Proteomic profiling of rapid non-genomic and concomitant genomic effects of acute restraint stress on rat thymocytes

Billing, Anja M.; Revets, Dominique; Hoffmann, Céline; Turner, Jonathan D.; Vernocchi, Sara

doi:10.1016/j.jprot.2012.01.008

Cited by 13 publications

(10 citation statements)

References 63 publications

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“…Higher concentrations of Cort-BSA may have elicited stronger GC effects, but their physiological relevance could be questionable. Interestingly, our proteomic experiments are in direct agreement with another recent 2D-DIGE study from our laboratory (40). After acute stress in vivo similar fold changes were observed in an overlapping set of proteins in rat thymocytes.…”

Section: Discussionsupporting

confidence: 91%

Membrane Glucocorticoid Receptor Activation Induces Proteomic Changes Aligning with Classical Glucocorticoid Effects

Vernocchi

Battello

Schmitz

et al. 2013

Molecular & Cellular Proteomics

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Glucocorticoids exert rapid nongenomic effects by several mechanisms including the activation of a membranebound glucocorticoid receptor (mGR). Here, we report the first proteomic study on the effects of mGR activation by BSA-conjugated cortisol (Cort-BSA). A subset of target proteins in the proteomic data set was validated by Western blot and we found them responding to mGR activation by BSA-conjugated cortisol in three additional cell lines, indicating a conserved effect in cells originating from different tissues. Changes in the proteome of BSA-conjugated cortisol treated CCRF-CEM leukemia cells were associated with early and rapid pro-apoptotic, immunemodulatory and metabolic effects aligning with and possibly "priming" classical activities of the cytosolic glucocorticoid receptor (cGR). PCR arrays investigating target genes of the major signaling pathways indicated that the mGR does not exert its effects through the transcriptional activity of any of the most common kinases in these leukemic cells, but RhoA signaling emerged from our pathway analysis. All cell lines tested displayed very low levels of mGR on their surface. Highly sensitive and specific in situ proximity ligation assay visualized low numbers of mGR even in cells previously thought to be mGR negative. We obtained similar results when using three distinct anti-GR monoclonal antibodies directed against the N-terminal half of the cGR. This strongly suggests that the mGR and the cGR have a high sequence homology and most probably originate from the same gene. Furthermore, the mGR appears to reside in caveolae and its association with caveolin-1 (Cav-1) was clearly detected in two of the four cell lines investigated using double recognition proximity ligation assay. Our results indicate however that Cav-1 is not necessary for membrane localization of the GR since CCRF-CEM and Jurkat cells have a functional mGR, but did not express this caveolar protein. However, if expressed, this membrane protein dimerizes with the mGR modulating its function. Molecular & Cellular

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Section: Discussionsupporting

confidence: 91%

Membrane Glucocorticoid Receptor Activation Induces Proteomic Changes Aligning with Classical Glucocorticoid Effects

Vernocchi

Battello

Schmitz

et al. 2013

Molecular & Cellular Proteomics

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“…These dams were kept on the same original supplementation until weaning of the litter of the second generation, when the pups were supplemented until 40 days of age. At day 41, adolescent male rats of each supplemented group (n = 7) were exposed to the acute restrain stress (AS) procedure [48]. After 24 h of AS exposure, animals were submitted to behavioral assessments.…”

Section: Methodsmentioning

confidence: 99%

Chronic consumption of trans fat can facilitate the development of hyperactive behavior in rats

Pase

Trevizol

Kuhn

et al. 2015

Physiology & Behavior

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“…Within the liver, the genomic effects of cortisol involve changes in the expression of genes involved in intermediary metabolic regulation (2,30). Although several studies have examined the genomic effects associated with stressor-induced plasma cortisol elevation (2,30,46), few have investigated the rapid, nongenomic effects of this steroid on peripheral tissues (4).…”

mentioning

confidence: 99%

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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Proteomic profiling of rapid non-genomic and concomitant genomic effects of acute restraint stress on rat thymocytes

Cited by 13 publications

References 63 publications

Membrane Glucocorticoid Receptor Activation Induces Proteomic Changes Aligning with Classical Glucocorticoid Effects

Membrane Glucocorticoid Receptor Activation Induces Proteomic Changes Aligning with Classical Glucocorticoid Effects

Chronic consumption of trans fat can facilitate the development of hyperactive behavior in rats

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

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