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Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer

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...

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Autores principales: Birkedal, Rikke, Laasmaa, Martin, Branovets, Jelena, Vendelin, Marko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9527910/
https://www.ncbi.nlm.nih.gov/pubmed/36189816
http://dx.doi.org/10.1098/rstb.2021.0321
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author Birkedal, Rikke
Laasmaa, Martin
Branovets, Jelena
Vendelin, Marko
author_facet Birkedal, Rikke
Laasmaa, Martin
Branovets, Jelena
Vendelin, Marko
author_sort Birkedal, Rikke
collection PubMed
description 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’.
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spelling pubmed-95279102022-10-27 Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer Birkedal, Rikke Laasmaa, Martin Branovets, Jelena Vendelin, Marko Philos Trans R Soc Lond B Biol Sci Articles 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 Royal Society 2022-11-21 2022-10-03 /pmc/articles/PMC9527910/ /pubmed/36189816 http://dx.doi.org/10.1098/rstb.2021.0321 Text en © 2022 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Articles
Birkedal, Rikke
Laasmaa, Martin
Branovets, Jelena
Vendelin, Marko
Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer
title Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer
title_full Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer
title_fullStr Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer
title_full_unstemmed Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer
title_short Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer
title_sort ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9527910/
https://www.ncbi.nlm.nih.gov/pubmed/36189816
http://dx.doi.org/10.1098/rstb.2021.0321
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