Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart
Abstract Background Cardiac outflow tract patterning and cell contribution are studied using an evo-devo approach to reveal insight into the development of aorto-pulmonary septation. Results We studied embryonic stages of reptile hearts (lizard, turtle and crocodile) and compared these to avian and...
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| Format: | Article |
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BMC
2017-05-01
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| Series: | EvoDevo |
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| Online Access: | http://link.springer.com/article/10.1186/s13227-017-0072-z |
| _version_ | 1818905736302821376 |
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| author | Robert E. Poelmann Adriana C. Gittenberger-de Groot Marcel W. M. Biermans Anne I. Dolfing Armand Jagessar Sam van Hattum Amanda Hoogenboom Lambertus J. Wisse Rebecca Vicente-Steijn Merijn A. G. de Bakker Freek J. Vonk Tatsuya Hirasawa Shigeru Kuratani Michael K. Richardson |
| author_facet | Robert E. Poelmann Adriana C. Gittenberger-de Groot Marcel W. M. Biermans Anne I. Dolfing Armand Jagessar Sam van Hattum Amanda Hoogenboom Lambertus J. Wisse Rebecca Vicente-Steijn Merijn A. G. de Bakker Freek J. Vonk Tatsuya Hirasawa Shigeru Kuratani Michael K. Richardson |
| author_sort | Robert E. Poelmann |
| collection | DOAJ |
| description | Abstract Background Cardiac outflow tract patterning and cell contribution are studied using an evo-devo approach to reveal insight into the development of aorto-pulmonary septation. Results We studied embryonic stages of reptile hearts (lizard, turtle and crocodile) and compared these to avian and mammalian development. Immunohistochemistry allowed us to indicate where the essential cell components in the outflow tract and aortic sac were deployed, more specifically endocardial, neural crest and second heart field cells. The neural crest-derived aorto-pulmonary septum separates the pulmonary trunk from both aortae in reptiles, presenting with a left visceral and a right systemic aorta arising from the unseptated ventricle. Second heart field-derived cells function as flow dividers between both aortae and between the two pulmonary arteries. In birds, the left visceral aorta disappears early in development, while the right systemic aorta persists. This leads to a fusion of the aorto-pulmonary septum and the aortic flow divider (second heart field population) forming an avian aorto-pulmonary septal complex. In mammals, there is also a second heart field-derived aortic flow divider, albeit at a more distal site, while the aorto-pulmonary septum separates the aortic trunk from the pulmonary trunk. As in birds there is fusion with second heart field-derived cells albeit from the pulmonary flow divider as the right 6th pharyngeal arch artery disappears, resulting in a mammalian aorto-pulmonary septal complex. In crocodiles, birds and mammals, the main septal and parietal endocardial cushions receive neural crest cells that are functional in fusion and myocardialization of the outflow tract septum. Longer-lasting septation in crocodiles demonstrates a heterochrony in development. In other reptiles with no indication of incursion of neural crest cells, there is either no myocardialized outflow tract septum (lizard) or it is vestigial (turtle). Crocodiles are unique in bearing a central shunt, the foramen of Panizza, between the roots of both aortae. Finally, the soft-shell turtle investigated here exhibits a spongy histology of the developing carotid arteries supposedly related to regulation of blood flow during pharyngeal excretion in this species. Conclusions This is the first time that is shown that an interplay of second heart field-derived flow dividers with a neural crest-derived cell population is a variable but common, denominator across all species studied for vascular patterning and outflow tract septation. The observed differences in normal development of reptiles may have impact on the understanding of development of human congenital outflow tract malformations. |
| first_indexed | 2024-12-19T21:28:04Z |
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| institution | Directory Open Access Journal |
| issn | 2041-9139 |
| language | English |
| last_indexed | 2024-12-19T21:28:04Z |
| publishDate | 2017-05-01 |
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| series | EvoDevo |
| spelling | doaj.art-6facba4458b147179aae26a24ddccbcf2022-12-21T20:05:03ZengBMCEvoDevo2041-91392017-05-018111710.1186/s13227-017-0072-zOutflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heartRobert E. Poelmann0Adriana C. Gittenberger-de Groot1Marcel W. M. Biermans2Anne I. Dolfing3Armand Jagessar4Sam van Hattum5Amanda Hoogenboom6Lambertus J. Wisse7Rebecca Vicente-Steijn8Merijn A. G. de Bakker9Freek J. Vonk10Tatsuya Hirasawa11Shigeru Kuratani12Michael K. Richardson13Department of Cardiology, Leiden University Medical CenterDepartment of Cardiology, Leiden University Medical CenterAnimal Sciences and Health, Sylvius Laboratories, University of LeidenAnimal Sciences and Health, Sylvius Laboratories, University of LeidenAnimal Sciences and Health, Sylvius Laboratories, University of LeidenAnimal Sciences and Health, Sylvius Laboratories, University of LeidenAnimal Sciences and Health, Sylvius Laboratories, University of LeidenDepartment of Anatomy and Embryology, Leiden University Medical CenterDepartment of Cardiology, Leiden University Medical CenterAnimal Sciences and Health, Sylvius Laboratories, University of LeidenAnimal Sciences and Health, Sylvius Laboratories, University of LeidenLaboratory for Evolutionary Morphology, RIKENLaboratory for Evolutionary Morphology, RIKENAnimal Sciences and Health, Sylvius Laboratories, University of LeidenAbstract Background Cardiac outflow tract patterning and cell contribution are studied using an evo-devo approach to reveal insight into the development of aorto-pulmonary septation. Results We studied embryonic stages of reptile hearts (lizard, turtle and crocodile) and compared these to avian and mammalian development. Immunohistochemistry allowed us to indicate where the essential cell components in the outflow tract and aortic sac were deployed, more specifically endocardial, neural crest and second heart field cells. The neural crest-derived aorto-pulmonary septum separates the pulmonary trunk from both aortae in reptiles, presenting with a left visceral and a right systemic aorta arising from the unseptated ventricle. Second heart field-derived cells function as flow dividers between both aortae and between the two pulmonary arteries. In birds, the left visceral aorta disappears early in development, while the right systemic aorta persists. This leads to a fusion of the aorto-pulmonary septum and the aortic flow divider (second heart field population) forming an avian aorto-pulmonary septal complex. In mammals, there is also a second heart field-derived aortic flow divider, albeit at a more distal site, while the aorto-pulmonary septum separates the aortic trunk from the pulmonary trunk. As in birds there is fusion with second heart field-derived cells albeit from the pulmonary flow divider as the right 6th pharyngeal arch artery disappears, resulting in a mammalian aorto-pulmonary septal complex. In crocodiles, birds and mammals, the main septal and parietal endocardial cushions receive neural crest cells that are functional in fusion and myocardialization of the outflow tract septum. Longer-lasting septation in crocodiles demonstrates a heterochrony in development. In other reptiles with no indication of incursion of neural crest cells, there is either no myocardialized outflow tract septum (lizard) or it is vestigial (turtle). Crocodiles are unique in bearing a central shunt, the foramen of Panizza, between the roots of both aortae. Finally, the soft-shell turtle investigated here exhibits a spongy histology of the developing carotid arteries supposedly related to regulation of blood flow during pharyngeal excretion in this species. Conclusions This is the first time that is shown that an interplay of second heart field-derived flow dividers with a neural crest-derived cell population is a variable but common, denominator across all species studied for vascular patterning and outflow tract septation. The observed differences in normal development of reptiles may have impact on the understanding of development of human congenital outflow tract malformations.http://link.springer.com/article/10.1186/s13227-017-0072-zCardiac developmentOutflow tract cushionsAorto-pulmonary septationFlow dividerNeural crestSecond heart field |
| spellingShingle | Robert E. Poelmann Adriana C. Gittenberger-de Groot Marcel W. M. Biermans Anne I. Dolfing Armand Jagessar Sam van Hattum Amanda Hoogenboom Lambertus J. Wisse Rebecca Vicente-Steijn Merijn A. G. de Bakker Freek J. Vonk Tatsuya Hirasawa Shigeru Kuratani Michael K. Richardson Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart EvoDevo Cardiac development Outflow tract cushions Aorto-pulmonary septation Flow divider Neural crest Second heart field |
| title | Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart |
| title_full | Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart |
| title_fullStr | Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart |
| title_full_unstemmed | Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart |
| title_short | Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart |
| title_sort | outflow tract septation and the aortic arch system in reptiles lessons for understanding the mammalian heart |
| topic | Cardiac development Outflow tract cushions Aorto-pulmonary septation Flow divider Neural crest Second heart field |
| url | http://link.springer.com/article/10.1186/s13227-017-0072-z |
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