Abstract
SummaryFew families of signaling factors have been implicated in the control of development. Here, we identify the neuropeptides nociceptin and somatostatin, a neurotransmitter and neuroendocrine hormone, as a class of developmental signals in both chick and zebrafish. We show that signals from the anterior mesendoderm are required for the formation of anterior placode progenitors, with one of the signals being somatostatin. Somatostatin controls ectodermal expression of nociceptin, and both peptides regulate Pax6 in lens and olfactory progenitors. Consequently, loss of somatostatin and nociceptin signaling leads to severe reduction of lens formation. Our findings not only uncover these neuropeptides as developmental signals but also identify a long-sought-after mechanism that initiates Pax6 in placode progenitors and may explain the ancient evolutionary origin of neuropeptides, predating a complex nervous system.
Highlights
In the vertebrate head, multipotent progenitor cells give rise to crucial components of sense organs and sensory ganglia (Schlosser, 2010; Streit, 2007)
Identification of Somatostatin and Nociceptin as Potential Developmental Signals Consistent with its function, Pax6 is initially confined to future lens and olfactory cells
Chick posterior placode progenitors upregulate Pax6 within only 5 hr when cultured in isolation and turn into lenses (Bailey et al, 2006), providing an experimental paradigm to screen for new Pax6 regulators
Summary
Multipotent progenitor cells give rise to crucial components of sense organs and sensory ganglia (Schlosser, 2010; Streit, 2007) They reside in the ectoderm next to the anterior neural plate, where they are induced by FGFs combined with Wnt and BMP attenuation (Ahrens and Schlosser, 2005; Brugmann et al, 2004; Litsiou et al, 2005). We demonstrate that the anterior mesendoderm is required for aPP formation and regulates Pax6 It does so by secreting the neuropeptide somatostatin (SST), which in turn activates nociceptin (Noc) in the overlying ectoderm. These neuropeptides control aPP fate as an early step in lens and olfactory epithelium development
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