The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafish

In the adult heart, acute adaptation of electrical and mechanical activity to changes in mechanical load occurs via feedback processes known as “mechano-electric coupling” and “mechano-mechanical coupling.” Whether this occurs during cardiac development is ill-defined, as acutely altering the heart’...

Full description

Bibliographic Details
Main Authors: Jonathan S. Baillie, Alex Gendernalik, Deborah M. Garrity, David Bark, T. Alexander Quinn
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1086050/full
_version_ 1797869568103809024
author Jonathan S. Baillie
Alex Gendernalik
Deborah M. Garrity
David Bark
David Bark
David Bark
T. Alexander Quinn
T. Alexander Quinn
author_facet Jonathan S. Baillie
Alex Gendernalik
Deborah M. Garrity
David Bark
David Bark
David Bark
T. Alexander Quinn
T. Alexander Quinn
author_sort Jonathan S. Baillie
collection DOAJ
description In the adult heart, acute adaptation of electrical and mechanical activity to changes in mechanical load occurs via feedback processes known as “mechano-electric coupling” and “mechano-mechanical coupling.” Whether this occurs during cardiac development is ill-defined, as acutely altering the heart’s mechanical load while measuring functional responses in traditional experimental models is difficult, as embryogenesis occurs in utero, making the heart inaccessible. These limitations can be overcome with zebrafish, as larvae develop in a dish and are nearly transparent, allowing for in vivo manipulation and measurement of cardiac structure and function. Here we present a novel approach for the in vivo study of mechano-electric and mechano-mechanical coupling in the developing zebrafish heart. This innovative methodology involves acute in vivo atrial dilation (i.e., increased atrial preload) in larval zebrafish by injection of a controlled volume into the venous circulation immediately upstream of the heart, combined with optical measurement of the acute electrical (change in heart rate) and mechanical (change in stroke area) response. In proof-of-concept experiments, we applied our new method to 48 h post-fertilisation zebrafish, which revealed differences between the electrical and mechanical response to atrial dilation. In response to an acute increase in atrial preload there is a large increase in atrial stroke area but no change in heart rate, demonstrating that in contrast to the fully developed heart, during early cardiac development mechano-mechanical coupling alone drives the adaptive increase in atrial output. Overall, in this methodological paper we present our new experimental approach for the study of mechano-electric and mechano-mechanical coupling during cardiac development and demonstrate its potential for understanding the essential adaptation of heart function to acute changes in mechanical load.
first_indexed 2024-04-10T00:14:44Z
format Article
id doaj.art-ac96dca868404c76992da6675c28be03
institution Directory Open Access Journal
issn 1664-042X
language English
last_indexed 2024-04-10T00:14:44Z
publishDate 2023-03-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Physiology
spelling doaj.art-ac96dca868404c76992da6675c28be032023-03-16T06:22:38ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-03-011410.3389/fphys.2023.10860501086050The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafishJonathan S. Baillie0Alex Gendernalik1Deborah M. Garrity2David Bark3David Bark4David Bark5T. Alexander Quinn6T. Alexander Quinn7Physiology & Biophysics, Dalhousie University, Halifax, NS, CanadaBiomedical Engineering, Colorado State University, Fort Collins, CO, United StatesBiology, Colorado State University, Fort Collins, CO, United StatesBiomedical Engineering, Colorado State University, Fort Collins, CO, United StatesMechanical Engineering, Colorado State University, Fort Collins, CO, United StatesDepartment of Pediatrics, Washington University in St. Louis, St. Louis, MO, United StatesPhysiology & Biophysics, Dalhousie University, Halifax, NS, CanadaBiomedical Engineering, Dalhousie University, Halifax, NS, CanadaIn the adult heart, acute adaptation of electrical and mechanical activity to changes in mechanical load occurs via feedback processes known as “mechano-electric coupling” and “mechano-mechanical coupling.” Whether this occurs during cardiac development is ill-defined, as acutely altering the heart’s mechanical load while measuring functional responses in traditional experimental models is difficult, as embryogenesis occurs in utero, making the heart inaccessible. These limitations can be overcome with zebrafish, as larvae develop in a dish and are nearly transparent, allowing for in vivo manipulation and measurement of cardiac structure and function. Here we present a novel approach for the in vivo study of mechano-electric and mechano-mechanical coupling in the developing zebrafish heart. This innovative methodology involves acute in vivo atrial dilation (i.e., increased atrial preload) in larval zebrafish by injection of a controlled volume into the venous circulation immediately upstream of the heart, combined with optical measurement of the acute electrical (change in heart rate) and mechanical (change in stroke area) response. In proof-of-concept experiments, we applied our new method to 48 h post-fertilisation zebrafish, which revealed differences between the electrical and mechanical response to atrial dilation. In response to an acute increase in atrial preload there is a large increase in atrial stroke area but no change in heart rate, demonstrating that in contrast to the fully developed heart, during early cardiac development mechano-mechanical coupling alone drives the adaptive increase in atrial output. Overall, in this methodological paper we present our new experimental approach for the study of mechano-electric and mechano-mechanical coupling during cardiac development and demonstrate its potential for understanding the essential adaptation of heart function to acute changes in mechanical load.https://www.frontiersin.org/articles/10.3389/fphys.2023.1086050/fullBainbridge effectcardiac outputend-diastolic areaFrank-Starling mechanismheart ratestretch
spellingShingle Jonathan S. Baillie
Alex Gendernalik
Deborah M. Garrity
David Bark
David Bark
David Bark
T. Alexander Quinn
T. Alexander Quinn
The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafish
Frontiers in Physiology
Bainbridge effect
cardiac output
end-diastolic area
Frank-Starling mechanism
heart rate
stretch
title The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafish
title_full The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafish
title_fullStr The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafish
title_full_unstemmed The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafish
title_short The in vivo study of cardiac mechano-electric and mechano-mechanical coupling during heart development in zebrafish
title_sort in vivo study of cardiac mechano electric and mechano mechanical coupling during heart development in zebrafish
topic Bainbridge effect
cardiac output
end-diastolic area
Frank-Starling mechanism
heart rate
stretch
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1086050/full
work_keys_str_mv AT jonathansbaillie theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT alexgendernalik theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT deborahmgarrity theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT davidbark theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT davidbark theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT davidbark theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT talexanderquinn theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT talexanderquinn theinvivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT jonathansbaillie invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT alexgendernalik invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT deborahmgarrity invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT davidbark invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT davidbark invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT davidbark invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT talexanderquinn invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish
AT talexanderquinn invivostudyofcardiacmechanoelectricandmechanomechanicalcouplingduringheartdevelopmentinzebrafish