| 1. |
- Brijs, Jeroen, et al.
(författare)
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Cardiac remodeling and increased central venous pressure underlie elevated stroke volume and cardiac output of seawater-acclimated rainbow trout
- 2017
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Ingår i: American Journal of Physiology - Regulatory Integrative and Comparative Physiology. - : American Physiological Society. - 0363-6119 .- 1522-1490. ; 312:1
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Tidskriftsartikel (refereegranskat)abstract
- © 2017 the American Physiological Society.Substantial increases in cardiac output (CO), stroke volume (SV), and gastrointestinal blood flow are essential for euryhaline rainbow trout (Oncorhyncus mykiss) osmoregulation in seawater. However, the underlying hemodynamic mechanisms responsible for these changes are unknown. By examining a range of circulatory and cardiac morphological variables of seawater-and freshwater-acclimated rainbow trout, the present study revealed a significantly higher central venous pressure (CVP) in seawater-acclimated trout (~0.09 vs. -0.02 kPa). This serves to increase cardiac end-diastolic volume in seawater and explains the elevations in SV (~0.41 vs. 0.27 ml/kg) and CO (~21.5 vs. 14.2 ml·min-1·kg-1) when compared with trout in freshwater. Furthermore, these hemodynamic modifications coincided with a significant increase in the proportion of compact myocardium, which may be necessary to compensate for the increased wall tension associated with a larger stroke volume. Following a temperature increase from 10 to 16.5°C, both acclimation groups exhibited similar increases in heart rate (Q10 of ~2), but SV tended to decrease in seawater-acclimated trout despite the fact that CVP was maintained in both groups. This resulted in CO of seawaterand freshwater-acclimated trout stabilizing at a similar level after warming (~26 ml·min-1·kg-1). The consistently higher CVP of seawater-acclimated trout suggests that factors other than compromised cardiac filling constrained the SV and CO of these individuals at high temperatures. The present study highlights, for the first time, the complex interacting effects of temperature and water salinity on cardiovascular responses in a euryhaline fish species.
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| 2. |
- Brijs, Jeroen, et al.
(författare)
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Increased mitochondrial coupling and anaerobic capacity minimizes aerobic costs of trout in the sea
- 2017
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Ingår i: Scientific Reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 7
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Tidskriftsartikel (refereegranskat)abstract
- Anadromy is a distinctive life-history strategy in fishes that has evolved independently many times. In an evolutionary context, the benefits of anadromy for a species or population must outweigh the costs and risks associated with the habitat switch. The migration of fish across the freshwater-ocean boundary coincides with potentially energetically costly osmoregulatory modifications occurring at numerous levels of biological organization. By integrating whole animal and sub-cellular metabolic measurements, this study presents significant findings demonstrating how an anadromous salmonid (i.e. rainbow trout, Oncorhynchus mykiss) is able to transform from a hyper- to hypo-osmoregulatory state without incurring significant increases in whole animal oxygen consumption rate. Instead, underlying metabolic mechanisms that fuel the osmoregulatory machinery at the organ level (i.e. intestine) are modulated, as mitochondrial coupling and anaerobic metabolism are increased to satisfy the elevated energetic demands. This may have positive implications for the relative fitness of the migrating individual, as aerobic capacity may be maintained for locomotion (i.e. foraging and predator avoidance) and growth. Furthermore, the ability to modulate mitochondrial metabolism in order to maintain osmotic balance suggests that mitochondria of anadromous fish may have been a key target for natural selection, driving species adaptations to different aquatic environments.
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| 3. |
- Ekström, Andreas, 1979, et al.
(författare)
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Influence of the coronary circulation on thermal tolerance and cardiac performance during warming in rainbow trout
- 2017
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Ingår i: American Journal of Physiology - Regulatory Integrative and Comparative Physiology. - : American Physiological Society. - 0363-6119 .- 1522-1490. ; 312:4
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Tidskriftsartikel (refereegranskat)abstract
- © 2017 the American Physiological Society. Thermal tolerance in fish may be related to an oxygen limitation of cardiac function. While the hearts of some fish species receive oxygenated blood via a coronary circulation, the influence of this oxygen supply on thermal tolerance and cardiac performance during warming remain unexplored. Here, we analyzed the effect in vivo of acute warming on coronary blood flow in adult sexually mature rainbow trout (Onchorhynchus mykiss) and the consequences of chronic coronary ligation on cardiac function and thermal tolerance in juvenile trout. Coronary blood flow at 10°C was higher in females than males (0.56 ± 0.08 vs. 0.30 ± 0.08 ml·min -1 ·g ventricle -1 ), and averaged 0.47 ± 0.07 ml·min -1 ·g ventricle -1 across sexes. Warming increased coronary flow in both sexes until 14°C, at which it peaked and plateaued at 0.78 ± 0.1 and 0.61 ± 0.1 ml·min -1 ·g ventricle -1 in females and males, respectively. Thus, the scope for increasing coronary flow was 101% in males, but only 39% in females. Coronary-ligated juvenile trout exhibited elevated heart rate across temperatures, reduced Arrhenius breakpoint temperature for heart rate (23.0 vs. 24.6°C), and reduced upper critical thermal maximum (25.3 vs. 26.3°C). To further analyze the effects of coronary flow restriction on cardiac rhythmicity, electrocardiogram characteristics were determined before and after coronary occlusion in anesthetized trout. Occlusion resulted in reduced R-wave amplitude and an elevated S-T segment, indicating myocardial ischemia, while heart rate was unaffected. This suggests that the tachy cardia in ligated trout across temperatures in vivo was mainly to compensate for reduced cardiac contractility to maintain cardiac output. Moreover, our findings show that coronary flow increases with warming in a sex-specific manner. This may improve whole animal thermal tolerance, presumably by sustaining cardiac oxygenation and contractility at high temperatures.
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| 4. |
- Ekström, Andreas, 1979, et al.
(författare)
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Thermal sensitivity and phenotypic plasticity of cardiac mitochondrial metabolism in European perch, Perca fluviatilis
- 2017
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Ingår i: Journal of Experimental Biology. - : The Company of Biologists. - 0022-0949 .- 1477-9145. ; 220:3, s. 386-396
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Tidskriftsartikel (refereegranskat)abstract
- Cellular and mitochondrial metabolic capacity of the heart has been suggested to limit performance of fish at warm temperatures. We investigated this hypothesis by studying the effects of acute temperature increases (16, 23, 30, 32.5 and 36 degrees C) on the thermal sensitivity of 10 key enzymes governing cardiac oxidative and glycolytic metabolism in two populations of European perch (Perca fluviatilis) field-acclimated to 15.5 and 22.5 degrees C, as well as the effects of acclimation on cardiac lipid composition. In both populations of perch, the activity of glycolytic (pyruvate kinase and lactate dehydrogenase) and tricarboxylic acid cycle (pyruvate dehydrogenase and citrate synthase) enzymes increased with acute warming. However, at temperatures exceeding 30 degrees C, a drastic thermally induced decline in citrate synthase activity was observed in the cold-and warm-acclimated populations, respectively, indicating a bottleneck for producing the reducing equivalents required for oxidative phosphorylation. Yet, the increase in aspartate aminotransferase and malate dehydrogenase activities occurring in both populations at temperatures exceeding 30 degrees C suggests that the malate-aspartate shuttle may help to maintain cardiac oxidative capacities at high temperatures. Warm acclimation resulted in a reorganization of the lipid profile, a general depression of enzymatic activity and an increased fatty acid metabolism and oxidative capacity. Although these compensatory mechanisms may help to maintain cardiac energy production at high temperatures, the activity of the electron transport system enzymes, such as complexes I and IV, declined at 36 degrees C in both populations, indicating a thermal limit of oxidative phosphorylation capacity in the heart of European perch.
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| 5. |
- Ekström, Andreas, 1979
(författare)
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Thermal tolerance in teleost fish –importance of cardiac oxygen supply, ATP production and autonomic control
- 2017
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Doktorsavhandling (övrigt vetenskapligt/konstnärligt)abstract
- Temperature tolerance is a key determinant of the resilience and adaptability of fish facing a warmer and more thermally variable future with climate change. Yet, the underlying physiological mechanisms determining the critical thermal maximum (CTmax) are poorly understood. This thesis investigated the physiological determinants of CTmax in teleost fish, focusing on cardiovascular function. An inability of the heart to pump and supply the body tissues with oxygenated blood could constrain whole animal tolerance to high temperatures. This has been hypothesized to be related to an oxygen limitation of the heart, which receives its oxygen supply via the venous blood (luminal circulation), and in some species also via a coronary circulation. This hypothesis was first tested by evaluating the relationship between luminal oxygen supply, via continuous recordings of the venous oxygen tension (PVO2), and in vivo cardiovascular performance and CTmax in European perch (Perca fluviatilis). Perch were sampled from the Baltic Sea (reference, 18°C) and the Biotest enclosure (24°C, Biotest) that is chronically warmed by cooling water effluents from a nuclear power plant. While CTmax was 2.2°C higher in Biotest compared to reference perch, cardiac failure (i.e. reduced heart rate and cardiac output) occurred at similar PVO2. By artificially increasing the oxygen availability to the heart through water hyperoxia (200% air saturation), it was revealed that while heart rate still declined at high temperatures, cardiac stroke volume and cardiac output were maintained. This demonstrates that mainly stroke volume is sensitive to limitations in luminal oxygen supply. In rainbow trout (Onchorhynchus mykiss), coronary blood flow first increased with moderate warming, but plateaued at higher temperatures suggesting limitations to the coronary vasodilatory reserve. Ligation of the coronary artery reduced CTmax and impaired cardiac performance during warming, which was reflected in an elevated heart rate across temperatures, possibly to compensate for an impaired myocardial contractility and stroke volume of the oxygen deprived ventricle. A thermal impairment of mitochondrial ATP production could also explain reductions in cardiac performance of acutely warmed fish. This hypothesis was tested by evaluating the catalytic capacities of key enzymes involved in ATP production in the perch heart. The main findings suggest that mitochondrial function is impaired at critically high temperatures by a reduced production of NADH and FADH2 in the tricarboxylic acid cycle, which provides the electrons necessary for driving mitochondrial ATP production. Moreover, a temperature dependent failure of several complexes in the electron transport chain was observed, which would also limit the synthesis of ATP at high temperatures. Indications of an increase in oxidative capacity were observed in the warm acclimated Biotest perch, which may be associated with their improved cardiac thermal performance and elevated CTmax. Finally, it was hypothesized that cholinergic inhibition of heart rate could improve cardiac oxygenation during warming, and that adrenergic stimulation may improve cardiac contractility at high temperatures and reduced cardiac oxygen availability. These hypotheses were tested in rainbow trout by pharmacologically blocking the cholinergic and adrenergic input to the heart. However, neither of the treatments resulted in earlier onset of cardiac failure during acute warming, or a reduced CTmax. This could reflect that the heart was adequately oxygenated via compensatory increases in coronary flow, and/or that an increased cardiac filling pressure served to maintain cardiac output. Collectively, these findings provide novel insights into the causal factors underlying thermal tolerance and cardiac failure during acute warming in teleost fish in vivo. While whole animal thermal tolerance limits likely involve thermal failure at several levels of physiological organization, a failing heart undoubtedly plays a crucial role for the sensitivity of fish to a warmer and more thermally extreme future.
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| 6. |
- Johansen, I. B., et al.
(författare)
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Bigger is not better: cortisol-induced cardiac growth and dysfunction in salmonids
- 2017
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Ingår i: Journal of Experimental Biology. - : The Company of Biologists. - 0022-0949 .- 1477-9145. ; 220:14, s. 2545-2553
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Tidskriftsartikel (refereegranskat)abstract
- Stress and elevated cortisol levels are associated with pathological heart growth and cardiovascular disease in humans and other mammals. We recently established a link between heritable variation in post-stress cortisol production and cardiac growth in salmonid fish too. A conserved stimulatory effect of the otherwise catabolic steroid hormone cortisol is probably implied, but has to date not been established experimentally. Furthermore, whereas cardiac growth is associated with failure of the mammalian heart, pathological cardiac hypertrophy has not previously been described in fish. Here, we show that rainbow trout (Oncorhynchus mykiss) treated with cortisol in the diet for 45 days have enlarged hearts with lower maximum stroke volume and cardiac output. In accordance with impaired cardiac performance, overall circulatory oxygen-transporting capacity was diminished as indicated by reduced aerobic swimming performance. In contrast to the well-known adaptive/physiological heart growth observed in fish, cortisol-induced growth is maladaptive. Furthermore, the observed heart growth was associated with up-regulated signature genes of mammalian cardiac pathology, suggesting that signalling pathways mediating cortisol-induced cardiac remodelling in fish are conserved from fish to mammals. Altogether, we show that excessive cortisol can induce pathological cardiac remodelling. This is the first study to report and integrate the etiology, physiology and molecular biology of cortisol-induced pathological remodelling in fish.
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| 7. |
- Pichaud, Nicolas, 1978, et al.
(författare)
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Dynamic changes in cardiac mitochondrial metabolism during warm acclimation in rainbow trout
- 2017
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Ingår i: Journal of Experimental Biology. - : The Company of Biologists. - 0022-0949 .- 1477-9145. ; 220:9, s. 1674-1683
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Tidskriftsartikel (refereegranskat)abstract
- Although the mitochondrial metabolism responses to warm acclimation have been widely studied in fish, the time course of this process is less understood. Here, we characterized the changes of rainbow trout (Oncorhynchus mykiss) cardiac mitochondrial metabolism during acute warming from 10 to 16 degrees C, and during the subsequent warm acclimation for 39 days. We repeatedly measured mitochondrial oxygen consumption in cardiac permeabilized fibers and the functional integrity of mitochondria (i.e. mitochondrial coupling and cytochrome c effect) at two assay temperatures (10 and 16 degrees C), as well as the activities of citrate synthase (CS) and lactate dehydrogenase (LDH) at room temperature. LDH and CS activities significantly increased between day 0 (10 degrees C acclimated fish) and day 1 (acute warming to 16 degrees C) while mitochondrial oxygen consumption measured at respective in vivo temperatures did not change. Enzymatic activities and mitochondrial oxygen consumption rates significantly decreased by day 2, and remained stable during warm acclimation (days 2-39). The decrease in rates of oxygen between day 0 and day 1 coincided with an increased cytochrome c effect and a decreased mitochondrial coupling, suggesting a structural/functional impairment of mitochondria during acute warming. We suggest that after 2 days of warm acclimation, a new homeostasis is reached, which may involve the removal of dysfunctional mitochondria. Interestingly, from day 2 onwards, there was a lack of differences in mitochondrial oxygen consumption rates between the assay temperatures, suggesting that warm acclimation reduces the acute thermal sensitivity of mitochondria. This study provides significant knowledge on the thermal sensitivity of cardiac mitochondria that is essential to delineate the contribution of cellular processes to warm acclimation.
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