Phylogeny informs ontogeny: a proposed common theme in the arterial pole of the vertebrate heart

Abstract

SUMMARY In chick and mouse embryogenesis, a population of cells described as the secondary heart field (SHF) adds both myocardium and smooth muscle to the developing cardiac outflow tract (OFT). Following this addition, at approximately HH stage 22 in chick embryos, for example, the SHF can be identified architecturally by an overlapping seam at the arterial pole, where beating myocardium forms a junction with the smooth muscle of the arterial system. Previously, using either immunohistochemistry or nitric oxide indicators such as diaminofluorescein 2-diacetate, we have shown that a similar overlapping architecture also exists in the arterial pole of zebrafish and some shark species. However, although recent work suggests that development of the zebrafish OFT may also proceed by addition of a SHF-like population of cells, the presence of a true SHF in zebrafish and in many other developmental biological models remains an open question. We performed a comprehensive morphological study of the OFT of a wide range of vertebrates. Our data suggest that all vertebrates possess three fundamental OFT components: a proximal myocardial component, a distal smooth muscle component, and a middle component that contains overlapping myocardium and smooth muscle surrounding and supporting the outflow valves. Because the middle OFT component of avians and mammals is derived from the SHF, our observations suggest that a SHF may be an evolutionarily conserved theme in vertebrate embryogenesis.

Zebrafish cardiac development requires a conserved secondary heart field

“…The adult zebrafish outflow tract, with the most proximal smooth muscle surrounded by a sleeve of myocardium, is homologous to that observed in animals with a divided arterial pole (Grimes et al, 2006;Grimes et al, 2010). Zebrafish also display a low level of proliferation in early differentiating cardiomyocytes, which would necessitate the addition of cells to the heart tube after its formation (de Pater et al, 2009) (K. A. Nembhard and M.L.K., unpublished).…”

Zebrafish Mef2ca and Mef2cb are essential for both first and second heart field cardiomyocyte differentiation

“…Recent studies have suggested that, like the amniote heart, zebrafish heart is built from FHF and SHF progenitor cell pools. Whereas the FHF is the source of cells contributing to the primitive heart tube, the putative SHF provides cells that are added to the two poles of the heart tube, and build the structures at the inflow and outflow tract (de Pater et al, 2009; Grimes et al, 2010; Grimes et al, 2006; Hami et al, 2011; Lazic and Scott, 2011; Zhou et al, 2011). This provides a new opportunity to increase understanding of the molecular regulation of cardiomyogenesis.…”

Morphology, innervation and its phylogenetic step in the heart of the longnose gar Lepisosteus Osseus

“…Grimes et al 2010) suggest that modern histological and immunohistochemical techniques may be a useful tool to infer phylogenic relationships. Grimes et al 2010) suggest that modern histological and immunohistochemical techniques may be a useful tool to infer phylogenic relationships.…”