Steady-state effects of temperature acclimation on the transcriptome of the rainbow trout heart

Abstract

phenotype of trout heart was induced by 4-wk acclimation at 4°C and was characterized by 32.7% increase in relative heart mass and 49.8% increase in ventricular myocyte size compared with warm-acclimated (WA; 18°C) fish (P Ͻ 0.001). Effect of temperature acclimation on transcriptome of the rainbow trout heart was examined using speciesspecific microarray chips containing 1,380 genes. After 4 wk of temperature acclimation, 8.8% (122) of the genes were differently expressed in CA and WA hearts, and most of them (82%) were upregulated in the cold (P Ͻ 0.01). Transcripts of genes engaged in protein synthesis and intermediary metabolism were most strongly upregulated, whereas genes contributing to the connective tissue matrix were clearly repressed. Extensive upregulation of the genes coding for ribosomal proteins and translation elongation and initiation factors suggest that the protein synthesis machinery of the trout heart is enhanced in the cold and is an essential part of the compensatory mechanism causing and maintaining the hypertrophy of cardiac myocytes. The prominent depression of collagen genes may be indicative of a reduced contribution of extracellular matrix to the remodeling of the CA fish heart. Temperature-related changes in transcripts of metabolic enzymes suggest that at mRNA level, glycolytic energy production from carbohydrates is compensated in the heart of CA rainbow trout, while metabolic compensation is absent in mitochondria. In addition, the analysis revealed three candidate genes: muscle LIM protein, atrial natriuretic peptide B, and myosin light chain 2, which might be central for induction and maintenance of the hypertrophic phenotype of the CA trout heart. These findings indicate that extensive modification of gene expression is needed to maintain the temperature-specific phenotype of the fish heart. gene expression; fish heart; temperature-induced hypertrophy PHYSIOLOGICAL PLASTICITY is needed to adapt body functions to changing environmental conditions and involves activation of proper genetic programs. Ectothermic animals of north-temperate latitudes experience large seasonal changes in temperature, which strongly affect the rate of body functions. To compensate for the effects of temperature changes, ectotherms can respond to chronic temperature changes by increasing the quantity of tissue or enzyme needed for different physiological tasks, or by expressing proteins isoforms that are more appropriate for the new thermal conditions (16,19,21). On the other hand, proteins which are needed in lesser amounts in the new thermal regime could be depressed or downregulated. Although expression of proteins can be changed by multiple mechanisms during synthesis and degradation, temperaturedependent changes in transcription of genes are one of the key events in modifying the proteome of the tissues (16, 37).Circulatory system integrates different body functions through the transport of material and humoral messages and serves the well being of all body cells by providing oxygen and fuels for e...

Proteomic analysis of cardiac response to thermal acclimation in the eurythermal goby fishGillichthys mirabilis

“…Several studies investigating vertebrate hearts including those of teleosts have shown an induction of cytoprotective networks including HSP expression and other molecular chaperones (Vornanen et al, 2005;Horowitz, 2010). One surprising finding -or lack thereof -in the current study is the absence of induction of a molecular chaperoning response.…”

“…6). Several studies on marine teleosts and invertebrates have implicated temperature-induced cytoskeletal reorganization at both the transcriptome and the proteome level (Podrabsky and Somero, 2004;Vornanen et al, 2005;Buckley et al, 2006;Lockwood et al, 2010;Tomanek and Zuzow, 2010). These cytoskeletal changes have been discussed in light of small heat shock protein (HSP) chaperoning activity; small HSPs are triggered by cytoskeletal perturbations and are thought to play a crucial role in stabilizing the cytoskeleton (Derham and Harding, 2002;Haslbeck et al, 2005).…”

“…However, despite the crucial role played by the cardiac system in determining thermal tolerance, little is known about gene and protein level responses to temperature in fish hearts, apart from a few transcriptomic studies focusing on highly active fish species (Vornanen et al, 2005;Castilho et al, 2009;Anttila et al, 2014). Recent developments in proteomics technology and the increasing availability of genomic sequence information to facilitate protein identification have allowed for the successful use of proteomic experimental approaches to investigate non-model organisms (Tomanek, 2005(Tomanek, , 2011(Tomanek, , 2014Dowd et al, 2008Dowd et al, , 2010Tomanek and Zuzow, 2010;Serafini et al, 2011;Fields et al, 2012).…”

Cold acclimation increases cardiac myofilament function and ventricular pressure generation in trout

“…This indicates that acclimation to 4°C did not cause cardiac hypertrophy. Although several studies describe hypertrophy in trout cardiac muscle in response to cold acclimation (Graham and Farrell, 1989;Klaiman et al, 2011;Vornanen et al, 2005), this phenomenon is not universally reported (Driedzic et al, 1996;Gamperl and Farrell, 2004). It has been proposed that other factors may be involved in triggering the hypertrophic response, including seasonal changes in photoperiod and thyroid hormones (Tiitu and Vornanen, 2003;Gamperl and Farrell, 2004).…”

Comparison of Gene Expression in the Gill of Salmon (Salmo salar) Smolts from Anadromous and Landlocked Populations

“…In studies of salmonid fish, DnaJA2 has turned out be more stable than e.g. the genes of β-actin or ribosomal RNA and similar to the elongation factor 1α during the parr-smolt transformation (Vornanen et al 2005, Hassinen et al 2007. The same RNA samples analyzed in the microarray were also used for qPCR, and represented the gill tissue pooled from 10 fishes (see Gill sampling and RNA isolation).…”