Two light‐activated neuroendocrine circuits arising in the eye trigger physiological and morphological pigmentation

Abstract

Two biological processes regulate light-induced skin colour change. A fast 'physiological pigmentation change' (i.e. circadian variations or camouflage) involves alterations in the distribution of pigment containing granules in the cytoplasm of chromatophores, while a slower 'morphological pigmentation change' (i.e. seasonal variations) entails changes in the number of pigment cells or pigment type. Although linked processes, the neuroendocrine coordination triggering each response remains largely obscure. By evaluating both events in Xenopus laevis embryos, we show that morphological pigmentation initiates by inhibiting the activity of the classical retinal ganglion cells. Morphological pigmentation is always accompanied by physiological pigmentation, and a melatonin receptor antagonist prevents both responses. Physiological pigmentation also initiates in the eye, but with repression of melanopsin-expressing retinal ganglion cell activity that leads to secretion of alpha-melanocyte-stimulating hormone (α-MSH). Our findings suggest a model in which eye photoperception links physiological and morphological pigmentation by altering α-MSH and melatonin production, respectively.

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

“…To understand whether in older animals the eye plays any role in the skin pigmentation response to ambient darkness, we measured skin pigmentation for larvae in which the eye or the pineal complex was surgically removed. As we showed previously (Bertolesi, Hehr, et al., ), the pineal complex did not appear to be involved in the darkening of the skin of stage 42 dark‐reared embryos, while the eye is critical in the process (Figure a,b). Embryos missing their pineal complex were still darker when reared in the dark versus the light, whereas eye removal blocked the ability of light to lighten the embryo, such that the pigment index of stage 42 embryos missing their eyes was indistinguishable from that of embryos reared under dark conditions (Figure a,b; control light versus control dark and no eye‐light).…”

“…Next, we asked whether stage 47/8 melanophores showed similar responses to exogenous melatonin and α‐MSH as we reported previously for stage 42 embryos (Bertolesi, Hehr, Munn, & McFarlane, ; Bertolesi, Vazhappilly, et al., ). Stage 39 embryos and 47 larvae were raised in light with a white background or in the dark for 24 hr, before adding melatonin (10 n m ) or α‐MSH (1 μ m ) (Figure a,b).…”

“…Embryos were maintained in a Marc's modified Ringer's (MMR) solution (100 m m NaCl, 2 m m KC1, 2 m m CaCl 2 , 1 m m MgCl 2 , 5 m m HEPES pH 7.4) and staged according to Nieuwkoop and Faber using the Xenbase websitehttp://www.xenbase.org. Growing conditions of the embryos, including light, temperature and chamber characteristics, as well as the assessment of physiological skin pigmentation indices from binary images, were described previously (Bertolesi et al., , Bertolesi, Vazhappilly, et al., , Bertolesi, Hehr, et al., ). Briefly, the embryos were reared from the specified stages at 16 or 23°C in a chamber under continuous light (2500 lux; approximately 3.6 × 10 −4 W/cm 2 ) on a white or a black background, or in dark conditions.…”

Transcriptomics reveals the molecular processes of light-induced rapid darkening of the non-obligate cave dweller Oreolalax rhodostigmatus (Megophryidae, Anura) and their genetic basis of pigmentation strategy

“…Both PCC and MCC may be involved in melanin-based pigmentation. Generally speaking, PCC is more active and rapid than MCC in response to environmental brightness in fish and amphibians [ 1 ], and in most studied cases, activation of MCC is always accompanied by PCC, as factors inducing MCC can also activate PCC [ 53 ]. However, in O. rhodostigmatus tadpoles, genes involved in MCC, or more exactly melanogenesis and melanocyte proliferating, increased with skin darkening, while those involved in PCC did not (Fig.…”

Seeing the light to change colour: An evolutionary perspective on the role of melanopsin in neuroendocrine circuits regulating light‐mediated skin pigmentation

“…In mammals, pupillary constriction (Chen et al, 2011;Gooley, Lu, Fischer, & Saper, 2003) and sleep induction Lupi et al, 2008) also depend on light activation of ipRGCs. It was only melanopsin expression by skin melanophores of LEI organisms that suggested a function in regulating pigmentation (Isoldi et al, 2005;Rollag et al, 2000), until we showed recently that retinal melanopsin in the eye indirectly regulates pigmentation through activation of a neuroendocrine circuit (Bertolesi, Hehr, & Mcfarlane, 2015;Bertolesi, Hehr, Munn, & McFarlane, 2016;Bertolesi, Song, Atkinson-Leadbeater, Yang, & McFarlane, 2017;Bertolesi, Vazhappilly, Hehr, & Mcfarlane, 2016). Indeed, ipRGCs regulate the secretion of melatonin (Lucas, Freedman, Muñoz, Garcia-Fernández, & Foster, 1999;Lupi et al, 2008;Sekaran et al, 2005) and α-MSH (Bertolesi et al, 2015), which modulate skin pigmentation of LEI and LPI organisms (Jenks, van Overbeeke, & McStay, 1977;Slominski, Tobin, Zmijewski, Wortsman, & Paus, 2008).…”