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Phasing of muscle gene expression with fasting-induced recovery growth in Atlantic salmon.

ABSTRACT: BACKGROUND:Many fish species experience long periods of fasting in nature often associated with seasonal reductions in water temperature and prey availability or spawning migrations. During periods of nutrient restriction, changes in metabolism occur to provide cellular energy via catabolic processes. Muscle is particularly affected by prolonged fasting as myofibrillar proteins act as a major energy source. To investigate the mechanisms of metabolic reorganisation with fasting and refeeding in a saltwater stage of Atlantic salmon (Salmo salar L.) we analysed the expression of genes involved in myogenesis, growth signalling, lipid biosynthesis and myofibrillar protein degradation and synthesis pathways using qPCR. RESULTS:Hierarchical clustering of gene expression data revealed three clusters. The first cluster comprised genes involved in lipid metabolism and triacylglycerol synthesis (ALDOB, DGAT1 and LPL) which had peak expression 3-14d after refeeding. The second cluster comprised ADIPOQ, MLC2, IGF-I and TALDO1, with peak expression 14-32d after refeeding. Cluster III contained genes strongly down regulated as an initial response to feeding and included the ubiquitin ligases MuRF1 and MAFbx, myogenic regulatory factors and some metabolic genes. CONCLUSION:Early responses to refeeding in fasted salmon included the synthesis of triacylglycerols and activation of the adipogenic differentiation program. Inhibition of MuRF1 and MAFbx respectively may result in decreased degradation and concomitant increased production of myofibrillar proteins. Both of these processes preceded any increase in expression of myogenic regulatory factors and IGF-I. These responses could be a necessary strategy for an animal adapted to long periods of food deprivation whereby energy reserves are replenished prior to the resumption of myogenesis.

SUBMITTER: Bower NI

PROVIDER: S-EPMC2739525 | biostudies-literature | 2009 Aug

REPOSITORIES: biostudies-literature

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Phasing of muscle gene expression with fasting-induced recovery growth in Atlantic salmon.

Bower Neil I NI Taylor Richard G RG Johnston Ian A IA

Frontiers in zoology 20090824

<h4>Background</h4>Many fish species experience long periods of fasting in nature often associated with seasonal reductions in water temperature and prey availability or spawning migrations. During periods of nutrient restriction, changes in metabolism occur to provide cellular energy via catabolic processes. Muscle is particularly affected by prolonged fasting as myofibrillar proteins act as a major energy source. To investigate the mechanisms of metabolic reorganisation with fasting and refeed ...[more]

PMID: 19703292

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Project description:BackgroundRecovery growth is a phase of rapid growth that is triggered by adequate refeeding of animals following a period of weight loss caused by starvation. In this study, to obtain more information on the system-wide integration of recovery growth in muscle, we undertook a time-course analysis of transcript expression in trout subjected to a food deprivation-refeeding sequence. For this purpose complex targets produced from muscle of trout fasted for one month and from muscle of trout fasted for one month and then refed for 4, 7, 11 and 36 days were hybridized to cDNA microarrays containing 9023 clones.ResultsSignificance analysis of microarrays (SAM) and temporal expression profiling led to the segregation of differentially expressed genes into four major clusters. One cluster comprising 1020 genes with high expression in muscle from fasted animals included a large set of genes involved in protein catabolism. A second cluster that included approximately 550 genes with transient induction 4 to 11 days post-refeeding was dominated by genes involved in transcription, ribosomal biogenesis, translation, chaperone activity, mitochondrial production of ATP and cell division. A third cluster that contained 480 genes that were up-regulated 7 to 36 days post-refeeding was enriched with genes involved in reticulum and Golgi dynamics and with genes indicative of myofiber and muscle remodelling such as genes encoding sarcomeric proteins and matrix compounds. Finally, a fourth cluster of 200 genes overexpressed only in 36-day refed trout muscle contained genes with function in carbohydrate metabolism and lipid biosynthesis. Remarkably, among the genes induced were several transcriptional regulators which might be important for the gene-specific transcriptional adaptations that underlie muscle recovery.ConclusionOur study is the first demonstration of a coordinated expression of functionally related genes during muscle recovery growth. Furthermore, the generation of a useful database of novel genes associated with muscle recovery growth will allow further investigations on particular genes, pathways or cellular process involved in muscle growth and regeneration.

Project description:Predicted future warming of aquatic environments could make fish vulnerable to naturally occurring fasting periods during migration between feeding and spawning sites, as these endeavours become energetically more expensive. In this study, Atlantic salmon (Salmo salar) acclimated to midrange (9°C) or elevated suboptimal (18°C) temperatures were subjected to critical (Ucrit) and sustained (4 hours at 80% Ucrit) swimming trials before and after 4 weeks of fasting. Fasting caused weight losses of 7.3% and 8.3% at 9°C and 18°C, respectively. The Ucrit was unaffected by fasting, but higher at 18°C. Fatigue was associated with higher plasma cortisol, osmolality, Na+ and Cl- at 18°C, and ionic disturbances were higher in fasted fish. All fish completed the sustained swim trials while maintaining constant oxygen uptake rates (ṀO2), indicating strictly aerobic swimming efforts. At low swimming speeds ṀO2 was downregulated in fasted fish by 23.8% and 15.6% at 9°C and 18°C, respectively, likely as an adaptation to preserve resources. However, at higher speeds ṀO2 became similar to fed fish showing that maximum metabolic rates were maintained. The changes in ṀO2 lowered costs of transport and optimal swimming speeds in fasted fish at both temperatures, but these energetic alterations were smaller at 18°C while routine ṀO2 was 57% higher than at 9°C. As such, this study shows that Atlantic salmon maintain both glycolytic and aerobic swimming capacities after extended fasting, even at elevated suboptimal temperatures, and adaptive metabolic downregulation provides increased swimming efficiency in fasted fish. Although, improved swimming energetics were smaller when fasting at the higher temperature while metabolism becomes elevated. This could affect migration success in warming climates, especially when considering interactions with other costly activities such as coping with parasites obtained when passing aquaculture sites during seaward travel or gonad development while being voluntarily anorexic during upriver travel to spawning grounds.

Project description:BackgroundFurunculosis, a disease caused with gram negative bacteria Aeromonas salmonicida produces heavy losses in aquaculture. Vaccination against furunculosis reduces mortality of Atlantic salmon but fails to eradicate infection. Factors that determine high individual variation of vaccination efficiency remain unknown. We used gene expression analyses to search for the correlates of vaccine protection against furunculosis in Atlantic salmon.ResultsNaïve and vaccinated fish were challenged by co-habitance. Fish with symptoms of furunculosis at the onset of mass mortality (LR - low resistance) and survivors (HR - high resistance) were sampled. Hepatic gene expression was analyzed with microarray (SFA2.0 - immunochip) and real-time qPCR. Comparison of LR and HR indicated changes associated with the protection and results obtained with naïve fish were used to find and filter the vaccine-independent responses. Genes involved in recruitment and migration of immune cells changed expression in both directions with greater magnitude in LR. Induction of the regulators of immune responses was either equal (NFkB) or greater (Jun) in LR. Expression levels of proteasome components and extracellular proteases were higher in LR while protease inhibitors were up-regulated in HR. Differences in chaperones and protein adaptors, scavengers of reactive oxygen species and genes for proteins of iron metabolism suggested cellular and oxidative stress in LR. Reduced levels of free iron and heme can be predicted in LR by gene expression profiles with no protection against pathogen. The level of complement regulation was greater in HR, which showed up-regulation of the components of membrane attack complex and the complement proteins that protect the host against the auto-immune damages. HR fish was also characterized with up-regulation of genes for proteins involved in the protection of extracellular matrix, lipid metabolism and clearance of endogenous and exogenous toxic compounds. A number of genes with marked expression difference between HR and LR can be considered as positive and negative correlates of vaccine protection against furunculosis.ConclusionEfficiency of vaccination against furunculosis depends largely on the ability of host to neutralize the negative impacts of immune responses combined with efficient clearance and prevention of tissue damages.

Dataset Information

Phasing of muscle gene expression with fasting-induced recovery growth in Atlantic salmon.

Publications

Phasing of muscle gene expression with fasting-induced recovery growth in Atlantic salmon.

Similar Datasets

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