Cortisol Induces Reactive Oxygen Species Through a Membrane Glucocorticoid Receptor in Rainbow Trout Myotubes

Abstract

Cortisol is an essential regulator of neuroendocrine stress responses in teleosts. Cortisol predominantly affects target tissues through the genomic pathway, which involves interacting with cytoplasmic glucocorticoid receptors, and thereby, modulating stress-response gene expressions. Cortisol also produces rapid effects via non-genomic pathways, which do not involve gene transcription. Although cortisol-mediated genomic pathways are well documented in teleosts, non-genomic pathways are not fully understood. Moreover, no studies have focused on the contribution of non-genomic cortisol pathways in compensatory stress responses in fish. In this study, rainbow trout (Oncorhynchus mykiss) skeletal myotubes were stimulated with physiological concentrations of cortisol and cortisol-BSA, a membrane-impermeable agent, resulting in an early induction of reactive oxygen species (ROS). This production was not suppressed by transcription or translation inhibitors, suggesting non-genomic pathway involvement. Moreover, myotube preincubation with RU486 and NAC completely suppressed cortisol- and cortisol-BSA-induced ROS production. Subcellular fractionation analysis revealed the presence of cell membrane glucocorticoid receptors. Finally, cortisol-BSA induced a significant increase in ERK1/2 and CREB phosphorylation, as well as in CREB-dependent transcriptional activation of the pgc1a gene expression. The obtained results strongly suggest that cortisol acts through a non-genomic glucocorticoid receptor-mediated pathway to induce ROS production and contribute to ERK/CREB/PGC1-α signaling pathway activation as stress compensation mechanisms. J. Cell. Biochem. 118: 718-725, 2017. © 2016 Wiley Periodicals, Inc.

Melatonin promotes secondary hair follicle development of early postnatal cashmere goat and improves cashmere quantity and quality by enhancing antioxidant capacity and suppressing apoptosis

“…Studies in Merino sheep showed that the initiation and maturation of secondary follicles during fetal life and early postnatal period were inhibited by malnutrition, this may be attributed to the reactive oxygen species (ROS) production and oxidative stress induced by malnutrition . In addition, studies on Merino sheep showed that secondary follicle development during fetal and early postnatal period under normal conditions was suppressed by plasma cortisol, a stress‐related hormone that was reported to induce ROS production and oxidative stress …”

“…[23][24][25] In addition, studies on Merino sheep showed that secondary follicle development during fetal and early postnatal period under normal conditions was suppressed by plasma cortisol, 17,18,26,27 a stress-related hormone that was reported to induce ROS production and oxidative stress. 28,29 Development of secondary follicles involves complex epithelium-mesenchyme interactions between follicular epithelial keratinocytes and underlying mesenchymal cells in the dermis 30,31 and depends on a delicate balance between cell proliferation and apoptosis. 32,33 Excessive ROS generation causes damage to all cellular components including proteins, lipids, and DNA and triggers apoptosis of mesenchymal stem cells (MSCs) and epithelial stem cells that are the progenitors of secondary hair follicle cells.…”

Contribution of Non-canonical Cortisol Actions in the Early Modulation of Glucose Metabolism of Gilthead Sea Bream (Sparus aurata)

“…In fish models, the non-genomic cortisol actions have been associated with the suppression of phagocytosis in the freshwater teleost Channa punctatus (17) and with the increased plasma membrane fluidity and activation of protein kinase cAMP-dependent (PKA), protein kinase B (PKB), and protein kinase C (PKC) signaling pathways in rainbow trout hepatocytes (20, 21). In addition, this cortisol action also induces the extracellular signal-regulated kinase (ERK)—cAMP-responsive element binding protein (CREB) signaling pathways activation and the up regulation of peroxisome proliferator-activated receptor γ co-activator 1 α ( pgc1a) expression in isolated rainbow trout myotubes (22). Even though, the mechanisms involved in the non-genomic cortisol pathways are complex and diverses, the impact in the adaptive response in fish are far from clear (23).…”

Maternal stress and fish reproduction: The role of cortisol revisited

“…Cortisol action on target tissues includes activation of the intracellular glucocorticoid receptor (GR) and/or the mineralocorticoid receptor (MR) as ligand‐bound transcription factors which are ubiquitously expressed (Faught, Aluru, & Vijayan, ; Mommsen et al., ; Stolte, Verburg van Kemenade, Savelkoul, & Flik, ). Recent work has also implicated the possibility of nongenomic and rapid cortisol signalling in fish tissues, including pituitary (Borski, Hyde, & Fruchtman, ), liver (Dindia, Faught, Leonenko, Thomas, & Vijayan, ; Dindia et al., ), gill and brain (Sunny, Lakshmy, & Oommen, ) and myotubes (Espinoza et al., ). While the primary role of cortisol during stress is energy repartitioning to metabolically allow the animals to cope with stressor insult (Pankhurst, ), the effect on reproduction is generally considered inhibitory (Pankhurst, ; Pankhurst & Van Der Kraak, ; Schreck et al., ).…”