Evolution and Development of Ventricular Septation in the Amniote Heart

During cardiogenesis the epicardium, covering the surface of the myocardial tube, has been ascribed several functions essential for normal heart development of vertebrates from lampreys to mammals. We investigated a novel function of the epicardium in ventricular development in species with partial...

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Main Authors: Poelmann, Robert E., Groot, Adriana C. Gittenberger-de, Vicente-Steijn, Rebecca, Wisse, Lambertus J., Bartelings, Margot M., Everts, Sonja, Hoppenbrouwers, Tamara, Kruithof, Boudewijn P. T., Jensen, Bjarke, de Bruin, Paul W., Hirasawa, Tatsuya, Kuratani, Shigeru, Vonk, Freek, van de Put, Jeanne M. M. S., de Bakker, Merijn A., Richardson, Michael K.
Format: Online
Language:English
Published: Public Library of Science 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4156344/
id pubmed-4156344
recordtype oai_dc
spelling pubmed-41563442014-09-09 Evolution and Development of Ventricular Septation in the Amniote Heart Poelmann, Robert E. Groot, Adriana C. Gittenberger-de Vicente-Steijn, Rebecca Wisse, Lambertus J. Bartelings, Margot M. Everts, Sonja Hoppenbrouwers, Tamara Kruithof, Boudewijn P. T. Jensen, Bjarke de Bruin, Paul W. Hirasawa, Tatsuya Kuratani, Shigeru Vonk, Freek van de Put, Jeanne M. M. S. de Bakker, Merijn A. Richardson, Michael K. Research Article During cardiogenesis the epicardium, covering the surface of the myocardial tube, has been ascribed several functions essential for normal heart development of vertebrates from lampreys to mammals. We investigated a novel function of the epicardium in ventricular development in species with partial and complete septation. These species include reptiles, birds and mammals. Adult turtles, lizards and snakes have a complex ventricle with three cava, partially separated by the horizontal and vertical septa. The crocodilians, birds and mammals with origins some 100 million years apart, however, have a left and right ventricle that are completely separated, being a clear example of convergent evolution. In specific embryonic stages these species show similarities in development, prompting us to investigate the mechanisms underlying epicardial involvement. The primitive ventricle of early embryos becomes septated by folding and fusion of the anterior ventricular wall, trapping epicardium in its core. This folding septum develops as the horizontal septum in reptiles and the anterior part of the interventricular septum in the other taxa. The mechanism of folding is confirmed using DiI tattoos of the ventricular surface. Trapping of epicardium-derived cells is studied by transplanting embryonic quail pro-epicardial organ into chicken hosts. The effect of decreased epicardium involvement is studied in knock-out mice, and pro-epicardium ablated chicken, resulting in diminished and even absent septum formation. Proper folding followed by diminished ventricular fusion may explain the deep interventricular cleft observed in elephants. The vertical septum, although indistinct in most reptiles except in crocodilians and pythonidsis apparently homologous to the inlet septum. Eventually the various septal components merge to form the completely septated heart. In our attempt to discover homologies between the various septum components we aim to elucidate the evolution and development of this part of the vertebrate heart as well as understand the etiology of septal defects in human congenital heart malformations. Public Library of Science 2014-09-05 /pmc/articles/PMC4156344/ /pubmed/25192012 http://dx.doi.org/10.1371/journal.pone.0106569 Text en © 2014 Poelmann et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Poelmann, Robert E.
Groot, Adriana C. Gittenberger-de
Vicente-Steijn, Rebecca
Wisse, Lambertus J.
Bartelings, Margot M.
Everts, Sonja
Hoppenbrouwers, Tamara
Kruithof, Boudewijn P. T.
Jensen, Bjarke
de Bruin, Paul W.
Hirasawa, Tatsuya
Kuratani, Shigeru
Vonk, Freek
van de Put, Jeanne M. M. S.
de Bakker, Merijn A.
Richardson, Michael K.
spellingShingle Poelmann, Robert E.
Groot, Adriana C. Gittenberger-de
Vicente-Steijn, Rebecca
Wisse, Lambertus J.
Bartelings, Margot M.
Everts, Sonja
Hoppenbrouwers, Tamara
Kruithof, Boudewijn P. T.
Jensen, Bjarke
de Bruin, Paul W.
Hirasawa, Tatsuya
Kuratani, Shigeru
Vonk, Freek
van de Put, Jeanne M. M. S.
de Bakker, Merijn A.
Richardson, Michael K.
Evolution and Development of Ventricular Septation in the Amniote Heart
author_facet Poelmann, Robert E.
Groot, Adriana C. Gittenberger-de
Vicente-Steijn, Rebecca
Wisse, Lambertus J.
Bartelings, Margot M.
Everts, Sonja
Hoppenbrouwers, Tamara
Kruithof, Boudewijn P. T.
Jensen, Bjarke
de Bruin, Paul W.
Hirasawa, Tatsuya
Kuratani, Shigeru
Vonk, Freek
van de Put, Jeanne M. M. S.
de Bakker, Merijn A.
Richardson, Michael K.
author_sort Poelmann, Robert E.
title Evolution and Development of Ventricular Septation in the Amniote Heart
title_short Evolution and Development of Ventricular Septation in the Amniote Heart
title_full Evolution and Development of Ventricular Septation in the Amniote Heart
title_fullStr Evolution and Development of Ventricular Septation in the Amniote Heart
title_full_unstemmed Evolution and Development of Ventricular Septation in the Amniote Heart
title_sort evolution and development of ventricular septation in the amniote heart
description During cardiogenesis the epicardium, covering the surface of the myocardial tube, has been ascribed several functions essential for normal heart development of vertebrates from lampreys to mammals. We investigated a novel function of the epicardium in ventricular development in species with partial and complete septation. These species include reptiles, birds and mammals. Adult turtles, lizards and snakes have a complex ventricle with three cava, partially separated by the horizontal and vertical septa. The crocodilians, birds and mammals with origins some 100 million years apart, however, have a left and right ventricle that are completely separated, being a clear example of convergent evolution. In specific embryonic stages these species show similarities in development, prompting us to investigate the mechanisms underlying epicardial involvement. The primitive ventricle of early embryos becomes septated by folding and fusion of the anterior ventricular wall, trapping epicardium in its core. This folding septum develops as the horizontal septum in reptiles and the anterior part of the interventricular septum in the other taxa. The mechanism of folding is confirmed using DiI tattoos of the ventricular surface. Trapping of epicardium-derived cells is studied by transplanting embryonic quail pro-epicardial organ into chicken hosts. The effect of decreased epicardium involvement is studied in knock-out mice, and pro-epicardium ablated chicken, resulting in diminished and even absent septum formation. Proper folding followed by diminished ventricular fusion may explain the deep interventricular cleft observed in elephants. The vertical septum, although indistinct in most reptiles except in crocodilians and pythonidsis apparently homologous to the inlet septum. Eventually the various septal components merge to form the completely septated heart. In our attempt to discover homologies between the various septum components we aim to elucidate the evolution and development of this part of the vertebrate heart as well as understand the etiology of septal defects in human congenital heart malformations.
publisher Public Library of Science
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4156344/
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