The gene expression profile of the glucocorticoid receptor 1 (gr1) but not gr2 is modulated in mucosal tissues of gilthead sea bream (Sparus aurata) exposed to acute air-exposure stress

Abstract

The perception of an acute stressor (short-duration; high-intensity) induces a physiological response that activates the hypothalamic-pituitary-interrenal (HPI) axis and the subsequent release of cortisol. Cortisol carries out its effect at the molecular level through its recognition by the mineralocorticoid receptor (MR) and the glucocorticoid receptor (GR). Recently, we unveiled the nucleotide sequence of the glucocorticoid receptor 1 (gr1) and gr2 in gilthead sea bream (Sparus aurata). Importantly, GR1 and GR2 respond to different levels of cortisol concentration in fish and, consequently, play a differential role in the stress response. To date, and despite their relevance, no data describes the modulation of these receptors in response to an acute stressor in gilthead sea bream (S. aurata). In this study, we evaluated the kinetics of modulation of cortisol receptors expression (gr1, gr2, mr), and its similarity with the expression pattern of selected genes associated with stress (hsp70; enolase) and immune response (lysozyme; c3; il-1β; tnf-α; il-10; tgf-β1) in gilthead sea bream mucosal tissues (skin; gills; anterior gut). To do it, fish were acutely stressed by three-minute air exposure, and the expression profile was evaluated at zero, 1 h, 6 h, and 24 h post-stress (hps). The cortisol level in plasma and skin mucus peaked at 1 hps. All the mucosal tissues showed a time-dependent and tissue-specific upregulation of gr1 and mr. The immune-related genes showed the upregulation of il-1β at 6 hps (gills; anterior gut), and tnf-α and c3 at 24 hps (anterior gut). Taking together, our study concludes that fish subjected to three-minute air exposure modulated the expression of gr1 but not gr2 in mucosal tissues (skin; gills; anterior gut). Furthermore, our data reinforce the idea of a stimulatory effect induced in genes associated with the innate immune response after acute stress but focused at the mucosal level and in a time- and tissue-dependent manner.

The insertion/deletion in the DNA-binding region allows the discrimination and subsequent identification of the glucocorticoid receptor 1 (gr1) and gr2 nucleotide sequences in gilthead sea bream (Sparus aurata): Standardizing the gr nomenclature for a better understanding of the stress response in teleost fish species

“…In the particular context of gilthead sea bream, it remains to elucidate the effect of the stress response upon the modulation of the gr1 and gr2 at the gene expression level. In this context, a recent study revealed that in mucosal tissues gr1 but not gr2 is modulated in gilthead sea bream exposed to acute airexposure stress (Vallejos-Vidal et al, 2022).…”

Transcriptional Evaluation of Neuropeptides, Hormones, and Tissue Repair Modulators in the Skin of Gilthead Sea Bream (Sparus aurata L.) Subjected to Mechanical Damage

“…In terms of the dynamic of the response, the evaluation of more time points in the experimental design will provide a clearer perspective on expression dynamics at dorsal and ventral lesions, particularly of those markers that, in our study, only showed downregulation or an increased trend (but not significant). In this way, the analysis of the activation of the stress response and transcriptional activity at earlier times (i.e., 1-, 6-, and 24-hours post-injury as a measure to evaluate the immediate effect of the stimulus [ 4 , 62 , 63 ]) will shed light on the mode of action orchestrated by different systems to ensure tissue repair, defense, and protection of the organism.…”

Validation of Non-lethal Biopsy Techniques in Freshwater Fish

“…Although beneficial for short term stress response, long-term upregulation may sequester energy from other essential functions (e.g., growth, reproduction, osmoregulation) (Kennedy and Janz 2023). The degree to which cortisol levels (and subsequent upregulation of Glucocorticoid Receptor 1) can vary widely between fish species (Vallejos-Vidal et al 2022), and quantification of stress based on expression requires specific previous knowledge on species and population (Aedo et al 2023). Given that no baseline is currently known for the Sandusky River spawning population, the important distinction in our study is that Glucocorticoid Receptor 1 expression was found to be consistent both across time periods (pre and post sampling) and across treatment groups (gill biopsy and combined treatment).…”

“…2021) that has evaluated the stress response in fish using expression of Glucocorticoid Receptor 1 has indicated that short-term stressors (e.g., air exposure, handling) result in increased expression or GR1 in a time and tissue dependent manner. Although this may be specific to individual species, generally GR1 expression is found to decrease within 24 hours of exposure to the stressor (Vallejos-Vidal et al 2022). In the case of chronic stress, however, GR1 expression remains elevated for longer durations (days to weeks; Tort 2011).…”

“…Additionally, taking samples from different tissues and expanding upon timepoints at which tissues were collected may provide greater context to the stress and immune response. In Vallejos-Vidal et al 2022, cortisol levels were noted to spike in blood and skin samples of Sea Bream (Sparus aurata) between 1-and 6-hours post air exposure.…”