Morpho-functional characterization of the goldfish (Carassius auratus L.) heart

Garofalo, Filippo; Imbrogno, Sandra; Tota, Bruno; Amelio, Daniela

doi:10.1016/j.cbpa.2012.05.206

Cited by 36 publications

(39 citation statements)

References 33 publications

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“…This differs from mammalian atria [75] and some previous data from the goldfish atrium where elastin fibres were visualised using orcein stain [20]. In addition, non-ECM components of the myocardium may alter atrial compliance following temperature acclimation, such as the titin [58] and the actin cytoskeleton [61], which could alter intrinsic stiffness of the cardiac myocytes.…”

Section: Discussionmentioning

confidence: 96%

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Keen

Fenna

McConnell

et al. 2018

Pflugers Arch - Eur J Physiol

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Numerous pathologies lead to remodelling of the mammalian ventricle, often associated with fibrosis. Recent work in fish has shown that fibrotic remodelling of the ventricle is ‘reversible’, changing seasonally as temperature-induced changes in blood viscosity alter haemodynamic load on the heart. The atrial response to varying haemodynamic load is less understood in mammals and completely unexplored in non-mammalian vertebrates. To investigate atrial remodelling, rainbow trout were chronically cooled (from 10 ± 1 to 5 ± 1 °C) and chronically warmed (from 10 ± 1 to 18 ± 1 °C) for a minimum of 8 weeks. We assessed the functional effects on compliance using ex vivo heart preparations and atomic force microscopy nano-indentation and found chronic cold increased passive stiffness of the whole atrium and micromechanical stiffness of tissue sections. We then performed histological, biochemical and molecular assays to probe the mechanisms underlying functional remodelling of the atrial tissue. We found cooling resulted in collagen deposition which was associated with an upregulation of collagen-promoting genes, including the fish-specific collagen I alpha 3 chain, and a reduction in gelatinase activity of collagen-degrading matrix metalloproteinases (MMPs). Finally, we found that cooling reduced mRNA expression of cardiac growth factors and hypertrophic markers. Following long-term warming, there was an opposing response to that seen with cooling; however, these changes were more moderate. Our findings suggest that chronic cooling causes atrial dilation and increased myocardial stiffness in trout atria analogous to pathological states defined by changes in preload or afterload of the mammalian atria. The reversal of this phenotype following chronic warming is particularly interesting as it suggests that typically pathological features of mammalian atrial remodelling may oscillate seasonally in the fish, revealing a more dynamic and plastic atrial remodelling response.Electronic supplementary materialThe online version of this article (10.1007/s00424-018-2140-1) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 96%

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Keen

Fenna

McConnell

et al. 2018

Pflugers Arch - Eur J Physiol

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“…Indeed, fish with pyramidal shaped ventricles display higher active physical activity than fish with saccular ventricles. A recent study in the goldfish concluded that its ventricle performs as a volume rather than a pressure pump, and that the goldfish may have limited cardiac functional reserve capacity (Garofalo et al, 2012). A comparative age-matched or developmentally-matched study of cardiac performance in these fish has not been reported.…”

Section: Discussionmentioning

confidence: 99%

Cardiac repair and regenerative potential in the goldfish (Carassius auratus) heart

Grivas

Haag

Johnson

et al. 2014

Comparative Biochemistry and Physiology Part C: Toxicology &

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The remarkable ability of the heart to regenerate has been demonstrated in the zebrafish and giant danio, two fish members of the cyprinid family. Here we use light and electron microscopy to examine the repair response in the heart of another cyprinid, the goldfish (Carassius auretus), following cautery injury to a small portion of its ventricular myocardium. We observed a robust inflammatory response in the first two weeks consisting primarily of infiltrating macrophages, heterophils, and melanomacrophages. These inflammatory cells were identified in the lumen of the spongy heart, within the site of the wound, and attached to endocardial cells adjacent to the site of injury. Marked accumulation of collagen fibers and increased connective tissue were also observed during the first and second week in a transition zone between healthy and injured myocardium as well as in adjacent sub-epicardial regions. The accumulation of collagen and connective tissue however did not persist. The presence of capillaries was also noted in the injured area during repair. The replacement of the cauterized region of the ventricle by myocardial tissue was achieved by 6 weeks. The presence of ethynyl deoxyuridine-positive cardiac myocytes and partially differentiated cardiac myocytes during repair suggest effective cardiac myocyte driven regeneration mechanisms also operate in the injured goldfish heart, and are similar to those observed in zebrafish and giant danio. Our data suggest the ability for cardiac regeneration may be widely conserved among cyprinids.

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“…The discovery of a putative nos3 gene in actinopterygian recently suggested that the nos1 gene must have duplicated early in gnathostome evolution, before the actinopterygian‐sarcopterygian split, but after the appearance of the chondrichthyan fish lineage . Despite the above data, studies mainly performed by our research group, using physio‐pharmacological approaches, as well as NADPH‐diaphorase and immunostaining with heterologous mammalian anti‐eNOS antibodies, show the presence of an “eNOS‐like” activity in the heart of several teleost species . These species belong to distinct phylogenies and ecophysiological habitats.…”

Section: Nos Cardiac Expression and Localizationmentioning

confidence: 95%

“…In poikilotherm vertebrates, the heart is a clear example of organ morpho‐functional flexibility. As largely documented in fish and amphibians, it supports the varying requirements of the animal by adjusting metabolism and haemodynamics in response to extrinsic and intrinsic stimuli, including circulating and intracardiac hormones and humoral autacoids (ie locally generated signalling substances) . Under normal and stressful conditions, these substances modulate the heart acting beat‐to‐beat (Frank‐Starling response), as well as in the short (myocardial contractility, excitation‐contraction coupling)‐ and long‐term (gene expression) .…”

Section: Introductionmentioning

confidence: 96%

NO, CO and H₂S: What about gasotransmitters in fish and amphibian heart?

et al. 2018

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The gasotransmitters nitric oxide (NO), carbon monoxide (CO), and hydrogen sulphide (H S), long considered only toxicant, are produced in vivo during the catabolism of common biological molecules and are crucial for a large variety of physiological processes. Mounting evidence is emerging that in poikilotherm vertebrates, as in mammals, they modulate the basal performance of the heart and the response to stress challenges. In this review, we will focus on teleost fish and amphibians to highlight the evolutionary importance in vertebrates of the cardiac control elicited by NO, CO and H S, and the conservation of the intracellular cascades they activate. Although many gaps are still present due to discontinuous information, we will use examples obtained by studies from our and other laboratories to illustrate the complexity of the mechanisms that, by involving gasotransmitters, allow beat-to-beat, short-, medium- and long-term cardiac homoeostasis. By presenting the latest data, we will also provide a framework in which the peculiar morpho-functional arrangement of the teleost and amphibian heart can be considered as a reference tool to decipher cardiac regulatory networks which are difficult to explore using more conventional vertebrates, such as mammals.

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Morpho-functional characterization of the goldfish (Carassius auratus L.) heart

Cited by 36 publications

References 33 publications

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Cardiac repair and regenerative potential in the goldfish (Carassius auratus) heart

NO, CO and H₂S: What about gasotransmitters in fish and amphibian heart?

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Morpho-functional characterization of the goldfish (Carassius auratus L.) heart

Cited by 36 publications

References 33 publications

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Cardiac repair and regenerative potential in the goldfish (Carassius auratus) heart

NO, CO and H2S: What about gasotransmitters in fish and amphibian heart?

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NO, CO and H₂S: What about gasotransmitters in fish and amphibian heart?