Cardiac dysfunction affects eye development and vision by reducing supply of lipids in fish

Elin Sørhus,Sonnich Meier,Carey E Donald,Tomasz Furmanek,Rolf B Edvardsen,Kai K Lie

doi:10.1016/j.scitotenv.2021.149460

Elin Sørhus, Sonnich Meier + Show 4 more

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https://doi.org/10.1016/j.scitotenv.2021.149460

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Abstract

Developing organisms are especially vulnerable to environmental stressors. Crude oil exposure in early life stages of fish result in multiple functional and developmental defects, including cardiac dysfunction and abnormal and smaller eyes. Phenanthrene (Phe) has a reversible impact on cardiac function, and under exposure Phe reduces cardiac contractility. Exposure to a known L-type channel blocker, nicardipine hydrochloride (Nic) also disrupts cardiac function and creates eye deformities. We aimed to investigate whether cardiac dysfunction was the major underlying mechanism of crude oil-, Phe- and Nic-induced eye malformations. We exposed Atlantic haddock (Melanogrammus aeglefinus) early embryos to Nic and crude oil (Oil) and late embryos/early larvae to Phe exposure. All three exposures resulted in cardiac abnormalities and lead to severe, eye, jaw and spinal deformities at early larval stages. At 3 days post hatching, larvae from the exposures and corresponding controls were dissected. Eyes, trunk, head and yolk sac were subjected to lipid profiling, and eyes were also subjected to transcriptomic profiling. Among most enriched pathways in the eye transcriptomes were fatty acid metabolism, calcium signaling and phototransduction. Changes in lipid profiles and the transcriptome suggested that the dysfunctional and abnormal eyes in our exposures were due to both disruption of signaling pathways and insufficient supply of essential fatty acids and other nutrients form the yolk.

Highlights

Developing organisms are vulnerable to environmental stressors, such as oil pollution
Both crude oil and Phe interfere with the excitation contraction coupling in cardiomyocytes by disrupting rectifier potassium currents and calcium cycling (Ainerua et al, 2020; Brette et al, 2014; Brette et al, 2017; Kompella et al, 2021)
The calcium regulated genes were induced by crude oil exposure prior to effects on cardiac function, suggesting that crude oil has a direct effect on calcium homeostasis (Sørhus et al, 2021)

Summary

Introduction

Developing organisms are vulnerable to environmental stressors, such as oil pollution. Cardiac function can be directly affected by both crude oil and single polycyclic aromatic hydrocarbons (PAHs), such as phenanthrene (Phe) Both crude oil and Phe interfere with the excitation contraction coupling in cardiomyocytes by disrupting rectifier potassium currents and calcium cycling (Ainerua et al, 2020; Brette et al, 2014; Brette et al, 2017; Kompella et al, 2021). The calcium regulated genes were induced by crude oil exposure prior to effects on cardiac function, suggesting that crude oil has a direct effect on calcium homeostasis (Sørhus et al, 2021) This direct effect on cardiac function is reversible (Marris et al, 2019), a transient effect on ion homeostasis may disrupt cardiac development and cause irreversible changes in a developing animal (Sørhus et al, 2017). A transient disruption of craniofacial muscular function could irreversibly affect the outgrowth of jaw structures (Shwartz et al, 2012)

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