossley Ii. D.A. Impacts of Deepwater Horizon crude oil on Mahi-Mahi (Coryphaena hippurus) heart cell function. Environ. Sci. Technol. 2019;53(16):9895–9904. Haverinen J., Abramochkin D.V., Kamkin A., Vornanen M. Maximum heart rate in brown trout (Salmo trutta fario) is not limited by firing rate of pacemaker cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2017;312(2):R165–R171. Abramochkin D.V., Filatova T.S., Pustovit K.B., Voronina Y.A., Kuzmin V.S., Vornanen M. Ionic currents underlying different patterns of electrical activity in working cardiac myocytes of mammals and non-mammalian vertebrates. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2022;268:111204. Filatova T.S., Abramochkin D.V., Pavlova N.S., Pustovit K.B., Konovalova O.P., Kuzmin V.S., Dobrzynski H. Repolarizing potassium currents in working myocardium of Japanese quail: a novel translational model for cardiac electrophysiology. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2021;255:110919. Abramochkin D.V., Vornanen M. Seasonal changes of cholinergic response in the atrium of Arctic navaga cod (Eleginus navaga). J. Comp. Physiol. B 2017;187(2):329–338. Belles B., Malécot C.O., Hescheler J., Trautwein W. “Run-down” of the Ca current during long whole-cell recordings in guinea pig heart cells: role of phosphorylation and intracellular calcium. Pflugers. Arch. 1988;411(4):353–360. https://vestnik-bio-msu.elpub.ru/jour/article/view/1384 doi:10.55959/MSU0137-0952-16-79-2S-9 Authors who publish with this journal agree to the following terms:Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access). Авторы, публикующие статьи в данном журнале, соглашаются на следующее:Авторы сохраняют за собой автороские права и предоставляют журналу право первой публикации работы, которая по истечении 6 месяцев после публикации автоматически лицензируется на условиях Creative Commons Attribution License , которая позволяет другим распространять данную работу с обязательным сохранением ссылок на авторов оригинальной работы и оригинальную публикацию в этом журнале.Авторы имеют право размещать их работу в сети Интернет (например, в институтском хранилище или на персональном сайте). Vestnik Moskovskogo universiteta. Seriya 16. Biologiya; Том 79, № 2S (2024); 89-97 Вестник Московского университета. Серия 16. Биология; Том 79, № 2S (2024); 89-97 0137-0952 нефть action potential patch-clamp polyaromatic hydrocarbons ionic currents oil потенциал действия пэтч-кламп полиароматические углеводороды ионные токи info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 2024 ftjhmub https://doi.org/10.55959/MSU0137-0952-16-79-2S-9 2024-09-02T23:37:29Z The intensive development of oil and gas industries in the Arctic threatens Arctic aquatic ecosystems. The toxic and primarily lethal cardiotoxic effects of oil in living organisms are believed to be associated with polyaromatic hydrocarbons (PAHs), and previous works revealed the electrophysiological mechanisms of action of individual oil-derived PAHs. However, the physiological effects of a complex PAHs mixture in oil water-soluble fraction (WSF) have not been previously studied. This study is focused on the effects of oil WSF on electrical activity and major ionic currents in the working myocardium of navaga (Eleginus nawaga), which is one of the most important commercial fish species in the Arctic. We found that 1% and 10% solutions of oil WSF cause a marked increase in the duration of action potentials (APs) in navaga cardiomyocytes. This effect appears to be due to the suppression of rapid delayed rectifying current IKr (IC50 about 3% in ventricular and atrial myocardium). At higher concentrations, oil WSF also suppressed calcium current ICaL (IC50 = 10.6%), which led to a decrease in the contractile activity in isolated myocardial preparations. Unlike individual tricyclic PAHs, oil WSF did not affect fast sodium current INa and AP upstroke velocity. An assessment of the content of tricyclic PAHs in 10% solution of oil WSF showed that their total concentration is relatively low and does not exceed 100 nM. Thus, oil WSF also has a powerful cardiotoxic effect in fish myocardium, but its effects differ from the previously studied effects of tricyclic PAHs and suggest the presence of yet unexplored oil compounds that have a more powerful toxic potential against ERG channels. Интенсивное развитие нефте- и газодобывающей отраслей в Арктике ставит под угрозу арктические водные экосистемы. Считается, что токсическое и, прежде всего, летальное кардиотоксическое действие нефти на живые организмы связано с полиароматическими углеводородами (ПАУ), и в предыдущих работах были рассмотрены электрофизиологические ... Article in Journal/Newspaper Arctic Arctic Herald of Moscow University. Series 16. Biology Arctic Navaga ENVELOPE(162.106,162.106,59.229,59.229)