Vertebrate Ancient Opsin Photopigment Spectra and the Avian

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Vertebrate Ancient Opsin Photopigment Spectra and the Avian View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central Biol. Lett. (2012) 8, 291–294 and vertebrate ancient (VA)opsin [6] all being proposed doi:10.1098/rsbl.2011.0864 as potential candidates. Traditionally, a number of cri- Published online 26 October 2011 teria must be satisfied before assigning a particular Neurobiology function to a photopigment. Specifically, the molecular candidate should: (i) be expressed in photoreceptors/ photosensitive areas; (ii) form a functional photo- Vertebrate ancient opsin pigment; and (iii) possess an absorption spectrum with a spectral maximum (lmax) that matches the action photopigment spectra and spectrum for the biological response. An additional sup- portive, association (iv) is whether the candidate the avian photoperiodic photopigment is spectrally ‘tuned’ to the prevailing response light conditions, as often seen in the visual pigments driving colour vision or the rod photopigments of Wayne I. L. Davies1, Michael Turton1, deep-sea fishes. Based upon criteria (i) and (ii), VA Stuart N. Peirson1, Brian K. Follett2, opsin [6] and OPN5 [5] have emerged as the strongest Stephanie Halford1, Jose M. Garcia-Fernandez3, candidates. However, their match to criteria (iii) and Peter J. Sharp4, Mark W. Hankins1,* (iv) is problematic as information is either confounding and Russell G. Foster1,* or lacking. In the case of chicken OPN5 (cOPN5), absorbance spectroscopy has demonstrated a photopig- 1Nuffield Laboratory of Ophthalmology, Oxford University, Oxford OX3 9DU, UK ment with a lmax at 360 nm [7]. Such a spectral 2Department of Zoology, Oxford University, Oxford OX1 3PS, UK maximum would not support cOPN5 as the photoperi- 3Departamento de Morfologı´a y Biologı´a Celular Facultad de Medicina, odic photopigment, based upon the finding that the Oviedo Universidad, Oviedo 33006, Spain action spectrum for the avian photoperiodic response 4The Roslin Institute, Edinburgh University, Edinburgh EH25 9PS, UK *Authors for correspondence ([email protected]; peaks at 492 nm [2] and the observation that little [email protected]). ultraviolet (UV) light can penetrate tissue [8]. In mammals, photoreception is restricted to Chicken VA (cVA) opsin encodes two isoforms, cones, rods and a subset of retinal ganglion cVALong (cVAL) and cVAShort (cVAS), that both cells. By contrast, non-mammalian vertebrates form functional photopigments with cVAS protein possess many extraocular photoreceptors but in being detected within the hypothalamus [6]. Until many cases the role of these photoreceptors and now, the absorption spectra for these photopigments their underlying photopigments is unknown. were not known, so any potential match between In birds, deep brain photoreceptors have been action and absorption spectra could not be evaluated. shown to sense photic changes in daylength This paper addresses this issue by reporting the (photoperiod) and mediate seasonal reproduc- absorption spectra for both chicken VA isoforms and tion. Nonetheless, the specific identity of the assessing whether their absorbance characteristics are opsin photopigment ‘sensor’ involved has remained elusive. Previously, we showed that appropriately tuned to the spectral composition of vertebrate ancient (VA) opsin is expressed in light penetrating the avian hypothalamus. avian hypothalamic neurons and forms a photo- We find that cVAS and cVAL exhibit a lmax at sensitive molecule. However, a direct functional approximately 490 nm, differing by only 2 nm from link between VA opsin and the regulation of the peak of the action spectrum for the avian photo- seasonal biology was absent. Here, we report periodic response at 492 nm. Furthermore, because the in vivo and in vitro absorption spectra of the absorbance characteristics of haemoglobin, ∼ (lmax 5 490 nm) for chicken VAphotopigments. there is a small ‘spectral window’ in hypothalamic Furthermore, the spectral sensitivity of these light penetration that peaks around 489 nm. Thus, photopigments match the peak absorbance of the spectral maxima of cVA photopigments are ideally the avian photoperiodic response (l 5 max suited to maximize photon capture within the bird 492 nm) and permits maximum photon capture within the restricted light environment of the hypothalamus. These new findings allow us to satisfy hypothalamus. Such a correspondence argues criteria (iii) and (iv) of assigning a candidate photo- strongly that VA opsin plays a key role in pigment to a physiological function, namely, that VA regulating seasonal reproduction in birds. opsin plays a central role in regulating the avian photoperiodic response. Keywords: avian; deep brain photoreceptor; hypothalamus; vertebrate ancient opsin; photoperiodic response 2. MATERIAL AND METHODS Hypothalamic lysates from dark-adapted chickens were homogenized in phosphate buffered saline/n-dodecyl-b-D-maltoside/phenylmethyl- sulphonylfluoride buffer (pH 7.4) [9] under dim red light. Native 1. INTRODUCTION cVAS photopigments, containing endogenous 11-cis retinal, were Birds possess photoreceptors located within the medio- extracted in the dark by affinity immunochromatography [9] by pas- basal hypothalamus (MBH) that regulate photoperiodic sing the hypothalamic lysates through a cyanogen bromide-sepharose responses to daylength [1]. An action spectrum for this binding column coupled to an anti-cVAantibody [6]. For recombinant expression experiments, cVAL was transfected into HEK293T cells response showed the involvement of an opsin/vitamin and incubated at 308Cor378C. Post-harvesting, membrane fractions A photopigment with a spectral maximum at 492 nm, were incubated with excess 11-cis retinal and cVAL photopigments suggesting that daylength measurements are mediated purified by affinity immunochromatography [9]. All absorbance spec- by such a molecule [2]. However, the specific molecular tra (dark and bleached) were recorded in triplicate using a Shimadzu UV-visible spectrophotometer, with difference spectra being calcu- identity of this opsin has remained ambiguous, with rod- lated prior to template fitting to minimize the spectral distortion of like opsin [3], melanopsin [4], neuropsin (OPN5) [5] underlying absorbance and scatter of the protein [10]. The spectral Received 5 September 2011 Accepted 4 October 2011 291 This journal is q 2011 The Royal Society 292 W. I. L. Davies et al. VA-based photoreception in birds (a) chicken VAS (b)(chicken VAL c) chicken VAL (lysate) (37°C) (30°C) l =491 nm no pigment l =490 nm max 1 max 1 1 0 0 normalized absorbance difference 0 –1 –1 350 400 450 500 550 600 350 400 450 500 550 600 350 400 450 500 550 600 wavelength (nm) wavelength (nm) wavelength (nm) (d)(1014 e) l =489 nm 1 max(window) 1 12 normalized absorbance 10 normalized absorbance –1 1013 –1 nm nm –1 –1 s s –2 –2 m m HbO2 photons 12 10 photons Hb 0 l max(action) = 492 nm 1011 1011 0 400 450 500 550 600 650 700 400 450 500 550 wavelength (nm) wavelength (nm) Figure 1. (a) Absorbance difference spectra (grey line) for cVAS opsin photopigments extracted from hypothalamic lysates and (b) HEK293T cells transfected with cVAL and incubated at 378Cor(c)308C. lmax values are shown, as determined by fitting to a modified Govardovskii template [10,11] (black circles). (d) Spectral composition of sunlight reaching the basal hypothala- mus (modified from [12]; black line) compared with the absorbance of oxygenated (HbO2; light grey line) and deoxygenated (Hb; dark grey line) haemoglobin (modified from [13]). Dotted box refers to the spectrum highlighted in (e), analysed within a physiological range for vitamin A1-based photopigments (lmax ¼ 360–560 nm). (e) Spectrum of light penetrance at the avian hypothalamus (black line; modified from [12]), showing a ‘spectral window’ with a lmax at 489 nm when fitted to a vitamin A1-based template (light grey circles), compared with the action spectrum for the avian photoperiodic response (dark grey line) with a lmax at 492 (modified from [2]). 2 peak absorbance (lmax) and coefficient of determination (r value) [6]. Therefore, we determined the spectral sensitivity of were determined by fitting these data around the peak and long- this photopigment by extracting in vivo protein from wavelength limb of a modified Govardovskii template [11]witha subtracted retinal oxime spectrum [10] using an EXCEL spreadsheet dark-adapted chicken hypothalamic lysates to ensure with a Solver function by the method of least squares [9]. that the native protein remained conjugated to its endogenous 11-cis retinal chromophore. As shown in figure 1a, UV-visible spectrophotometry yielded a 3. RESULTS cVAS photopigment spectrum with a lmax at 491 nm Chicken VA exists as two isoforms (cVAL and cVAS), (r2 ¼ 0.5). The spectral characteristics of cVAL were with Western blot analysis showing that cVAS is the determined by in vitro recombinant expression in only expressed VAisoform detected in the hypothalamus HEK293T cells (at 378C), followed by reconstitution Biol. Lett. (2012) VA-based photoreception in birds W. I. L. Davies et al. 293 with 11-cis retinal and UV-visible spectrophotometry. (figure 1d). The supportive criterion (iv), namely that Despite repeated attempts, characteristic photopig- the absorbance characteristics of the VA opsin photopig- ment-like difference spectra were not obtained (figure ment should be appropriately matched to the spectral 1b). These experiments were then repeated at 308C. qualities of the available light within the hypothalamus Our rationale was that the lower temperature
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