Hormonal modulation of the heat shock response: insights from fish with divergent cortisol stress responses

Abstract

LeBlanc S, Höglund E, Gilmour KM, Currie S. Hormonal modulation of the heat shock response: insights from fish with divergent cortisol stress responses. Am J Physiol Regul Integr Comp Physiol 302: R184-R192, 2012. First published October 26, 2011 doi:10.1152/ajpregu.00196.2011.-Acute temperature stress in animals results in increases in heat shock proteins (HSPs) and stress hormones. There is evidence that stress hormones influence the magnitude of the heat shock response; however, their role is equivocal. To determine whether and how stress hormones may affect the heat shock response, we capitalized on two lines of rainbow trout specifically bred for their high (HR) and low (LR) cortisol response to stress. We predicted that LR fish, with a low cortisol but high catecholamine response to stress, would induce higher levels of HSPs after acute heat stress than HR trout. We found that HR fish have significantly higher increases in both catecholamines and cortisol compared with LR fish, and LR fish had no appreciable stress hormone response to heat shock. This unexpected finding prevented further interpretation of the hormonal modulation of the heat shock response but provided insight into stress-coping styles and environmental stress. HR fish also had a significantly greater and faster heat shock response and less oxidative protein damage than LR fish. Despite these clear differences in the physiological and cellular responses to heat shock, there were no differences in the thermal tolerance of HR and LR fish. Our results support the hypothesis that responsiveness to environmental change underpins the physiological differences in stress-coping styles. Here, we demonstrate that the heat shock response is a distinguishing feature of the HR and LR lines and suggest that it may have been coselected with the hormonal responses to stress. heat shock protein; catecholamines; heat stress; thermal tolerance; high-responding; low-responding HEAT SHOCK PROTEINS (HSPs) are molecular chaperones responsible for the repair of damaged proteins and assist in folding of new proteins. They increase following cellular stress resulting from exposure to high temperature, ischemia-reperfusion, or oxidative damage, and they have been found in every organism in which they have been sought (13, 21). The putative trigger for HSP induction is an increase in damaged proteins within the cell (1), which frees the heat shock transcription factor (e.g., HSF1) to initiate rapid increases in gene transcription followed by translation into HSPs (31). Although an increase in damaged proteins is likely the primary trigger for HSP induction following stress; stress hormones, including catecholamines and cortisol, influence transcription and translation of HSP genes and proteins. Catecholamines appear to augment stress-induced HSP gene transcripts and proteins in mammals (32, 39, 54), fish (9), and invertebrates (23). The glucocorticoid receptor is chaperoned by several HSPs, mainly the HSP90 and HSP70 families (17), so it is perhaps not surprising tha...

Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is associated with hypoxia tolerance, ventricle size and myoglobin level

“…For example, increased expression of HSC 70 is thought to be related to high temperature tolerance in killifish (Fangue et al, 2006). Instead, our results are consistent with those of a recent study of LeBlanc et al (LeBlanc et al, 2012), who found that rainbow trout with a low cortisol response to stress did not increase HSP/HSC expression after heat stress as much as fish with a high cortisol response and, even though there was significant difference in HPS/HSC levels, CT max values were similar. Perhaps in salmonids, the resting HSP 90β and HSC 70 levels are not as important in defining CT max per se as other cellular and physiological traits.…”

Chaperone roles for TMAO and HSP70 during hyposmotic stress in the spiny dogfish shark (Squalus acanthias)

“…Reconstituted DNase (8 µL; 15,000 U/mL) was added to each aliquot of saline-diluted RBCs along with protease inhibitor cocktail (0.98 mM; Sigma Aldrich). Soluble protein from RBCs was then extracted as in LeBlanc et al (2011). Both tissue and RBC protein concentrations were determined using the Bio-Rad DC Protein Assay for microtitre plates.…”

HSP70 Abundance and Antioxidant Capacity in Feeding and Fasting Gray Seal Pups: Suckling Is Associated with Higher Levels of Key Cellular Defenses

“…Protein extraction and Western blotting were performed to detect and quantify HSP70 in liver, blubber, and plasma as in LeBlanc et al (2012). Lung tissue from the same animals was also examined (data not shown).…”