Coronary stem development in wild‐type and <i>Tbx1</i> null mouse hearts

Théveniau-Ruissy, Magali; Pérez‐Pomares, J. M.; Parisot, Pauline; Baldini, Antonio; Miquerol, Lucile; Kelly, Robert G.

doi:10.1002/dvdy.24380

Cited by 28 publications

(30 citation statements)

References 40 publications

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“…Note that Tbx1 is also expressed in the conotruncus (arrow in Fig. 1A, a), as previously reported (10) (11).…”

Section: Tbx1 and Vegfr3 Expression Overlap In Cardiac Lymphaticssupporting

confidence: 87%

Tbx1interacts genetically withVegfr3to regulate cardiac lymphangiogenesis in mice

Martucciello

Cioffi

et al. 2019

Preprint

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The transcription factor TBX1 is the major gene implicated in 22q11.2 deletion syndrome. The complex clinical phenotype includes vascular anomalies and a recent report presented new cases of primary lymphedema in 22q11.2DS patients. We have previously shown that Tbx1 activates Vegfr3 gene expression in lymphatic endothelial cells and that this activation is critical for lymphatic vessel development in prenatal mice and for their survival post-natally. Using loss-of-function genetics and transgenesis, we show a strong genetic interaction between Tbx1 and Vegfr3 in cardiac lymphangiogenesis that causes cardiac lymphatic vessel anomalies in compound heterozygotes.Intriguingly, different aspects of the cardiac lymphatic phenotype were regulated independently by the two genes. Tbx1 Cre -activated Vegfr3 transgene expression was able to rescue the morphological abnormalities in the cardiac lymphatic vessels of compound heterozygotes, but it did not rescue the severe cardiac lymphatic vessel hypoplasia observed in Tbx1 homozygotes. Moreover, our study revealed a differential sensitivity between the ventral and dorsal cardiac lymphatic networks to the effects of altered Tbx1 and Vegfr3 gene dosage. Overall, our study demonstrates that a fine dosage balance between Tbx1 and Vegfr3 is required to regulate the number and morphology of cardiac lymphatic vessels.

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“…Note that Tbx1 is also expressed in the conotruncus (arrow in Fig. 1A, a), as previously reported (10) (11).…”

Section: Tbx1 and Vegfr3 Expression Overlap In Cardiac Lymphaticssupporting

confidence: 87%

Tbx1interacts genetically withVegfr3to regulate cardiac lymphangiogenesis in mice

Martucciello

Cioffi

et al. 2019

Preprint

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“…The formation of the stems of the coronary arteries by the ingrowth into the aorta has been described in birds and mammals [75, 76] and is modulated by contact with the aortic endothelium and regulated by differential Tbx1 expression responsible for differences in left/right ingrowth [77]. Usually, in mammals the left and right coronary ostia can be found in the sinus of Valsalva of the left and right leaflet of the aortic semilunar valve, while the aortic intercalated leaflet and the pulmonary trunk are in most cases devoid of a coronary ostium.…”

Section: Discussionmentioning

confidence: 99%

Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart

Poelmann

Groot

Biermans

et al. 2017

EvoDevo

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BackgroundCardiac outflow tract patterning and cell contribution are studied using an evo-devo approach to reveal insight into the development of aorto-pulmonary septation.ResultsWe 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.ConclusionsThis 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.

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“…The signals that promote the coronary arteries to grow toward the aorta and perforate the aortic wall are unknown, as yet. Erroneous connections are found when development of the outflow tract is affected (Theveniau‐Ruissy et al, ). It is, however, not known whether these primary or secondary defects are due to abnormal OFT development.…”

Section: Epicardium and Its Derivativesmentioning

confidence: 99%

Development of the human heart

Buijtendijk

Barnett

Hoff

2020

American J of Med Genetics Pt C

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In 2014, an extensive review discussing the major steps of cardiac development focusing on growth, formation of primary and chamber myocardium and the development of the cardiac electrical system, was published. Molecular genetic lineage analyses have since furthered our insight in the developmental origin of the various component parts of the heart, which currently can be unambiguously identified by their unique molecular phenotype. Moreover, genetic, molecular and cell biological analyses have driven insights into the mechanisms underlying the development of the different cardiac components. Here, we build on our previous review and provide an insight into the molecular mechanistic revelations that have forwarded the field of cardiac development. Despite the enormous advances in our knowledge over the last decade, the development of congenital cardiac malformations remains poorly understood. The challenge for the next decade will be to evaluate the different developmental processes using newly developed molecular genetic techniques to further unveil the gene regulatory networks operational during normal and abnormal cardiac development.

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Coronary stem development in wild‐type and Tbx1 null mouse hearts

Cited by 28 publications

References 40 publications

Tbx1interacts genetically withVegfr3to regulate cardiac lymphangiogenesis in mice

Tbx1interacts genetically withVegfr3to regulate cardiac lymphangiogenesis in mice

Outflow tract septation and the aortic arch system in reptiles: lessons for understanding the mammalian heart

Development of the human heart

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