Cargando…

Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature

BACKGROUND: The development of blood flow in the heart is crucial for heart function and embryonic survival. Recent studies have revealed the importance of the extracellular matrix and the mechanical stress applied to the valve cushion that controls blood flow to the formation of the cardiac valve d...

Descripción completa

Detalles Bibliográficos
Autores principales: Watanabe-Asaka, Tomomi, Sekiya, Yoshio, Wada, Hironori, Yasuda, Takako, Okubo, Ikuya, Oda, Shoji, Mitani, Hiroshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3936829/
https://www.ncbi.nlm.nih.gov/pubmed/24564206
http://dx.doi.org/10.1186/1471-213X-14-12
_version_ 1782305372509306880
author Watanabe-Asaka, Tomomi
Sekiya, Yoshio
Wada, Hironori
Yasuda, Takako
Okubo, Ikuya
Oda, Shoji
Mitani, Hiroshi
author_facet Watanabe-Asaka, Tomomi
Sekiya, Yoshio
Wada, Hironori
Yasuda, Takako
Okubo, Ikuya
Oda, Shoji
Mitani, Hiroshi
author_sort Watanabe-Asaka, Tomomi
collection PubMed
description BACKGROUND: The development of blood flow in the heart is crucial for heart function and embryonic survival. Recent studies have revealed the importance of the extracellular matrix and the mechanical stress applied to the valve cushion that controls blood flow to the formation of the cardiac valve during embryogenesis. However, the events that trigger such valve formation and mechanical stress, and their temperature dependence have not been explained completely. Medaka (Oryzias latipes) inhabits a wide range of East Asia and adapts to a wide range of climates. We used medaka embryos from different genomic backgrounds and analyzed heartbeat characteristics including back-and-forth blood flow and bradyarrhythmia in embryos incubated at low temperature. We also used high-speed imaging analysis to examine the heartbeat of these animals after transient exposure to low temperature. RESULTS: Embryos of the Hd-rR medaka strain exhibited back-and-forth blood flow in the heart (blood regurgitation) after incubation at 15°C. This regurgitation was induced by exposure to low temperature around the heartbeat initiation period and was related to abnormalities in the maintenance or pattern of contraction of the atrium or the atrioventricular canal. The Odate strain from the northern Japanese group exhibited normal blood flow after incubation at 15°C. High-speed time-lapse analysis of the heartbeat revealed that bradyarrhythmia occurred only in Hd-rR embryos incubated at 15°C. The coefficient of contraction, defined as the quotient of the length of the atrium at systole divided by its length at diastole, was not affected in either strain. The average heart rate after removing the effect of arrhythmia did not differ significantly between the two strains, suggesting that the mechanical stress of individual myocardial contractions and the total mechanical stress could be equivalent, regardless of the presence of arrhythmia or the heart rate. Test-cross experiments suggested that this circulation phenotype was caused by a single major genomic locus. CONCLUSIONS: These results suggest that cardiogenesis at low temperature requires a constant heartbeat. Abnormal contraction rhythms at the stage of heartbeat initiation may cause regurgitation at later stages. From the evolutionary viewpoint, strains that exhibit normal cardiogenesis during development at low temperature inhabit northern environments.
format Online
Article
Text
id pubmed-3936829
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-39368292014-02-28 Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature Watanabe-Asaka, Tomomi Sekiya, Yoshio Wada, Hironori Yasuda, Takako Okubo, Ikuya Oda, Shoji Mitani, Hiroshi BMC Dev Biol Research Article BACKGROUND: The development of blood flow in the heart is crucial for heart function and embryonic survival. Recent studies have revealed the importance of the extracellular matrix and the mechanical stress applied to the valve cushion that controls blood flow to the formation of the cardiac valve during embryogenesis. However, the events that trigger such valve formation and mechanical stress, and their temperature dependence have not been explained completely. Medaka (Oryzias latipes) inhabits a wide range of East Asia and adapts to a wide range of climates. We used medaka embryos from different genomic backgrounds and analyzed heartbeat characteristics including back-and-forth blood flow and bradyarrhythmia in embryos incubated at low temperature. We also used high-speed imaging analysis to examine the heartbeat of these animals after transient exposure to low temperature. RESULTS: Embryos of the Hd-rR medaka strain exhibited back-and-forth blood flow in the heart (blood regurgitation) after incubation at 15°C. This regurgitation was induced by exposure to low temperature around the heartbeat initiation period and was related to abnormalities in the maintenance or pattern of contraction of the atrium or the atrioventricular canal. The Odate strain from the northern Japanese group exhibited normal blood flow after incubation at 15°C. High-speed time-lapse analysis of the heartbeat revealed that bradyarrhythmia occurred only in Hd-rR embryos incubated at 15°C. The coefficient of contraction, defined as the quotient of the length of the atrium at systole divided by its length at diastole, was not affected in either strain. The average heart rate after removing the effect of arrhythmia did not differ significantly between the two strains, suggesting that the mechanical stress of individual myocardial contractions and the total mechanical stress could be equivalent, regardless of the presence of arrhythmia or the heart rate. Test-cross experiments suggested that this circulation phenotype was caused by a single major genomic locus. CONCLUSIONS: These results suggest that cardiogenesis at low temperature requires a constant heartbeat. Abnormal contraction rhythms at the stage of heartbeat initiation may cause regurgitation at later stages. From the evolutionary viewpoint, strains that exhibit normal cardiogenesis during development at low temperature inhabit northern environments. BioMed Central 2014-02-25 /pmc/articles/PMC3936829/ /pubmed/24564206 http://dx.doi.org/10.1186/1471-213X-14-12 Text en Copyright © 2014 Watanabe-Asaka et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Watanabe-Asaka, Tomomi
Sekiya, Yoshio
Wada, Hironori
Yasuda, Takako
Okubo, Ikuya
Oda, Shoji
Mitani, Hiroshi
Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature
title Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature
title_full Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature
title_fullStr Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature
title_full_unstemmed Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature
title_short Regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature
title_sort regular heartbeat rhythm at the heartbeat initiation stage is essential for normal cardiogenesis at low temperature
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3936829/
https://www.ncbi.nlm.nih.gov/pubmed/24564206
http://dx.doi.org/10.1186/1471-213X-14-12
work_keys_str_mv AT watanabeasakatomomi regularheartbeatrhythmattheheartbeatinitiationstageisessentialfornormalcardiogenesisatlowtemperature
AT sekiyayoshio regularheartbeatrhythmattheheartbeatinitiationstageisessentialfornormalcardiogenesisatlowtemperature
AT wadahironori regularheartbeatrhythmattheheartbeatinitiationstageisessentialfornormalcardiogenesisatlowtemperature
AT yasudatakako regularheartbeatrhythmattheheartbeatinitiationstageisessentialfornormalcardiogenesisatlowtemperature
AT okuboikuya regularheartbeatrhythmattheheartbeatinitiationstageisessentialfornormalcardiogenesisatlowtemperature
AT odashoji regularheartbeatrhythmattheheartbeatinitiationstageisessentialfornormalcardiogenesisatlowtemperature
AT mitanihiroshi regularheartbeatrhythmattheheartbeatinitiationstageisessentialfornormalcardiogenesisatlowtemperature