Long-term warm or cold acclimation elicits a specific transcriptional response and affects energy metabolism in zebrafish

Vergauwen, Lucia; Benoot, D.; Blust, Ronny; Knapen, Dries

doi:10.1016/j.cbpa.2010.06.160

Cited by 100 publications

(59 citation statements)

References 49 publications

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“…A proteomic approach investigating hyperoxic insults to the brain of heat acclimated rats, demonstrated upregulation of HSP70 and increased enzymatic activity of the antioxidant CuZnSOD (42). Interestingly, our suggestion of a two-tier adaptive response is also supported by the findings of Vergauwen et al (233) regarding thermal acclimation in Zebra fish and of Kultz (114), who reported that the onset of adaptation to hypertonic stress is accompanied by the upregulation of genes encoding proteins associated with the maintenance of DNA integrity, indicating that the kinetics of acclimation are evolutionarily conserved.…”

Section: Genomic Responsessupporting

confidence: 84%

Heat Acclimation, Epigenetics, and Cytoprotection Memory

Horowitz

2014

Comprehensive Physiology

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Heat acclimation is a within-life phenotypic adaptation to heat. Plasticity of the thermoregulatory system is crucial for the induction of heat acclimation. In the last two decades, it has become clear that heat causes adaptive shifts in gene expression which adjust the protein balance. These changes are part of the evolvement of the acclimated phenotype. The molecular-cellular aspects of some acclimatory mechanisms that have only been explained by physiological-effectorial mechanisms have been discovered. This review attempts to bridge the gap between the classic physiological heat acclimation profile and the molecular/cellular mechanisms underlying the evolvement of the acclimated phenotype. Heat acclimation leads to leftward and rightward shifts in temperature thresholds of heat dissipation organs and thermal injury, respectively, thereby expanding the acclimated dynamic thermoregulatory range. Interactions between ambient temperature and afferent drives from effector organs to the hypothalamic thermoregulatory center with modifications in warm/cold sensitive neuron ratio and excitability contribute to the threshold changes. The altered threshold for thermal injury is associated with progressive enhancement of inducible cytoprotective networks, including HSP70, HSF1, and HIF-1ɑ. These molecules are also important in acclimatory kinetics. Aspects of cross-adaption, cross-tolerance and interference with heat acclimation are explained using molecular-cellular physiological interactions, with the heart, skeletal muscles, and water secretory glands as models. Lastly, the roles of epigenetic mechanisms in transcriptional regulation during induction of the acclimated phenotype, its decay, and reinduction are discussed. Posttranslational histone modifications in the promoters of hsp70 and hsp90 form part of our prototype model of heat-acclimation-mediated cytoprotective memory.

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Section: Genomic Responsessupporting

confidence: 84%

Heat Acclimation, Epigenetics, and Cytoprotection Memory

Horowitz

2014

Comprehensive Physiology

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“…7). Consistent with this idea, carbohydrate content of the muscle increases in response to 34°C acclimation in zebrafish raised under control conditions, but has no effect on total muscle lipid stores (Vergauwen et al, 2010). Differences between T E groups in other processes that are important for warm acclimation, such as the induction of heat shock proteins (Vergauwen et al, 2010), may also contribute to the observed differences in performance.…”

Section: Developmental Plasticity Of Metabolic Temperature Acclimationmentioning

confidence: 70%

“…Consistent with this idea, carbohydrate content of the muscle increases in response to 34°C acclimation in zebrafish raised under control conditions, but has no effect on total muscle lipid stores (Vergauwen et al, 2010). Differences between T E groups in other processes that are important for warm acclimation, such as the induction of heat shock proteins (Vergauwen et al, 2010), may also contribute to the observed differences in performance. Even though our second hypothesis was not supported, our current findings are generally consistent with our previous observation that T E has a persistent effect on thermal acclimation capacity (Scott and Johnston, 2012).…”

Section: Developmental Plasticity Of Metabolic Temperature Acclimationmentioning

confidence: 70%

Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish

Schnurr

Scott

2013

Journal of Experimental Biology

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Global warming is intensifying interest in the physiological consequences of temperature change in ectotherms, but we still have a relatively poor understanding of the effects of temperature on early life stages. This study determined how embryonic temperature (T E ) affects development and the activity of metabolic enzymes in the swimming muscle of zebrafish. Embryos developed successfully to hatching (survival ≥88%) from 22 to 32°C, but suffered sharp increases in mortality outside of this range. Embryos that were incubated until hatching at a control T E (27°C) or near the extremes for successful development (22 or 32°C) were next raised to adulthood under control conditions at 27°C. Growth trajectories after hatching were altered in the 22°C and 32°C T E groups compared with 27°C T E controls, but growth slowed after 3 months of age in all groups. Maximal enzyme activities of cytochrome c oxidase (COX), citrate synthase (CS), hydroxyacyl-coA dehydrogenase (HOAD), pyruvate kinase (PK) and lactate dehydrogenase (LDH) were measured across a range of assay temperatures (22, 27, 32 and 36°C) in adults from each T E group that were acclimated to 27 or 32°C. Substrate affinities (K m ) were also determined for COX and LDH. In adult fish acclimated to 27°C, COX and PK activities were higher in 22°C and 32°C T E groups than in 27°C T E controls, and the temperature optimum for COX activity was higher in the 32°C T E group than in the 22°C T E group. Warm acclimation reduced COX, CS and/or PK activities in the 22 and 32°C T E groups, possibly to compensate for thermal effects on molecular activity. This response did not occur in the 27°C T E controls, which instead increased LDH and HOAD activities. Warm acclimation also increased thermal sensitivity (Q 10 ) of HOAD to cool temperatures across all T E groups. We conclude that the temperature experienced during early development can have a persistent impact on energy metabolism pathways and acclimation capacity in later life.

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“…The Journal of Experimental Biology (2014) Kullgren et al, 2013), it was only recently reported that the balance between metabolic performance and metabolic cost establishes physiological condition and critical swimming speed (Vergauwen et al, 2013;Vergauwen et al, 2010). Indeed, the two-way signaling between SCs and muscle fibers has not been investigated previously in teleosts, despite the important gap in our understanding of processes enabling their indeterminate growth (fiber hyperplasia and hypertrophy) in comparison to restriction to fiber hypertrophy (without hyperplasia) in postnatal mammals.…”

Section: Research Articlementioning

confidence: 99%

Satellite cell activation and populations on single muscle-fiber cultures from adult zebrafish (Danio rerio)

Zhang

Anderson

2014

Journal of Experimental Biology

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Satellite cells (SCs), stem cells in skeletal muscle, are mitotically quiescent in adult mammals until activated for growth or regeneration. In mouse muscle, SCs are activated by nitric oxide (NO), hepatocyte growth factor (HGF) and the mechanically induced NO-HGF signaling cascade. Here, the SC population on fibers from the adult, ectothermic zebrafish and SC responsiveness to activating stimuli were assessed using the model system of isolated fibers cultured at 27 and 21°C. SCs were identified by immunostaining for the HGF receptor, c-met, and activation was determined using bromodeoxyuridine uptake in culture or in vivo. In dose-response studies, SC activation was increased by treatment with the NO-donor drug isosorbide dinitrate (1 mmol l −1 ) or HGF (10 ng ml −1 ) to maximum activation at lower concentrations of both than in previous studies of mouse fibers. HGF-induced activation was blocked by anti-c-met antibody, and reduced by culture at 21°C. The effect of cyclical stretch (3 h at 4 cycles per minute) increased activation and was blocked by nitric oxide synthase inhibition and reduced by culture at 21°C. The number of c-met+ SCs per fiber increased rapidly (by 3 h) after stretching. The character of signaling in SC activation on zebrafish fibers, in particular temperature-dependent responses to HGF and stretch, gives new insights into the influence of ectothermy on regulation of muscle growth in teleosts and suggests the use of the single-fiber model system to explore the basis of fiber hyperplasia and the conservation of regulatory pathways between species. KEY WORDS: Stem cells, Ectothermy, Proliferation, c-met, Hepatocyte growth factor INTRODUCTIONSkeletal muscle function in fish is fundamentally important for survival using high-and low-speed swimming (Fauconneau et al., 1995), and the zebrafish [Danio rerio (Hamilton 1822)], an ectothermic teleost, is an important vertebrate model for studying development, physiology and pathology (Lieschke and Currie, 2007). In teleosts, muscle mass [over 90% white fibers (Wakeling and Johnston, 1999)] grows by increases in fiber number and size (Bird and Mabee, 2003;Buckingham and Vincent, 2009). The combination of hyperplasia and hypertrophy is termed indeterminate growth (Fauconneau and Paboeuf, 2001;Rowlerson and Veggetti, 2001;Johnston, 2006), and the growth potential is strongly influenced by temperature (Steinbacher et al., 2011). By comparison, in postnatal mammals, fibers hypertrophy and show accretion of post-mitotic myonuclei, but fibers do not increase in number (Petrella et al., 2008;O'Connor and Pavlath, 2007). Satellite RESEARCH ARTICLEDepartment of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada R3T 2N2. Anderson and Pilipowicz, 2002;Bischoff, 1975;Bischoff, 1986;Bischoff, 1990) and in vivo (Anderson, 2000;Anderson and Wozniak, 2004;Tatsumi and Allen, 2008). Calcium-dependent stretch-activated signals release NO from mechano-sensitive NOS-1μ, which induces HGF release from the extracellular matrix (Tatsumi et al., 2002;Y...

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Long-term warm or cold acclimation elicits a specific transcriptional response and affects energy metabolism in zebrafish

Cited by 100 publications

References 49 publications

Heat Acclimation, Epigenetics, and Cytoprotection Memory

Heat Acclimation, Epigenetics, and Cytoprotection Memory

Temperature during embryonic development has persistent effects on metabolic enzymes in the muscle of zebrafish

Satellite cell activation and populations on single muscle-fiber cultures from adult zebrafish (Danio rerio)

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