Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model

Abstract

Salem M, Kenney PB, Rexroad CE 3rd, Yao J. Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol Genomics 28: 33-45, 2006. First published August 1, 2006; doi:10.1152/physiolgenomics.00114.2006.-Muscle atrophy is a physiological response to diverse physiological and pathological conditions that trigger muscle deterioration through specific cellular mechanisms. Despite different signals, the biochemical changes in atrophying muscle share many common cascades. Muscle deterioration as a physiological response to the energetic demands of fish vitellogenesis represents a unique model for studying the mechanisms of muscle degradation in non-mammalian animals. A salmonid microarray, containing 16,006 cDNAs, was used to study the transcriptome response to atrophy of fast-switch muscles from gravid rainbow trout compared with sterile fish. Eighty-two unique transcripts were upregulated and 120 transcripts were downregulated in atrophying muscles. Transcripts having gene ontology identifiers were grouped according to their functions. Muscle deterioration was associated with elevated expression of genes involved in the catheptic and collagenase proteolytic pathways; the aerobic production, buffering, and utilization of ATP; and growth arrest; whereas atrophying muscle showed downregulation of genes encoding a serine proteinase inhibitor, enzymes of anaerobic respiration, muscle proteins as well as genes required for RNA and protein biosynthesis/processing. Therefore, gene transcription of the trout muscle atrophy changed in a manner similar to mammalian muscle atrophy. These changes result in an arrest of normal cell growth, protein degradation, and decreased glycolytic cellular respiration that is characteristic of the fast-switch muscle. For the first time, other changes/mechanisms unique to fish were discussed including genes associated with muscle atrophy. atrophy; Oncorhynchus mykiss SEVERAL PHYSIOLOGICAL and pathological conditions can cause muscle atrophy by triggering unique responses through distinct cellular stimuli. Transcriptional mechanisms of muscle wastage are well characterized at the transcriptome level in mammalian models as a response to nutritional restriction (7), fasting, severe diseases, including cancer, renal failure, diabetes (41, 42), and sepsis (42), as well as muscle disuse or denervation (4, 57). Some studies have dealt with fish muscle atrophy at the level of individual genes/mechanisms (46, 51, 58, 60 -62). The molecular basis of mammalian muscle atrophy has received considerable attention in the literature (25,30). Losing muscle mass results from elevated rate of proteolysis and decreased rate of protein synthesis. Despite the significant amount of literature (30,32,42), the specific roles of the proteolytic systems in degrading mammalian muscle still are unclear. Moreover, we recently showed that fish use different muscle degrading proteolytic strategies compared with mammals (58). The ubiquitin-proteasome pathway,...

Autophagy as a defense strategy against stress: focus on Paracentrotus lividus sea urchin embryos exposed to cadmium

“…As it belongs to salmonids, the rainbow trout migrate long distances to the spawning sites, experiencing long fasting periods during which it degrades a major part of its lipids and about half of its white muscle mass for recycling cytoplasmic components to provide nutrients to other tissues (Mommsen et al 1980;Mizushima et al 2004). Several studies indicate that autophagy plays a key role in controlling muscle mass by protein degradation (Mommsen 2004;Salem et al 2006;Seiliez et al 2012). Most components of autophagy and its associated signaling pathways (AKT1, TOR, AMPK, FOXO) are evolutionarily conserved in the rainbow trout (Polakof et al 2011;Seiliez et al 2008;Seiliez et al 2012).…”

Elevated expression of protein biosynthesis genes in liver and muscle of hibernating black bears (Ursus americanus)

“…Decrease in protein synthesis, including underexpression of genes involved in translation, has been shown to contribute to muscle degradation and protein loss due to disuse in mammals and fish (19,34). Bears demonstrate a unique ability to conserve muscle mass and retain strength through prolonged periods of inactivity and starvation during hibernation.…”

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“…Similarly, salmonid microarray containing about 16006 cDNA has been used to study the transcriptomics response to fast-twitching muscle atrophy from gravid trout compared to those of sterile fishes (Ewart et al, 2005;Salem et al, 2006). These are all personalized microarrays.…”

“…These are all personalized microarrays. Furthermore, Panicker et al (2004) Microarray have also been used to explore the response of rainbow trout transcriptome to chemical contaminants (Koskinen et al, 2004), toxicogenomic profiling of hepatic tumour promoters (Tilton et al, 2006), and gene expression in atrophying muscle (Salem et al, 2006). The application of DNA microarray in fish biology and aquaculture could have immense significance through discovery of novel genes, their expression profiles and response to various environmental stimulations at genome level.…”