α‐Melanophore‐stimulating hormone in the brain, cranial placode derivatives, and retina of Xenopus laevis during development in relation to background adaptation

Abstract

The amphibian Xenopus laevis can adapt the color of its skin to the light intensity of the background. A key peptide in this adaptation process is alpha-melanophore-stimulating hormone (alpha-MSH), which is derived from proopiomelanocortin (POMC) and released by the endocrine melanotrope cells in the pituitary pars intermedia. In this study, the presence of alpha-MSH in the brain, cranial placode derivatives, and retina of developing Xenopus laevis was investigated using immunocytochemistry, to test the hypothesis that POMC peptide-producing neurons and endocrine cells have a common embryonic origin and a common function, i.e., controlling each other's activities and/or being involved in the process of physiological adaptation. The presence of alpha-MSH-positive cells in the suprachiasmatic nucleus, ventral hypothalamic nucleus, epiphysis, and endocrine melanotrope and corticotrope cells, which are all involved in regulation of adaptation processes, has been detected from stage 37/38 onward. This is consistent with the presumed common origin of these cells, the anterior neural ridge (ANR) of the neural-plate-stage embryo. The olfactory epithelium and the otic and epibranchial ganglia also contain alpha-MSH, indicating that these placodal derivatives originate from a common placodal domain continuous with the ANR. Furthermore, we demonstrate the presence of alpha-MSH in a subpopulation of retinal ganglion cells (RGCs), which is possibly also derived from the ANR. Immunoreactivity for alpha-MSH in RGCs that are located in the dorsal part of the retina is dependent on the background light intensity, suggesting that these cells are involved in the regulation of background adaptation. Taken together, the results support the hypothesis that POMC peptide-producing cells have a common embryonic origin and are involved in adaptation processes.

Mutagenesis studies in transgenic Xenopus intermediate pituitary cells reveal structural elements necessary for correct prion protein biosynthesis

“…Moreover, the patterns are in line with the expression pattern of the endogenous POMC-derived a-MSH-peptide in developing Xenopus (Kramer et al, 2003). In the tadpoles transgenic for the GFP-PrP C K81A, GFP-PrP C DGPI, GFPPrP C octa, or GFP-GPI fusion proteins, we never observed nonspecific brain fluorescence other than the fluorescence found in the intermediate pituitary.…”

Interaction and developmental activation of two neuroendocrine systems that regulate light‐mediated skin pigmentation

“…Interestingly, the eye/α‐MSH circuit does not require prior exposure to a light–dark cycle to be fully functional in the embryo. The system is fully primed by stage 42, with an increase in the immunoreactivity to α‐MSH in the pars intermedia pituitary, a 30% increase in the size of pituitary, and higher systemic levels of α‐MSH compared with light reared embryos (Bertolesi, Vazhappilly, et al., ; Kramer et al., ; Verburg‐van Kemenade et al., ).…”

“…Light perceived by the eye activates a neural circuit that negatively regulates α‐MSH secretion from melanotropes of the pars intermedia pituitary (Kramer et al., ; Roubos et al., ). α‐MSH levels increase in adult frogs adapted to a black background (Chiao, Chubb, & Hanlon, ; Fernandez & Bagnara, ; de Rijk, Jenks, & Wendelaar Bonga, ; Roubos et al., ; Verburg‐van Kemenade, Willems, Jenks, & van Overbeeke, ) and in young Xenopus embryos reared in continuous darkness (Bertolesi et al., , Bertolesi, Vazhappilly, et al., ).…”

Melanopsin photoreception in the eye regulates light‐induced skin colour changes through the production of α‐MSH in the pituitary gland

“…A possible systemic mediator of the effects of melanopsin inhibition on skin pigmentation is a-MSH: (i) a-MSH is a powerful inducer of pigmentation in amphibians (Roubos et al, 2010), and in humans (Abdel-Malek et al, 1995); (ii) blinded Xenopus increase the release of hypothalamic a-MSH, and dark induction of pigmentation is blocked completely in hypophysectomized animals (Imai and Takahashi, 1971); (iii) a-MSH levels are regulated by dark/white adaptation, and the onset of a-MSH biosynthesis in the pars intermedia pituitary correlates with when retinal circuits become light sensitive (Ayoubi et al, 1991;Bertolesi et al, 2014;Corstens et al, 2005;Kramer et al, 2003).…”