Early transcriptomic responses associated with the membrane-initiated action of cortisol in the skeletal muscle of rainbow trout (Oncorhynchus mykiss)

Abstract

Cortisol is a critical neuroendocrine regulator of the stress response in fish. Cortisol practically affects all tissues by interacting with an intracellular receptor and modulating target gene expression. However, cortisol also interacts with components of the plasma membrane in a nongenomic process that activates rapid signaling. Until now, the implication of this novel cortisol signaling for the global transcriptional response has not been explored. In the present work, we evaluated the effects of the membrane-initiated actions of cortisol on the in vivo transcriptome of rainbow trout ( Oncorhynchus mykiss) skeletal muscle. RNA-Seq analyses were performed to examine the transcriptomic changes in rainbow trout stimulated by physiological concentrations of cortisol and cortisol coupled with bovine serum albumin (cortisol-BSA), a membrane-impermeable analog of cortisol. A total of 660 million paired-ends reads were generated. Reads mapped onto the reference genome revealed that 1,737; 897; and 1,012 transcripts were differentially expressed after 1, 3, and 9 h of cortisol-BSA treatment, respectively. Gene Ontology analysis showed that this novel action of cortisol modulates several biological processes, such as mRNA processing, ubiquitin-dependent protein catabolic processes, and transcription regulation. In addition, a KEGG analysis revealed that focal adhesion was the main signaling pathway that was upregulated at all the times tested. Taking these results together, we propose that the membrane-initiated cortisol action contributes significantly in the regulation of stress-mediated gene expression.

RNA-Seq-Based Analysis of Cortisol-Induced Differential Gene Expression Associated with Piscirickettsia salmonis Infection in Rainbow Trout (Oncorhynchus mykiss) Myotubes

“…Here, we performed RNA-seq analysis to evaluate the effects of cortisol on rainbow trout myotubes infected with P. salmonis. The quality obtained from RNA-seq data was as expected, and the mapping results against the rainbow trout reference genome were in line with studies using this strategy [25,38]. According to these results, other recent reports in trout presented similar results using comparable parameters of RNA-seq analysis [39,40].…”

“…Additionally, CTRL and INF, but without cortisol, were included as controls during the assay. All RNA-seq analyses were performed according to [ 25 ], with minor modifications. Briefly, raw reads were visualized using CLC Genomic Workbench 9.0 software.…”

Consequences of pharmacophagous uptake from plants and conspecifics in a sawfly elucidated using chemical and molecular techniques

“…The cGMP-PKG signalling pathway was also significantly upregulated in AC+ individuals compared to both the control (C-) and C+ and plays a role in a number of processes including muscle contraction and memory formation in insects (Matsumoto et al, 2018). Furthermore, the focal adhesion pathway, the turnover of which increases with stress (Aedo et al, 2019), was significantly upregulated in AC+ individuals compared to the control (C-). Finally, the 'ribosome' pathway was significantly downregulated in AC+ individuals in comparison to the two other treatments and interestingly it was also downregulated in C+ compared to the control (C-).…”

Differential Metabolic and Transcriptional Responses of Gilthead Seabream (Sparus aurata) Administered with Cortisol or Cortisol-BSA

“…Overall, cortisol metabolic effects are associated with classical/genomic mechanisms involving interaction of intracellular glucocorticoid (GR) and mineralocorticoid receptors (MR), and the subsequent regulation of target genes [ 15 ]. Additionally, cortisol can also interact with plasma membrane-localized components activating rapid/intracellular GR-independent signaling pathways with novel features related to early compensatory responses to stress [ 16 , 17 , 18 ]. In this context, we recently determined that short-term cortisol treatment (1 to 6 h) triggers a metabolic response in the liver of gilthead seabream, characterized by glucose and lactate plasma levels enhancement, hepatic glucose, and glycogen mobilization, as well as the regulation of both glycolysis and gluconeogenesis-related genes [ 16 ].…”

“…In this context, we recently determined that short-term cortisol treatment (1 to 6 h) triggers a metabolic response in the liver of gilthead seabream, characterized by glucose and lactate plasma levels enhancement, hepatic glucose, and glycogen mobilization, as well as the regulation of both glycolysis and gluconeogenesis-related genes [ 16 ]. All these metabolic effects were further validated using a specific impermeable-membrane cortisol analog, cortisol-BSA [ 16 , 17 ]. Nevertheless, as of yet, the contribution of long-term membrane-initiated cortisol action on metabolic responses in fish remains unknown.…”