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Arvicanthis Niloticus) Topographic Arrangement of S-cone Photoreceptors in the Retina of the Diurnal Nile Grass Rat (Arvicanthis niloticus) Fre´de´ric Gaillard,1 Sharee Kuny,2,3 and Yves Sauve´ 2,3 1,2 PURPOSE. The retina of Arvicanthis niloticus, a diurnal murine become available, ground squirrels, guinea pigs, or tree rodent closely related to Rattus (rats) and Mus (mice), contains shrews remain popular models for investigating structure, Ϸ30% to 35% cones and has several cone-driven functional function, and pathologic features of cone-rich mammalian ret- characteristics found in humans. In this study the organization inas. Members of the Arvicanthis genus (a genus closely re- of these cone photoreceptors was examined, with emphasis lated to Rattus and Mus, but with a diurnal lifestyle) may be a on those expressing the S-opsin photopigment (S-cones). useful alternative.3 The first immunohistochemical investiga- METHODS. Cones were labeled with antibodies against M- and tions dedicated to the visual system of two geographically S-opsins. Their topographic arrangement was examined on distant Arvicanthis species, the Sudanian (A. ansorgei) and the images of retinal flatmounts using density measures, nearest- Nile (A. niloticus) grass rats, pointed out the efficiency of neighbor distance, and Voronoi domain analysis. Partial se- preexisting antibodies in these species and established that their retinas contain Ϸ30% to 35% cones.3–5 Additional exper- quencing of the S-opsin DNA was also performed to determine 5,6 whether this visual pigment was blue/violet or UV sensitive. iments in A. niloticus showed that its retina displays post- receptoral neural features commonly observed in diurnal RESULTS. Cone photoreceptors (estimated total population Ϸ mammals and that it has several cone-driven functional char- 1.450 million) came in two distinct types that express either acteristics (as assessed with the electroretinogram) found in M/L- or S-opsin. Both types were present across the retinal Ϸ human retinas (large photopic a-wave amplitudes, photopic surface. S-cones ( 7–8% of the total cone population) hill effect, and critical flicker fusion beyond 60 Hz). In the achieved a higher density in a discrete temporodorsal sector of present study, we determined the distribution of the cone the retina. The S-cone mosaic was irregular. Finally, S-cones population (more specifically those expressing the S-opsin were likely to be UV sensitive, according to genetic analysis. photopigment) in A. niloticus with the rationale of acquiring CONCLUSIONS. The topographic arrangement of cone photore- normative data against which to compare the effects of exper- ceptors in the retina of the diurnal Nile grass rat A. niloticus imental manipulations and/or aging. represents a highly pertinent model to improve understanding of the pathologic course of and related therapy for retinal disease involving cones. (Invest Ophthalmol Vis Sci. 2009;50: MATERIAL AND METHODS 5426–5434) DOI:10.1167/iovs.09-3896 Animals one photoreceptors in human retinas achieve their highest This study was performed on young adult (2–6 months of age) Nile Cdensities in the fovea. They mediate high-spatial-resolution grass rats (A. niloticus) of both sexes derived from a breeding colony daylight vision and color discrimination. Their progressive loss established at the University of Alberta. The animals were raised on a in a variety of retinal degenerations induces a central visual 12:12 light–dark cycle (lights on at 5 AM; ambient temperature 21 Ϯ field scotoma, which almost inevitably leads to legal blindness 1°C; relative humidity Ϸ50%) and supplied ad libitum with water and (visual acuity of 20/200 or less). Ideally, such diseases would standard rodent diet (formula 5001 LabDiet; Nutrition International, be investigated in animal species with dense cone populations. Richmond, IN). Experiments were performed in accordance with the Although genetically engineered rodless mice have recently ARVO Statement for the Use of Animals in Ophthalmic and Visual Research and with the guidelines laid down by the NIH (National Institutes of Health) in the United States regarding the care and use of 1 animals for experimental procedures. The University of Alberta Animal From the Institut de Physiologie et Biologie Cellulaires, Universite´ Care and Use Committee approved the present work. de Poitiers, UMR 6187, CNRS (Centre National de la Recherche Scien- tifique), Poitiers, France; and the Departments of 2Physiology and 3Ophthalmology, University of Alberta, Edmonton, Alberta, Canada. Primary Antibodies Supported by Canadian Institutes of Health Research (CIHR) Grant Cone photoreceptors were screened using anti-M/L- and anti-S-opsin 151145; an Alberta Heritage Foundation for Medical Research (AH- FMR) equipment grant; the Canadian National Institute for the Blind; polyclonal antibodies (AB5405 and AB5407, working dilution 1:500; the Olive Young Foundation; and The Lena McLaughlin Foundation both from Chemicon, Temecula, CA;) raised in rabbit against the last (Mona & Rod McLennan). FG was supported by the International 42 and 38 amino acids respectively, at the C-terminus of recombinant Society for Clinical Electrophysiology of Vision (ISCEV; short lab visit human red/green- and blue opsins.7 These antibodies have been re- grant 2008). YS is an AHFMR Senior Scholar. ported to label the outer segments (OS) and cell membranes of specific Submitted for publication April 22, 2009; revised May 25, 2009; types of cones in human, mouse, and ground squirrel retinas.8,9 Their accepted August 5, 2009. specificity was confirmed in Western blot analyses from Nile grass rat Disclosure: F. Gaillard, None; S. Kuny, None; Y. Sauve´, None retinal tissue (described later). For double-labeling experiments, the The publication costs of this article were defrayed in part by page S-opsin AB5407 rabbit polyclonal antibody was replaced with an affin- charge payment. This article must therefore be marked “advertise- ment” in accordance with 18 U.S.C. §1734 solely to indicate this fact. ity-purified goat polyclonal antibody raised against a 20-amino-acid Corresponding author: Yves Sauve´, Assistant Professor of Ophthal- synthetic peptide mapping within amino acids 1 to 50 of human mology and Physiology, Department of Physiology, 7-55 Medical Sci- blue-sensitive opsin (EFYLFKNISSVGPWDGPQYH; sc-14363; Santa ences Building, University of Alberta, Edmonton AB, Canada, T6G 2H7; Cruz Biotechnology Inc., Santa Cruz, CA; working dilution 1:200). This [email protected]. antibody has been used to identify S-opsin expressing cones in a range Investigative Ophthalmology & Visual Science, November 2009, Vol. 50, No. 11 5426 Copyright © Association for Research in Vision and Ophthalmology Downloaded from iovs.arvojournals.org on 09/24/2021 IOVS, November 2009, Vol. 50, No. 11 Cone Photoreceptors in Arvicanthis 5427 FIGURE 1. Cone distribution in cross sections and flatmounted retinas. (A) Western blots of A. niloticus retinal tissue. AB5405 and AB5407 antibod- ies detect major products at Ϸ39 and Ϸ37 kDa (lanes M and S, respec- tively) as expected for M/L- and S- opsins. A long exposure time (Ͼ4 minutes) may explain the faint bands (at Ϸ80 and Ϸ130 kDa) observed with the M/L-opsin antibody. (B) Near-central retinal cross section treated with M/L (AB5405; red)- and S (sc-14363; green)-opsin antibodies. These antibodies stain distinct OS. Pseudo co-localization of both opsins in the leftmost cone is due to acci- dental superimposition of two OS (the thickness of the sections is 20 ␮m). (C) M/L-cone entirely labeled with antibody AB5405. (D) S-cone as revealed with antibody sc-14363. (E) Cross section treated with anti-S-op- sin antibody AB5407. (F) Same cross section treated with anti-S-opsin anti- body sc-14363. (G) Merged pictures show that these two antibodies de- tected the same S-cone OS. (H) Ex- ample of M/L- (red) and S- (green) opsin expressing cones as viewed in a flatmounted retina (nasodorsal pe- riphery). (I) Enlargement of the inset in (H) illustrates that expression of M/L- and S-opsins was mutually ex- clusive in the cones of A. niloticus. (J, K) Absence of opsin coexpression in an additional double-labeled flat- mount retina. Pictures taken in the midperiphery of the ventral quadrant where dual-pigment cones are most evident in the mouse. OS, outer seg- ment; IS, inner segment; ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; RPE, retinal pigment epithelium. of species.10–14 Competition controls where sc-14363 was preincu- major products at Ϸ39 and Ϸ37 kDa, respectively corresponding to bated with the antigenic peptide11,13 yielded no labeling. M/L- and S-opsin (Fig. 1A). Western Blot Analysis Immunohistochemistry Freshly dissected retinas (n ϭ 3; 2 months of age) were homogenized Cryosections were collected from 4% paraformaldehyde-fixed retinas in SDS buffer (4% [wt/vol] sodium dodecyl sulfate, 0.13 M Tris, 2% (n ϭ 2; 4 months of age) cut serially at 20 ␮m, parallel to the [vol/vol] 2-mercaptoethanol, 20% [vol/vol] glycerol; pH 6.8) with a nasotemporal axis, and mounted on glass slides (Superfrost/Plus; protease inhibitor cocktail (Complete; Roche Applied Science, Mann- Fisher Scientific, Pittsburgh, PA). After they were extensively washed ␮ heim, Germany). Samples (25 g protein) were resolved by SDS-PAGE in PBS (137 mM NaCl, 2.7 mM KCl, 4.3 mM Na2HPO4-7H2O, 1.4 mM on 8% to 10% acrylamide gels. Proteins were transferred to polyvinyli- KH2PO4; pH 7.3), the sections were blocked for 2 hours in a medium dene fluoride (PVDF) membranes, blocked for 1 hour with 5% nonfat containing PBS ϩ0.1% Triton X-100ϩ5% nonfat milk, and reacted milk diluted in TBS-T (20 mM Tris, 137 mM NaCl, and 0.1% Tween-20; overnight with anti-M/L- and anti-S-opsin antibodies diluted appropri- pH 7.6), incubated overnight with anti-M/L-opsin (AB5405) or anti-S- ately in a 1:10 solution of the previous blocking medium.
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