Abstract
Semi-anadromous animals experience salinity fluctuations during their life-span period. Alterations of environmental conditions induce stress response where catecholamines (CA) play a central role. Physiological stress and changes in external and internal osmolarity are frequently associated with increased production of reactive oxygen species (ROS). In this work, we studied the involvement of the cAMP/PKA pathway in mediating catecholamine-dependent effects on osmoregulatory responses, intracellular production of ROS, and mitochondrial membrane potential of the river lamprey (Lampetra fluviatilis, Linnaeus, 1758) red blood cells (RBCs). We also investigated the role of hypoosmotic shock in the process of ROS production and mitochondrial respiration of RBCs. For this, osmotic stability and the dynamics of the regulatory volume decrease (RVD) following hypoosmotic swelling, intracellular ROS levels, and changes in mitochondrial membrane potential were assessed in RBCs treated with epinephrine (Epi, 25 μM) and forskolin (Forsk, 20 μM). Epi and Forsk markedly reduced the osmotic stability of the lamprey RBCs whereas did not affect the dynamics of the RVD response in a hypoosmotic environment. Activation of PKA with Epi and Forsk increased ROS levels and decreased mitochondrial membrane potential of the lamprey RBCs. In contrast, upon hypoosmotic shock enhanced ROS production in RBCs was accompanied by increased mitochondrial membrane potential. Overall, a decrease in RBC osmotic stability and the enhancement of ROS formation induced by β-adrenergic stimulation raises concerns about stress-associated changes in RBC functions in agnathans. Increased ROS production in RBCs under hypoosmotic shock indicates that a decrease in blood osmolarity may be associated with oxidative damage of RBCs during lamprey migration.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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Funding
The study of epinephrine and forskolin effects on the osmotic fragility and regulatory volume decrease response, ROS metabolism, and mitochondrial membrane potential in lamprey RBCs was supported by the State Assignment of the Ministry of Science and Higher Education of the Russian Federation (project no. 075-00967-23-00 to A.A.Yu., M.I.V., G.S.). The study of the effects of hypoosmotic stimulation on ROS levels and mitochondrial membrane potential in lamprey RBCs was funded by the State Assignment (state registration number N 121102500161-4 to A.A.Yu., K.E.S., and Ch.E.S).
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Conducting experiments and data analysis (E.S.K., A.Yu.A., Ch.E.S); graphic data representation and statistical data processing (E.S.K., Ch.E.S); preparing and correcting a manuscript (M.I.V., G.S.).
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Chelebieva, E.S., Kladchenko, E.S., Mindukshev, I.V. et al. ROS formation, mitochondrial potential and osmotic stability of the lamprey red blood cells: effect of adrenergic stimulation and hypoosmotic stress. Fish Physiol Biochem (2024). https://doi.org/10.1007/s10695-024-01342-5
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DOI: https://doi.org/10.1007/s10695-024-01342-5