Heart inflow tract of the African lungfish <i>Protopterus dolloi</i>

Icardo, José M.; Ojeda, José L.; Colvée, Elvira; Tota, Bruno; Wong, Wai P.; Ip, Yuen K.

doi:10.1002/jmor.10286

Cited by 23 publications

(31 citation statements)

References 18 publications

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“…9). The structures populated by Hh-induced cardiac progenitors in mice, the atrial septum in the inflow and the pulmonary trunk in the outflow tract, are orthologous to the earliest ancestral cardiac septal structures observed in basal tetrapods (Icardo et al, 2005). We speculate that cardiac septal structures and the respiratory apparatus coevolved and that Hh signaling from primordial respiratory structures to splanchnic mesoderm of the SHF might underlie early events in the evolution of cardiac septation.…”

Section: Research Articlementioning

confidence: 83%

sonic hedgehog is required in pulmonary endoderm for atrial septation

et al. 2009

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The genesis of the septal structures of the mammalian heart is central to understanding the ontogeny of congenital heart disease and the evolution of cardiac organogenesis. We found that Hedgehog (Hh) signaling marked a subset of cardiac progenitors specific to the atrial septum and the pulmonary trunk in the mouse. Using genetic inducible fate mapping with Gli1CreERT2, we marked Hh-receiving progenitors in anterior and posterior second heart field splanchnic mesoderm between E8 and E10. In the inflow tract, Hh-receiving progenitors migrated from the posterior second heart field through the dorsal mesocardium to form the atrial septum,including both the primary atrial septum and dorsal mesenchymal protrusion(DMP). In the outflow tract, Hh-receiving progenitors migrated from the anterior second heart field to populate the pulmonary trunk. Abrogation of Hh signaling during atrial septal progenitor specification resulted in atrial and atrioventricular septal defects and hypoplasia of the developing DMP. Hedgehog signaling appeared necessary and sufficient for atrial septal progenitor fate:Hh-receiving cells rendered unresponsive to the Hh ligand migrated into the atrium in normal numbers but populated the atrial free wall rather than the atrial septum. Conversely, constitutive activation of Hh signaling caused inappropriate enlargement of the atrial septum. The close proximity of posterior second heart field cardiac progenitors to pulmonary endoderm suggested a pulmonary source for the Hh ligand. We found that Shh is required in the pulmonary endoderm for atrial septation. Therefore, Hh signaling from distinct pulmonary and pharyngeal endoderm is required for inflow and outflow septation, respectively. These data suggest a model in which respiratory endoderm patterns the morphogenesis of cardiac structural components required for efficient cardiopulmonary circulation.

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Section: Research Articlementioning

confidence: 83%

sonic hedgehog is required in pulmonary endoderm for atrial septation

et al. 2009

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“…(1) mesenchymal cap, (2) atrioventricular cushions, (3, 4) dorsal mesocardium, vestibular spine, (5) primary myocardial septum, (6) primary foramen, (7) secondary perforations, (8) closure of the primary foramen, (9) coalescence of the secondary perforations to form the secondary foramen, (10, 11) superior fold of the atrial roof, (12) muscularised mesenchyme of the vestibular spine, (13) muscularised mesenchyme of the mesenchymal cap, (14) oval fossa (based on de Bakker et al ,23 Rowlatt,24 Robertson,25 Icardo et al ,26 Jensen et al ,27 Icardo et al 28…”

Section: Discussionmentioning

confidence: 99%

Development of the atrial septum in relation to postnatal anatomy and interatrial communications

Jensen

Spicer

Sheppard³

et al. 2016

Heart

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The atrial septum is probe patent in some 30% of the population, and is prone to have overt defects. Atrial septation is the coming together of several myocardial structures and mesenchymal tissues of intracardiac and extracardiac origin that must change identity to myocardium. We propose that the propensity for malformation of the atrial septum reflects this complicated morphogenesis. The morphogenesis of the atrial septum initiates from a ridge of mesenchyme, only a few hundred micrometres long, in the roof of the undivided atrial cavity. By growth of the myocardial primary septum, the mesenchymal ridge will be approximated to, and ultimately fuse, with the mesenchyme of the atrioventricular cushions. This fusion also takes in the so-called vestibular spine, and serves to close the primary atrial foramen. Interatrial communication is maintained by the development of perforations in the myocardial septum that will coalesce to produce the secondary foramen. Late in gestation, an infolding of the right atrial roof, previously identified as the secondary septum, will come to form the roof of the secondary foramen. Muscularisation of the mesenchymal ridge and vestibular spine serves to reinforce the attachment of the primary muscular septum to the atrioventricular insulating plane, with the muscularised components, and the cranial infolding, then producing the rims of the oval fossa as seen in the postnatal heart. We show that other lesions that produce the potential for interatrial shunting are outside the confines of the atrial septum, and hence are best considered as interatrial communications, rather than 'atrial septal defects'.

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“…It is supplied by the intracavitary venous blood, which perfuses the inter-trabecular (lacunae) spaces. In elasmobranchs and many teleosts, the spongiosa is covered by a subepicardial outer layer of densely arranged myocardial bundles, the 'compacta', thus forming a 'mixed type' of ventricle (Tota, 1983;Tota et al, 1983;Icardo et al, 2005). In a variety of species, the entirely trabeculated ventricle, in addition to the lacunary supply, can receive a vascular supply; the compacta is always vascularized Tota, 1989;Farmer, 1997).…”

Section: The Basic Fish and Amphibian Heartsmentioning

confidence: 99%

Catecholamines, cardiac natriuretic peptides and chromogranin A: evolution and physiopathology of a ‘whip-brake’ system of the endocrine heart

Tota

Cerra

Gattuso

2010

Journal of Experimental Biology

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Summary In the past 50 years, extensive evidence has shown the ability of vertebrate cardiac non-neuronal cells to synthesize and release catecholamines (CA). This formed the mindset behind the search for the intrinsic endocrine heart properties, culminating in 1981 with the discovery of the natriuretic peptides (NP). CA and NP, co-existing in the endocrine secretion granules and acting as major cardiovascular regulators in health and disease, have become of great biomedical relevance for their potent diagnostic and therapeutic use. The concept of the endocrine heart was later enriched by the identification of a growing number of cardiac hormonal substances involved in organ modulation under normal and stress-induced conditions. Recently, chromogranin A (CgA), a major constituent of the secretory granules, and its derived cardio-suppressive and antiadrenergic peptides, vasostatin-1 and catestatin, were shown as new players in this framework, functioning as cardiac counter-regulators in ‘zero steady-state error’ homeostasis, particularly under intense excitatory stimuli, e.g. CA-induced myocardial stress. Here, we present evidence for the hypothesis that is gaining support, particularly among human cardiologists. The actions of CA, NP and CgA, we argue, may be viewed as a hallmark of the cardiac capacity to organize ‘whip-brake’ connection-integration processes in spatio-temporal networks. The involvement of the nitric oxide synthase (NOS)/nitric oxide (NO) system in this configuration is discussed. The use of fish and amphibian paradigms will illustrate the ways that incipient endocrine-humoral agents have evolved as components of cardiac molecular loops and important intermediates during evolutionary transitions, or in a distinct phylogenetic lineage, or under stress challenges. This may help to grasp the old evolutionary roots of these intracardiac endocrine/paracrine networks and how they have evolved from relatively less complicated designs. The latter can also be used as an intellectual tool to disentangle the experimental complexity of the mammalian and human endocrine hearts, suggesting future investigational avenues.

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Heart inflow tract of the African lungfish Protopterus dolloi

Cited by 23 publications

References 18 publications

sonic hedgehog is required in pulmonary endoderm for atrial septation

sonic hedgehog is required in pulmonary endoderm for atrial septation

Development of the atrial septum in relation to postnatal anatomy and interatrial communications

Catecholamines, cardiac natriuretic peptides and chromogranin A: evolution and physiopathology of a ‘whip-brake’ system of the endocrine heart

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