Abstract
During animal ontogenesis, body axis patterning is finely regulated by complex interactions among several signaling pathways. Nitric oxide (NO) and retinoic acid (RA) are potent morphogens that play a pivotal role in vertebrate development. Their involvement in axial patterning of the head and pharynx shows conserved features in the chordate phylum. Indeed, in the cephalochordate amphioxus, NO and RA are crucial for the correct development of pharyngeal structures. Here, we demonstrate the functional cooperation between NO and RA that occurs during amphioxus embryogenesis. During neurulation, NO modulates RA production through the transcriptional regulation of Aldh1a.2 that irreversibly converts retinaldehyde into RA. On the other hand, RA directly or indirectly regulates the transcription of Nos genes. This reciprocal regulation of NO and RA pathways is essential for the normal pharyngeal development in amphioxus and it could be conserved in vertebrates.
Highlights
The ontogenesis of the vertebrate head is a complex developmental process in which both neural crest and non-neural crest cells participate
To better characterize the key role of nitric oxide (NO) during embryonic development, we narrowed down the time window of pharmacological treatment by defining the exact timing during which an inhibition of endogenous NO production affects the development of the pharynx
During the selected time window, the endogenous NO mainly derives from the activity of NosC, whose gene expression is observed from the N2 stage until the larval stage (L1, 72 hpf at 18 ̊C) (Figure 1—figure supplement 1; Annona et al, 2017)
Summary
The ontogenesis of the vertebrate head is a complex developmental process in which both neural crest and non-neural crest cells participate. The craniofacial development and the correct anteroposterior patterning of head structures are driven by complex interactions among several signaling pathways and epigenetic mechanisms (Haworth et al, 2007; Jacox et al, 2014; Kong et al, 2014; Francis-West and Crespo-Enriquez, 2016). In this context nitric oxide (NO) is a potent morphogen playing crucial roles in head structures development. The antero-posterior patterning and development of amphioxus pharyngeal slits are driven by a conserved set of transcription factor genes, among which Hox, Pax2/5/8, Pitx, and Tbx1/10, that are involved in vertebrate pharyngeal arches formation (Schubert et al, 2005; Bertrand et al, 2015; Wang et al, 2019)
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