Novel Nongenomic Signaling by Glucocorticoid May Involve Changes to Liver Membrane Order in Rainbow Trout

Dindia, Laura; Murray, Josh; Faught, Erin; Davis, Tracy L.; Leonenko, Zoya; Vijayan, Mathilakath M.

doi:10.1371/journal.pone.0046859

Cited by 32 publications

(27 citation statements)

References 44 publications

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“…This is in agreement with our recent finding that cortisol treatment in vitro rapidly fluidizes liver plasma membrane and activates stress-related signaling pathways in trout hepatocytes (12). Most studies have focused on the genomic actions of cortisol in stress adaptation (2), whereas this study highlights a novel rapid action of cortisol that may be nongenomic and involves membrane structure alterations and modulation of stress-related signaling pathways in trout liver.…”

Section: Discussionsupporting

confidence: 91%

“…Recently, we reported that in vitro exposure to cortisol rapidly alters fluidity, surface topography, and elasticity of hepatic plasma membranes in rainbow trout (Oncorhynchus mykiss) (12). In addition to modulating plasma membrane properties, stress levels of cortisol rapidly phosphorylated putative substrate proteins of protein kinase C (PKC), protein kinase A (PKA), and Akt in hepatocytes.…”

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confidence: 99%

“…In addition to modulating plasma membrane properties, stress levels of cortisol rapidly phosphorylated putative substrate proteins of protein kinase C (PKC), protein kinase A (PKA), and Akt in hepatocytes. Benzyl alcohol, a well-documented membrane fluidizer, also activated these kinase pathways, suggesting that changes in membrane fluidity may be initiating stress-signaling cascades in trout hepatic tissue (12). This led us to hypothesize that acute stressorinduced plasma cortisol elevation rapidly alters hepatic membrane order in vivo and may modulate the hepatic response to acute physical stressors.…”

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confidence: 99%

“…All steps, including centrifugation, were carried out at 4°C. The enrichment of the membrane fraction was determined as described previously by measuring the activities of Na ϩ /K ϩ -ATPase (24), 5=-nucleotidase (12), and lactate dehydrogenase (14 The hepatic plasma membrane fluidity of sham and metyrapone-treated trout before and after acute stress was analyzed by measuring the steady-state fluorescence polarization, using the membrane fluorescent probe, 1,6-diphenyl-1,3,5 hexatriene (DPH; Life Technologies, Burlington, ON, Canada) exactly as described previously (12). Membrane samples were added to 96-well opaque plates (100 l with approximate protein concentration of 0.3 mg/ml; Corning) and incubated with DPH (1:100 of 4.7 mM stock dissolved in tetrahydrafuran) in the dark for 30 min.…”

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confidence: 99%

“…All samples were diluted in Laemmli's sample buffer (60 mM Tris·HCl, pH 6.8, 25% glycerol, 2% SDS, 14.4 mM ␤-mercaptoethanol, and 0.1% bromophenol blue), and the immunodetection was carried out exactly as described in Ref. 12. Briefly, total protein (40 g) was separated on 10% SDS-PAGE and transferred to nitrocellulose membrane and blocked with a 5% solution of nonfat dry milk in 1ϫ TTBS (2 mM Tris, 30 mM NaCl, and 0.01% Tween, pH 7.5) for 1 h at room temperature.…”

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Rapid cortisol signaling in response to acute stress involves changes in plasma membrane order in rainbow trout liver

Dindia

Faught

Leonenko

et al. 2013

American Journal of Physiology-Endocrinology and Metabolism

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Dindia L, Faught E, Leonenko Z, Thomas R, Vijayan MM. Rapid cortisol signaling in response to acute stress involves changes in plasma membrane order in rainbow trout liver. Am J Physiol Endocrinol Metab 304: E1157-E1166, 2013. First published March 26, 2013 doi:10.1152/ajpendo.00500.2012.-The activation of genomic signaling in response to stressor-mediated cortisol elevation has been studied extensively in teleosts. However, very little is known about the rapid signaling events elicited by this steroid. We tested the hypothesis that cortisol modulates key stress-related signaling pathways in response to an acute stressor in fish liver. To this end, we investigated the effect of an acute stressor on biophysical properties of plasma membrane and on stressor-related protein phosphorylation in rainbow trout (Oncorhynchus mykiss) liver. A role for cortisol in modulating the acute cellular stress response was ascertained by blocking the stressor-induced elevation of this steroid by metyrapone. The acute stressor exposure increased plasma cortisol levels and liver membrane fluidity (measured by anisotropy of 1,6-diphenyl-1,3,5-hexatriene), but these responses were abolished by metyrapone. Atomic force microscopy further confirmed biophysical alterations in liver plasma membrane in response to stress, including changes in membrane domain topography. The changes in membrane order did not correspond to any changes in membrane fatty acid components after stress, suggesting that changes in membrane structure may be associated with cortisol incorporation into the lipid bilayer. Plasma cortisol elevation poststress correlated positively with activation of intracellular stress signaling pathways, including increased phosphorylation of extracellular signal-related kinases as well as several putative PKA and PKC but not Akt substrate proteins. Together, our results indicate that stressor-induced elevation of plasma cortisol level is associated with alterations in plasma membrane fluidity and rapid activation of stress-related signaling pathways in trout liver. fish; oncorhynchus mykiss; salmonid; glucocorticoid; stress response; membrane fluidity; cell signaling IN RESPONSE TO AN ACUTE STRESSOR, a conserved physiological response is initiated, which involves elevation of stress hormones and subsequent metabolic adjustments, to ensure homeostasis (37). The principal stress hormones, epinephrine and glucocorticoids, have critical functions in the stress adaptation process (9). The fight-or-flight response involves the activation of the sympathetic nervous system, leading to the rapid release of epinephrine from chromaffin cells (9). This catecholamine plays a major role in the acute cardiovascular and metabolic adjustments associated with the fight-or-flight response. The synthesis and release of cortisol, the principal glucocorticoid in teleost, comprises the second phase of the neuroendocrine response, which has a longer-term effect on stress adaptation.

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confidence: 91%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Rapid cortisol signaling in response to acute stress involves changes in plasma membrane order in rainbow trout liver

Dindia

Faught

Leonenko

et al. 2013

American Journal of Physiology-Endocrinology and Metabolism

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

Espinoza

Aedo

Zuloaga

et al. 2016

J of Cellular Biochemistry

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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.

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Localization and Dynamics of Glucocorticoid Receptor at the Plasma Membrane of Activated Mast Cells

Oppong

Hedde

Sekula-Neuner

et al. 2014

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In addition to their actions in the cell nucleus, glucocorticoids exhibit rapid non-nuclear responses that are mechanistically not well understood. To explain these effects, the localization of a glucocorticoid receptor (GR) expressed in mast cells as a GFP fusion was analyzed after activation of the cells on allergenic lipid arrays. These arrays were produced on glass slides by dip-pen nanolithography (DPN) and total internal reflection (TIRF) microscopy was used to visualize the GR. A rapid glucocorticoid-independent and -dependent recruitment of the GR-GFP to the plasma cell membrane was observed following contact of the cells with the allergenic array. In addition, the mobility of the GR at the membrane was monitored by fluorescence recovery after photobleaching (FRAP) and shown to follow binding kinetics demonstrating interactions of the receptor with membrane-bound factors. Furthermore the recruitment of the GR to the cell membrane was shown to result in a glucocorticoid-mediated increase in Erk phosphorylation. This is evidenced by findings that destruction of the membrane composition of the mast cells by cholesterol depletion impairs the membrane localization of the GR and subsequent glucocorticoid-mediated enhancement of Erk phosphorylation. These results demonstrate a membrane localization and function of the GR in mast cell signaling.

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Novel Nongenomic Signaling by Glucocorticoid May Involve Changes to Liver Membrane Order in Rainbow Trout

Cited by 32 publications

References 44 publications

Rapid cortisol signaling in response to acute stress involves changes in plasma membrane order in rainbow trout liver

Rapid cortisol signaling in response to acute stress involves changes in plasma membrane order in rainbow trout liver

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

Localization and Dynamics of Glucocorticoid Receptor at the Plasma Membrane of Activated Mast Cells

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