A novel role for pigment genes in the stress response in rainbow trout (Oncorhynchus mykiss)

Khan, Uniza W.; Øverli, Øyvind; Hinkle, Patricia M.; Pasha, Farhan Ahmad; Johansen, Ida Beitnes; Berget, Ingunn; Silva, Patricia I.M.; Kittilsen, Silje; Höglund, Erik; Omholt, Stig W.; Våge, Dag Inge

doi:10.1038/srep28969

Cited by 20 publications

(17 citation statements)

References 58 publications

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“…To conclude, we think that the newly available matrices and measuring tools for quantifying cortisol will continue to increase interest towards this steroid for research on well‐being and life histories. However, other proxies to describe stress in fish should not be ignored; e.g ., behaviour (Sadoul et al, ), skin pigment colour (Khan et al, ), oxygen consumption (Madaro et al, ) or cardiac rhythm (Laitinen & Valtonen, ) have all been proposed as fruitful monitoring tools for measuring stress in fishes.…”

Section: Towards a Gold Standardmentioning

confidence: 99%

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Measuring cortisol, the major stress hormone in fishes

Sadoul

Geffroy

2019

Journal of Fish Biology

247

141

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Stress in teleosts is an increasingly studied topic because of its interaction with growth, reproduction, immune system and ultimately fitness of the animal. Whether it is for evaluating welfare in aquaculture, adaptive capacities in fish ecology, or to investigate effects of human‐induced rapid environmental change, new experimental methods to describe stress physiology in captive or wild fish have flourished. Cortisol has proven to be a reliable indicator of stress and is considered the major stress hormone. Initially principally measured in blood, cortisol measurement methods are now evolving towards lower invasiveness and to allow repeated measurements over time. We present an overview of recent achievements in the field of cortisol measurement in fishes, discussing new alternatives to blood, whole body and eggs as matrices for cortisol measurement, notably mucus, faeces, water, scales and fins. In parallel, new analytical tools are being developed to increase specificity, sensitivity and automation of the measure. The review provides the founding principles of these techniques and introduces their potential as continuous monitoring tools. Finally, we consider promising avenues of research that could be prioritised in the field of stress physiology of fishes.

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Section: Towards a Gold Standardmentioning

confidence: 99%

“…However, other proxies to describe stress in fish should not be ignored; e.g., behaviour (Sadoul et al, 2014), skin pigment colour (Khan et al, 2016), oxygen consumption (Madaro et al, 2018) or cardiac rhythm (Laitinen & Valtonen, 1994) have all been proposed as fruitful monitoring tools for measuring stress in fishes.…”

Section: Towards a Gold Standardmentioning

confidence: 99%

Measuring cortisol, the major stress hormone in fishes

Sadoul

Geffroy

2019

Journal of Fish Biology

247

141

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“…We previously established a link between cortisol responsiveness to stress and cardiac remodelling in rainbow trout (Oncorhynchus mykiss) high responsive (HR) and low responsive (LR) strains and wild-type brown trout (Salmo trutta) (Johansen et al, 2011). High post-stress cortisol production is also associated with a range of behavioural and cognitive traits indicating a reactive coping style (Øverli et al, 2005Sørensen et al, 2013), rendering the salmonids a productive model to study proximate physiological mechanisms underlying consistent trait associations (Khan et al, 2016). Regarding cardiac function, individuals responding to stress with high cortisol levels (HR fish) have notably larger ventricles compared with individuals with a low cortisol response (LR fish).…”

Section: Introductionmentioning

confidence: 99%

Bigger is not better: cortisol-induced cardiac growth and dysfunction in salmonids

Johansen

Sandblom

Skov

et al. 2017

Journal of Experimental Biology

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Stress and elevated cortisol levels are associated with pathological heart growth and cardiovascular disease in humans and other mammals. We recently established a link between heritable variation in post-stress cortisol production and cardiac growth in salmonid fish too. A conserved stimulatory effect of the otherwise catabolic steroid hormone cortisol is probably implied, but has to date not been established experimentally. Furthermore, whereas cardiac growth is associated with failure of the mammalian heart, pathological cardiac hypertrophy has not previously been described in fish. Here, we show that rainbow trout (Oncorhynchus mykiss) treated with cortisol in the diet for 45 days have enlarged hearts with lower maximum stroke volume and cardiac output. In accordance with impaired cardiac performance, overall circulatory oxygen-transporting capacity was diminished as indicated by reduced aerobic swimming performance. In contrast to the well-known adaptive/physiological heart growth observed in fish, cortisol-induced growth is maladaptive. Furthermore, the observed heart growth was associated with up-regulated signature genes of mammalian cardiac pathology, suggesting that signalling pathways mediating cortisol-induced cardiac remodelling in fish are conserved from fish to mammals. Altogether, we show that excessive cortisol can induce pathological cardiac remodelling. This is the first study to report and integrate the etiology, physiology and molecular biology of cortisol-induced pathological remodelling in fish.

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“…Moreover, the significant correlation between the expression of mc2r and resting plasma cortisol levels suggests that the expression of mc2r between LR and HR fish could partly explain the differences in resting cortisol concentrations between these phenotypes. A higher expression of mc2r in HR than LR fish has also been reported in rainbow trout head kidney [ 27 ], leading these authors to suggest that this explained the increased cortisol response to ACTH observed in HR fish by [ 26 ].…”

Section: Discussionmentioning

confidence: 93%

“…In rainbow trout, higher cortisol production in HR compared to LR fish has been observed after stimulation with ACTH [ 26 ]. Moreover, higher expression of mc2r in the head kidney of these fish has been reported [ 27 ]. Additionally, an upregulation of mRNA expression of genes encoding for enzymes regulating cortisol synthesis (StAR, P450scc, 3βHSD) has been observed in HR individuals of Atlantic cod, Gadus morhua , [ 15 ].…”

Section: Introductionmentioning

confidence: 99%

Regulation of divergent cortisol responsiveness in European sea bass, Dicentrarchus labrax L.

Σαμαράς¹,

Pavlidis²

2018

PLoS ONE

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Mechanisms regulating differences in cortisol responsiveness between low (LR) and high response (HR) individuals have been poorly studied. In this context, we aimed to study key regulatory processes in cortisol dynamics at the head kidneys of LR and HR European sea bass. To do so, resting plasma cortisol and ACTH concentrations were quantified in these fish. Additionally, the head kidneys of these individuals were superfused through an in vitro superfusion system and stimulated with the same amount of ACTH to assess their cortisol biosynthetic capacity. Moreover, the expression of important genes in cortisol regulation was assessed. Results showed that LR fish had lower resting cortisol concentrations than HR, although no differences existed in the circulating levels of ACTH. Additionally, the biosynthetic capacity of HR was higher than that of LR fish when in vitro stimulated with ACTH. At the molecular level, a statistically significant 3.4-fold higher expression of the ACTH receptor, mc2r, and a 2.3-fold, though not significant, higher expression of 11β-hydroxylase (cyp11b1), an enzyme involved in cortisol biosynthesis, was observed in the HR fish. Finally, a statistically significant 1.3-fold lower expression of 11β-hydroxysteroid dehydrogenase 2 (hsd11b2), an enzyme involved in cortisol inactivation, was observed in HR when compared to LR fish. Therefore, it was for the first time indicated that cortisol dynamics can also be regulated at the post-production level in the head kidney. Collectively, our results highlight the crucial role of the interrenal tissue in the regulation of differences in cortisol response between LR and HR sea bass individuals.

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A novel role for pigment genes in the stress response in rainbow trout (Oncorhynchus mykiss)

Cited by 20 publications

References 58 publications

Measuring cortisol, the major stress hormone in fishes

Measuring cortisol, the major stress hormone in fishes

Bigger is not better: cortisol-induced cardiac growth and dysfunction in salmonids

Regulation of divergent cortisol responsiveness in European sea bass, Dicentrarchus labrax L.

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