scholarly journals Endoplasmic reticulum stress as a key mechanism in stunted growth of seawater rainbow trout (Oncorhynchus mykiss)

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Bernat Morro ◽  
Richard Broughton ◽  
Pablo Balseiro ◽  
Sigurd O. Handeland ◽  
Simon Mackenzie ◽  
...  

Abstract Background Rainbow trout (Oncorhynchus mykiss) is a salmonid species with a complex life-history. Wild populations are naturally divided into freshwater residents and sea-run migrants. Migrants undergo an energy-demanding adaptation for life in seawater, known as smoltification, while freshwater residents display these changes in an attenuated magnitude and rate. Despite this, in seawater rainbow trout farming all fish are transferred to seawater. Under these circumstances, weeks after seawater transfer, a significant portion of the fish die (around 10%) or experience growth stunting (GS; around 10%), which represents an important profitability and welfare issue. The underlying causes leading to GS in seawater-transferred rainbow trout remain unknown. In this study, we aimed at characterising the GS phenotype in seawater-transferred rainbow trout using untargeted and targeted approaches. To this end, the liver proteome (LC-MS/MS) and lipidome (LC-MS) of GS and fast-growing phenotypes were profiled to identify molecules and processes that are characteristic of the GS phenotype. Moreover, the transcription, abundance or activity of key proteins and hormones related to osmoregulation (Gill Na+, K + –ATPase activity), growth (plasma IGF-I, and liver igf1, igfbp1b, ghr1 and ctsl) and stress (plasma cortisol) were measured using targeted approaches. Results No differences in Gill Na+, K + –ATPase activity and plasma cortisol were detected between the two groups. However, a significant downregulation in plasma IGF-I and liver igf1 transcription pointed at this growth factor as an important pathomechanism for GS. Changes in the liver proteome revealed reactive-oxygen-species-mediated endoplasmic reticulum stress as a key mechanism underlying the GS phenotype. From the lipidomic analysis, key observations include a reduction in triacylglycerols and elevated amounts of cardiolipins, a characteristic lipid class associated with oxidative stress, in GS phenotype. Conclusion While the triggers to the activation of endoplasmic reticulum stress are still unknown, data from this study point towards a nutritional deficiency as an underlying driver of this phenotype.

2021 ◽  
Author(s):  
Bernat Morro ◽  
Richard Broughton ◽  
Pablo Balseiro ◽  
Sigurd O. Handeland ◽  
Simon Mackenzie ◽  
...  

Abstract Background: Rainbow trout (Oncorhynchus mykiss) is a salmonid species with a complex life-history. Wild populations are naturally divided into freshwater residents and sea-run migrants. Migrants undergo an energy-demanding adaptation for life in seawater, known as smoltification, while freshwater residents display these changes in an attenuated magnitude and rate. Despite this, in seawater rainbow trout farming all animals are transferred to seawater. Under these circumstances, weeks after seawater transfer, a significant portion of the fish die (around 10%) or experience growth stunting (GS; around 10%), which represents an important profitability and welfare issue. The underlying causes leading to GS in seawater-transferred rainbow trout remain unknown. In this study, we aimed at characterising the GS phenotype in seawater-transferred rainbow trout using untargeted and targeted approaches. To this end, the liver proteome (LC-MS/MS) and lipidome (LC-MS) of GS and fast-growing phenotypes were profiled to identify molecules and processes that are characteristic of the GS phenotype. Moreover, the transcription, abundance or activity of key proteins and hormones related to osmoregulation (Gill Na+, K+–ATPase activity), growth (plasma IGF-I, and liver igf1, igfbp1b, ghr1 and ctsl) and stress (plasma cortisol) were measured using targeted approaches. Results: No differences in Gill Na+, K+–ATPase activity and plasma cortisol were detected between the two groups. However, a significant downregulation in plasma IGF-I and liver igf1 transcription pointed at this growth factor as an important pathomechanism for GS. Changes in the liver proteome revealed reactive-oxygen-species-mediated endoplasmic reticulum stress as a key mechanism underlying the GS phenotype. From the lipidomic analysis, key observations include a reduction in triacylglycerols and elevated amounts of cardiolipins, a characteristic lipid class associated with oxidative stress, in GS phenotype. Conclusion: While the triggers to the activation of endoplasmic reticulum stress are still unknown, data from this study point towards either an unresolved infection or a nutritional deficiency as underlying drivers of this phenotype.


2010 ◽  
Vol 299 (1) ◽  
pp. R33-R41 ◽  
Author(s):  
L. Bouraoui ◽  
E. Capilla ◽  
J. Gutiérrez ◽  
I. Navarro

Primary cultures of rainbow trout ( Oncorhynchus mykiss ) adipocytes were used to examine the main signaling pathways of insulin and insulin-like growth factor I (IGF-I) during adipogenesis. We first determined the presence of IGF-I receptors (IGF-IR) and insulin receptors (IR) in trout preadipocytes ( day 5) and adipocytes ( day 14). IGF-IRs were more abundant and appeared to be in higher levels in differentiated cells than in preadipocytes, whereas IRs were detected in lower but constant levels throughout the culture. The cells were immunoreactive against ERK1/2 MAPK, and AKT/PI3K, components of the two main signal transduction pathways for insulin and IGF-I receptors. Stimulation of MAPK phosphorylation by IGF-I was higher in preadipocytes than in adipocytes, while no effects were observed in MAPK phosphorylation after incubation of cells with insulin. AKT phosphorylation increased in the presence of both insulin and IGF-I, with higher levels of stimulation in adipocytes than in preadipocytes. Activation of both pathways was blocked by the use of specific inhibitors of MAPK (PD98059) and AKT (wortmannin). We describe here, for the first time, the effects of IGF-I and insulin on 2-deoxyglucose uptake in primary culture of trout adipocytes. IGF-I was more potent in stimulating glucose uptake than insulin, and PD98059 and wortmannin inhibited the stimulation of glucose uptake by this growth factor, suggesting that IGF-I plays an important metabolic role in trout adipocytes. Our results suggest that differential activation of the MAPK and AKT pathways are involved in the IGF-I- and insulin-induced effects of trout adipocytes during the various stages of adipogenesis.


2001 ◽  
Vol 170 (3) ◽  
pp. 619-628 ◽  
Author(s):  
◽  
A Garmong ◽  
P Swanson ◽  
J Moore ◽  
M Lin ◽  
...  

Rainbow trout (Oncorhynchus mykiss) serum contains several IGF-binding proteins (IGFBPs) that specifically bind to IGFs. The structures of these fish IGFBPs have not been determined and their physiological functions are poorly defined. In this study, we identified a 30 kDa IGFBP present in rainbow trout serum and secreted by cultured trout hepatoma cells. This IGFBP binds to IGFs but not to insulin. This IGFBP was purified to homogeneity using a three-step procedure involving Phenyl-Sepharose chromatography, IGF-I affinity chromatography and reverse-phase HPLC. Affinity cross-linking studies indicated that this IGFBP binds to IGF-I with a higher affinity than to IGF-II. N-terminal sequence analysis of the trout IGFBP suggests that it shares high sequence identity with that of human IGFBP-1 in the N-terminal region. When added to cultured fish and human cells, the trout IGFBP inhibited IGF-I-stimulated DNA synthesis and cell proliferation in a concentration-dependent manner. The inhibitory effect of the fish IGFBP was comparable to those of human IGFBP-1 and -4. These results indicate that the IGFBP molecule is structurally and functionally conserved in evolutionarily ancient vertebrate species such as bony fish.


2007 ◽  
Vol 64 (10) ◽  
pp. 1382-1389 ◽  
Author(s):  
Takashi Yada ◽  
Teruo Azuma ◽  
Susumu Hyodo ◽  
Tetsuya Hirano ◽  
E Gordon Grau ◽  
...  

Expression of distinct corticosteroid receptor genes, glucocorticoid receptors 1 and 2 (GR-1 and GR-2, respectively) and mineralcorticoid receptor (MR), was quantified by real-time polymerase chain reaction (PCR) in peripheral blood leucocytes (PBL), spleen, and gill of rainbow trout (Oncorhynchus mykiss) after an acute netting stress. Plasma cortisol levels were significantly increased 2 h after stress and returned to prestress levels within 24 h. Consistent with changes in plasma cortisol, GR-2 mRNA levels in PBL increased significantly at 2 h after stress, returning to initial levels by 8 h. In contrast, GR-1 and MR levels in PBL decreased significantly at 24 h after stress, and these reduced levels were maintained for 7 days. Splenic mRNA levels of GR-1 and GR-2 also decreased at 8 h and 24 h after stress, returning to control levels by 7 days, whereas no significant change was observed in MR. In gill, there was no obvious change in corticosteroid receptor mRNA levels after stress, except for a transient decrease at 8 h in MR. These results suggest a variety of roles for the three corticosteroid receptors during immunosuppression in response to acute stress in trout.


1998 ◽  
Vol 55 (7) ◽  
pp. 1583-1590 ◽  
Author(s):  
T Ryan Gregory ◽  
Chris M Wood

Variation among individuals in specific growth rate (SGR), feeding, and two measures of swimming performance and their possible interrelationships were investigated in juvenile rainbow trout (Oncorhynchus mykiss) kept in groups on either satiation or half-satiation rations. Maximum sustainable velocity (Ucrit) was measured as an index of aerobic swimming performance and stamina (fatigue time in a fixed-velocity test at 6 body lengths ·s-1) as an index of anaerobic performance. Individual performance in both of these tests was found to be significantly repeatable. Trout fed on half-satiation ration exhibited significantly lower mean values of SGR and body size and higher levels of aggression-related fin damage, but no significant differences in stamina, relative or absolute Ucrit, glycogen content, or plasma cortisol. However, in these fish, there was a significant negative relationship between SGR and relative Ucrit, a significant positive relationship between SGR and stamina, and a significant positive relationship between SGR and total daily meal. None of these relationships were seen in fish fed to satiation. Plasma cortisol and tissue glycogen stores were not related to SGR. These results indicate that under the intensified competition of restricted ration, there are trade-offs between growth, feeding, and different types of swimming performance.


2010 ◽  
Vol 299 (2) ◽  
pp. R562-R572 ◽  
Author(s):  
Joan Sánchez-Gurmaches ◽  
Lourdes Cruz-Garcia ◽  
Joaquím Gutiérrez ◽  
Isabel Navarro

The effects of insulin and IGF-I on fatty acid (FA) and glucose metabolism were examined using oleic acid or glucose as tracers in differentiated rainbow trout ( Oncorhynchus mykiss ) myotubes. Insulin and IGF-I significantly reduced the production of CO2 from oleic acid with respect to the control values. IGF-I also significantly reduced the production of acid-soluble products (ASP) and the concentration of FA in the medium, while cellular triacylglycerols (TAG) tended to increase. Only insulin produced a significant accumulation of glycogen inside the cells in glucose distribution experiments. Incubation with catecholamines did not affect oleic acid metabolism. Cells treated with rapamycin [a target of rapamycin (TOR) inhibitor] significantly increased the oxidation of oleic acid to CO2 and ASP, while the accumulation of TAG diminished. Rosiglitazone (a peroxisome proliferator-activated receptor γ agonist) and etomoxir (a CPT-1 inhibitor) produced a severe and significant reduction in the production of CO2 and ASP. Rosiglitazone and etomoxir also produced a significant accumulation of FA outside and inside the cells, respectively. No significant effects of these drugs on glucose distribution were observed. These data indicate that insulin and IGF-I act as anabolic hormones in trout myotubes in both oleic acid and glucose metabolism, although glucose oxidation appears to be less sensitive than FA oxidation to insulin and IGF-I. The use of rapamycin, etomoxir, and rosiglitazone may help us to understand the mechanisms of regulation of lipid metabolism in fish.


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