Abstract:Rainbow trout (Oncorhynchus mykiss) cardiomyocytes have a simple morphology with fewer membrane structures such as sarcoplasmic reticulum and t-tubules penetrating the cytosol. Despite this, intracellular ADP diffusion is restricted. Intriguingly, although diffusion is restricted, trout cardiomyocytes seem to lack the coupling between mitochondrial creatine kinase (CK) and respiration. Our aim was to study the distribution of diffusion restrictions in permeabilized trout cardiomyocytes and verify the role of C… Show more
“…The sarcoplasmic reticulum (SR) is present, but sparse and looks to be positioned mainly just below the sarcolemma [26]. This resembles the overall morphology of cardiomyocytes from most fishes, including trout, mackerel and tuna [9,10,15,21,25,36,38].…”
Section: Changes In Morphology During Ontogenymentioning
confidence: 90%
“…The sarcoplasmic reticulum (SR) is present, but sparse and looks to be positioned mainly just below the sarcolemma [26]. This resembles the overall morphology of cardiomyocytes from most fishes, including trout, mackerel and tuna [9,10,15,21,25,36,38]. Figure 1Schematic of ( a ) fish cardiomyocyte, ( b ) neonatal mammalian cardiomyocyte, and ( c ) adult mammalian cardiomyocyte drawn on the basis of the references in table 1.…”
Section: Changes In Morphology During Ontogenymentioning
confidence: 99%
“…Within each table cell, references are in square brackets.) fishes neonatal mammals adult mammals ventricular morphology outer compact and inner spongy layer, trabecular sheets form smaller luminae radiating from the central lumen [10][11][12] compact wall and central chamber [13] compact wall, central chamber mean aortic pressure (mmHg) 40-60 (trout) [5] approximately 30 [3,4] approximately 100 [14] cardiomyocyte length (µm) [15,16,23] 1.05 [24] 4.5-8.5 [20] myofibril positioning usually a single peripheral ring [10,21,22,25] single peripheral ring [26,27] multiple rows throughout the cell [28] myofibrillar volume 45-55% [10,29] 30% [30] 55-60% [30] SR positioning mainly peripheral, but some in the cytoplasm [9,10,21] mainly peripheral [26] continuous network throughout the cell, junctional SR associated with the t-tubules is connected by network SR [28,31] SR µm 2 area µm −3 vol 0.15-0.25 (tuna) [9,32] 0.18 [24] 0.27-1 [19,24,33] SR contribution to Ca 2+ fluxes in e-c coupling highly variable between species, 50% in trout [34] 40% [35] 70-90% [19,35] mitochondrial positioning central core, sometimes a few peripheral [9,…”
Section: Changes In Excitation-contraction Coupling During Ontogenymentioning
confidence: 99%
“…Within each table cell, references are in square brackets. )fishesneonatal mammalsadult mammalsventricular morphologyouter compact and inner spongy layer, trabecular sheets form smaller luminae radiating from the central lumen [10–12]compact wall and central chamber [13]compact wall, central chambermean aortic pressure (mmHg)40–60 (trout) [5]approximately 30 [3,4]approximately 100 [14]cardiomyocyte length (µm)100–170 [15–17]70 [18]120–140 [18–20]cardiomyocyte diameter (µm)4–8 [15–17,21,22]8 [18]22–32 [18–20]cardiomyocyte volume (pl)1.1–3.4 [15–17]30–35 [20]t-tubulesNoNoYessarcolemma µm 2 area µm − 3 cell volapproximately 1.2 [15,16,23]1.05 [24]4.5–8.5 [20]myofibril positioningusually a single peripheral ring [10,21,22,25]single peripheral ring [26,27]multiple rows throughout the cell [28…”
Section: Changes In Morphology During Ontogenymentioning
The ontogeny of the heart describes its development from the fetal to the adult stage. In newborn mammals, blood pressure and thus cardiac performance are relatively low. The cardiomyocytes are thin, and with a central core of mitochondria surrounded by a ring of myofilaments, while the sarcoplasmic reticulum (SR) is sparse. During development, as blood pressure and performance increase, the cardiomyocytes become more packed with structures involved in excitation–contraction (e-c) coupling (SR and myofilaments) and the generation of ATP (mitochondria) to fuel the contraction. In parallel, the e-c coupling relies increasingly on calcium fluxes through the SR, while metabolism relies increasingly on fatty acid oxidation. The development of transverse tubules and SR brings channels and transporters interacting via calcium closer to each other and is crucial for e-c coupling. However, for energy transfer, it may seem counterintuitive that the increased structural density restricts the overall ATP/ADP diffusion. In this review, we discuss how this is because of the organization of all these structures forming modules. Although the overall diffusion across modules is more restricted, the energy transfer within modules is fast. A few studies suggest that in failing hearts this modular design is disrupted, and this may compromise intracellular energy transfer.
This article is part of the theme issue ‘The cardiomyocyte: new revelations on the interplay between architecture and function in growth, health, and disease’.
“…The sarcoplasmic reticulum (SR) is present, but sparse and looks to be positioned mainly just below the sarcolemma [26]. This resembles the overall morphology of cardiomyocytes from most fishes, including trout, mackerel and tuna [9,10,15,21,25,36,38].…”
Section: Changes In Morphology During Ontogenymentioning
confidence: 90%
“…The sarcoplasmic reticulum (SR) is present, but sparse and looks to be positioned mainly just below the sarcolemma [26]. This resembles the overall morphology of cardiomyocytes from most fishes, including trout, mackerel and tuna [9,10,15,21,25,36,38]. Figure 1Schematic of ( a ) fish cardiomyocyte, ( b ) neonatal mammalian cardiomyocyte, and ( c ) adult mammalian cardiomyocyte drawn on the basis of the references in table 1.…”
Section: Changes In Morphology During Ontogenymentioning
confidence: 99%
“…Within each table cell, references are in square brackets.) fishes neonatal mammals adult mammals ventricular morphology outer compact and inner spongy layer, trabecular sheets form smaller luminae radiating from the central lumen [10][11][12] compact wall and central chamber [13] compact wall, central chamber mean aortic pressure (mmHg) 40-60 (trout) [5] approximately 30 [3,4] approximately 100 [14] cardiomyocyte length (µm) [15,16,23] 1.05 [24] 4.5-8.5 [20] myofibril positioning usually a single peripheral ring [10,21,22,25] single peripheral ring [26,27] multiple rows throughout the cell [28] myofibrillar volume 45-55% [10,29] 30% [30] 55-60% [30] SR positioning mainly peripheral, but some in the cytoplasm [9,10,21] mainly peripheral [26] continuous network throughout the cell, junctional SR associated with the t-tubules is connected by network SR [28,31] SR µm 2 area µm −3 vol 0.15-0.25 (tuna) [9,32] 0.18 [24] 0.27-1 [19,24,33] SR contribution to Ca 2+ fluxes in e-c coupling highly variable between species, 50% in trout [34] 40% [35] 70-90% [19,35] mitochondrial positioning central core, sometimes a few peripheral [9,…”
Section: Changes In Excitation-contraction Coupling During Ontogenymentioning
confidence: 99%
“…Within each table cell, references are in square brackets. )fishesneonatal mammalsadult mammalsventricular morphologyouter compact and inner spongy layer, trabecular sheets form smaller luminae radiating from the central lumen [10–12]compact wall and central chamber [13]compact wall, central chambermean aortic pressure (mmHg)40–60 (trout) [5]approximately 30 [3,4]approximately 100 [14]cardiomyocyte length (µm)100–170 [15–17]70 [18]120–140 [18–20]cardiomyocyte diameter (µm)4–8 [15–17,21,22]8 [18]22–32 [18–20]cardiomyocyte volume (pl)1.1–3.4 [15–17]30–35 [20]t-tubulesNoNoYessarcolemma µm 2 area µm − 3 cell volapproximately 1.2 [15,16,23]1.05 [24]4.5–8.5 [20]myofibril positioningusually a single peripheral ring [10,21,22,25]single peripheral ring [26,27]multiple rows throughout the cell [28…”
Section: Changes In Morphology During Ontogenymentioning
The ontogeny of the heart describes its development from the fetal to the adult stage. In newborn mammals, blood pressure and thus cardiac performance are relatively low. The cardiomyocytes are thin, and with a central core of mitochondria surrounded by a ring of myofilaments, while the sarcoplasmic reticulum (SR) is sparse. During development, as blood pressure and performance increase, the cardiomyocytes become more packed with structures involved in excitation–contraction (e-c) coupling (SR and myofilaments) and the generation of ATP (mitochondria) to fuel the contraction. In parallel, the e-c coupling relies increasingly on calcium fluxes through the SR, while metabolism relies increasingly on fatty acid oxidation. The development of transverse tubules and SR brings channels and transporters interacting via calcium closer to each other and is crucial for e-c coupling. However, for energy transfer, it may seem counterintuitive that the increased structural density restricts the overall ATP/ADP diffusion. In this review, we discuss how this is because of the organization of all these structures forming modules. Although the overall diffusion across modules is more restricted, the energy transfer within modules is fast. A few studies suggest that in failing hearts this modular design is disrupted, and this may compromise intracellular energy transfer.
This article is part of the theme issue ‘The cardiomyocyte: new revelations on the interplay between architecture and function in growth, health, and disease’.
“…The binding of HK to mitochondria may provide relief from G6P inhibition while PFK bound to contractile protein is preferentially activated. In trout myocytes, HK is functionally coupled to mitochondrial respiration and supports flux of ADP across the outer mitochondrial membrane (Karro et al, 2017). The role of HK in providing hypoxic protection to the catfish heart is intriguing in view of the findings that the interaction of HK with mitochondria is associated with the prevention of death in many cell types, in part by regulating mitochondrial permeability transition pores (Calmettes et al, 2014).…”
Section: Hearts Of Armoured Catfish Under Hypoxia and Acidosismentioning
The heart of tropical fishes is a particularly useful model system in which to investigate mechanisms of hypoxic tolerance. Here we focus on insights gained from two groups of fishes, cichlids and armoured catfishes. Cichlids respond to hypoxia by entering a sustained hypometabolism with decreased heart performance to match whole animal circulatory needs. Heart rate is decreased along with protein turnover to reduce adenosine triphosphate demand. This occurs despite the inherent capacity for high levels of cardiac power development. Although highly hypoxic tolerant at the whole animal level, the heart of cichlids does not have high constitutive activities of glycolytic enzymes compared to other species. Information is conflicting with respect to changes in glycolytic gene expression and enzyme activity following hypoxic exposure with some studies showing increases and others decreases. In contrast to cichlids, species of armoured catfish, that are routinely exposed to water of low oxygen content, do not display hypoxic bradycardia. Under hypoxia there are early changes in glucose trafficking suggestive of activation of glycolysis before lactate accumulation. Thereafter, heart glycogen is mobilized and lactate accumulates in both heart and blood, in some species to very high levels. Heart performance under hypoxia is enhanced by defense of intracellular pH. A functional sarcoplasmic reticulum and binding of hexokinase to the outer mitochondrial membrane may also play a role in cardioprotection. Maintenance of heart performance under hypoxia may relate to a tradeoff between air breathing via a modified stomach and circulatory demands for digestion.
Intracellular molecules are transported by motor proteins or move by diffusion resulting from random molecular motion. Cardiomyocytes are packed with structures that are crucial for function, but also confine the diffusional spaces, providing cells with a means to control diffusion. They form compartments in which local concentrations are different from the overall, average concentrations. For example, calcium and cyclic AMP are highly compartmentalized, allowing these versatile second messengers to send different signals depending on their location. In energetic compartmentalization, the ratios of AMP and ADP to ATP are different from the average ratios. This is important for the performance of ATPases fuelling cardiac excitation‐contraction coupling and mechanical work. A recent study suggested that compartmentalization modulates the activity of creatine kinase and adenylate kinase in situ. This could have implications for energetic signaling through, for example, AMP‐activated kinase. It highlights the importance of taking compartmentalization into account in our interpretation of cellular physiology and developing methods to assess local concentrations of AMP and ADP to enhance our understanding of compartmentalization in different cell types.
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