Tryptophan Modulatory Role in European Seabass (Dicentrarchus labrax) Immune Response to Acute Inflammation under Stressful Conditions

Abstract

The present work aimed to study the role of dietary tryptophan supplementation in modulating the European seabass (Dicentrarchus labrax) immune condition during stressful rearing conditions (i.e., 15 days exposure to high density), as well as the immune response to acute inflammation after intraperitoneal injection of a bacterial pathogen. Stress alone did not compromise seabass health indicators. In contrast, a clear peripheral and local inflammatory response was observed in response to the inoculated bacteria. Moreover, exposure to a high stocking density seemed to exacerbate the inflammatory response at early sampling points, compared to fish stocked at a lower density. In contrast, stressed fish presented some immune-suppressing effects on the T-cell surface glycoprotein receptor expressions at a late sampling point following inflammation. Regarding the effects of dietary tryptophan, no changes were observed on seabass immune indicators prior to inflammation, while a small number of immunosuppressive effects were observed in response to inflammation, supporting tryptophan’s role in the promotion of immune-tolerance signals during inflammation. Nonetheless, tryptophan dietary supplementation improved the inflammatory response against a bacterial pathogen during stressful conditions, supported by a reduction of plasma cortisol levels, an up-regulation of several immune-related genes at 48 h, and an inversion of the previously observed, stress-induced T-cell suppression. Finally, the involvement of tryptophan catabolism in macrophages was confirmed by the up-regulation of genes involved in the kynurenine pathway. The present study brings new insights regarding the immune modulatory role of tryptophan during stressful conditions in fish, thus allowing for the development of novel prophylactic protocols during vaccination by intraperitoneal injection in the European seabass.

Dietary tryptophan intervention counteracts stress-induced transcriptional changes in a teleost fish HPI axis during inflammation

“…The attenuation of transcription rates of serotonin-related genes in these groups pointed again to a TRP-led condition that implies changes in serotonergic activity. The abovementioned lessened state of neuroendocrine activation was translated into a general reduction of circulating cortisol levels observed in a parallel approach 28 , and highlights a soothing effect of dietary tryptophan during stressful conditions. These results are therefore in line with previous approaches in rainbow trout 25,26 and Senegalese sole 29 , where a dietary tryptophan intervention has a clear impact on stressed trout cortisol levels and was efficient in increasing disease resistance of stressed sole against bacterial infection.…”

“…7). This was reflected by a further enhancement of regulatory mechanisms www.nature.com/scientificreports/ (anti-inflammatory cytokines and glucocorticoid receptors) but also by lower ACTH-precursor transcripts, that ultimately reduced peripheral cortisol levels (parallel approach by Machado et al 28 ).…”

“…A classic inflammation panorama is characterized by an early increase of pro-inflammatory cytokines such as IL1β in the head-kidney, and indeed a robust upregulation of il1β was observed in the head-kidney of i.p. injected fish, irrespective of dietary treatment 28 . Tryptophan dietary supplementation did not seem to significantly affect gene expression in the head-kidney during the inflammatory response, but it induced changes at the brain and pituitary gland levels.…”

“…The inflammatory bacterial challenge was performed using Photobacterium damselae piscicida (Phdp) strain PP3, isolated from yellowtail (Seriola quinqueradiata; Japan) by Doctor Andrew C. Barnes (Marine Laboratory, Aberdeen, UK), following the methodology described in Machado et al 28 .…”

“…Interestingly, a different, recently published approach to the hereby presented experiment, reported several changes in the inflammatory response of Photobacterium damselae subsp. piscicida (Phdp)-infected seabass when fish were given a tryptophan surplus for 15 days, such as upregulation of immune-related genes, the inversion of the stress-induced T-cell suppression and an impairment of bacterial injection-induced cortisol production 28 . Moreover, chronically stressed Senegalese sole (i.e., held at high stocking density) fed a tryptophan-supplemented diet (4× the requirement level) for 38 days presented an alleviated stress response (lower cortisol levels and downregulation of pro-opiomelanocortin gene expression) that enabled a more efficient immune response and increased disease resistance 29 .…”