Functional Genomics of Stress Responses in Fish

Prunet, Patrick; Cairns, Michael T.; Winberg, Svante; Pottinger, T.G.

doi:10.1080/10641260802341838

Cited by 50 publications

(29 citation statements)

References 68 publications

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“…Given the ecological and economic importance of fishes, functional genomic approaches are being increasingly favored for exploration of the interaction between fishes and their abiotic environment through the modulation of GE (Cossins and Crawford, 2005;Goetz and MacKenzie, 2008;Prunet et al, 2008;Hook, 2010;Tort and Teles, 2012). Fish are poikilotherms that often inhabit thermally variable environments and many aspects of their biology are acutely attuned to temperature.…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic responses to environmental temperature in eurythermal and stenothermal fishes

Logan

Buckley

2015

Journal of Experimental Biology

138

116

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Ectothermic species like fishes differ greatly in the thermal ranges they tolerate; some eurythermal species may encounter temperature ranges in excess of 25°C, whereas stenothermal species in polar and tropical waters live at essentially constant temperatures. Thermal specialization comes with fitness trade-offs and as temperature increases due to global warming, the physiological basis of specialization and thermal plasticity has become of great interest. Over the past 50 years, comparative physiologists have studied the physiological and molecular differences between stenothermal and eurythermal fishes. It is now well known that many stenothermal fishes have lost an inducible heat shock response (HSR). Recent advances in transcriptomics have now made it possible to examine genome-wide changes in gene expression (GE) in non-model ecologically important fish, broadening our view beyond the HSR to regulation of genes involved in hundreds of other cellular processes. Here, we review the major findings from transcriptomic studies of extreme eurythermal and stenothermal fishes in response to acute and long-term exposure to temperature, both time scales being critically important for predicting climate change responses. We consider possible molecular adaptations that underlie eurythermy and stenothermy in teleosts. Furthermore, we highlight the challenges that still face the field of comparative environmental genomics and suggest fruitful paths of future investigation.

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Section: Introductionmentioning

confidence: 99%

Transcriptomic responses to environmental temperature in eurythermal and stenothermal fishes

Logan

Buckley

2015

Journal of Experimental Biology

138

116

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“…A key target tissue involved in metabolic adjustments during stress adaptation is the liver. 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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“…The proximate and ultimate mechanisms involved in maintaining individual variation in stress-coping style are, however, poorly understood in teleost fishes. Both genetic and environmental factors contribute to extensive inter-individual variation in how stress affects individuals (e.g., Øverli et al 2007;Prunet et al 2008). A direct link between coping style and variation in gene expression as a response to adaptive physiological changes was recently described in a teleost fish species, the common carp Cyprinus carpio (MacKenzie et al 2009).…”

Section: Coping Style and Individual Variationmentioning

confidence: 98%

“…While the analysis of candidate genes has provided useful information on particular mechanisms underlying the physiology of stress response and could lead to description of biomarkers for stress responses, genomic screening approaches using microarray technology have been recently applied to the study of the stress responses in fish (see review Prunet et al 2008). These new approaches provide a system-wide assessment of alterations of gene expression which should generate both overviews of the biological pathways involved in the stress responses (Cossins et al 2006).…”

Section: Functional Genomics Studies and Fish Welfarementioning

confidence: 99%

Fish welfare and genomics

Prunet¹,

Øverli

Douxfils

et al. 2011

Fish Physiol Biochem

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There is a considerable public and scientific debate concerning welfare of fish in aquaculture. In this review, we will consider fish welfare as an integration of physiological, behavioral, and cognitive/emotional responses, all of which are essentially adaptative responses to stressful situations. An overview of fish welfare in this context suggests that understanding will rely on knowledge of all components of allostatic responses to stress and environmental perturbations. The development of genomic technologies provides new approaches to this task, exemplified by how genome-wide analysis of genetic structures and corresponding expression patterns can lead to the discovery of new aspects of adaptative responses. We will illustrate how the genomic approach may give rise to new biomarkers for fish welfare and also increase our understanding of the interaction between physiological, behavioral, and emotional responses. In a first part, we present data on expression of candidate genes selected a priori. This is a common avenue to develop molecular biomarkers capable of diagnosing a stress condition at its earliest onset, in order to allow quick corrective intervention in an aquaculture setting. However, most of these studies address isolated physiological functions and stress responses that may not be truly indicative of animal welfare, and there is only rudimentary understanding of genes related to possible cognitive and emotional responses in fish. We also present an overview on transcriptomic analysis related to the effect of aquaculture stressors, environmental changes (temperature, salinity, hypoxia), or concerning specific behavioral patterns. These studies illustrate the potential of genomic approaches to characterize the complexity of the molecular mechanisms which underlies not only physiological but also behavioral responses in relation to fish welfare. Thirdly, we address proteomic studies on biological responses to stressors such as salinity change and hypoxia. We will also consider proteomic studies developed in mammals in relation to anxiety and depressive status which may lead to new potential candidates in fish. Finally, in the conclusion, we will suggest new developments to facilitate an integrated view of fish welfare. This includes use of laser microdissection in the transcriptomic/proteomic studies, development of meta-analysis methods for extracting information from genomic data sets, and implementation of technological advances for high-throughput proteomic studies. Development of these new approaches should be as productive for our understanding of the biological processes underlying fish welfare as it has been for the progress of pathophysiological research.

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Functional Genomics of Stress Responses in Fish

Cited by 50 publications

References 68 publications

Transcriptomic responses to environmental temperature in eurythermal and stenothermal fishes

Transcriptomic responses to environmental temperature in eurythermal and stenothermal fishes

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

Fish welfare and genomics

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