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Transcriptome Profiling of Developing Photoreceptor Subtypes Reveals RESEARCH ARTICLE Transcriptome Profiling of Developing Photoreceptor Subtypes Reveals Candidate Genes Involved in Avian Photoreceptor Diversification Jennifer M. Enright, Karen A. Lawrence, Tarik Hadzic, and Joseph C. Corbo* Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, Missouri 63110-1024 ABSTRACT dopsin, red opsin, green opsin, and violet opsin report- Avian photoreceptors are a diverse class of neurons, ers, we have identified hundreds of differentially comprised of four single cones, the two members of expressed genes that may underlie the distinctive fea- the double cone, and rods. The signaling events and tures of these photoreceptor subtypes. These genes transcriptional regulators driving the differentiation of are involved in a variety of processes, including photo- these diverse photoreceptors are largely unknown. In transduction, transcriptional regulation, cell adhesion, addition, many distinctive features of photoreceptor maintenance of intra- and extracellular structure, and subtypes, including spectral tuning, oil droplet size and metabolism. Of particular note are a variety of differen- pigmentation, synaptic targets, and spatial patterning, tially expressed transcription factors, which may drive have been well characterized, but the molecular mecha- and maintain photoreceptor diversity, and cell adhesion nisms underlying these attributes have not been molecules, which may mediate spatial patterning of explored. To identify genes specifically expressed in dis- photoreceptors and act to establish retinal circuitry. tinct chicken (Gallus gallus) photoreceptor subtypes, we These analyses provide a framework for future studies developed fluorescent reporters that label photorecep- that will dissect the role of these various factors in the tor subpopulations, isolated these subpopulations by differentiation of avian photoreceptor subtypes. using fluorescence-activated cell sorting, and subjected J. Comp. Neurol. 523:649–668, 2015. them to next-generation sequencing. By comparing the expression profiles of photoreceptors labeled with rho- VC 2014 Wiley Periodicals, Inc. INDEXING TERMS: chicken; photoreceptor; rod; cone; RNA-Seq; transcriptome; TopHat (RRID:OMICS_01257); Cuf- flinks (RRID:OMICS_01304); Cuffdiff (RRID: OMICS_01969); edgeR (RRID:OMICS_01308); HTSeq (RRID:O- MICS_01053); SAMtools (RRID:nlx_154607); Bowtie (RRID:OMICS_00653) Diurnal organisms typically have a much higher pro- portion of cones relative to rods and a greater diversity of cone subtypes than nocturnal organisms (Walls, Additional Supporting Information may be found in the online ver- 1942). The primary feature that distinguishes cone pho- sion of this article. Grant sponsor: Human Frontier Science Program; Grant number: toreceptor subtypes is their spectral tuning, which RGP0017/2011 (to J.C.C.); Grant sponsor: the National Institute of arises from the expression of different opsin genes Neurological Disorders and Stroke; Grant number: F32NS083170 (to J.M.E.); Grant sponsor: the National Eye Institute; Grant numbers: (Bruhn and Cepko, 1996; Okano et al., 1989; Yen and R01EY018826 (to J.C.C.) and 5-T32EY013360-13 (to J.M.E.); Grant Fager, 1984). However, cone subtypes also have a vari- sponsor: National Cancer Institute Cancer Center Support; Grant num- ber: P30 CA91842 to the Siteman Cancer Center (to G.T.A.C.); Grant ety of additional specialized adaptations that allow for sponsor: Institute of Clinical and Translational Sciences/ Clinical and improved color discrimination and functional vision in Translational Science (ICTS/CTSA), National Center for Research Resources, National Institutes of Health (NIH), NIH Roadmap for Medi- bright light (Walls, 1942). Although these adaptations cal Research; Grant number: UL1 TR000448 (to G.T.A.C.). have been thoroughly characterized by electron micros- *CORRESPONDENCE TO: Joseph C. Corbo, Dept. of Pathology and Immunology, Washington University School of Medicine, 660 S. Euclid copy, electrophysiology, biochemical assays, and physi- Ave., Campus Box 8118, St. Louis, MO 63110. cal models (Bowmaker and Knowles, 1977; Goldsmith E-mail: [email protected] et al., 1984; Hart and Vorobyev, 2005; Kram et al., Received May 9, 2014; Revised October 21, 2014; 2010; Morris, 1970; Morris and Shorey, 1967), tran- Accepted October 22, 2014. DOI 10.1002/cne.23702 Published online October 28, 2014 in Wiley Online Library VC 2014 Wiley Periodicals, Inc. (wileyonlinelibrary.com) The Journal of Comparative Neurology | Research in Systems Neuroscience 523:649–668 (2015) 649 J.M. Enright et al Figure 1. Rhodopsin and cone opsin promoters drive expression in non-overlapping subsets of avian photoreceptors. A: The complement of avian photoreceptors includes the violet, blue, green, and red single cones, the two components of the double cone, and rods. (A is adapted from Kram et al., 2010). In addition to expressing different opsins, these cells differ in a number of morphologic features includ- ing inner and outer segment structure, oil droplet size and pigmentation, axon length and synaptic targets. B: To isolate specific subpopu- lations of avian photoreceptors, fluorescent reporters were constructed by placing GFP and DsRed under the control of 1.5–3-kb upstream promoters of rhodopsin, red opsin, green opsin, and violet opsin. These reporters were electroporated pairwise into embryonic day 6 reti- nas, which were then grown in culture for 8 days prior to harvesting and processing for frozen section. Reporters driving GFP are listed along the top (B), and reporters driving DsRed are listed along the side. DAPI nuclear stain is shown in blue (B). Each reporter drives expression restricted to the outer nuclear layer (ONL), with little expression seen in the inner nuclear layer (INL) or ganglion cell layer (GCL). Strong colocalization occurs when the same promoter drives both GFP and DsRed (B, diagonal). Only rare coexpression is detected when different promoters drive GFP and DsRed. Scale bar 5 50 lminB. scriptomic diversity between cone subtypes is largely The diurnal avian retina is an excellent model for unstudied. With recent advances in next-generation studying functional diversity in photoreceptors because sequencing, we are now able to assay genome-wide dif- it contains a variety of different types of photorecep- ferences in gene expression between relatively small tors. These include four single cones, the principal and populations of cells, a necessary step in understanding accessory members of the double cone, and rods, each the molecular mechanisms that drive cone photorecep- of which has a number of specialized properties (Fig. tor diversification. 1A). For example, cone photoreceptors contain an 650 The Journal of Comparative Neurology | Research in Systems Neuroscience Transcriptome profiling of avian photoreceptors optical organelle in the inner segment, the oil droplet, MATERIALS AND METHODS which acts as a long-pass filter to narrow the spectrum Animal husbandry of light reaching the outer segment and enhance color All procedures were carried out in accordance with an discrimination (Goldsmith et al., 1984; Hart and Voro- animal protocol approved by the Animal Studies Commit- byev, 2005; Lind and Kelber, 2009; Partridge, 1989). tee of Washington University (No. 20110089). Pathogen- Oil droplets in each cone subtype are pigmented by a free White Leghorn eggs were obtained from Charles unique set of carotenoids (the exception being the vio- River (North Franklin, CT) and stored at 14Cuponarrival. let cone oil droplets that lack carotenoids), resulting in Eggs were warmed to room temperature for 2 hours, and spectral filtering specifically tuned for the opsin present then incubated in a humidified, rocking chamber held at in that subtype (Bowmaker and Knowles, 1977; Gold- 38C for up to 20 days for embryonic time points, or smith et al., 1984; Hart and Vorobyev, 2005). Photore- were hatched and used for postembryonic time points. ceptors also differ in their interactions with neighboring cells. Each photoreceptor subtype tiles the retina as an independent, semiregular mosaic (Jiao et al., 2014; Construction of fluorescent reporters Kram et al., 2010) and forms synapses with specific The upstream promoter regions of rhodopsin, red horizontal and bipolar cells at different levels of the opsin, green opsin, and violet opsin were isolated by outer plexiform layer (Mariani, 1987; Wahlin et al., polymerase chain reaction (PCR) of genomic DNA 2008). The molecules mediating these various features (gDNA). Rhodopsin and green opsin promoters were iso- of avian photoreceptor subtype specialization have not lated from chicken (Gallus gallus) gDNA (nucleotides been identified. 21,949 to 288 relative to the transcription start site Furthermore, subtype-specific transcription factors [TSS] 511, corresponding to chr12:19,499,638– likely drive photoreceptor differentiation and regulate 19,501,514 in galGal4 and nucleotides 2,975 to 28, cor- the expression of the genes that mediate the special- responding to chr26:4,504,913–4,501,931 in galGal4, ized properties described above. The transcriptional reg- respectively). Because the red and violet opsin loci are ulation of photoreceptor differentiation has been not fully represented in the current chicken genome relatively well studied in the rod-dominant mammalian assembly (galGal4), we screened a chicken genomic bac- retina, in which RORB, NRL, and NR2E3 drive rod differ- terial artificial chromosome (BAC) library with red
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